# AGING AND MENTAL HEALTH

EDITED BY: Lia Fernandes and Constança Paúl PUBLISHED IN: Frontiers in Aging Neuroscience

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ISSN 1664-8714 ISBN 978-2-88945-188-3 DOI 10.3389/978-2-88945-188-3

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## **AGING AND MENTAL HEALTH**

Topic Editors:

**Lia Fernandes,** Faculty of Medicine, University of Porto. Center for Health Technology and Services Research (CINTESIS), Portugal

**Constança Paúl,** Institute of Biomedical Sciences Abel Salazar, University of Porto, CINTESIS, Portugal

Cover image: "An Old Woman Reading" by Gerard Dou Available at: http://hdl.handle.net/10934/RM0001.COLLECT.8320 under CC0 1.0 licence

People are progressively ageing all over the world, and it is estimated that the number of persons aged 60 or over will more than triple by 2100. This emerging population will experience an inevitable rise in dementia, mental health problems and chronic diseases.

According to GBD (2010), neuropsychiatric disorders among older adults account for 6.6% of the total disability (DALYs) for this age group, with 15% suffering from a mental disorder.

Multiple social, psychological and biological factors are determinant of mental health, as well as life stressors. Among these, the lack of independence, limited mobility, chronic diseases, pain, frailty or other mental and physical problems require long-term care.

Beyond this, the elderly are more prone to experience events such as bereavement, a drop in socio-economic status, disability, which leads to isolation, loss of independence, loneliness and psychological distress.

Mental health problems and needs assessment by health-care professionals and older people themselves are under-recognised, and the stigma surrounding mental illness makes people reluctant to seek help.

The early investigation and diagnosis of these situations are crucial, as well as prior management with an important combination of pharmacological and psychosocial interventions, in conjunction with caregivers' and families' support.

The present book aims to contribute to the development of knowledge in Aging and Mental Health, taking different approaches from authors, coming from diverse scientific fields, with the final goal being the improvement of quality of life and healthy aging for this growing population.

**Citation:** Fernandes, L., Paúl, C., eds. (2017). Aging and Mental Health. Lausanne: Frontiers Media. doi: 10.3389/978-2-88945-188-3

# Table of Contents

Carolin Gall, Doreen Brösel and Gabriele H. Franke

## Editorial: Aging and Mental Health

#### Lia Fernandes 1 \* and Constança Paúl 2

1 Faculty of Medicine, University of Porto, Center for Health Technology and Services Research (CINTESIS), Porto, Portugal, 2 Research and Education Unit on Ageing (UNIFAI), Institute of Biomedical Sciences Abel Salazar, University of Porto, Porto, Portugal

Keywords: aging, mental health, dementia, depression, delirium, chronic diseases, frailty, disability

#### **Editorial on the Research Topic**

#### **Aging and Mental Health**

According to the "Mental Health Action Plan 2013–2020" (WHO, 2013), mental health is an integral part of health and well-being and includes not only individual characteristics but also social, cultural, economic political, and environmental factors. The report recognizes that depending on the context certain groups, such as older people, are at higher risk of having mental health problems and consequently having higher rates of disability and mortality.

The main issues concerning aging and mental health are prevention, early diagnosis, recognition of major diseases, treatment and quality of life interventions, at both individual and community level.

Available knowledge about the aging process and mental health is still insufficient and the challenges of aging populations claim more research efforts into clinical conditions, older people's needs, and pathways of care. With the increase in average life expectancy, chronic conditions inherent to aging, such as dementias (in particular Alzheimer's Disease), are inevitably growing along with related behavioral and psychological disorders, which highlights the need for specific interventions in elderly mental health problems. Beside dementia and mild cognitive impairment, other issues like frailty, delirium and the risk for mental health problems or the unmet needs of older people, require substantially more attention from professionals and policy agents. The burden of mental health problems is frequently considered as an inevitable part of the process of aging, worsening the already negative stereotype about being old. Mental health issues, particularly those affecting old age are frequently underestimated, adding to the suffering of a large number of people who could be treated and benefit from diverse social and health care interventions to enhance their well-being. The comprehension of mechanisms underlying diseases, on a time diagnosis, and customized interventions will be much more cost-effective than just allowing the disease to progress, leading to the institutionalization of individuals, which has proved to be an adverse and expensive outcome, both for individuals and the community.

Taking this into consideration, the present Research Topic on "Aging and Mental Health" by Frontiers in Aging Neuroscience makes a contribution with updates and different perspectives on this important theme, developed over 17 papers. These updates focus on cognitive functions, neural and cellular mechanisms, delirium and mild cognitive impairment as well as the effects of exercise and health care settings.

The authors Lim and Yu have conducted an interesting review on the relation between aging and wisdom: age-related changes in economic and social decision making. They discuss this topic based on a model proposing five subcomponents of wisdom: (1) prosocial behavior in experimental economic games and competitive situations; (2) resolving social conflicts; (3) emotional homeostasis; (4) self-reflection; (5) dealing effectively with uncertainty in the domains

#### Edited by:

Ying Xu, University at Buffalo, USA

#### Reviewed by:

Carlos Tomaz, University CEUMA, Brazil Eleni Konsolaki, American College of Greece, Greece

#### \*Correspondence: Lia Fernandes<EMAIL_ADDRESS>
Received: 26 August 2016 Accepted: 27 January 2017 Published: 10 February 2017

#### Citation:

Fernandes L and Paúl C (2017) Editorial: Aging and Mental Health. Front. Aging Neurosci. 9:25. doi: 10.3389/fnagi.2017.00025 of risk, ambiguity and intertemporal choice. They highlight that older adults outperform young adults in certain subcomponents of wisdom, but the exact relationship between old age and each subcomponent remains unclear.

Alves et al. addresses an interesting topic, based on the diversion paradigm developed by Delaney et al. (2010). The authors aim to determine whether thinking about an autobiographical memory interferes with the recall of recently encoded information, and to explore the degree of forgetfulness depending on the temporal distance from the diversionary thought. They conclude that the expected amnesic effect of diversionary thought was reached, but the temporal distance (old event vs. recent event) did not influence the recall of previously encoded information.

Szatloczki et al. point out the role of linguistic screening for early detection of Alzheimer's disease. The authors have produced a comprehensive review, concluding that AD can be more sensitively detected with the help of linguistic analysis than with other cognitive examinations, which would have relevant clinical implications.

