The autonomic nervous system (ANS) readies the body for appropriate response to environmental challenge. It controls the activation of the cardio-respiratory system, the gastro-intestinal tract, sweat glands, hair follicles, and pupillary dilation via the sympathetic and parasympathetic nerves, as well as controlling aspects of the endocrine system by way of the pituitary. The ANS also strongly influences the motor system, controlling muscle tone via activation of the gamma efferent neurons, which influence the responsiveness of the muscles in preparation for complex defensive or appetitive movements (Kennard, 1947; Gellhorn, 1953, 1967a; Hamm et al., 2003). Electrical stimulation of the hypothalamus (the principal controller of the ANS) is known to produce coordinated defensive or appetitive responses accompanied by signs of emotional arousal (Hess, 1925; Gellhorn, 1970) via projections to midbrain nuclei (PAG, locus coeruleus) and the pontine and medullary reticulum (Gellhorn, 1967a). Any activation of the muscular system also involves circulatory and cardio-respiratory adjustments mediated by the ANS; significantly for the PS concept, even imagined movement activates an autonomic response appropriate to the anticipated exertion (Collet and Guillot, 2010). The ANS is strongly linked to the subcortical affective centers, and there is evidence that each emotion has a specific autonomic signature (Ekman et al., 1983; Levenson, 1992; Hamm et al., 2003).

Early concepts of the ANS regarded it as a simple reciprocal bivalent system composed of a sympathetic and a parasympathetic division, which stimulated or calmed visceral functioning (Hess, 1925). Hess (1925), an early researcher into the functioning of the hypothalamus, recognized that the ANS did not function in isolation but was part of an integrated response including the motor system, the arousal/attentional system, and neuro-humoral response. He used the terms ergotropic (energyseeking) and trophotropic (nourishment-seeking) to refer to the integrated functioning associated with the sympathetic and parasympathetic systems respectively. These terms have fallen into relative disuse, but they facilitate description of our concept of unitary subcortical action, and we will use these terms in this paper.

The bivalent view of the ANS has been replaced by a view of the ANS as being capable of complex and nuanced responses to varied circumstances (Saper, 2002). Gellhorn (1970), Levine (1977), and Berntson (Berntson et al., 1994) demonstrated that sympathetic and parasympathetic branches were not limited to reciprocal action; the could vary independently, or co-vary in the same direction. Saper has shown that the hypothalamus is capable of orchestrating complex autonomic responses to varying physiological demands such as thermoregulation, hunger and thirst, and a range of emotional states (Saper, 2002).

Porges (2007) has suggested a three-fold division of the ANS: (a) the evolutionarily primitive, dorsal vagal system that promotes immobility and shut-down, (b) the sympathetic system that mobilizes the fight-or-flight response, and (c) the ventral vagal system that facilitates social engagement. On this basis Porges identifies five global states, involving varying combinations of these: relaxed social engagement, vigorous social play, aggressive/defensive mobilization, relaxed resting immobility, and fear-based freeze or collapse (Porges, 2001). Each of these can be seen as a form of PS, involving coordinated autonomic, motor, affective, and cognitive states.

Interoception is the name given to the perception of information coming to the brain from the viscera (Vaitl, 1996); this also includes afferents from skin (Björnsdotter et al., 2010) and fascia (Schleip, 2012). Craig and Critchley have delineated the pathways whereby some of this information can reach consciousness and bring information about affective and autonomic state (Craig, 2002; Critchley et al., 2004) Damasio (Damasio et al., 1996) suggests that interoception may carry important information about the environment. It has been shown that even unconscious visceral afferents can strongly influence affective experience and behavior (Ádám, 1998). Training can enhance conscious awareness of interoception (Holzel et al., 2011b; Farb et al., 2013) and thereby increase emotional self-regulation (Vago and Silbersweig, 2012).

#### Emotional/Motivational Response

A widely held view is that emotion is strongly related to a disposition toward action (for instance (Bull, 1945, 1951; Lang et al., 1990, 1993; Frijda, 2004) Bull's attitude theory of emotion states that emotional affect emerges out of the preparation for action rather than the action itself (Bull, 1951, 1955). Her investigation of hypnotically induced emotion demonstrates that the preparatory movement responses to emotion constitute an integral aspect of the experience of emotion. If a certain preparatory movement state was (hypnotically) suggested to the subject (for instance, leaning back in the chair), they were unable to experience a (hypnotically suggested) emotion that contradicted this (for instance, anger) (Bull and Gidro-Frank, 1950). De Rivera (1977) extended Bull's work, offering a conceptual schema using five dimensions of movement to characterize a broader range of human emotional experience. His schema has not been investigated, beyond one study of consistency and reliability, but his ideas suggest the possibility of more detailed correlations between emotion and movement preparation. One possible line of investigation would be to produce abstract animations embodying the dynamics suggested by De Rivera ("move myself away from the other person," "move the other person away from me," etc.) and discover whether subjects attribute emotional motivation to the images.

Panksepp identifies seven core emotional systems (Panksepp, 2005), each associated with specific subcortical nuclei and neurotransmitter profile. He regards the motoric and affective aspects of these as equally important Each emotional system involves motivational feeling as well as characteristic movement and movement preparation patterns, supporting our hypotheses. He argues for these systems as the source of both human and animal basic emotions; his arguments are as follows.

• Direct brain stimulation in animals and humans produces strong unconditioned emotional reactions, whereas cortical stimulation has much less effect.

For a detailed exposition see (Panksepp, 1998, 2005, 2011).

# Attentional Response (Awareness)

Attending is an act as well as a receptive experience; and there is a spectrum from purely reflexive to fully volitional attending. Fan (Fan and Posner, 2004) proposes a distinction between alerting, orienting, and executive direction of attention. The initial alerting reflex is automatic and unconscious. It involves hippocampus, superior and inferior colliculus and the locus coeruleus, PAG, ventromedial medullary reticular formation, and medullary nuclei controlling head movement (Radulovacki and Adey, 1965; ´ Öhman et al., 2000). At this level a rapid automatic evaluation is already being made (Porges, 2004) and we suggest that the PS begins to be organized. Next a more complex and nuanced orientation process begins, directing the appropriate senses in the appropriate directions, orienting to available resources, and completing the PS process. More rostral areas become involved later: the parietal lobe and the frontal eye fields (for visual stimuli), and finally, with volitional direction of attention, anterior cingulate and prefrontal cortex (Fan and Posner, 2004). The exact point at which this process becomes conscious is not clear. We suggest a continuum of awareness from completely unconscious and automatic to fully conscious and voluntary, and that the training of voluntary attention may lower the threshold so that previously automatic responses may come under voluntary influence. Such alterations have been demonstrated, see for instance (Brown et al., 1984).

Affect influences attention at a fundamental level: for instance, negative emotions narrow and focus the field of attention in specific ways, whereas positive emotions open the attentional field beyond that of neutral attention (Fredrickson and Branigan, 2005). We hypothesize that this influence goes in both directions: voluntarily broadening the field of attention may induce a more positive affective state. BTES make such claims, which could be tested as described below.

The PS has been explored extensively in the context of simple perceptual attentional tasks, involving the study of anticipatory saccadic eye movements (Ruge et al., 2013). These studies are of limited relevance here as they deal with very short time frames and affectively neutral situations. Brunia points out the strong relation between anticipatory attention and motor preparation, and suggests that the reticular nucleus of the thalamus has a central role in both (Brunia, 1999). It has been shown that anticipated action mobilizes the ANS in accordance with how much effort is anticipated; and that uncertainty increases the amount of activation (Brunia, 1993). This supports our hypothesis of the link between attention and motor and autonomic state, suggesting the possibility (as claimed by the BTES) of altering muscle tension, posture and autonomic arousal by voluntary modulation of attention. Meditation has been studied primarily as an attentional strategy, and its positive effects on autonomic, affective and cognitive processes are well documented (Raffone and Srinivasan, 2010; Chen et al., 2012; Desbordes, 2012; Fox, 2012; Friese et al., 2012; Kox et al., 2012; Sedlmeier et al., 2012; Vollestad et al., 2012; Tang et al., 2014).

#### Expectation: Cognitive Response, Appraisal, Implicit Memory

The term "cognitive" can be ambiguous (Canamero, 1998). While it refers broadly to knowledge and awareness it may conflate different kinds of knowledge. It may confuse explicit fully conscious verbal and conceptual knowledge with implicit, emotional, nonverbal knowledge. This distinction has recently been explored by Stott (2007) as "rational-emotive dissociation." In memory research a clear distinction is made between explicit and implicit (Schacter et al., 1993). Explicit (autobiographical and episodic) memory can be brought into full consciousness, considered and re-evaluated. Implicit (including procedural) memory usually cannot, and is stored in different parts of the brain (Reber, 2013). Implicit memories influence behavior without one being conscious of this influence (Roediger, 1990). Procedural memory stores the action patterns associated with different situations and activities. The appraisal of events is largely based on memory (Glenberg, 1997). If that memory is explicit (subject to conscious thought and decision), we could term it explicit appraisal; if the memory is implicit it is implicit appraisal (Castelfranchi, 2000; Stott, 2007), or what Polanyi termed "tacit knowledge" (Polanyi, 1962).

Implicit and procedural memories are quickly activated and are accessed at a subcortical level (Roediger, 1990). They activate a set of expectations about the situation. Glenberg (1997)suggests that the main function of memory is to guide appropriate action (and therefore preparation for action) in the present moment. The simulation of bodily experienced states and actions are significantly involved in memory (Ross et al., 2007), understanding (Barsalou et al., 2003; Pulvermüller, 2005), interpersonal communication (Hostetter and Alibali, 2004), social interaction (Sebanz et al., 2006), and spatial perception (Tversky, 2003). This supports the idea that the expectancy aspects of the PS are intrinsically linked with affect and bodily preparedness.

Fully conscious appraisal involving explicit memory is slower, and comes after the rapid initial appraisal. Although cortical processing can and does modify the activity of the subcortical centers ("top-down"), the "bottom-up" connections are more extensive and arguably at least as powerful (Critchley, 2013). People frequently find themselves reacting and deciding "emotionally," often based on early implicit learning (Hovdestad and Kristiansen, 1996; Luethi et al., 2008; Orange, 2011). Appeals to "reason" concerning emotional reactions are often ineffective (Langer, 1975; Langer et al., 1978; Goleman, 2006; Goel, 2014). The theory of cognitive dissonance states that, once a certain set of expectations is in place, people tend to ignore disconfirming perceptions and notice confirming ones (Festinger, 1962).

Appraisal at a subcortical level has a direct and immediate effect on affective, visceral and motor function, and is not easily accessible to change (Critchley, 2013). Cortical (explicit) appraisal is easy to access consciously, fairly easy to change, but may not have much effect on emotion and autonomic state (van der Kolk, 2002).

We suggest that subcortical, implicit appraisal is a core aspect of the PS, to be distinguished from fully conscious rational appraisal. In this paper we will use the term "expectancy" or "expectation." We define this as a rapid, automatic, marginally conscious process of appraisal, accessing implicit and procedural memory and generating a set of expectations concerning the present situation. Porges' concept of "neuroception" (Porges, 2004) is an example of such a process. He postulates a largely unconscious, sub-cortically processed perception of the safety, or lack thereof, of the environment.

# Categories of PS

The concept of PS leads to the question: what different kinds of PS are there? The early view of the ANS as bivalent (ergotropic and trophotropic) suggests two PSs: readiness for active mobilization, and preparedness for quiet recuperation.

Levine (1977) and Berntson (Berntson et al., 1994) have demonstrated that the parasympathetic and sympathetic branches are not limited to reciprocal activation, suggesting a range of possible states.

Porges' polyvagal theory suggests five states (based on combinations of dorsal vagal, sympathetic, and ventral vagal activity): immobility without fear (dorsal vagal) immobility with fear (dorsal vagal and sympathetic); fight-or-flight mobilization (sympathetic), play (sympathetic and ventral vagal), and social engagement (ventral vagal).

Panksepp defines seven core subcortical emotional circuits, each of which is neurologically and chemically distinct and has its own characteristic postural, affective, autonomic, attentional, and cognitive patterns: SEEKING, FEAR, ANGER, LUST, NUR-TURANCE, PLAY, GRIEF (Panksepp, 2011) (The use of capitals is Panksepp's way of distinguishing his proposed classification from the ordinary use of these words). This schema partly overlaps Porges', and could form the basis for a partial taxonomy of PSs. The instinctive appetitive drives such as hunger, thirst, and thermoregulation, could also define specific PSs. Our theory suggests that any of these PSs (a preparatory state oriented to escape, attack, sexual activity, exploration, nurturance, etc.) could become maladaptive through persistence or disorganization, and form the basis for various kinds of distress, not all of which would currently be termed "stress."

#### Stress and the PS

How is the PS relevant to stress, and how does this differ from the view that stress is excess sympathetic arousal? Cannon's (1939) and Selye's (1954) early theories of stress hypothesized a unitary "stress response" involving a series of automatic neurophysiological reactions: activation of the sympathetic and inhibition of the parasympathetic nervous systems, triggering of the adrenal medulla and cortex, the release of catecholamines and cortisol. More recent research reveals the complex modulation of this response in the face of different forms of physiological challenges (Saper, 2002), the complex dynamics of the interaction between sympathetic and parasympathetic branches of the ANS (Gellhorn, 1967b; Levine, 1977; Berntson et al., 1994), the interactions between the ANS, the immune system (Mignini et al., 2003), and other subcortical structures modulating arousal, attention, affect, motivation, and movement (Tucker et al., 2000; Öhman et al., 2000; Strominger et al., 2012; Leventhal, 2014; Norman et al., 2014), and the neurochemical details of allostatic load and overload (Seeman et al., 2001; Lupien et al., 2006), as well as the involvement of cortical structures in these subcortical processes (Berntson and Cacioppo, 2007). Despite these developments the single word "stress" continues to be used. To our knowledge, our hypothesis that stress can be understood in terms of preparation for action has not previously been proposed.

Stress is not a single phenomenon, and we believe that the use of the word in a scientific context is no longer justified. Instead we suggest that the broad range of phenomena subsumed under the term can be discussed in terms of whether the current PS is adaptive or maladaptive to the current situation. Some ambiguity may be involved, in that there could be more than one kind of response that might be adaptive in certain situations.

This framework allows the discussion of all the phenomena referred to as stress, the clarification of the five questions about stress raised above, and the discussion of a number of dysfunctional states not normally referred to as stress. In addition it allows the consideration of healthy and optimal responses. The discussion below focuses mainly on ergotropic and trophotropic PSs; we hypothesize that similar dynamics are involved in all PSs, but there is as yet little data to support this.

#### Adaptive PS

The simplest form of stress is sympathetic (ergotropic) arousal in a challenging situation: fight or flight. This is necessary, appropriate, and not problematic. In response to moderate acute challenge, there is a rapid increase in sympathetic activation accompanied by a decrease in parasympathetic activity. This ergotropic state facilitates vigorous response to the challenge. This is followed by a parasympathetic "rebound," and a return to baseline of the sympathetic activation (Gellhorn, 1956). This is usually referred to as acute stress (Everly and Lating, 2013). In PS terms, the adaptive PS leads to effective action, the situation is successfully resolved, and the PS of arousal subsides and is replaced by one of recuperation (trophotropic). This process occurs both in sudden threatening situations, and also in voluntary activities such as sports and risky recreation. This short-term activation of adaptive ergotropic PS has been called "good" stress (Everly and Lating, 2013). It usually leads to increased ability to handle stress: "stress inoculation" (Meichenbaum et al., 2009) or resilience (Karatsoreos, 2013; Wu et al., 2013). We hypothesize this involves an increased ability to adopt and relinquish PSs. This could be tested by observing whether exposure to successfully resolved moderate stress increases performance on a "stop signal" task (Logan, 1994) (which measures the ability to let go of expectations).

However, if the threatening situation is prolonged, negative neurophysiological consequences [allostatic overload (Lupien et al., 2006)] may occur despite the adaptive nature of the PS. Thisis one form of chronic stress, which can only be prevented by ending exposure to the challenging event. If the situation is very extreme, it may exceed the realistic capacities of the organism to cope. In this case, the PS may nevertheless remain coherent and organized, in which case there may be few lasting consequences once the event is over. Or the PS may become disorganized (competing PSs may be simultaneously aroused—see below for discussion), which increases the chance of post-traumatic stress (PTS) (Bovin et al., 2008) (See **Table 1**).

#### Maladaptive PS

We define four kinds of maladaptive PS; see **Table 2** below. First, the PS could be well-organized but not well matched to handling this particular situation. Second, the PS itself could be disorganized. In either case, the maladaptive PS may be "persistent" (a PS which arose in response to an earlier situation but has continued beyond its utility) or "situational" (a PS in response to the present situation which is not well adapted to handling that situation. By definition, a PS is organized to enable effective action. Once the action is successfully completed, the PS subsides. We suggest that one cause for a PS not subsiding (persisting) is the

#### TABLE 1 | Outcomes of adaptive PS in four situations.

*When the PS is well matched to the challenging situation (adaptive), there can be a variety of outcomes depending on the situation. If the situation is successfully resolved within a short time, there will be increased long-term resilience. If the situation fails to resolve quickly, there may be increased allostatic load. If the situation overwhelms the capacity to cope but the PS stays organized, there may be few long-term consequences. However if the PS becomes disorganized (see text for explanation) there may be lasting post-traumatic stress. (AL, allostatic load; PTS, post-traumatic stress.)*

#### TABLE 2 | Two dimensions of maladaptive PS.

*Maladaptive PSs can be categorized in two dimensions. First, whether they have arisen in (poorly matched) response to the present situation, or whether they are chronic, persisting unresolved from a previous situation.  Mandler's experiments on the interruption of organized behavior as a principal cause of anxiety and disorganized behavior are supportive of our suggestion (Mandler, 1964; Mandler and Watson, 1966).

#### **Persistent PS**

If ergotropic arousal [in Panksepp's terms, the FEAR and RAGE circuits (Panksepp, 2011)] persists long after the situation has passed, this is problematic. The PS does not end, and the organism continues to prepare for challenge. Ergotropic arousal is designed to handle time-limited challenges and has deleterious neural and neurochemical effects ("allopathic load") if sustained. Since the challenging situation is no longer present, action cannot be taken and the PS does not resolve (Mandler and Watson, 1966). This usually leads to decreased resilience as allopathic load increases (Seeman et al., 2001).

The question "what are the neurochemical details of allopathic load" is different from "what causes the PS (and thus the accumulation of allopathic load) to persist?" The PS perspective distinguishes the effects of "stress" from the actual nature of "stress" itself : the maladaptive PS. In our view, it is the ending of the maladaptive PS that ends the core stress response, not the correction of neuro-humoral imbalance or the removal of the challenging situation. (Of course, correcting neuro-humoral imbalance due to disease or genetics, and remedying the external situation, are crucial where possible.)

Gellhorn has shown in rats that a shock above a certain threshold of duration and intensity prevents the normal parasympathetic rebound, and the sympathetic system may remain activated indefinitely (persistent PS). He refers to this as "tuning" (Gellhorn, 1968). A similar phenomenon, heightened reactivity of the amygdala, is termed "kindling" (Cottrell and Nyakas, 2013). We suggest that both are examples of persistent PS.

If this hypothesis is correct, it would suggest that if the rat is given an opportunity to complete the PS in vigorous action, the PS would be released and the behavioral problems disappear. This has been shown to be the case. A rat alone in a cage may develop behavioral problems in response to shock; but if the rat is in a cage with another rat with which it can fight, it is much less likely to develop problems (Weinberg et al., 1980). In humans, subjects startled by a pistol shot but instructed not to move remained in a state of elevated sympathetic activation afterwards, but if encouraged to move vigorously their system returned to normal (Freeman and Pathman, 1942). If rats are subjected to shock but restrained from escaping, they develop

behavioral problems (Mandler and Watson, 1966). If the rats are later placed in the original situation and given an opportunity to escape through vigorous action, the conditioned fear rapidly disappears (LeDoux and Gorman, 2001). We suggest this is because the PS is now given the opportunity to resolve and the action patterns can complete. These results suggest that if adequate ergotropic activity does not occur the ANS may not return to balance and the PS generated in response to the threat may persist. This supports our hypothesis that completing the action pattern of a PS ["biological completion" (Levine, 2010; Payne et al., 2015)] enables it to subside (See **Figure 2** for a summary).

#### **Disorganized PS**

If the threat is extreme, inescapable, or very prolonged, there may be an apparent "spillover" of activation from the ergotropic to the trophotropic systems, possibly due to spreading neural arousal from anterior to posterior hypothalamic nuclei (Gellhorn, 1967a). Several researchers have documented this phenomenon (Gellhorn, 1959, 1967a; Paton et al., 2006). It involves simultaneous high activation of sympathetic and parasympathetic systems and the loss of effective coping ["co-activation": see (Berntson et al., 1994)]. Such a reaction can be induced in animals by physically restraining them from escaping shock (Mandler and Watson, 1966; Shors et al., 1989; Amorapanth et al., 2000). This is the canonical way of inducing PTSD-like symptoms in animals. This response has been called tonic immobility (TI) (Hoagland, 1928; Bovin et al., 2014; Marx et al., 2008). TI and similar symptoms have been associated with increased likelihood of PTSD in humans, and develop under similar conditions of restraint (Suarez and Gallup, 1979; Volchan et al., 2011; TeBockhorst et al., 2015). TI prevents effective completion of the defensive response. Porges' polyvagal theory characterizes this fear-based immobility as a simultaneous activation of the sympathetic and the evolutionarily more primitive dorsal vagal system (Porges, 2001).We suggest this can be conceptualized in our framework as the simultaneous arising of mutually incompatible PSs (flight and freeze), which leads to a disorganized and ineffective response. We suggest that the ensuing "stress" and behavioral problems can be explained as the maladaptive persistence of the disorganized and interrupted PSs. This may provide an alternate way of viewing "dissociative" behavioral phenomena. The PS perspective suggests that resolution of these symptoms can come about by enabling the PSs to be released through completion of the action pattern. However, this resolution may not happen as readily in animals with TI as with sympathetically "tuned" animals: when animals with TI are placed again in the cage they may not spontaneously try to escape. The researcher may have to physically move them to safety before the instinctive defensive action will take place (Gellhorn, 1967c), indicating a clear distinction between what we are calling "organized" and "disorganized" PS. Our theory suggests that in such cases two contradictory PSs must be released before resolution can take place: the escape and the immobility. This suggests greater clinical difficulty in dealing with the latter, which is widely recognized to be the case. See **Table 3** for further discussion, see below under

Biological Completion, also (Levine and Buczynski, 2013; Payne et al., 2015).

#### Varieties of "Stress"

As discussed above, one advantage of the PS framework is that it enables identification of a wide range of specific dysfunctional conditions. These conditions may be referred to collectively as "stress," even though they are quite distinct; or they may be excluded from this category despite the fact that it would not be true to claim they are "not stressful." We suggest that any maladaptive PS, is problematic for the organism, not only ergotropic PS involving anger and fear. We suggest that different maladaptive PSs will have discrete harmful consequences on all levels from physiological to psychological. Animal experiments aimed at frustrating specific drives could test this.

We further suggest that our model of disorganized PSs could apply more broadly than in the above example of conflicting immobility and escape impulses. We suggest it might be possible for extreme activation of any PS to spread into another, competing PS, and cause disorganization and ensuing behavioral problems. In animals, this could be tested through direct brain stimulation.

Following Panksepp's model of seven primary emotional states, each with its own neural and neuro-chemical substrate (Panksepp, 2011), we suggest that a persistent FEAR PS will have different neurochemical, neural, and psychological consequences from a persistent RAGE PS. Likewise, the intrusion of a NUR-TURANCE PS into a situation that requires RAGE, a LUST PS when NURTURANCE is required, a GRIEF PS when SEEKING is required, each will have different negative consequences, each with a distinct profile. It is hardly useful to call them all "stress," nor to debate which constitute "stress" and which not. We believe the PS framework offers a more precise and nuanced way of characterizing a wide variety of problems, and could guide targeted therapeutic approaches. Bos and Panksepp have already used a similar framework to suggest novel pharmaceutical approaches to different forms of stress (Bos et al., 2012). The identification of the specific PS involved in particular forms of emotional or autonomic dysfunction could guide effective intervention via BTES or cognitive-behavioral therapies. A nuanced understanding of

*The PS perspective suggests that the four kinds of maladaptive PS (organized/situational, organized/persistent, disorganized/situational, disorganized/persistent) each call for a different therapeutic response. If the PS is well organized and arises in response to the current situation, but is poorly matched, a process of conscious re-organization may be effective. A well-organized but persistent maladaptive PS could be termed a "bad habit"; a resolution through increased awareness of the origins of the PS may help. If the PS is disorganized, and the direct result of the present situation, immediate trauma "first aid" may be very effective. If on the other hand the disorganized PS is the result of past unresolved experiences, PTSD or "disorders of extreme stress not otherwise specified" (DESNOS) may follow, which require specific trauma-oriented therapy. DESNOS is a term from DSM V which covers a variety of trauma sequelae which fail to fall into the category of PTSD. (DESNOS: Disorders of Extreme Stress Not Otherwise Specified)*

maladaptive PS, could increase the effectiveness of a wide range of medical diagnoses and interventions.