The paper by Meng et al. examines the impact of aging on the brain's susceptibility to affective pictures of varying emotional intensities, with results that suggest that older adults are more resistant to the impact of negative stimuli, while they are equipped with enhanced attentional bias for positive stimuli.

Two studies about delirium are presented in this Research Topic. The first one by Androsova et al. is an interesting, clinically relevant literature review focused on the "Biomarkers of postoperative delirium and cognitive dysfunction". Bearing in mind that the pathogenesis of these postoperative cognitive impairments is multifactorial, the authors emphasize that the application of integrated systems biology has the potential to reconstruct the underlying network of molecular mechanisms and help in the identification of prognostic and diagnostic biomarkers. The second one, produced by Shi et al., finds a good reliability of MDAS and the cutoff point for diagnosis of delirium.

Coelho et al. have written an article about "Determinants of frailty: the added value of assessing medication". With this they analyse in general the determinants that predict frailty, as well as each frailty domain (physical, psychological, and social), considering the integral conceptual model of frailty. Particularly, the contribution of different daily-consumed medication is analyzed. The results add important information about which factors may precipitate states of high vulnerability in community dwelling elderly.

The article "Mismatch negativity (MMN) latency as a biomarker of amnestic mild cognitive impairment in Chinese rural elders" by Ji et al., aims to assess the mismatch negativity (MMN) component, a correlate of the automatic detection of changes in the acoustic environment, in healthy adults, and adults with amnestic mild cognitive impairment (aMCI). They find that while no difference was observed in amplitude between the two groups, there was a significant increase in the latency of the MMN in the aMCI group, which could be a sensitive, specific biomarker.

Akintola et al. have written a broad systematic review and meta-analysis concerning "Subclinical hypothyroidism (SCH) and cognitive function in people over 60 years". This meta-analysis, performed to assess available evidence on the association of SCH with cognition in community dwelling, relatively healthy older adults, found no evidence concerning this association.

Bearing in mind the well-known importance of regular exercise in benefiting mental and physical health in the elderly Santa Mina et al. have written the article "The acute effects of exercise on cortical excitation and psychosocial outcomes in men treated for prostate cancer: a randomized controlled trial". They have evaluated and presented novel findings of the effect of a single bout of exercise (low-moderate intensity) on psychological well-being and cortical silent period in prostate cancer survivors.

Paúl et al. have conducted a cross-sectional study about "Perceived risk of mental health problems in primary care" using the Portuguese version of RISC as a useful tool for early identification of mental health concerns in older patients. This study emphasizes the importance of healthcare professionals identifying patients at high risk of adverse outcomes early on in order to direct an appropriate intervention.

Bearing in mind that unmet needs are becoming acknowledged as better predictors of the worst prognostic outcomes than common measures of functional or cognitive decline, the article "Needs in nursing homes and their relation with cognitive and functional decline, behavioral and psychological symptoms" by Ferreira et al. will be a valuable aid to all those interested in learning about this issue. The authors have found more unmet needs associated with the worst outcomes, demonstrating that the needs of those institutionalized elderly remain under-diagnosed and untreated.

In the same setting of the nursing home, Caravau and Martin have written the paper "Direct costs of dementia in nursing homes". The authors deal with an interesting and poorly-studied topic, concluding that direct costs of dementia patients in Portugal exceed the costs of similar non-demented patients by a significant degree, which is in agreement with previous European studies, with direct implications for the provision of services for the management of the increasing prevalence of dementia.

The manuscript by Bastos et al. analyses "The importance of neighborhood ecological assets in community-dwelling old people's aging outcomes: A study in Northern Portugal," concludes that cognitive performance decreases in persons with the worst outdoor mobility, and also that depressive symptoms are less common with a greater number of recreation opportunities, suggesting that aging policies and practices must be ecologically embedded.

Finally, two commentaries have been written, the first of which also has a response. Craig has written a commentary on "Mental distress in patients with cerebral visual injury assessed with the German Brief Symptom Inventory" by Gall et al.. The second commentary written by Heine is about the article "Mental health and dual sensory loss (DSL) in older adults: a systematic review", by Heine and Browning (2014). This text focuses on the lack of solid data on the present subject, and also the need to diagnose and manage DSL early and effectively.

We hope that this Frontiers Research Topic will be an enrichment for Ageing and Mental Health issues, with the efforts and commitments of all authors to whom we give our acknowledgement, as well as to the reviewers who have contributed by improving and clarifying these diverse contributions.

Finally, a special thanks for the support for publishing by the sponsor Pfizer, for three articles (Paúl et al.; Caravau and Martin; Bastos et al.). The sponsor did not play any role in the design,

#### REFERENCES

methods, data collection and analyses, or in the preparation of these articles.

#### AUTHOR CONTRIBUTIONS

LF and CP have written this editorial for the Research Topic they have edited.

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2017 Fernandes and Paúl. 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.

## Aging and wisdom: age-related changes in economic and social decision making

#### Kenneth Teck Kiat Lim1 and Rongjun Yu1,2,3 \*

1 Department of Psychology, National University of Singapore, Singapore, Singapore, 2 Neurobiology/Aging Programme, Life Sciences Institute, National University of Singapore, Singapore, Singapore, 3 Center for Life Sciences, Singapore Institute for Neurotechnology (SINAPSE), National University of Singapore, Singapore, Singapore

World life expectancy is increasing and many populations will begin to age rapidly. The impeding prevalence of a greater number of older people living longer lives will have significant social and economic implications. It is important to understand how older people make economic and social decisions. Aging can be associated with a "phenomenon of decline" and also greater wisdom. This paper seeks to examine the relationship between wisdom and aging. It reviews and connects the behavioral sciences and neuroscience literature on age differences in the following social and economic decision making domains that represent subcomponents of wisdom: (1) prosocial behavior in experimental economic games and competitive situations; (2) resolving social conflicts; (3) emotional homeostasis; (4) self-reflection; (5) dealing effectively with uncertainty in the domains of risk, ambiguity and intertemporal choice. Overall, we find a lack of research into how older people make economic and social decisions. There is, however, some evidence that older adults outperform young adults on certain subcomponents of wisdom, but the exact relationship between old age and each subcomponent remains unclear. A better understanding of these relationships holds the potential to alleviate a wide range of mental health problems, and has broad implications for social policies aimed at the elderly.