#### Five Questions about Stress

Below we restate the five questions about stress posed at the beginning of the paper, and indicate briefly how the PS perspective can clarify them. Many of these issues have already been addressed above and are summarized below.

#### **"Good" stress/"bad" stress**

The mobilization of organismic resources in response to challenge is necessary and beneficial, and yet under some circumstances mobilization can lead to significant problems. A distinction has been made between "good" stress and "bad" stress (Selye, 1985), but the exact nature of the difference between them is not clear. The PS perspective distinguishes adaptive and maladaptive PSs; the former generally lead to greater resilience ("good" stress), the latter to various harmful consequences ("bad" stress).

## **Acute, chronic, and traumatic stress**

Stress has been classified as acute, chronic and traumatic. This classification has been made on the basis of differing neurophysiological reactions (Everly and Lating, 2013); but it remains unclear what determines these differing responses. The PS perspective suggests that acute stress involves an appropriate, timelimited PS appropriate to threat or challenge (mobilization of active resources); chronic stress involves either a persistent maladaptive PS or adaptive response to prolonged challenge; and traumatic stress involves a disorganized PS characterized by regression to a phylogenetically more primitive (Porges, 1995) form of PS (Halvorsen, 2014).

# **What is resilience?**

It is widely recognized that different people exposed to almost identical events can respond in very different ways. It has been shown that the presence or lack of resilience may be due to genetic factors, adverse childhood experience, and personality make-up (Karatsoreos, 2013). However, there is little clarity about exactly what this resilience is.

The PS perspective suggests that resilience is in part the ability to let go of inappropriate PSs and to adopt functionally appropriate ones. Adverse childhood experience may cause persistent maladaptive PSs, and some measures of personality associated with poor resilience may be measures of maladaptive persistent PSs. We suggests that resilience may be improved by ending persistent maladaptive PSs as well as by learning new adaptive ones. We also suggest that cognitive techniques will be effective only to the degree they influence subcortical organization (van der Kolk, 2002). This suggests the value of methods (such as those used by BTES) which more directly affect subcortical areas.

#### **Appraisal and expectation**

A distinction has been made between physical and physiological stressors (such as cold or toxin) and psycho-social stressors (such as a challenging social situation or a negative thought) (Everly and Lating, 2013). In the latter, the person's appraisal (and consequent expectations) of the situation is regarded as largely determining the response (Olff et al., 2005). However, the organism's response even to physical stressors can be altered voluntarily. For instance Hof and volunteers trained by him have been studied for their anomalous physiological responses to extremes of cold exposure and inflammatory challenge (Gard et al., 2014; Riley and Park, 2014). A significant part of this training involves the re-appraisal of the nature of cold as well as BTES techniques of breath control, posture and imagery (Kox et al., 2012, 2014).

On the other hand the concept of the "appraisal" of a psychosocial stressor is not clear. The mere thought that a situation will not be stressful is unlikely to change a person's response; and yet the previous examples, as well as the proven effects of cognitive restructuring therapy, show that appraisal can have a significant impact. Why should appraisal sometimes appear to determine outcome and at other times not?

The PS perspective suggests that re-appraisal occurring only on a verbal/conceptual level is less likely to alter the PS, and thus the stress response; but altered subcortical expectations may be more effective. This suggests that attention to interoceptive and proprioceptive experience may be more effective in handling stress than attention to ideas and thoughts alone, because bodily experience enables more direct access to the PS.

# **What is the stress response itself?**

Recent work on "allostatic load" (Cicchetti, 2011), the accumulated "wear and tear" from continual adjustment to changing life conditions, has provided detailed knowledge about the neurochemical and neuroplastic effects of stress. In our view, this still leaves unaddressed the core of what the stress response itself is and how it can best be changed.

The PS perspective suggests that the essence of the stress response is the perpetuation of maladaptive PSs, and that effective treatment of stress should involve a focus on changing subcortical preparatory organization. The BTES offer methods with this focus.

# BTES

# What are BTES and How Do They Relate to PS?

BTES present a specific challenge to the scientific investigation of human suffering and its remediation. Traditional science has been based on the Cartesian dualism of mind and body (Damasio, 2005), whereas the BTES are firmly based in a non-Cartesian view. Despite the current interest in "mind-body medicine," this paradigm persists, as does the continuing gulf between the BTES and mainstream medical and psychiatric theory (Leder, 1992). In presenting the PS as an explanatory framework we hope to demonstrate that current neuroscience supports the view of the BTES that bodily aspects (movement, posture, proprioception, interoception) are, at a basic level, inseparable from affective and cognitive aspects of the organism.

#### Defining BTES

We define BTES as a diverse group of educational and therapeutic practices, of traditional Asian and modern Western origin, which share a common set of assumptions and practices. They encourage attention to posture, breathing, movement, and proprioceptive and interoceptive sensation, as well as tactile and spatial awareness; and they use this bodily attention as well as voluntary movement and imagery as the principal means to accomplish therapeutic change (Read and Stoll, 2009). They do not deny "disease," but do not use a disease framework in evaluation or treatment (This distinction can be a central issue in studies of efficacy related to medically defined disease states.). Importantly, BTES do not make a fundamental distinction between body and mind, tending to regard them as poles on a continuum rather than fundamentally different realms (Rosenthal, 1991). Our hypothesis is that the PS is an integrated subcortical state that is significant in physical and emotional distress, and that interventions on any one of its components will tend to alter all the components. Further, that BTES interventions are based on this view; see **Table 4**. At the end of this article we summarize the suggestions we have made for testing these hypotheses.

#### **BTES are normative**

BTES aim to increase overall human health, physical, emotional and mental, toward optimal functioning, and not only to remedy ill health. They all include the concept of an optimal state which maximizes adaptive ability across a wide range of situations. This is generally defined (Johnson, 1995, 1996) as a state that is flexible, balanced, open, and capable of adjusting quickly to the varying demands of the environment. Such a state allows the rapid adoption of specific adaptive PSs as well as the ability to quickly relinquish them. It is variously described as involving proprioceptive experiences of balance, stability, and lightness (Jones, 1976); an open flexible attention (Brown and Ryan, 2003); interoceptive experiences of calm, warmth, and flow (Csikszentmihalyi, 2008); flexible expectations (Farb, 2012); and affective feelings of openness, confidence and curiosity (Ekman et al., 2005). BTES claim that optimal PS is quite rare, that most people are stuck in maladaptive PSs.

#### Changing PS

We have suggested that stress can be resolved by releasing the maladaptive PS, and that this is the primary aim of BTES. A broad examination of the BTES suggests that there are two principal ways PSs can be changed. The first is by becoming conscious of the process of maintaining the PS, voluntarily letting go of it and replacing it by a more adaptive PS. The second is through "biological completion," in which the originally obstructed impulse is enabled, in a safe context, to complete itself.

#### **Awareness of PS**

Both of these processes, voluntarily letting go of a maladaptive PS and biological completion, require awareness of the PS. Since PS are primarily sub-cortical, it may not be easy for a person to be fully, reflectively aware of their PSs, especially in the case of persistent maladaptive PS. BTES claim that this lack of awareness is the major obstacle to being able to let go of the PS, and that by cultivating the capacity to attend to subtle aspects of proprioception and interoception (as well as attentional orientation and affective state) it is possible to become aware of the PS and of one's active (if involuntary) process of adopting and maintaining it.

Damasio's theory of somatic markers (Damasio et al., 1996; Damasio and Carvalho, 2013) emphasizes the important role of interoceptive awareness in becoming aware of one's inner state. Interoception enables one to become aware of the (autonomic) state of the body, and is strongly related to emotional response and affective and visceral aspects of the PS.  The anterior insula and anterior cingulate cortex are where this information reaches full awareness. Proprioceptive and kinesthetic information likewise bring to consciousness other essential aspects of the PS including posture, muscle tone, and movement preparation (Suetterlin and Sayer, 2013). The cortex receives this information in the sensorimotor, pre-motor and supplementary motor cortexes (Gellhorn, 1964; Prochazka, 2011)

*The listed BTES use interventions that involve several of the components of the PS. Stated claims of influencing other components of the PS are also listed. Although the BTES differ in emphasis and in the details of the intervention, they share a similar framework. The references in this table are to substantiate that the BTES claim to use these forms of intervention and to have these effects; they refer mainly to the writings of the founders or prominent practitioners, not to peer-reviewed publications. Key: P, Principal form of intervention C, Effect claimed.*

as well as in the body schema area in the inferior parietal and extra-striate body area (Arzy et al., 2006; Daprati et al., 2010; Ionta et al., 2011). Proprioceptive and kinesthetic feedback bring information from the basic and EMS (Holstege et al., 1996), and thus can inform the conscious mind about unintended automatic or emotionally driven motion, bringing information about current PS.

#### **Voluntary change**

The BTES claim that once awareness has been achieved it is possible to alter the PS through the use of the following voluntary procedures:

As indicated above, there is evidence for the effectiveness of each of these in altering stress responses. We suggest that the anterior cingulate (ACC) and the premotor cortex (PMC), as well as portions of the orbito-frontal cortex (OFC), are the principal originations of these actions. It has already been shown that ACC has significant effects on amygdala (Posner et al., 2007) and other subcortical autonomic, affective and motor areas (Critchley et al., 2005), as well being involved with acts of intention (Shenhav et al., 2013). PMC has rich connections to subcortical motor centers, alters posture, muscle tone and autonomic state (Jeannerod, 1994; Desmurget and Sirigu, 2009). OFC likewise has extensive connections to subcortical areas and is central to several executive networks (Price, 2007)}. It has been shown that both motor (Collet and Guillot, 2010; Anema and Dijkerman, 2013) and affective (Lang, 1979) imagery can alter subcortical activity.

#### **Biological completion**

In our discussion of maladaptive PS above, we referred to "biological completion." This involves the completion, through imagery or safe re-enactment, of the impulses of the persistent maladaptive PS. Several forms of BTES use this approach, especially the more psychotherapeutically oriented ones. The term itself comes from Somatic Experiencing (SE), but many other BTES use methods others use methods which may involve this mechanism. This includes body-oriented therapies generally. Movement practices such as Spontaneous Qigong (Cohen, 1999), Kriya and Tandava Yoga (Odier, 2003), and T'ai Chi, may involve similar processes. Clinical experience in SE shows that biological completion often involves autonomic discharge such as trembling, flushing, or crying (Levine, 2010; Payne et al., 2015) which appear to result in a normalization of autonomic activity. These processes have been very little studied, although Gracanin (2014) ˇ has demonstrated that crying can facilitate autonomic and affective balance, and trembling, which has been documented during TI in response to rape (Suarez and Gallup, 1979), may be the beginning of such a discharge (Payne et al., 2015). Facilitating the completion of the defensive reaction, in a safe therapeutic context, restores balanced functioning to the ANS and the network of core subcortical centers, resolves the stress response, and allows the patient to let go of the trauma-oriented PS in which they had been stuck since the precipitating event. This completion happens through the use of imagery and subtle movement to enact a successful resolution of the situation. Biological completion is discussed at greater length in Payne et al. (2015) and Levine (2010).

We believe there is supportive evidence for this process; as mentioned above, of restrained animals recovering from trauma through completion of the escape response, as well as the role of TI in PTSD in humans. However this theory is still speculative. Systematized manualized application of this procedure in randomized controlled trials, with measurement of affective and autonomic variables, would help to clarify the impact of biological completion as compared with cognitive-behavioral and exposure therapies. It should be determined whether generalized vigorous movements have the same effect as specific completion of the movements involved in the original traumatic situation. In rats this might be tested by shocking and restraining the rat in a situation requiring a given response, then later offering some of the rats an opportunity to complete that response (e.g., running to safety), while offering others a quite different activity (such as climbing to get food). The biological completion hypothesis would suggest that the former group would recover more completely than the latter.

#### Research on BTES

Seated meditation (Raffone and Srinivasan, 2010; Travis and Shear, 2010; Holzel et al., 2011a) and Yoga (Gard et al., 2014) have received the most research attention, with Qigong (Jahnke et al., 2010; Payne and Crane-Godreau, 2013) a close third. Somatics and body psychotherapy have has the least research reported, although clinical and anecdotal evidence for their efficacy is evidenced by informal published accounts, the authors' experience, and personal communications from practitioners. Given their promise to support and optimize health, we hope our proposed framework might facilitate research into their mechanisms. Research into Somatics particularly has been hampered by poor quality of experimental design, inadequate controls, small study size, poorly standardized interventions and most significantly for our paper, a lack of full understanding on the part of researchers of the concepts and techniques of BTES (Kerr, 2002). See for instance this study contrasting the philosophical approaches of the Feldenkrais Method and conventional exercise (Wright, 2000).

#### Examples of BTES

A complete survey of all forms of BTES is well beyond the scope of this paper. We will confine our discussion to several of the better-known systems. BTES fall into three broad categories:

here we will discuss the Alexander Technique, the Feldenkrais Method, Continuum, and Rolfing.

• Western forms of "body psychotherapy." We will discuss Reichian Therapy and its off-shoots Bioenergetics, Formative Psychology, and Levine's Somatic Experiencing trauma therapy.

#### Modern Forms of Traditional Asian Psychophysical Practices

#### **Qigong and Taijiquan**

"Meditative movement" (MM) has been proposed as a term referring to a broad range of Asian contemplative practices (Larkey et al., 2009) including Yoga, Qigong ("Chi Kung") and Taijiquan ("Tai Chi"). There are however significant differences between Yoga and Qigong, so we will discuss them separately.

Qigong teaches balanced standing and movement accompanied by spatial, proprioceptive and interoceptive awareness (Cohen, 1999). It brings conscious awareness to the (mechanical) postural processes of grounding, orientation, and correct relation of the longitudinal axis to gravity (Cohen, 2012), thus promoting optimal postural preparedness and a sense of self-efficacy; and through the monitoring of breathing and other interoceptive information, muscle tone and movement (proprioception), and thought activity, brings about a calm, centered state in which one is responding to the actual present condition rather than preparing for past or future events. Further, it trains one to let go of inappropriate anticipatory tension, to maintain resilient flexible posture with balanced muscle tone, and to maintain this balanced preparatory state while moving in simple or complex ways, moving with a partner, or even simulating attack and defense (Diepersloot, 1997). One of the great benefits of martial forms of Qigong (like Taijiquan) is that it teaches one to prepare for extreme challenge by remaining flexible, grounded and aware rather than tensing in fear or anger or collapsing in fear. Although Qigong practice may not specifically address past traumatic memories, we suggest it may facilitate processing such memories by retraining the dysfunctional PSs associated with them. Qigong practice characteristically involves using imagined movement to create very subtle changes in bodily posture and proprioceptive experience. This engages the premotor areas (Gerardin et al., 2000), central to our concept of the PS. The methods of Qigong are fully congruent with our hypotheses concerning the PS.

Research into Qigong has been hampered by poor experimental design, small studies, and difficulty translating the traditional theory into scientific terms; for a discussion, see (Kerr, 2002; Payne and Crane-Godreau, 2013). However most studies point to positive results in a wide range of physical and psychological conditions, in some cases even when compared to standard treatments (Ng and Tsang, 2009; Jahnke et al., 2010; Lee et al., 2011).

#### **Yoga**

Yoga has been shown to be of benefit in a wide variety of conditions, and its literature is quite extensive. For a recent review, including extensive speculation on mechanisms, see Gard (Gard et al., 2014). Hatha Yoga (the principle form of Yoga practiced in the West) uses specific postures, often held for periods of time, to stretch and strengthen the body and to focus the mind (Iyengar, 1966; Singleton and Byrne, 2008; Jois, 2010). In our theory, persistent PSs will involve chronic muscle tension. It is widely accepted in Yoga and the manual therapies that chronic muscle tension results in a shortening of the fascia (Chaitow, 2010). Yoga postures restore appropriate length and alignment to the musculoskeletal structure, which may provide a new proprioceptive experience which may in turn help establish more flexible PSs. Carney's research supports the effect of posture on affect and neurochemical secretion (Carney et al., 2010). Yoga also uses breath control to alter the autonomic state (Brown and Gerbarg, 2005a,b) as well as the control of the attention. Yoga explicitly aims at establishing a more optimal overall psychophysical state (Jois, 1999). This is consistent with our hypothesis that Yoga addresses the PS through intervention on its components.

#### **Meditation**

Meditation, in particular "mindfulness" meditation from the Buddhist tradition, has been studied extensively. However, the focus has been mostly on cognitive and attentional aspects of meditation (Raffone and Srinivasan, 2010; Travis and Shear, 2010; Holzel et al., 2011a). A distinction has been made between static seated meditation (such as the traditional Buddhist Shamata/Vipassana practices) and "movement meditations," such as traditional Chinese Taijiquan (Larkey et al., 2009). While it is true that some forms of meditation emphasize primarily cognitive processes, the emphasis on posture in meditation is so widespread and so basic that this distinction must be questioned. In this paper we include seated meditation in the BTES category unless it places no significant emphasis on posture, breathing or physical sensation.

Although some authors have looked at the body awareness cultivated in some forms of meditation (Kerr et al., 2013), a crucial aspect has been almost completely ignored in the literature: posture. In almost all traditional systems of meditation, correct posture is stressed as an absolutely essential component (Johnson, 1996). In seated meditation, upright balanced posture is intrinsic to the meditative attitude (Johnson, 2000). We suggest that meditative awareness is a specific PS. In mindfulness, one prepares to meet each new experience without grasping, without shrinking away, but with flexible open presence, a balanced posture of mind, body and emotion. We believe meditation can be understood as a PS, a specific state of preparedness characterized by the absence of fixed maladaptive PSs.

# Somatic Approaches

#### **Alexander technique**

The Alexander Technique (AT), developed by F.M. Alexander in the early 20th century (Alexander and McGowan, 1997), is a method for changing habitual patterns of posture and movement, and claims far-reaching effects on physical and psychological health. It points to the prevalence of poor habit patterns, but goes beyond a purely physical focus to define these faulty habits as "poor use of the self "; the self is defined as "the entire psycho-physical organism" (Alexander and Maisel, 1989). These unconscious patterns of behavior involve attention, thought and emotion as well as the body The principal method involves helping the student to become aware of their subtle preparatory physical and mental tensions; learning to pause and to "inhibit" these tensions; and then to complete the desired movement without the interfering tensions (Alexander and Maisel, 1989). This is a clear example of working with the PS; Jones, a student of Alexander's published a book summarizing his early investigations of the AT as producing change through the inhibition of postural sets (Jones, 1976). Jones makes it clear that the "postural set" is not the simple adoption of a physical posture, but an integrated change in attitude involving attentional, cognitive and affective components, largely equivalent to our concept of the PS. The "inhibition" referred to by Jones and Alexander is the process of relinquishing chronic maladaptive sets, very similar to the process we discuss above under Changing PS. Jones documents the increased mechanical efficiency of movement (using stroboscopic photography) as well as the subjective experiences of lightness, height and smoothness (in a questionnaire given to new students) (Jones, 1976). Extensive anecdotal and informal written accounts, as well as one of the authors' clinical experience, suggests that students also experience positive changes in physical and emotional health and improved cognitive function, consistent with our view that the PS links motor, affective and cognitive functioning.

There have been few scientific studies of the AT. It has been shown to be more effective than massage in treating back pain (Little et al., 2008), to increase functional reach (Dennis, 1999), to benefit patients with Parkinson's disease (Stallibrass et al., 2002), asthma (Dennis and Cates, 2000), and performance anxiety (Urbanski, 2012); for general reviews, see (Ernst and Canter, 2004; Jain et al., 2004). Stuart offers an interesting discussion of the AT and neurophenomenology (Stuart, 2013).

# **Feldenkrais Method**

Strongly influenced by the AT, the Feldenkrais Method (FM) uses either complex movements guided by verbal instruction (Awareness through Movement) (Feldenkrais, 1990) or passive manipulation of the body by an instructor (Functional Integration) (Rywerant and Feldenkrais, 2003). It emphasizes proprioceptive awareness, fine motor discrimination, and the use of imagined movement. The stated aim is to offer the motor nervous systems a wider range of alternatives for movement, removing the constraints of limited habit patterns; the assumption is that the nervous system will then automatically choose the most efficient alternatives. Feldenkrais believes these changes will positively affect emotional and cognitive state; his theories are congruent with our hypothesis of the PS. Extensive anecdotal evidence supports this claim although there are only a few published studies. Most studies have positive results (Gutman et al., 1977; James et al., 1998; Lundblad et al., 1999; Kolt and McConville, 2000; Gomes and Vieira, 2013; Ramli et al., 2013; Pugh and Williams, 2014), although they are generally of poor quality.

A study of the use of language in the teaching of physical education versus the FM provides an interesting perspective on the differing world-views of BTES and conventional physical education (Wright, 2000).

## **Rolfing**

Rolfing adopts a point of view similar to that of AT and FM, that physical structure and movement are foundational to well-being and have intrinsic links to autonomic, affective, cognitive and attentional aspects of the person (Rolf, 1977). This is congruent with our hypothesis. Rolfing uses deep massage on the connective tissue to undo the effects of chronic patterns of poor posture and movement (Larson, 1990). In an extensive but non-scientific literature, participants report substantial alterations in proprioceptive and interoceptive experience that affect their emotional and mental state, including transformative emotional releases and spontaneous re-evaluations of past trauma (Fahey, 1989; Karrasch, 2009). We suggest that the altered proprioceptive feedback from the muscles, and the newly available freedom of movement, may alter PSs and allow the subject to have a different "attitude" toward life; an attitude with affective and cognitive repercussions. This hypothesis is similar to the stated theory of Rolfing (Fahey, 1989; Sise, 2005).

There has been little scientific research on Rolfing. Studies are of poor quality and point to the need for more research and for the development of appropriate outcome measures. Studies have shown positive effects on balance (Findley et al., 2004), parasympathetic tone and pelvic angle (Cottingham et al., 1988) and neck pain (James et al., 2009), but no effect was shown on cerebral palsy based on measures of limb range of movement and gait velocity and efficiency (Perry et al., 1981).

# Body Psychotherapy

Body-oriented psychotherapy pre-dates the development of verbal psychotherapies. Freud's mentor Pierre Janet first formulated and practiced body-oriented psychotherapy, using massage, breathing techniques, and guided movement to encourage the release of emotional blockages (Boadella, 1859). Freud initially used these techniques, but later abandoned them to focus on cognitive insight and the working through of the relationship between therapist and patient. Freud's student Reich continued to develop body-oriented psychotherapy (Boadella, 1974), and strongly influenced later methods (Boadella, 1976).

There has been little scientific research on body psychotherapy. There have been studies (more in Europe than in the States) which confirm its effectiveness for severe mental disorders (Ventling, 2002; Price et al., 2007, 2012; Levy Berg et al., 2009; Röhricht, 2014). Surprisingly, there has been little investigation into its mechanisms, although current neuropsychology seems to offer supportive and suggestive evidence. For a good survey of the field see (Heller, 2012). Exposure therapy may share some of the mechanisms of body psychotherapy, although the theory behind it is quite different (McNally, 2007).

# **Reichian Therapy**

Reichian Therapy maintains that dysfunctional emotional/cognitive patterns are embodied in patterns of muscular tension ("character armor") (Boadella, 1974). In addition to insight techniques, Reich used massage, breathing exercises and guided movement to release the tensions. He believed that the tension patterns served to hold back instinctive emotional, physical and sexual impulses, blocking the natural charge/discharge process of the body (Boadella, 1974). The holding patterns identified by Reich are very similar to our concept of maladaptive persistent PSs: the restraint of instinctive responses may lead to a failure of the PS to subside and its persistence as a maladaptive pattern. Note that in our discussion of types of PS above, we suggest that any of the core emotional patterns (described by Panksepp) may lead to maladaptive PSs, including sexual responses and nurture-oriented impulses as well as the more familiar fear and rage responses. Reich's idea of health as a flexible state in which impulses are not chronically suppressed but allowed healthy expression is congruent with our suggestion that stress can be alleviated by the release of persistent and disorganized PSs.

In his later years Reich brought elements into his approach which eventually drew legal action from the government; his books were burned and he ended his life in prison. His successors have avoided these extremes, and have developed the embodied aspects of his approach, discarding the more analytical Freudian legacy.

#### **Formative Psychology**

Stanley Keleman's Formative Psychology (Keleman, 1979) is a sophisticated refinement of Reich's approach. Keleman emphasizes the use of conscious voluntary effort in forming ones attitude toward life and life events. "Forming" is not a metaphor, but literally the adopting of a certain shape; flexing or extending, shrinking or inflating, altering both musculo-skeletal configuration as well as visceral tone. According to Keleman, problems arise when, through early childhood events, we get "stuck" in a certain shape (Keleman, 1971); we adopt a fixed, maladaptive attitude toward life, which may be automatic and unconscious, inaccessible for modification. Keleman draws the attention of his clients to "how they do that," to the proprioceptive, interoceptive and kinesthetic subtle cues through which they can recover awareness of the original action, and make a voluntary choice to un-do it and to form oneself in a more functional way (Keleman, 2013). His approach is thus very similar to our hypothesis of the PS.