Keywords: aging, wisdom, decision making, social conflicts, emotion

#### Introduction

''With age comes wisdom, but sometimes age comes alone.'' —Oscar Wilde

World life expectancy has been steadily rising in the past two centuries and is expected to continue increasing for the foreseeable future (Oeppen and Vaupel, 2002). Increased longevity is especially pronounced in developed countries compared to developing ones (Mathers et al., 2001). Based on a steady increase of almost 3 months of life per year, it may not be uncommon for those born since 2000 in certain developed countries, such as USA, the UK, Japan and other western European countries, to live for 100 years (Christensen et al., 2009; Vaupel, 2010). This is astonishing given that the average life expectancy in developed countries was under 45 years in 1900 (Juvin, 2010). The population is also expected to continue to age rapidly over the next few decades (Lutz et al., 2008). There are serious economic and social implications of our increasing longevity and rapidly aging population (Schneider and Guralnik, 1990; Lloyd-Sherlock, 2000; Tinker, 2002; Poterba, 2004; Bloom et al., 2010b; see Bloom et al., 2010a).

#### Edited by:

Lia Fernandes, University of Porto, Portugal

#### Reviewed by:

Rui Mata, Max Planck Institute for Human Development, Germany Yansong Li, Cognitive Neuroscience Center, CNRS, France

#### \*Correspondence:

Rongjun Yu, Department of Psychology, National University of Singapore, 9 Arts Link, Singapore 117570, Singapore<EMAIL_ADDRESS>
> Received: 10 April 2015 Accepted: 03 June 2015 Published: 18 June 2015

#### Citation:

Lim KTK and Yu R (2015) Aging and wisdom: age-related changes in economic and social decision making. Front. Aging Neurosci. 7:120. doi: 10.3389/fnagi.2015.00120 Lim and Yu Aging and wisdom

The extra years of lives will need to be financed and there will be less people in the labor force than outside of it based on current retirement age laws (Sierra et al., 2009). The roles of social norms surrounding education, employment and retirement will need to be rethought so that the elderly can continue to contribute without impinging on the prospects of the younger citizens (Vaupel and Gowan, 1986; Vaupel and Loichinger, 2006).

Traditionally, research on aging has focused on the cognitive aspects of age-related changes. Old age is associated with declines in many aspects of cognition (reviewed in Hedden and Gabrieli, 2004; Raz and Rodrigue, 2006; Park and Reuter-Lorenz, 2009), as well as with a variety of detrimental stereotypes of incompetence (see Cuddy et al., 2005; Kite et al., 2005; North and Fiske, 2012). Recent major theories on aging, however, emphasize that emotion and motivation play a fundamental role in shaping age related changes in decision making and well-being. The Socioemotional Selectivity Theory (Carstensen et al., 1999) proposes that time horizons influence goals and people engage in a lifelong selection process of strategically and adaptively cultivating their social networks to maximize social and emotional gains and minimize social and emotional risks. When time is perceived as open-ended, goals are most likely to be preparatory and to be used to optimize the future, e.g., gathering information, experiencing novelty and expanding breadth of knowledge. As a result, young adults may place the greatest emphasis on the potential for information gain and future contact. When constraints on time are perceived, goals focus more on objectives that can be realized in their pursuit to maximize meaningful activities in the present. As a consequence, goals emphasize feeling states, particularly regulating emotional states to optimize well-being. Thus, elderly people tend to place the greatest emphasis on the potential for affective gain. Strength and Vulnerability Integration Theory (Charles, 2010) incorporates the socioemotional selectivity theory and further states that aging is associated with strengths in emotion regulation that entail the use of attentional, appraisal, and behavioral strategies of emotion, as well as vulnerabilities in emotion regulation as a consequence of reduced physiological flexibility, especially in situations that elicit high levels of sustained emotional arousal. The Motivational Theory of Life-Span Development (Heckhausen et al., 2010) proposes that individuals in late adulthood shift from primary control processes that are directed at changing the world by bringing the environment in line with one's wishes to secondary control processes aimed at changing the self to bring oneself in line with environmental forces. To meet the major challenges faced in old age, individuals need to increasingly resort to secondary control strategies of adjusting expectations, values, and attributions in order to pursue more attainable goals when certain primary control goals become unattainable. These theories suggest that aging is associated with dramatic changes in personal goals and highlight the strategies and skills used to achieve these new goals.

While aging is generally viewed as a ''phenomenon of decline'', there is an aspect to it that ''holds more promise than present reality may reveal'': wisdom (Baltes and Staudinger, 1993). The concept of wisdom has its roots in religion and philosophy (see Ardelt, 2004; Baltes and Smith, 2008). Wisdom is a complex, multi-faceted construct and there is no consensus on its definition, instead there are a variety, of mostly overlapping, theories of wisdom (Baltes and Staudinger, 2000). This has been largely encapsulated and distilled into six subcomponents by Meeks and Jeste (2009): (1) prosocial attitudes/behaviors; (2) social decision making/pragmatic knowledge of life; (3) emotional homeostasis; (4) reflection/self-understanding; (5) value relativism/tolerance; and (6) acknowledgment of and dealing effectively with uncertainty.

Despite empirical research into the construct of wisdom spanning more than three decades, the topic of wisdom continues to be overlooked by the neuroscience and psychology communities (Jeste and Harris, 2010) and only has gained attention in recent years in the field of aging-related research. This paper will review and connect the behavioral sciences and neuroscience literature on wisdom and aging, and will be organized around the theoretical framework of Meeks and Jeste (2009). For this review, we integrate the two subcomponents of (2) social decision making/pragmatic knowledge of life, i.e., knowing how to successfully navigate challenging social situations, and (5) value relativism, i.e., tolerance of another person's or culture's value systems, into one: ''resolving social conflicts''. Our rationale is that both of these subcomponents of wisdom are essential to making sound social decisions. We begin with a review of the literature on age differences in prosocial behaviors, specifically on experimental economic games.