#### **Somatic Experiencing**

Peter A. Levine, is a PhD in psychology and psychophysiology, trained as a body psychotherapist and as a Rolfer. He developed Somatic Experiencing, a form of psycho-physical therapy specifically designed to resolve the effects of traumatic stress. He noted that animals in the wild, subject to extremes of stress, may exhibit freeze or collapse behavior similar to that of humans with PTSD (Hoagland, 1928; Nijenhuis et al., 1998). This has been documented as TI (Volchan et al., 2011). In animals this state seemed to generally be time-limited; the animal would go through an apparent physical "discharge" process, involving heavy breathing, shaking or trembling, and subtle locomotor motions; after which they appeared to have thrown off the effects of the stress (Levine and Buczynski, 2013). These naturalistic observations have not yet been documented in the literature but have been recorded on film by wildlife biologists (Lipscomb, 1982). SE addresses PTS by guiding the client to become aware, through interoception and proprioception, of unresolved defensive impulses, and then releasing these impulses through biological completion, described above.

The theories of SE are congruent with the PS framework, and the PS framework provides an explanation for the potential effectiveness of SE. Its methods and theory are discussed in Payne et al. (2015). Peer-reviewed research publications into the efficacy of SE methods are as yet limited to special applications of SE (See Payne et al., 2015–Corrigendum). Its methods and theory are discussed in Payne et al. (2015).

# Suggestions for Further Research

Our hypothesis is that the five aspects of the PS–posture, autonomic state, affective state, attention, and expectation—tend to co-vary, suggesting a central integrated response we term the PS. Further, that the BTES involve changing one or more of these with the aim of changing the others too, bringing about a reorganization of PS, a more adaptive state of the organism, and a reduction of physiological and psychological markers of excess ergotropic activity (the most common usage of the term "stress").

There are readily available means for measuring the five aspects of the PS:

A randomized controlled study could evaluate BTES interventions on one of these variables by using the other variables as outcome measures. We would suggest the use of an attention control group as well as an active control using a standard intervention such as relaxation or Cognitive therapy.

For example, one could monitor autonomic reactivity to a challenge such as picture viewing (Lang et al., 1993), and determine whether the guidance by a teacher of Qigong or the Alexander technique into a "centered" postures would bring about an alteration in reactivity, in comparison to a control activity or to a self-adopted posture. Further, one could determine whether this same postural guidance also brought about a widening of peripheral attention, a more positive set of expectations, and a more positive affective state, as our hypothesis would

suggest. Similar experiments could be done with a BTES intervention on autonomic state (using controlled breathing), affective state (using methods from body psychotherapy), attention, or expectation.

Our hypothesis that the neural substructures involved in the PS are largely sub-cortical is more challenging to verify in humans, as it is technically demanding to monitor subcortical activity in humans since it is situated deep in the brain. Panksepp makes a case for the validity of generalizing from animal data to humans (Panksepp, 2011). fMRI studies of humans undergoing BTES procedures are possible in some cases, although hampered by the limitations the fMRI procedure places on movement. Prepost-procedure fMRIs would yield useful data on subcortical changes following BTES interventions.

As noted in several places above, experiments of this sort have already been done with results suggesting support of our hypotheses.

#### Summary

Here we have proposed that the concept of the PS as an important but underemphasized phase of the organism's response to challenge. The PS is an integrated, largely sub-cortical, organization of the organism in readiness to handle events. We suggest that the PS may persist inappropriately or become disorganized in states of chronic or traumatic stress, and that intervention

# References

through attention to interoceptive and proprioceptive experience is more likely to be an effective therapeutic approach than one focused on verbal meaning. We have laid out the various aspects of the PS—movement, posture, orientation, autonomic state, emotion, expectation—and the neurological substrates of each. We suggest that since the PS is primarily subcortical, it is quicker and more fundamental, and may override or bias cortical executive function. We have presented a brief overview of various forms of BTES, and suggest that they share an approach very similar to the one we present with the PS framework, and that the PS framework therefore offers a way of approaching the neuroscience of the BTES. We hope that our suggestions facilitate further research and integration of these concepts that have application into virtually all aspects of human health and well-being.

# Acknowledgments

We thank the Flight Attendant Medical Research Institute (FAMRI), ZRT Laboratory, The American Academy of Pediatrics and Norris Cotton Cancer Center for support of our research work. Funders had no role in preparation of this manuscript or our decision to publish it. We also thank Drs. Paul Guyre, Steven Fiering, James Bernat, Stephen Porges, and Peter Levine for sharing insights that support our work.

by North Atlantic Books; Distributed to the trade by Publishers Group West.

Iyengar, B. K. S. (1966). Light on Yoga. New York, NY: Schoken Books.

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evidence from victims of traumatic stress. Biol. Psychol. 88, 13–19. doi: 10.1016/j.biopsycho.2011.06.002

**Conflict of Interest Statement:** Peter Payne is an SE practitioner (SEP) who derives income from his practice. Mardi A. Crane-Godreau is an SEP and a nonpaid member of the Board of Directors of the Somatic Experiencing Trauma Institute.

Copyright © 2015 Payne and Crane-Godreau. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

# Potential self-regulatory mechanisms of yoga for psychological health

#### *Tim Gard1,2,3 †, Jessica J. Noggle4 †, Crystal L. Park5 †, David R. Vago6 \*† and Angela Wilson7 †*

#### *Edited by:*

Laura Schmalzl, University of California, San Diego, USA

#### *Reviewed by:*

Bessel A. Van Der Kolk, Trauma Center, USA Jeffery Dusek, Allina Health, USA

#### *\*Correspondence:*

David R. Vago, Functional Neuroimaging Laboratory, Department of Psychiatry, Brigham and Women's Hospital and Harvard Medical School, 824 Boylston Street, Chestnut Hill, Boston, MA 02467, USA

e-mail<EMAIL_ADDRESS>
†Tim Gard, Jessica J. Noggle, Crystal L. Park, David R. Vago and Angela Wilson have contributed equally to this work as part of the Kripalu Research Consortium.

Research suggesting the beneficial effects of yoga on myriad aspects of psychological health has proliferated in recent years, yet there is currently no overarching framework by which to understand yoga's potential beneficial effects. Here we provide a theoretical framework and systems-based network model of yoga that focuses on integration of top-down and bottom-up forms of self-regulation. We begin by contextualizing yoga in historical and contemporary settings, and then detail how specific components of yoga practice may affect cognitive, emotional, behavioral, and autonomic output under stress through an emphasis on interoception and bottom-up input, resulting in physical and psychological health. The model describes yoga practice as a comprehensive skillset of synergistic process tools that facilitate bidirectional feedback and integration between high- and low-level brain networks, and afferent and re-afferent input from interoceptive processes (somatosensory, viscerosensory, chemosensory). From a predictive coding perspective we propose a shift to perceptual inference for stress modulation and optimal self-regulation. We describe how the processes that sub-serve self-regulation become more automatized and efficient over time and practice, requiring less effort to initiate when necessary and terminate more rapidly when no longer needed. To support our proposed model, we present the available evidence for yoga affecting self-regulatory pathways, integrating existing constructs from behavior theory and cognitive neuroscience with emerging yoga and meditation research. This paper is intended to guide future basic and clinical research, specifically targeting areas of development in the treatment of stress-mediated psychological disorders.

**Keywords: yoga, self-regulation, stress, executive control, viscerosomatic, top-down, bottom-up**

#### **INTRODUCTION**

Research suggesting the beneficial effects of yoga interventions on myriad aspects of psychological health has proliferated in recent years: the extant literature suggests that yoga can improve symptoms of depression, anxiety, stress, post-traumatic stress disorder, and other psychological problems (for reviews, see Kuntsevich et al., 2010; Field, 2011; Balasubramaniam et al., 2012; Li and Goldsmith, 2012) as well as promote well-being, including life satisfaction and happiness (Woodyard, 2011). Many different explanations or pathways for these salutary effects have been proposed, but as yet there is no overarching framework in which to understand them. One useful framework for doing so is that of self-regulation.

Theories of self-regulation are assuming an increasingly central role within various sub-disciplines of cognitive science, psychology, and medicine (see Eisenberg, 2000; Watts, 2000; Gross and Thompson, 2007; McCullough and Willoughby, 2009; Hagger, 2010; Hofmann et al., 2012). Generally speaking, *self-regulation*

refers to efforts of monitoring, willpower, and motivation to manage or alter one's incipient responses and impulses so as to pursue or maintain explicit goals or standards (Luszczynska et al., 2004; Baumeister et al., 2007; Zell and Baumeister, 2013). A focus of contemporary psychotherapy is the development of self-regulation tools to reduce psychological distress and improve well-being. For example, many current cognitivebehavioral treatments focus on using top-down cognitive means of self-regulation, such as cognitive reappraisal, reframing, and goal-setting (e.g., Berking et al., 2008). More recent "third-wave" behavioral and cognitive therapies, such as acceptance and commitment therapy (ACT; Hayes and Wilson, 1994), dialectical behavior therapy (DBT; Hayes et al., 1999), and mindfulnessbased cognitive therapy (MBCT; Segal et al., 2002) also target self-regulation, through the development of mindfulness-related skills (Baer, 2005). There have been suggestions in the recent literature that such mindfulness-based approaches may function through both top-down and bottom-up mechanisms of

<sup>1</sup> Department of Psychiatry, Massachusetts General Hospital, Boston, MA, USA

<sup>2</sup> Bender Institute of Neuroimaging, Justus Liebig Universität Giessen, Giessen, Germany

self-regulation (Chambers et al., 2009; Taylor et al., 2010; van den Hurk et al., 2010; Hölzel et al., 2011b; Vago and Silbersweig, 2012; Chiesa et al., 2013; Westbrook et al., 2013). Top-down strategies are thought to occur in more novice meditators, where there is an emphasis on attentional control and thus, top-down executive mechanisms. As the meditation practice deepens, emphasis on interoception increases, evaluation processes decrease across contexts, and bottom-up strategies may be more strongly present. Bottom-up regulation strategies have been described as modulation of emotion-generative brain regions (i.e., limbic) without recruitment of "higher" brain regions (i.e., frontal) that are responsible for cognitive forms of regulation (e.g., reappraisal, suppression; Taylor et al., 2010; van den Hurk et al., 2010; Gard et al., 2012b; Vago and Silbersweig, 2012; Chiesa et al., 2013). More specifically, bottom-up processes involve the influence of peripheral sensory, visceral, cardiovascular, immune, and autonomic input upon central neural processing and mental activities via ascending pathways (Taylor et al., 2010; McRae et al., 2012). Yoga, as we describe the practice here, is a complex, adaptive and widely applicable method of physical and mental training with multiple tools for self-development, and, as we propose, for improving self-regulation through both top-down and bottom-up mechanisms.

In our integrative systems network model, we propose that specific aspects of yoga practice affect self-regulation through tonic feed-forward and feed-back loops across multiple systems, which, in turn, promote psychological and physical health and well-being. *Specifically, we describe how yoga may function through top-down and bottom-up mechanisms for the regulation of cognition, emotions, behaviors, and peripheral physiology, as well as for improving efficiency and integration of the processes that subserve self-regulation.* We begin by contextualizing the system of yoga in historical and contemporary settings. Then we detail how specific components of yoga practice may affect cognitive, emotional, and behavioral systems under stress, potentially resulting in improvements in physical and psychological functioning during practice and in the midst of living everyday life. The hypothesized mechanisms are then integrated in a theoretical model for self-regulation through yoga and finally scientific evidence in support of this model is provided. The intention for this paper is to provide a theoretical framework that can guide future basic and clinical research and specifically guide development in the treatment and prevention of stress-mediated psychological disorders.

#### **YOGA PHILOSOPHY: A FOUNDATION FOR SELF-REGULATION1**

In this section a brief historical and philosophical background of yoga will be provided. Yoga, originating from India, is an ancient contemplative practice dating back over 3,500 years, which aims at one thing – to alleviate suffering and promote optimal physical and mental thriving (Cope, 1999; Feuerstein, 2011). In Western contemporary settings, yoga tends to be synonymous with yoga postures, breathing, and some meditation practices. Historically, however, the practice of yoga was understood to be much broader and more comprehensive, including a wider range of techniques to promote wellbeing and balance among mind–brain–body functions. These included paths oriented to service, devotion, intellectual discernment, and meditation, and each offered practices to mitigate suffering and produce higher levels of consciousness (Feuerstein, 2011).