#### Prosocial Behaviors

Wisdom entails the ability to achieve a common social good. Prosocial behavior broadly refers to acting beyond one's self-interest to benefit other people in one's social group and/or society (Penner et al., 2005). In economics, there are three major types of prosocial behavior: reciprocity, inequity aversion and altruism (see Fehr and Fischbacher, 2002). They are usually measured by the amount of a finite amount of money that is split with another person in experimental economic games. Reciprocity refers to responding in a similar manner to the actions of another person. This depends on the perception of (un)fairness of the actions of the other person, which is determined by whether split amounts are deemed equitable. Inequity aversion refers to wanting to achieve an equitable split of outcomes. This includes wanting to increase or decrease the amount allocated to another person who falls short or exceeds the equitable threshold respectively. Altruism refers to always, i.e., unconditionally, responding positively to another person's action. This means never wanting to decrease another person's allocated amount.

Standard economic theory assumes that ''all people are exclusively motivated by their material self-interest'' and thus, do not care about the well-being of others (Fehr and Schmidt, 1999). That is, players will maximize their selfinterest at the expense of others—even in experimental games. Lim and Yu Aging and wisdom

However, an overwhelming number of studies have consistently rejected this standard economic ''self-interest hypothesis'' and have provided evidence showing that individuals also have prosocial motivation (for reviews, see: Fehr and Schmidt, 2001; Meier, 2006; Levitt and List, 2007; Henrich et al., 2010). There are at least five common economic games to measure prosocial behavior: ultimatum, dictator, trust, prisoner's dilemma and public goods. These experimental games are traditionally played under complete anonymity (to the other player and the experimenter). Depending on the type of prosocial behavior of interest, these games may be played either one-shot, i.e., once, or repeated. These games differ in whether they are played simultaneously, i.e., players make their moves at the same time, or sequentially, i.e., players move one at a time and the move of a preceding player is known. In the next section, we will review older people's prosocial behavior on these games. Although there are numerous studies examining prosocial behavior on these games, only a handful have examined its relationship with old age. We will begin with a review of ultimatum game (UG)s (see **Figure 1A**).

#### Ultimatum Game

The classic UG is a two-player, sequential game that involves splitting a sum of money between a Proposer and a Responder (Güth et al., 1982). The Proposer is endowed with a fixed amount of money, say, \$10, and has to propose some amount, x, to another person, whose identity is not known. The Responder has two choices: accept or reject the proposed offer. If the offer is accepted, the Responder gets x, while the Proposer gets \$10-x; if the offer is rejected, both players receive nothing (See Thaler, 1988, for a readable description of the common UG variations). The standard economic ''self-interest hypothesis'' predicts that the Proposer will offer the minimum amount possible (e.g., one cent), which would be accepted by the Responder who values this over nothing. However, this is very rarely the case (see Güth and Tietz, 1990; Güth, 1995; Cooper and Dutcher, 2011; Güth and Kocher, 2014). A meta-analysis of 37 papers found that, on average, Proposers offered 40% of their ''pie'', i.e., endowment, to Responders (Oosterbeek et al., 2004). Offers for larger pie sizes and shares tend to be rejected less often (Oosterbeek et al., 2004); many studies report that it is not uncommon for offers of less than 40–50% of the pie to be rejected (see Cooper and Dutcher, 2011). This willingness to punish unfair behavior while incurring a cost reflects the degree of social inequity aversion.

We report a total of five studies that examine the prosocial behavior of older people on UGs. Two studies examined age differences for Proposers and reported different results. One study found that older participants proposed more generous offers than younger participants in the standard UG (Bailey et al., 2013), while another found no age differences (Beadle et al., 2012). Studies examined age differences for Responders' acceptance/rejection rates with mixed results. Two studies did not find any age differences (Beadle et al., 2012; Bailey et al., 2013). One study reported no difference for fair (50% of the pie) and unfair (10% and 20% of the pie) offers but older participants were more likely to reject moderately unfair (30% of the pie) offers (Harlé and Sanfey, 2012). It was found that older participants rejected more unfair offers (Roalf et al., 2012). When the unfairness was selfadvantageous, older participants were more likely to reject very high offers, which suggests inequity aversion since they do not want to be unfair to the other party (Bellemare et al., 2011).

Overall, older participants exhibit at least equal, or perhaps even more, prosocial behavior as Proposers. As Responders, older people appear to display greater inequity aversion, even in self-advantageous conditions.

#### Dictator Game

The classic dictator game (DG; see **Figure 1B**) is similar to the UG, except that the Responder cannot reject, and must accept, the amount offered by the Proposer, i.e., the ''dictator'' (Kahneman et al., 1986; Forsythe et al., 1994). The standard economic ''self-interest hypothesis'' predicts that the Proposer will offer nothing. However, a meta-analysis of 129 experiments reported that 63.89% of participants offered a positive amount with an average of 42.64% of the pie, while 36.11% offered nothing (Engel, 2011). Further, age had ''a strong effect'': giving nothing decreased with age and ''never happens in the elderly'', who give at least 50% of the pie almost all of the time (Engel, 2011). It is also worth reporting the results of three other studies that specifically examined the relationship between prosocial behavior on DG and older people. These studies were published after the meta-analysis. Two studies did not find any significant relationship (Roalf et al., 2012; Rieger and Mata, 2015). The other study used a modified DG by inducing empathy into dictators and found older people to give significantly more (Beadle et al., 2013).

Overall, older people seem to exhibit more prosocial behavior in the DG. It is worth highlighting a surprising finding from the meta-analysis: the mode for elderly contribution was 100% of the pie (Engel, 2011). However, more studies are needed to investigate age differences in the DG since 94.7% of dictators in the meta-analysis were students and only 0.7% was elderly people.

#### Trust Game

The classic trust game (TG; see **Figure 1C**) is a two-player, sequential game that involves splitting a sum of endowed money between an Investor and Trustee in two stages (Berg et al., 1995). In the first stage, both players are endowed with a fixed amount of money, say, \$10, which the Investor can choose to invest or keep. If the Investor chooses to keep the money, the game ends. If the Investor chooses to invest, then an amount, x, must be specified. This amount, x, is then tripled by the experimenter so that the Trustee receives 3x In the second stage, the Trustee can decide whether to return the money to the Investor. If the Trustee decides to keep the money then the game ends with the Investor having a total of \$10−x and the Trustee, \$10 + 3x If the Trustee chooses to return some money, y, then the game ends with the Trustee

earning a total of \$10 + 3x −y and the Investor, \$10−x+y. However, in many replications of game, the Trustee is not endowed with any money at the beginning (Johnson and Mislin, 2011).