There are many branches of yoga that have developed historically; however, we focus specifically on *Raja* and *Hatha* yoga because of their prevalence in modern practice and their emphasis on developing self-regulation. *Raja* or classical yoga is a system of meditation, while *Hatha* or postclassical yoga followed *Raja* yoga and elaborated upon postures and breathing techniques largely to prepare for meditation. Accordingly, modern yoga practitioners—who practice for purposes beyond physical fitness—study *Hatha* yoga within the context of *Raja* yoga (Vivekananda, 2001). We also focus on *Raja* yoga because many of its components can be linked to modern physical and mental self-regulation concepts. As will be discussed in more detail in the next section, these components can be linked to self-regulatory processes such as goal-setting (top-down ethics), observation of one's behaviors in relation to these goals (top-down attentional processes and bottom-up sensing during postures, pranayamas, and meditation) and cultivation of the ability to override incipient responses in order to move closer to goals (including ethical motivations; McCullough and Willoughby, 2009; Zell and Baumeister, 2013).

The focus of *Raja* yoga, as outlined by Patanjali (author of the *Yoga Sutras,* a historic text of *Raja* yoga, circa start of the common era), was primarily cognitive. Patanjali described yoga as the stilling of distorted fluctuations or ruminations in the mind, which are the sources of suffering (Vivekananda, 2001; Cope, 2006). The multicomponent process of *Raja* yoga is aimed toward training the mind to be effortlessly quiet, focused, and self-aware. These cognitive goals of *Raja* yoga overlap with some goals of other meditative traditions such as Buddhism (Feuerstein, 2011), from which the modern concept of mindfulness has sprung (Kabat-Zinn, 1994; Bodhi, 2011). Some scholars in the humanities consider Patanjali and Shakyamuni Buddha as contemporaries. According to them, in the process of his self-transformation, the Buddha studied and mastered Upanishadic yoga techniques, and his teachings were influenced by these experiences (Feuerstein, 2008; Gombrich, 2009; Gethin, 2011), but see (Bronkhorst, 2007, 2013). Furthermore, the cross-pollination of yoga and Buddhism is most evident in the overlap of Vajrayana Buddhism and *Hatha* yoga (Feuerstein, 2011). A modern example of this overlap is the mindfulness-based stress reduction (MBSR) program, which includes some Hatha yoga postures (Kabat-Zinn, 1990). Although much of the mindfulness-based practices emphasize the mental form of training, some elements of yoga asana and pranayama remain in MBSR. Interestingly, one study of participants from nine different MBSR courses found yoga practice time to be more strongly correlated with self-reported improvements in mindfulness, perceived stress, anxiety, and psychological

<sup>1</sup>In the following summary of yogic concepts that may relate to self-regulation, we included key yogic terms italicized in Sanskrit for historical reference.

well-being than formal sitting meditation time during the 8 weeks (Carmody and Baer, 2008).

Patanjali's *Raja* yoga offers eight different groups of practices aimed toward self-regulation. In Patanjali's *Yoga Sutras*, these different groups of practices are called the eight limbs (**Table 1**), and include: moral observances (ethics when interacting with others); self-discipline (ethics geared toward the self); physical postures and exercises; breath regulation; sensory withdrawal (minimizing sensory input); concentration (effortful, focused attention); meditation (effortless, unbroken flow of attention), and self-transcendence (Stone, 2009). Collectively, the eight limbs may be conceptualized as methods to regulate emotions, thoughts, or behaviors and to increase

well-being (Cope, 2006). The diversity of limbs allows students to begin yoga by working with practices that are most appealing and accessible, often the physical postures for Western students.

#### **YOGA'S TOOLS FOR SELF-REGULATION: HISTORICAL AND MODERN INTERPRETATIONS**

In this section, we describe the components of *Raja* yoga on which we base our proposed model of self-regulation. To this end we linked classical components of yoga to modern, scientific concepts. We have grouped the eight limbs under the following four categories referred to herein as "process tools" (**Table 1**), because a combination of these four categories encompasses most modern

These components are described by their modern usage, and grouped into four operational categories that are used to conceptualize how yoga may influence self-regulatory processes.

yoga classes (Field, 2011) and most research on yoga emphasizes these particular practices (Li and Goldsmith, 2012): (1) Ethics, based on the two ethical limbs (moral observances (Sanskrit*: yama*) and self-disciplines (Sanskrit*: niyama*)); (2) Postures (Sanskrit: *asana*); (3) Breath regulation (Sanskrit*: pranayama*); and (4) Meditation, including the four meditative limbs (sensory withdrawal (*Sanskrit: pratyahara*), concentration (Sanskrit*: dharana*), meditation (Sanskrit*: dhyana*), and a deep level of concentration or absorption also described as self-transcendence (Sanskrit*: samadhi*)).

#### **ETHICS (YAMA AND NIYAMA)**

On the foundation of the yogic path of self-regulation lie ethical and moral precepts, which are specific examples of the standards or guidelines that contribute to self-control suggested by Zell and Baumeister (2013). These ethical precepts are contained in the first and second limb of Patanjali's eightfold *Raja* yoga path, namely *yama* and *niyama,* respectively. *Yama* refers to ethics regarding the outside world, and therefore is particularly important in social contexts. It comprises non-violence (Sanskrit: *ahimsa*), truthfulness non-stealing*,* moderation of senses*,* and greedlessness*. Niyama* refers to ethics regarding the inner world. It comprises purification or cleanliness and contentment, austerity (Sanskrit: *tapas*), self-reflection and surrender or devotion to something greater than oneself. As such, the ethics suggested in yoga are devoid of religious connection—they are not based on moral value judgments of right and wrong—but are rather seen as actions that help to quiet an overactive mind, regulate emotions, and enhance prosocial and skillful behaviors (Cope, 2006).

#### **POSTURES (ASANA)**

In Patanjali's *Yoga Sutras*, the limb of *asana* is defined as steady and comfortable posture (Cope, 2006). Physically challenging postures are further described to be sustained through the fluctuations of the mind (Faulds, 2005). Postures are one of the most commonly utilized yoga practices in modern interpretations. Historically, postures were used to physically control the body in preparation for controlling the mind in meditation for extended periods of time (Feuerstein, 2011). A common premise behind modern yoga classes is that practicing various postures may help to reduce physical and emotional stress. A typical yoga class will include a series of postures targeting different parts of the body. For example a class might include forward and backward bends, twists, standing poses, and balancing poses (**Table 1**). Modern and historic yoga practice manuals such as *Light on Yoga* (Iyengar, 1995) often suggest a connection between emotional states, physical health, and postures. Although this link has not scientifically been established yet for any particular poses (or set of poses) specifically, there is evidence linking posture, emotion, and mental health (Michalak et al., 2009, 2011, 2014). We attempt to address these hypothesized benefits in the following section.

#### **BREATH REGULATION (PRANAYAMA)**

The Sanskrit word *pranayama* is composed of the word *prana*, which translates to breath as a life-sustaining force, and the word *ayama* which translates to freedom or release.  Traditionally, two benefits of *pranayama* are described to help the practitioner down-regulate arousal and increase awareness of the interaction between the body and the mind (Sovik, 1999). Similar to *asana* as preparation of the body for meditation, *pranayama* is meant to prepare the mind for meditation. *Pranayamas* differ from normal breathing on a number of dimensions, including the duration of the in breath, the out breath, the holding of the breath, and the ratio of these. All *pranayamas* involve diaphragmatic breathing, mostly deep and slow in quality through the nose (Jerath et al., 2006). Popular pranayama techniques include deep, even, three-part inhales and exhales, alternate nostril breathing, forceful expulsion of breath using the diaphragm and abdominal muscles, and slow diaphragmatic breathing with partial closure of the glottis creating an audible sound of rushing air described "like an ocean." For a more extensive overview of *pranayamas* see Singh et al. (2009).

#### **MEDITATION (PRATYAHARA, DHARANA, DHYANA, SAMADHI)**

Postures and breathing practices are traditionally described to support and foster meditation practices (Faulds, 2005). In the yoga tradition, the concentrative meditation techniques described in *Raja* yoga help the practitioner begin to see the conditions that lead to mental and emotional suffering (fluctuations) and the conditions that remedy suffering (i.e., mental stillness). Suffering is further described as a time when the mind is in an afflicted state—either grasping onto an experience, not wanting to let it go, or experiencing aversion, trying to push some object of experience away with force. In both cases, how one relates to one's inner experience will create either more or less suffering. Such suffering can also be described as a mental state that prevents the mind from seeing reality without emotional bias. The ability to see reality clearly without bias, through meditation practices, is a revered tool of self-regulation within yoga (Cope, 2006) and similarly in mindfulness traditions (Vago and Silbersweig, 2012).

The various forms of meditation in the *Raja* yoga tradition are considered key tools in the regulation of the mind (**Table 1**). Specifically, *Raja* yoga includes a set of concentration practices. For example, sensory withdrawal (*Sanskrit*: *pratyahara*) involves techniques to minimize external distractions from sensory information, facilitating a calm mind and allowing attention to turn inward. Many modern yoga classes conclude with supine rest pose (*Sanskrit: savasana*), the body relaxed and eyes closed. *Pratyahara* techniques include guided relaxation (e.g., *yoga nidra*), which serve as an invitation for students to draw their attention to their inner experience.

The next phase of meditation is called *dharana*, coming from the Sanskrit word "dhr" or to hold tight. In *dharana* the practitioner aims to focus the mind on a single object of meditation such as the breath, a point on the body or an external object (e.g., candle flame) and attempts to maintain focus on that object. At this stage of practice, focused attention requires effort as the mind repeatedly wanders. A key goal of *dharana* is to minimize mind wandering (similar to focused attention meditation (see Benson, 2000; Lutz et al.,2008; Hasenkamp et al.,2012), such that when one

realizes the mind has turned away from the object of meditation, the mind is continually brought back to the object.

Occasionally the mind ceases wandering, and meditation shifts into what *Raja* yogis consider more advanced meditative practices, *dhyana*. With time and practice, wandering decreases, as does effort to maintain focus, and an unbroken chain of awareness rests on the object of meditation (Telles et al., 2010; Feuerstein, 2011). As this mastery occurs, there is less effort to keep the mind on the object of concentration and a natural concentrative ease begins to happen. The mind begins to become completely absorbed in the object of attention and a sense of union with the object of attention can begin to occur (Cope, 2006). An analogous process is the psychological flow state experienced by advanced musicians and athletes (Csikszentmihalyi, 1997; Khalsa et al., 2009).

This leads to the final meditative limb, *Samadhi,* which represents transcendent states of conscious awareness and absorption associated with a non-dual subject/object distinction (Josipovic, 2010; Travis and Shear, 2010). *Samadhi* has been described as an experience of no conceptualization, where the object is known directly, beyond name and form. This state of meditation offers a deep sense of interconnection and "sameness" with all phenomena (Cope, 2006). While these experiences of *dhyana* and *samadhi* are said to have profound effects on the mind, these advanced practices are not commonly taught in modern styles of yoga.

Rather than being taught as explicit practices, these meditative limbs are often offered as a process of meditative focus throughout practice. For example, Kripalu yoga, a modern style of *Raja* and *Hatha* yoga, emphasizes witness consciousness, or the observation of experience without reaction (Cope, 2006). Witness consciousness can be likened to the state of mindfulness, often described as "paying attention in a particular way: on purpose, in the present moment, and nonjudgmentally" (Kabat-Zinn, 1994, p. 4). In yoga class, students are guided into a pose, invited to deepen their breath, and then to witness (be mindful of) their experience. The specific limbs that fall under the category of "meditation" are all essential factors that are described to co-arise through the prescribed practices and with the other limbs for progression and mastery. Importantly, witness consciousness can be thought of as a critical mental factor that arises with the other factors serving yoga, but also with the quality of monitoring the development and balance of the other limbs.

The modern use of yoga tends to synergize some of the meditative techniques with postures, breathing, and ethics (**Table 1**). As such, yoga is a unique practice because it offers a variety of complementary tools with which the practitioner can increase self-regulation.