The TG can be viewed as a variant of the DG, where the Trustee dictates an amount that was initially allocated by the Investor (Camerer and Fehr, 2004). The standard economic ''selfinterest hypothesis'' predicts that no money will be invested since the Investor will anticipate the Trustee keeping all of the investment and not returning anything. This hypothesis is, however, not supported by empirical findings. A meta-analysis of 162 experiments involving more than 23,000 participants found Investors to invest 50% of the endowment on average, and Trustees to return 37% of the total amount they had available (Johnson and Mislin, 2011).

Individual studies examining the relationship of older people's prosocial behavior on TGs report mixed results. Three studies found no significant relationship for amount invested and amount returned by Trustees (Etang et al., 2011; Johansson-Stenman et al., 2013; Rieger and Mata, 2015). One study found older people to invest and return more (Sutter and Kocher, 2007). Three studies found older people to invest less, of which two found older people to return more (Fehr et al., 2003; Bellemare and Kröger, 2007), while the other did not measure this relationship (Holm and Nystedt, 2005). The meta-analysis did not examine age but found students to return less money compared to non-students and no difference for amount invested (Johnson and Mislin, 2011), which could suggest that older people invest more since non-students are generally older than students.

Overall, there is no clear evidence on the prosocial behavior of older people playing TGs based on the seven studies reviewed. Of the seven studies that examined Investor behavior, three found no significant relationship with age, three found a negative relationship and one found a positive relationship. Six of the seven studies examined Trustee behavior and half found no significant relationship with age while the other half found a positive relationship.

#### Prisoner's Dilemma

The classic prisoner's dilemma (PD; see **Figure 1D**) is a twoplayer, simultaneous game where each player can either choose to cooperate or defect. How much each player earns depends jointly on the choices made by both players. There are three possible scenarios with their respective payoffs in parentheses, where a larger number represents a higher payoff: one player cooperates while the other defects (1:4), both players cooperate (3:3), and both players defect (2:2).

The PD tests whether players reciprocate expected cooperation (Camerer and Fehr, 2004). The standard economic ''self-interest hypothesis'' predicts that each player will choose to defect, which would lead to both players earning the second lowest payoff. Although mutual cooperation would lead to the second best outcome, there is the possibility of earning the worst payoff if the other player defects. This is also known as the Nash equilibrium: both players can do no better in terms of payoffs than to defect (Nash, 1951). However, there is overwhelming evidence of cooperation in experimental PD games (Dawes, 1980; Sally, 1995; Cooper et al., 1996; Brosig, 2002; Jones, 2008; Balliet, 2009).

Although the PD is one of the most well-known games, there are no studies examining the performance of older people. We identified 124 unique PD studies from four meta-analysis studies (Balliet, 2009; Balliet et al., 2009, 2011a,b). Of the 119 studies that we could access, 108 used student samples (90.7%). The remaining 11 studies either did not report age, or had a mean age of <37 years old. More studies involving older participants are required for a better understanding of their performance on PD.

#### Public Goods Game

The classic public goods game (PGG; see **Figure 1E**) is a generalized form of PD involving multiple players. Players are endowed with some amount of money, which they can choose whether to contribute to a ''public good'' or not. If players contribute (cooperate), the sum of contributions are multiplied by some factor, m, and distributed evenly to all players, including those who did not contribute. If players do not contribute (defect), they keep their money and stand to gain from the distribution based on the contribution of other players.

While the group would benefit most if everyone contributed, the standard economic ''self-interest'' hypothesis predicts no contribution at all. This hypothesis, is however, not supported by empirical findings (Ledyard, 1995; Chaudhuri, 2011). A meta-analysis of 27 studies involving 711 groups of participants found the average contribution to be 37.7% of the total endowment (Zelmer, 2003). Only one study examined the relationship between older people's prosocial behavior in a PGG and it reported a concave result, i.e., the middleaged participants contributed the most compared to older and younger participants (Rieger and Mata, 2015). More studies involving older participants are required for a better understanding of their performance on PGG.

#### Competitive Behavior

The willingness and ability to compete is usually important for the economy. It has been suggested that prosocial tendencies increase while competitive behavior declines with older age (see Mayr et al., 2012). There are three behavioral experiments that examine competitive behavior in old age (Charness and Villeval, 2009; Mayr et al., 2012; Sproten and Schwieren, 2015). In these experiments, participants are given a task, e.g., simple mental arithmetic, and the choice of payment based on absolute or relative performance. Choosing to be paid based on performance relative to other participants and doing well reflects a willingness and ability to compete respectively. Two of the three studies found no significant age differences in willingness to compete (Charness and Villeval, 2009; Sproten and Schwieren, 2015), while the other found an inverted U-shaped relationship: willingness increased up to 50 years old and declined after Mayr et al. (2012). All three studies report no significant age differences in ability to compete. Taken together, these findings mostly suggest that older people remain willing and able to compete.

#### Summary

We surveyed the literature on the prosocial behavior of elderly people across five common types of experimental games. Results were mixed and there was no clear evidence of age differences in prosocial behavior across these games. We also identified several important issues consistent across games that need to be addressed in the future. First, there are only a few studies involving older participants. For some games such as PD, there were no studies examining age differences. Second, most of these studies involve small samples, e.g., 18 young adults vs. 20 older adults (Harlé and Sanfey, 2012). Third, there were many sources of heterogeneity across studies. There were differences in whether studies employed a between- or within-subjects design and controlled for confounding factors such as income, as well as the average age of participants and in the design of the games, e.g., one-shot vs. repeated, amount endowed, etc. We also surveyed the literature examining the competitive behavior of older people in experiments where participants can choose to be paid based on absolute or relative performance. Overall results from three studies suggest that older people generally remain willing and able to compete.

#### Resolving Social Conflicts

The ability to resolve social conflicts can be viewed as possessing social wisdom and refers to recognizing and respecting differences in individuals' value systems and employing pragmatic reasoning to successfully navigate social issues in life with a preference for compromise (Basseches, 1980; Kramer, 1990; Baltes and Smith, 2008). There is empirical evidence that social wisdom improves with age. Older people tend to use more complex reasoning schemas that emphasize multiple perspectives and compromise when faced with various social dilemma scenarios (Grossmann et al., 2010). However, gains in social wisdom may be influenced by cultural differences in the socialization of interpersonal harmony and conflict avoidance. For example, there were age differences in social wisdom between Japanese and American adults, but this depended on whether the dilemma was interpersonal or intergroup (Grossmann et al., 2012). Further, contrary to the adage ''with age comes wisdom, a recent study found no age differences in wise reasoning about personal conflicts in American adults (Grossmann and Kross, 2014). Moreover, both younger and older adults exhibited similar amounts of the self-distancing effect, i.e., reasoning more wisely about other people's social problems than about their own. The lack of age-related difference in wise reasoning was also observed in another study, which asked participants about nonthreatening, but still rather age-neutral area of the self, e.g., ''Please think aloud about yourself as a friend'' (Mickler and Staudinger, 2008). These findings suggest that social wisdom may not be a universal and homogenous construct, and highlight the need for more studies on samples from different countries and cultures.

Everyday problem-solving/decision-making effectiveness (EPSE) is another domain that involves resolving social conflicts. EPSE incorporates both real world decision making and everyday problem solving abilities (see Thornton and Dumke, 2005). EPSE tasks typically assess the number of ''safe and effective'' solutions participants can generate to everyday social problems, e.g., ''What should an elderly woman who has no other source of income do if her social security check does not come in 1 month?'' (Heidrich and Denney, 1994). A higher number of solutions generated reflects greater EPSE. A meta-analysis of 28 studies (N = 4482) found an overall decline in EPSE among older participants (Thornton and Dumke, 2005). Moderator analyses revealed that age differences in EPSE were substantially reduced when problems were interpersonal and when older adults were highly educated (Thornton and Dumke, 2005). We also found that most, if not all, of the 28 studies were conducted in Anglo countries.

#### Emotional Homeostasis

Successful emotion regulation that maintains emotional homeostasis is crucial to wisdom. Old age is generally perceived as ''Doom and gloom'', which characterizes later life as a time of profound physical, cognitive, and emotional declines. Yet recent empirical and theoretical work challenges this view by illustrating the ''bright side'' of aging. Accumulating evidence shows that older adults attend to and remember positive vs. negative information to a greater extent than younger adults (Mather and Carstensen, 2005). A recent meta-analysis of age-related positivity effect confirmed that older adults show a significant information processing bias toward positive, but not negative, information (Reed et al., 2014). In corroborating with these behavioral evidence, recent neuroimaging studies found a relative reduction in activation during loss anticipation paralleled by significantly weaker negative arousal for large loss cues in older adults, despite intact striatal and insular activation during gain anticipation with age (Samanez-Larkin et al., 2007). Healthy older adults also exhibited enhanced activity in the nucleus accumbens in response to an expected reward value (Chowdhury et al., 2013). A recent neuroimaging study demonstrated that responsiveness to regret was specifically reduced in successful aging paralleled by autonomic and frontostriatal characteristics indicating adaptive shifts in emotion regulation, suggesting that disengagement from regret reflects a critical resilience factor for emotional health in older age (Brassen et al., 2012). Taken together, recent research indicates that older adults may outperform younger adults in maintaining emotional homeostasis, which might contribute to their wisdom in dealing with life challenges.

#### Self-Reflection

The concept of self is very complex and includes various types of self-directed internal thought processes including autobiographical reminiscence, self-referencing, self-esteem, and so on. The ability to reflect on self is an essential prerequisite for insight. To date, the vast majority of studies examining age-related changes in self-understanding have focused on selfreferential processes. Self-referential processing takes place when an individual encodes information into memory in reference to the self (Rogers et al., 1977; Symons and Johnson, 1997). Recent behavioral studies found that self- and close other-referencing similarly enhance memory for both young and older adults relative to the distant other people condition, suggesting that self-referencing provides an age-equivalent boost in memory (Hamami et al., 2011). Other studies found that elderly subjects were lower on self-consciousness and their pattern of recall was similar for self- vs. other-referenced items. Neuroimaging studies have demonstrated that the default network regions such as medial prefrontal cortex and posterior cingulate gyrus are implicated in the processing of self-relevant social information (Gusnard et al., 2001; Martinelli et al., 2013). The default network is engaged during baseline rest periods when participants are not focused on task-directed thought and is suppressed during attention-demanding tasks (Raichle et al., 2001). Aging also alters the neural activity associated with the successful formation of memories for self-referenced information (Gutchess et al., 2010). Future studies need to directly link changes in selfunderstanding and performance in social problem solving and personal well-being.

#### Dealing Effectively with Uncertainty

Decisions often need to be made in situations of risk and ambiguity, i.e., uncertainty. Dealing with such situations effectively is a crucial component of wisdom. In decision theory, a distinction is made between risk and ambiguity based on whether the probability associated with an outcome is known. If the objective probability of an outcome is known, it is risky; if the objective probability of an outcome is not known, it is ambiguous (Tversky and Fox, 1995). The two classic economic theories for understanding decisions under risk and ambiguity are expected utility (EU) and subjective expected utility (SEU). In EU (Morgenstern and Von Neumann, 1947), outcomes are evaluated based on their objective probabilities. In SEU (Savage, 1954), objective probabilities may not be known and outcomes are evaluated based on the decision maker's subjective probabilities of outcomes. In both theories, decision makers multiply the probabilities and values associated with outcomes and choose the outcome that yields the greatest expected value. Attitudes towards risk and ambiguity are generally classified as ''aversion'' or ''seeking''. Risk aversion is defined as preferring a less risky outcome to a more risky outcome with equal or greater expected value (Rabin and Thaler, 2001), e.g., choosing between \$10 for sure and a 50% chance to win \$20 or nothing. Conversely, risk seeking is defined as preferring a more risky outcome to a less risky outcome with equal or greater expected value. Ambiguity aversion is defined as preferring outcomes with known probabilities to outcomes with unknown probabilities; conversely, ambiguity seeking is defined preferring outcomes with unknown probabilities to outcomes with known probabilities (Epstein, 1999).

#### Risk

Risky choices are usually elicited in laboratory experimental settings using a variety of behavioral tasks. These tasks can be classified as requiring decision makers to make their decisions from description or experience (Hertwig et al., 2004). In tasks requiring decisions from description, options are described with their outcomes and probabilities. In tasks requiring decisions from experience, these descriptions are not explicitly provided and decision makers instead rely on personal experience from making previous similar choices.