# **A THEORETICAL MODEL OF SELF-REGULATION THROUGH YOGA PRACTICE: HOW CURRENT COGNITIVE NEUROSCIENCE AND PSYCHOLOGICAL THEORY CONTRIBUTES TO REVEALING MECHANISMS OF YOGA**

As discussed above, yoga can be broken down into a skillset of four tools for self-regulation: (1) ethical precepts, (2) sustained postures, (3) breath regulation, and (4) meditation techniques. Here we propose a model (**Figure 1**) that describes how this skillset may facilitate self-regulation and results in psychological and physical well-being. In this model, we propose how yoga skills facilitate bidirectional feedback and improve integration and efficiency of high-level (e.g., central executive network, frontal– parietal control network) and low-level brain networks (e.g., autonomic systems, vagal complex, striatopallidal–thalamocortical network) along with viscerosomatic, musculoskeletal, cardiac, respiratory, and sensory information coming from the periphery (see **Table 2** for description of networks). As depicted in **Figure 1**, maladaptive cognitive, emotional, and behavioral output (e.g., negative appraisal, emotional reactivity, rumination), as well as physiological output initiated by lower-level brain systems (e.g., sympathetic-related vaso- and pulmonary constriction, inflammation, muscle pain/tension) that disrupt homeostatic conditions across bodily systems (including cardiovascular, neuroendocrine, and musculoskeletal) are extinguished and replaced with more adaptive output to the challenging demands of stress in the context of practice and in more generalizable settings. Integration between top-down and bottom-up processes is also proposed to improve accuracy of prediction and error correction mechanisms associated with the stress response across domains, resulting in further improving accuracy in detecting and efficiently responding to perceived threats and reducing consequences of prolonged stress exposure. Finally, the model poses that regular practice is partially motivated and enhanced by a particular set of ethical beliefs promoting benefits toward oneself and others, including direct reward resulting from the practice. Thus, increased activation of a higher level moral cognitive network (see **Table 2**) is hypothesized to be associated with improved ethical skills. It is understood that placebo-related mechanisms may also operate to fuel effective top-down control and motivation; however, such mechanisms remain unclear. Nonetheless, motivation provides realistic goals and positive intentions to fuel approach behavior and provides the scaffolding to support the ethical framework built in to the practice.

#### **TOP-DOWN INFLUENCES ON SELF-REGULATION**

Here, we propose top-down self-regulatory mechanisms of yoga include control of intentional/motivational drive (e.g., goalsetting and maintenance), working memory, attention, executive monitoring, response inhibition, reappraisal, and meta-awareness (see yellow boxes within high-level brain networks in **Figure 1**). Such control signals include generation and maintenance of attention on the object of practice, which includes a continuous focus on an object of visual attention (e.g., point in space), aspect of the breath, or interoceptive feedback from body sensation or mental activity. Furthermore, cognitive reappraisal of feedback from the body is proposed to facilitate inhibitory tone toward maladaptive cognitions, emotions, or behavior.

Yoga is often called "meditation in motion" (e.g., Khalsa et al., 2009) for its highly focused attention during bodily movements. Attention is often directed to a specific part of one's body (e.g., ball of foot, fingertips) or an external point (Sanskrit: *drishti*); similarly, in pranayama, practice involves focusing on the breath as it moves through the body. The focus of one's gaze on one point facilitates the "withdrawing" of the sense of vision away

postures. Application of these skills (limbs of yoga) across cognitive, emotional, behavioral, and autonomic domains in the context of physical and emotional stress is proposed to generalize to similar challenges off the yoga mat and in everyday life. Together, these tools of yoga improve the efficiency, bidirectional feedback, and integration (+ black lines) between high- and low-level brain networks, and afferent and re-afferent input from interoceptive processes (e.g., multi-sensory, proprioceptive, vestibular, cardiovascular, pulmonary, musculoskeletal) in the context of stress. Through an emphasis on interoception and bottom-up input, integration facilitates inhibition (red lines) of maladaptive forms of cognitive, emotional, and behavioral output as well as autonomic output associated with stress. Efficiency improves the communication and flexibility between brain and bodily systems to inform behavioral output. Yoga's four tools are described to involve particular regulatory processes associated with each set of brain networks (indicated in yellow boxes). With mastery of practice, regulatory processes become more

monitoring for proper goal-directed behavior followed by self-correction if needed. A FPCN supports executive monitoring, meta-awareness, reappraisal, and response inhibition mechanisms. A moral cognition network supports motivation and intention setting associated with self-care and prosocial behavior. The dorsal attention network helps to support attentional orienting, and engagement. Hypothlamic–pituitary–adrenal (HPA) axis communication with brainstem vagal efferents support parasympathetic control and homeostasis across systems. A striatopallidal–thalamocortical network is responsible for facilitating extinction learning and reconsolidation of maladaptive habits into behavior that is aligned with intentions and outcomes into adaptive habits. Dotted lines represent new, adaptive pathways for responding to stress. A focus toward bottom-up processes facilitates a shift toward perceptual inference rather than active inference, and improves prediction and error correction processes, thus supporting optimal self-regulation.

from distraction, while the focus of one's attention inward and on body sensation contributes to the "withdrawing" of the other senses from distractions. Distraction is the loss of selective attention and focus on sensory experience outside of a single point or prescribed focal points. Rapid disengagement from distraction and re-engagement on the object of focus is also believed to be a top-down strategy (Koster et al., 2011), although early attentional filtering may involve more bottom-up sensory processing (Kerr et al., 2013). Attentional stability in the context

of stressors induced through yoga practice is thought to reduce negative forms of appraisal and ruminative thought processes by maintaining awareness and attentional engagement with sensation in the body (McCall, 2007). This form of intentional concentration on particular sensations and not others is critical to cognitive flexibility of attention and inhibitory control – the ability to sustain attention on meaningful information and disregard irrelevant information from the external and internal environment. Sensory withdrawal, one of the originally described "limbs" of

#### **Table 2 | High-level and low-level brain networks.**

Patanjali's yoga, is therefore conceptualized here as contributing to cognitive factors of selective attention and response inhibition, further reducing autonomic reactivity and habitual tendencies to respond to external and internal experience in maladaptive ways.

A central executive network has been found to be most consistently active for the described forms of explicit attention and cognitive regulation, including the dorsal parietal cortex along the intraparietal sulcus, extending dorsomedially into the superior parietal lobe, and anteriorly toward the post-central sulcus, and the dorsal frontal cortex (Corbetta and Shulman, 2002). In addition to the central executive network, a fronto-parietal control network (FPCN) is also proposed to help facilitate executive monitoring (of internal and external information) and meta-awareness, guidance of decision making, salience detection, and integration of information from the external and internal environment (Seeley et al., 2007; Vincent et al., 2008). This network includes the frontopolar cortex (FPC), dorsolateral and ventrolateral prefrontal (dlPFC, vlPFC), dorsomedial superior frontal/anterior cingulate cortex (ACC), anterior inferior parietal lobe (aIPL), temporoparietal junction (TPJ), and anterior insular cortex (AIC;Vincent et al., 2008; Spreng et al., 2013). One central aspect of yoga practice thought to facilitate the engagement of this network is meditation and its associated skills for fostering stable attention through active inhibition of specific brain regions responsible for processing internally generated contents of our attention (e.g., default mode network DMN) and facilitation of executive monitoring and present-centered sensory processing.

Meta-awareness or self-awareness (Zell and Baumeister, 2013) may be another mechanism through which yoga improves selfregulation. Increased meta-awareness would allow individuals to clearly compare their current status *vis à vis* their goals and to make any necessary behavioral adjustments. Meta-awareness is often cited along with psychological distancing (Ayduk and Kross, 2010) or decentering (Fresco et al., 2007), a process that allows the individual to uncouple the sensory experience from the"narrative" self

and gain perspective of one's world-view and habits, and increases the likelihood of behavioral change (Critchley et al., 2004; Vago, 2014). Furthermore, the de-centered perspective allows one to experience thoughts and emotions in terms of their subjectivity (rather than an assumed validity) and their transient nature (rather than their assumed permanence; Fresco et al., 2007). Such awareness is thought to override short-term impulses in favor of long-term considerations, effectively improving one's ability to reflect upon the past and use that information accurately to anticipate the future, and to more accurately assess the present (Baumeister et al., 2011). This form of awareness has also been shown to facilitate prediction of error detection and correction, and as a result, more rapidly improve behavioral correction processes when regulating emotional responses to stress (Compton et al., 2008).

With support from the neuroscientific literature (Critchley et al., 2004; Craig, 2009; Taylor et al., 2010), our model suggests that meta-awareness of interoceptive experience facilitates integration across primary sensory, visceral, homeostatic, environmental, hedonic, and social levels via feedforward and feedback between higher-level and lower-level brain networks. For example, there is good evidence that salience-specific nodes of the FPCN (ACC, and insula), interact to develop modulatory influence over viscerosomatic afferent activity arising through the spinal–thalamo-cortical pathway (Craig, 2004). The insula specifically processes interoceptive input in a hierarchical fashion – in a posterior to anterior direction (Craig, 2009), with more basic sensory and homeostatic information in the posterior and more salient, hedonic, and social information in the anterior. Such interaction and integration are proposed to result from the strengthening of the executive monitoring system similarly to mindfulness-based meditative practices (Vago and Silbersweig, 2012; Desbordes et al., 2014). Mindfulness practice encourages practitioners to take a meta-cognitive view of their experience, to notice the experience without judging it or modifying it and is thus, a form of self-regulation. Yoga offers a

way to practice mindful awareness in this way, described above as "witness consciousness."

Self-regulation of emotion refers to the management of the felt experience of emotions, both positive and negative in valence, its behavioral expression, and associated autonomic output, through cognitive reappraisal and through a process of non-appraisal that involves awareness alone, a form of attentional control that does not involve evaluation or judgment (Davidson and Irwin, 1999; Critchley et al., 2003;Vago and Silbersweig, 2012). We theorize that emotional stability and rapid recovery from perturbation arises from either strategy. Similarly to the difference between beginning and experienced mindfulness meditators, non-appraisal is believed to be more advanced and more likely in experienced yoga practitioners than in novices (Taylor et al., 2011). The rapid recovery from emotional perturbation has been referred to as equanimity in the Buddhist and secular mindfulness literature. Equanimity, defined as an even-minded mental state or dispositional tendency toward all experience, regardless of affective valence or source (Desbordes et al., 2014), is proposed to be a skill that is manifested through efficient feed-forward and feedback between somatic, autonomic, viscerosensory, and high-level brain network activity that continually manages stressors that arise on and off the yoga mat.

Positive reappraisal is yet another important cognitive and emotion regulation skill that can be enhanced by yoga. Positive reappraisal has been proposed to mediate the stress-reductive effect of mindfulness through an upward spiral process (Garland et al., 2011). For example, much of yoga practice involves learning to reframe experiences (e.g., from discomfort to sensation), teaching a more objective, observational, and non-judgmental stance to one's experience (Garland et al., 2011). Other reappraisal resources can be acquired through yoga practice. For example, in the course of yoga classes, teachers often instruct students about deeper aspects of yoga philosophy, such as compassion and impermanence, which are useful in appraising or reappraising situations as less stressful (Nyklíˇcek, 2011). Kripalu yoga promotes a technique of "riding the wave" (Faulds, 2005), which involves reappraisal and behavioral change that allows toleration of discomfort – reframing the discomfort of muscle fatigue to a temporary sensation that will pass. Recent theories on self-regulation postulate that explicit reappraisal strategies can reduce the negative impact of prolonged and repeated high stress-related neuroendocrine activity (Koole et al., 2011; Geisler et al., 2013). Reductions in perceived stress lead to conserved cognitive resources and less prolonged (or perseverative) negative emotion (e.g., anger, frustration) along with peripheral effects (e.g., increased vasodilation) that improve outcomes (Jamieson et al., 2012; Keller et al., 2012). The development of equanimity and meta-awareness may also improve self-other interactions and therefore contribute to ethically informed pro-social behavior.

Yoga is also proposed to enhance behavioral forms of selfregulation through goal-directed influence over one's behavior "on and off the yoga mat." This is a topic particularly relevant to health psychology (Mann et al., 2013), such that health-promoting behaviors are more likely once a practitioner has committed to the system and practice of yoga and has an attitude supporting

"readiness" or "willingness to change." For example, readiness to change has been found to be a significant factor driving clinical change in addiction settings (DiClemente et al., 2004). Regulation is proposed to occur via continual adjustment and guidance of one's behavior (e.g., maintain a particular body position even if one's muscles ache and the impulse is to relax) in pursuit of ethically motivated actions associated with self-care, healthpromoting behavior, and pro-social interactions (e.g., increased empathic behavior). Behavioral strategies may also limit exposure to stressful situations. For example, the individual may avoid potentially stressful situations and employ proactive coping strategies to prevent them (Aspinwall and Taylor, 1997) or engage in socially adaptive behaviors (e.g., seek social support; Geisler et al., 2013), both of which are behavioral forms of selfregulation. In addition, yoga practitioners may move toward more healthy lifestyles (e.g., involving less substance abuse, decreasing their risk for substance-related accidents, healthy eating habits; Khalsa et al., 2008; Carei et al., 2010). Thus, behavioral regulation also encompasses a range of inhibitory response behaviors, such as overriding impulses, habits, or cravings, employing approach-focused coping (van Gaal et al., 2011), and facilitating ethical behavior. The effects of yoga on cravings and aversions remain unclear and pose an interesting question for future research.