An example of a task requiring decisions from description would be choosing between \$10 for sure and a 50% chance to win \$20 or nothing. A large number of studies investigating risk employ this approach (Weber et al., 2004). However, this approach has been criticized on the grounds of being an unrealistic representation of typical real world situations where summary descriptions of choice outcomes and probabilities are not provided (Hertwig et al., 2004). Instead, it was argued, tasks requiring decisions from experience are more reflective of everyday life (Hertwig et al., 2004). An example of such a task would be repeatedly choosing between outcomes sampled from unknown probability distributions and this is usually done on a computer. It is worth noting that decisions from experience contain a degree of uncertainty, i.e., it is not strictly uncertain because the statistical probability can be estimated (see Rakow and Newell, 2010). Intuitively, one would expect choices to be similar on both tasks when payments are the same on average. However, this is not the case: on a decision from description task, the modal choice tends to be the risky option while the sure outcome tends to be preferred on a decision from experience task (see Hau et al., 2008; Rakow and Newell, 2010). This difference in risky choice is known as the description-experience gap. Several explanations for this gap have been proposed (for a review, see Hertwig and Erev, 2009).

A meta-analysis of 29 studies (N = 4093) using various behavioral tasks to investigate age differences in risky decision making reported mixed results (Mata et al., 2011). There was no overall significant age difference in tasks involving decisions from description although age differences varied across individual tasks. On tasks involving decisions from experience, there was a significant overall age difference: older adults were slightly more risk seeking (d = 0.28). However, age differences varied across individual tasks. Combining tasks involving both decisions from experience and description yielded a negligible age difference (d = 0.07). The authors conclude that ''different tasks characteristics engender age-related differences in risky choice'' (Mata et al., 2011).

#### Ambiguity

An ambiguity-averse individual would rather choose an alternative where the probability distribution of the outcomes is known over one where the probabilities are unknown. Regarding uncertain outcomes, people are generally believed to display ambiguity aversion (Camerer and Weber, 1992; Keren and Gerritsen, 1999). However, there is a dearth of studies examining age differences in decision making in ambiguous situations. One study found no significant age differences in gambles (Kovalchik et al., 2005), while another found older participants to be less ambiguity-averse in gambles (Sproten et al., 2010) i.e., they were more likely to choose the ambiguous outcome to the certain outcome. The lack of studies could be due to the general difficulty in measuring pure ambiguity in laboratory experiments (Lopes, 1983). As such, more studies investigating how older people make ambiguous choices are needed.

#### Intertemporal Choice

Wisdom is required to make good decisions about future life plans and goals (Baltes and Smith, 2008). Many important life decisions require making intertemporal choices, i.e., trading off time and outcomes such as money, health or happiness. For example, deciding whether to pursue higher education while earning little to no money over a few years for a potentially greater lifetime earnings in the future (Read et al., 2013). Intertemporal choices involve ambiguity since the future is uncertain (Read and Read, 2004). In experiments, participants are typically asked to choose between smallersooner (SS) and larger-later (LL) amounts of money, e.g., \$100 today or \$110 in 1 year. Standard economic theory assumes exponential, i.e., constant per period, discounting, although this is not supported by empirical evidence, which suggests that individuals tend to be impatient, i.e., they prefer SS outcomes, and discount future outcomes more (Frederick et al., 2002).

Fourteen studies examined the relationship between impatience and age.1 Half studies found older people to be more patient (Green et al., 1994; Harrison et al., 2002; Reimers et al., 2009; Whelan and Mchugh, 2010; Löckenhoff et al., 2011; Halfmann et al., 2013; Li et al., 2013). Four studies found no difference (Chao et al., 2009; Samanez-Larkin et al., 2011; Roalf et al., 2012; Rieger and Mata, 2015). Two studies found older people to be more impatient (Green et al., 1996; Albert and Duffy, 2012).2 Finally one study found a curvilinear relationship with middle-aged people the most patient, while older people were more impatient than younger people (Read and Read, 2004). The only two studies that investigated intertemporal discounting on losses both found no age effects (Löckenhoff et al., 2011; Halfmann et al., 2013).

There are several possible explanations for the discrepancies in results across studies. For example, Read and Read (2004) pointed out that an earlier study by Green et al. (1994) focussed on incomparable samples, which were quite small (n = 12 per group), without controlling for confounding factors such as income, etc. Similar criticisms may apply to more recent studies as well (e.g., Whelan and Mchugh, 2010; Samanez-Larkin et al., 2011; Halfmann et al., 2013). Rieger and Mata (2015) proposed another reason for their finding of no age effects in 700 Moroccans: age differences may not generalize across cultures and nationalities. Another reason pointed out by Li et al. (2013) is the difference in the average age of older participants across studies, with few studies having sufficient data for participants above 65 years old.

Finally, we noticed large differences in the questions asked across studies. For example, monetary amounts offered ranged

1 Studies either measure the discount rate or impatience but holding the amounts and time constant, a higher discount rate implies greater impatience. 2To be precise, Green et al. (1996) found lower income adults more impatient than upper income younger adults but no differences between upper income younger and older adults.

from less than \$10 to \$1800 and the interval length between SS and LL varied from a few days to weeks, months and even years. Studies have found impatience to be influenced by the magnitude of the outcome, the interval length between outcomes and the delay from the present to the availability of the outcomes (e.g., Thaler, 1981; Kirby et al., 1999; Read, 2001; Read and Roelofsma, 2003). These factors may influence people of different ages differently, although no studies have examined this yet. There were also few studies investigating age differences and intertemporal choices involving losses.

#### Summary

Taken together, these studies revealed that age-related changes in economic decisions involving risk, ambiguity, and intertemporal choices are determined by task characteristics, the specific age range, and a variety of other methodological factors (Frederick et al., 2002; Mata et al., 2011). There is insufficient evidence to accurately determine whether older adults make risky, ambiguous and intertemporal choices differently from younger adults.

#### Concluding Remarks

Overall, the relationships between age and each of the subcomponents of wisdom remain unclear. This is a relatively young field, and it is still a challenging prospect to integrate the conflicting findings often found in this field. Several issues may contribute to the inconsistency in findings. First, there were differences in the average age across studies, with few studies having sufficient data for participants above 65 years old. For studies that used a between-subjects design, the average age for both the older and younger, i.e., comparison, group of participants could differ substantially across studies. Second, there were significant methodological variations across studies. Studies differed in the types of task used, study designs employed and in controlling for potential confounding factors. Third, a number of studies, especially in the neurosciences, used small sample sizes, which undermines the reliability of the findings due to a lack of statistical power (Button et al., 2013). These issues have been consistently

#### References

documented in the aging literature (Rhodes, 1983; Kite and Johnson, 1988; Thornton and Dumke, 2005; Ng and Feldman, 2008).