Yoga can be considered a "wisdom-based" contemplative practice (Cope, 2006), providing an ethical framework that is based on discernment of right and wrong action. Particular ethical precepts of yoga practice are rarely taught formally in Western yoga classes, but they may be conveyed in more indirect ways, such as through modeling, suggestions for goal-setting, or technique instructions that may include attitude and awareness of self and other. In Kripalu yoga, for example, gentleness and respecting one's own boundaries are important aspects of the instructions. These instructions may convey the ethics of non-violence (*ahimsa*) and contentment (*santosha*). Conceptually these two ethics may be related to (self)-compassion, which has been shown to be cultivated through yoga and which mediates the positive effects of yoga on well-being and perceived stress (Gard et al., 2012a). Shapiro et al. (2012) argue that while ethics form the foundation for the cultivation of other mental qualities as described in yoga as well as in Buddhist traditions, the cultivation of states of discernment and meta-awareness even in the absence of explicit training in ethics would affect moral reasoning and decision making in an implicit way. Such changes have been suggested to be mediated by mechanisms of sensory–perceptual clarity, enhanced compassion, values clarifications, and increased emotional awareness and regulation (Eisenberg, 2000). Indeed, improved moral reasoning and decision making along with improvements in witness consciousness, which includes states of discernment like mindfulness, have been reported two months after a MBSR intervention, suggesting that contemplative interventions that incorporate mindfulness and yoga can result in development of these ethical aspects without explicit teaching of them (Shapiro et al., 2012). Similarly, Thiel et al. (2012) propose that emotion regulation, self-reflection, and information integration are three of the four strategies affecting ethical decision making. Interestingly, all of these three constructs are thought to be affected by MBSR and trait mindfulness (Hölzel

et al., 2011b), a trait found to be cultivated through yoga (Gard et al., 2012a).

Numerous neuroimaging studies have investigated the neural underpinnings of moral decision making.  This network has several nodes in common with networks supporting theory of mind and empathy, suggesting that moral cognition and prosocial behavior involve integration of both socio-cognitive and socio-affective networks (Bzdok et al., 2012). Interestingly, MBSR has been shown to improve moral cognition (Shapiro et al., 2012) and empathy (Shapiro et al., 2011) and modulate structures associated with perspective taking (Lazar et al., 2005; Hölzel et al., 2011a,b). Likewise, we propose yoga practice engages this network to influence and regulate behavior and prosocial skills.

#### **BOTTOM-UP INFLUENCES ON SELF-REGULATION**

We emphasize that as opposed to classical psychotherapeutic approaches for self-regulation that rely only on cognitive strategies, mind–body approaches including yoga involve both top-down and bottom-up mechanisms (see Taylor et al., 2010; Chiesa et al., 2013). Successful self-regulation through bottomup mechanisms is proposed to facilitate improved function in a network of low-level brain structures (associated regulatory processes indicated by yellow boxes in **Figure 1**) responsible for peripheral physiological activity and reorganization, including stimulation of somatic, visceral, and sensory receptors, extinction processes, and integration with homeostatic physiology. Specifically, we propose yoga practice involves coupling between the body and environment that facilitates embodied viscerosomatic integration and action (see bottom of **Figure 1**). Building upon past theories of somatic processing which emphasize the representation of emotional states in subcortical maps as it interacts with the environment (Damasio, 2010), here we similarly emphasize embodied, situated forms of processing. Viscerosomatic information from the body, including primary sensory and homeostatic information, is proposed here to be continually and reciprocally integrated with motor output and ongoing cognition during sustained body postures, diaphragmatic breath control, attentional control, and dynamic patterns of representative neural activity. The shift in attentional orientation toward the body and significant ongoing reciprocal communication between sensory-motor afferent and re-afferent input supports a model for integration and embodied cognition and behavior (Wilson, 2002; Taylor et al., 2010; Schmalzl et al., 2014).

Embodiment implicitly refers to action coupled with and not separate from the bodily experience. Merleau-Ponty (1996) refers to this experience as, "I am not in front of my body, I am in my body, or rather I am my body." Yoga may offer additional tools of embodiment (e.g., explicitly inducing gross levels of physical sensations) for some populations that sitting meditation alone cannot provide. For example, a few studies have suggested how mindful yoga may be more suited for those with chronic illness or for patients with psychopathology and a history of trauma (van der Kolk et al., 2014). Yoga may support changes in chronic illness schema by challenging beliefs about the limits of one's physical body. As students practice poses and bring awareness to sensation in the body in ways they initially may have felt they could not, they may come to see that while some aspects of their bodies are limited, other parts of the body are still healthy (Hamilton et al., 2006). van der Kolk (2006) described how movement and touch-based practices that focus on the body [embodiment] have demonstrated some level of effective self-regulation, including Feldenkrais, Rolfing, the F. M. Alexander technique, somatic experiencing, among others. van der Kolk (2006) further suggests it is the trauma patients who specifically have learned helplessness and immobility associated with their emotional trauma. Frewen and Lanius (2006) describe how individuals with PTSD are often unable to up regulate their level of arousal during periods of anhedonia or "emotional numbness," which further prevents effective regulation in the context of affective arousal or distress. Thus, body movement during yoga practice and activation of motor and inhibitory control circuits like the striatopallidal–thalamocortical loops in the context of physical arousal may be a more effective way of triggering exposure, extinction, and adaptive reconsolidation of emotions. With embodiment, we propose sensory and perceptual faculties are sharpened – a sense of clarity or greater phenomenal intensity in which sensation is experienced emerges.

Early attentional filtering, a form of primary sensory processing of the environment, may also be affected by yoga practice. For example, a dorsal attention network of brain structures [i.e., frontal eye fields (FEF), ventral premotor cortex (vPMC), superior parietal lobe (sPL), intraparietal sulcus (IPS)] selects information from the sensory world (with direction from top-down influences) and is most associated with covert and overt shifts of spatial attention, eye movements, and hand–eye coordination directed from brainstem nuclei and pre-motor areas (Corbetta and Shulman, 2002; Vincent et al., 2008). Low-level brain networks for this process are typically described to function under conscious awareness, contributing to affective biases of perception (Todd et al., 2012), but also to neuro-visceral integration as described by Thayer and Lane (2000). For example, the "experiential enactive self" network (e.g., supplementary motor area (SMA), ventromedial posterior nucleus of the thalamus (VMpo), pulvinar, posterior insula, and superior colliculus (SC; Vago and Silbersweig, 2012) has been described to contribute to perceptual biases, and to be modulated by mindfulness practice. The posterior insula, a primary node in this network, has been implicated in processing the most basic primary interoceptive information along with homeostatic sensory-motor information (Craig, 2009). It remains unclear how these networks specifically interact as a result of yoga training, but we hypothesize that they are reconditioned to facilitate engagement with body sensations, reduce bias and be more functionally integrated with viscerosomatic input, executive control, and adaptive motor output.

In the context of yoga-induced physical stress and associated emotional reactivity, there is a coordinated set of homeostatic responses involving the interaction among the nervous, endocrine, and immune systems (McEwen, 1998). Overactive or

inefficiently managed homeostatic responses can lead to cumulative wear and tear on the body and brain (Sterling and Eyer, 1988; McEwen, 2004). Pathophysiological processes with unfavorable psychopathological outcomes may occur given the following prolonged conditions: (1) if the release of neuroendocrine mediators are not effectively terminated (in the presence or absence of a stress-related physiological challenge), (2) if there is failure to habituate to repeated stress-related challenges, or (3) if there is a failure to mount an adequate response to the stressor (McEwen, 2004). Within this framework, we propose that yoga affects self-regulation through parasympathetic control, in part by physiologically reducing prolonged emotional reactivity and associated autonomic responses, both in terms of acute forms (e.g., during/immediately following a yoga practice) and by shifting a physiological set point for baseline reactivity over repeated, long-term yoga practice. In other words, it may take more physical stress or more intense emotional reactivity to induce a typical "stress response" in addition to promoting parasympathetic tone more rapidly in response to stress. The current model predicts physiological mediators such as the catecholamines (e.g., epinephrine, norepinephrine) from the adrenal medulla, glucocorticoids (e.g., cortisol) from the adrenal cortex, pituitary hormones (e.g., ACTH, prolactin, growth hormones), and inflammatory cytokines (e.g., IL-1, IL-6, TNF-α) from cells of the immune system are modulated directly in various bodily tissues and organs to facilitate rapid homeostasis across all bodily systems effectively managing the bodily responses to the stress of challenging postures and distraction. Furthermore, there is some evidence that meditative components of yoga can increase levels of brain-derived neurotrophic factors (BDNF; Balasubramaniam et al., 2012), a growth factor thought to help support the survival of existing neurons and counteract degenerative effects of inflammation by encouraging the growth and differentiation of new neurons (Huang and Reichardt, 2001). Properly managed stress through the challenges of focusing attention with stillness, balance, and breath control across repeated yoga practice has the potential to promote neurogenesis, dendritic arborization, and increased synaptic connectivity, and can be reinforcing by enhancing neural activity in the "pleasure pathways" of the nervous system (i.e., basal forebrain; Chrousos and Gold, 1992b; Logan and Barksdale, 2008). This change in homeostatic responsivity is a form of skillful optimization of autonomic control to keep arousal at lower levels, helping the practitioner stay relaxed with less effort, and facilitate recovery of bodily systems under stress. Such "calming" effects by contemplative practices have been previously described as the "relaxation response" (Benson, 2000; Dusek and Benson, 2009) and refer to what is described in the extant yoga literature as "steadying the mind." Similarly, it has been suggested that yoga promotes continual neurovisceral feedback and a mechanism of increased inhibition of sympathetic responses post-arousal via branches of the 10th cranial nerve, the vagus nerve, and specific parasympathetic nuclei in the medulla (Streeter et al., 2012). In contrast the to the "relaxation response," the "stress response" refers to both the sympathetic output and cognitive, emotional, and behavioral output that are associated with detection of threat (Benson, 2000).

Parasympathetic responsivity, a form of autonomic nervous system regulation, is described to manifest in cardiac variability or vagal tone (Porges, 1995; Thayer and Lane, 2000). Cardiac vagal tone, measured by respiratory sinus arrhythmia (RSA) and heart rate variability (HRV), indexes the efficiency of central–peripheral feedback mechanisms (Thayer and Lane, 2000). Specifically, RSA is a cardiorespiratory phenomenon that indexes the influence of respiratory frequency and depth of ventilation (i.e., tidal volume) on vagal control of heart rate (HR); whereas, HRV refers to the peak-to-peak variability between successive beats (Grossman and Taylor, 2007). Yoga practice may facilitate high vagal tone (Streeter et al., 2012), which is associated with greater behavioral flexibility in a changing environment and can manifest in decreases in low-frequency HRV, increases in high-frequency HRV, and increased RSA. Vagal tone refers to the activity of the vagus nerve, and its ability to convey afferent (sensory) information about the state of the body's organs to the central nervous system. Porges' (1995) polyvagal theory specifies two functionally distinct branches of the vagus nerve that control the parasympathetic response in opposition to the sympathetic-adrenal system that mobilizes energy in times of stress. One branch, the ventral vagal complex (VVC), originates from the medullary nucleus ambiguous (NA) and provides efferents to supradiaphragmatic target organs (e.g., soft palate, pharynx, larynx, esophagus, bronchi, and heart). The NA also receives input from the trigeminal and facial nerves (Porges, 1995), suggesting influence of facial muscles in controlling cardiovascular, pulmonary, and parasympathetic output. The other branch originates from the medullary dorsal motor nucleus (DMX) and innervates subdiaphragmatic organs (e.g., stomach, intestines; Porges, 1995). Parasympathetic outflow is mediated largely by descending outputs from these nuclei and are under the direct influence of limbic regions associated with emotion-generation and conditioning of behavioral responses to emotional stimuli (Ulrich-Lai and Herman, 2009). One way that breath regulation may modulate parasympathetic output is through VVC efferents that regulate autonomic output, or indirectly through limbic inhibitory projections (Ulrich-Lai and Herman, 2009).

In yoga practice, breath regulation is a key tool for impacting physical and mental states, and vice versa (Faulds, 2005; Telles and Singh, 2013). In this context, diaphragmatic breath control is consciously mediated, but non-consciously influencing parasympathetic activation. The most common form of breath regulation during yoga practice is described as slow, deep, diaphragmatic, and paced along with each movement of the postures (Faulds, 2005); there are however, many other very specific practices that are described. A number of authors have proposed mechanisms for the self-regulatory properties of *pranayama* that support our model. In the late 1970s, *pranayama* was proposed to result in "a steadying of the mind" through the Hering–Berueter reflex (Pratap et al., 1978). Pauses after deep inhalation would result in excitation of baroreceptors (stretch receptors) in the lungs, providing feedback to vagal nuclei and facilitating increased vagal tone (Porges, 1995; described as a low-level brain mechanism in **Figure 1**). Action potentials would then travel along the vagus nerve to the lower pons, signaling inspiration. Increased stimulation of