We also uncovered several gaps in the literature that future research can address. First, participants in most of the studies were mainly from Anglo countries. This is consistent with findings from Henrich et al. (2010) who questioned generalizability of behavioral science findings across human populations due to the overwhelming number of studies on student samples from Western, Educated, Industrialized, Rich and Democratic countries, and in particular USA. The need for non-Anglo samples is relevant given the finding of agerelated differences in social wisdom between Japanese and American adults (Grossmann et al., 2012). Second, there is a lack of research into how factors such as gender, individual differences in personality, culture and the environment influence wisdom in the elderly. Third, studies typically employed crosssectional and not longitudinal designs, which is in line with other fields examining age differences (Rhodes, 1983; Ng and Feldman, 2008). This results in cohort effects (Rhodes, 1983), which threaten the internal validity of studies and limit our understanding of age-related changes in the subcomponents of wisdom over the lifetime.

There is a compelling need for future studies to address the aforementioned issues in order to better understand how older people make economic and social decisions. This is especially important given the impending demographic shift to an older society. The prejudice and stereotypes may limit meaningful participation in society, e.g., jobs, and affect the mental health states of old people, who may even internalize and play into the stereotypes in self-fulfilling prophecies (Taylor and Walker, 1994, 1998; Levy, 2001; Coudin and Alexopoulos, 2010). A better understanding of the actual changes in old age can help foster a more inclusive society that taps on the expertise and skills of those older. This in turn may help alleviate feelings of social isolation, loneliness and depression (Perlman and Peplau, 1981). Understanding these issues is pertinent to implementing early interventions aimed at preventing a wide range of mental health problems, and has broad implications for social policies aimed at the elderly.

Juvin, H. (2010). The Coming of the Body. London, UK: Verso.

**Conflict of Interest Statement**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2015 Lim and Yu. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and 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.

## Memory impairment in older adults' diversionary thoughts

#### Fátima Alves , Flávia Resende and Maria Salomé Pinho\*

Laboratory of Memory, Language and Executive Functions, Faculty of Psychology and Educational Sciences, University of Coimbra, Coimbra, Portugal

The diversion paradigm was created in the context of explaining the effect of the instruction to forget some recently encoded material in the list-method of the directed forgetting paradigm. The current study of healthy older adults employed the diversion paradigm with two main goals: to determine whether thinking about an autobiographical memory interferes with the recall of recently encoded information and to explore whether the degree of forgetting depends on the temporal distance created by the diversionary thought. Ninety non-institutionalized Portuguese older adults (47 females and 43 males), aged 65–69 years, with education levels of between 3 and 6 years participated in this study. The exclusion criteria were as follows: presence of depressive symptomatology (assessed with the Geriatric Depression Scale-30) and global cognitive deterioration (assessed with the Mini–Mental State Examination). Concerning the diversion paradigm, one group was instructed to think about an autobiographical event (remembering one's childhood home or the last party that one had attended) after studying one word list (List 1) and before viewing the second word list (List 2). After a brief distraction task, the participant had to recall the words from both of the studied lists. In the control group, the procedure was the same, but the diversionary thought was substituted by a speed reading task. The obtained results showed the amnesic effect of diversionary thought but did not show a greater degree of forgetting when the autobiographical events in the diversionary thoughts were temporally more distant. Considering the practical implications of these results, this study alerts us to the importance of promoting strategies that enable older adults to better remember important information and effectively forget irrelevant information.

#### Edited by:

Lia Fernandes, Faculty of Medicine - University of Porto, Portugal

#### Reviewed by:

Sónia Martins, University of Porto, Portugal Manuela Guerreiro, Faculty of Medicine of Lisbon, Portugal

#### \*Correspondence:

Maria Salomé Pinho, Laboratory of Memory, Language and Executive Functions, Faculty of Psychology and Educational Sciences, University of Coimbra, Rua do Colégio Novo, 3000-115 Coimbra, Portugal<EMAIL_ADDRESS>
Received: 30 April 2015 Accepted: 16 September 2015 Published: 21 October 2015

#### Citation:

Alves F, Resende F and Pinho MS (2015) Memory impairment in older adults' diversionary thoughts. Front. Aging Neurosci. 7:189. doi: 10.3389/fnagi.2015.00189 Keywords: diversion paradigm, older adults, amnesic effect, autobiographical memories, free recall

#### Introduction

Certainly, many of us have experienced boring or uninteresting contexts in our lives that have led our minds to journeys into the past, present or future that are full of idyllic images and that concern moments, problems or fantasies (Klinger, 1978). Who does not remember that time when the classroom teacher told us not to be distracted and to stop daydreaming? Actually, we were not distracted; we were only shifting our mind's focus to a different mental context induced by the mind's wandering or a mental diversion (Sahakyan and Kelley, 2002). Diversion thinking refers to off-task thoughts; in other words, our attention is dissociated from the current context and attached to the mind's wandering context (Smallwood and Schooler, 2006). Returning to the classroom after our mini mental journey, we attempt to remember the information that we acquired before we began to wander, and we acknowledge the difficulty of recalling this information. The amnesic effect of daydreaming has occurred (Delaney et al., 2010).

Forgetting is commonly believed to be problematic, especially in the aging context. Its importance is underestimated, and it is viewed as a memory failure (Sheard and MacLeod, 2005). However, scientific evidence indicates that human beings have structures for suppressing irrelevant information, disallowing the buildup of information interference and improving learning and retrieval abilities (e.g., Hasher et al., 1999; Anderson and Craik, 2000). Forgetting is essential to an efficient memory system (Bjork et al., 2006), and it has been widely studied using the directed-forgetting paradigm (e.g., Bjork, 1970, 1989; Johnson, 1994; MacLeod, 1998). This paradigm has two procedures: the list method and the item method. In the item method, the forgetting instruction is given item-by-item (e.g., Basden and Basden, 1996; MacLeod, 1999; Sahakyan and Foster, 2009). By contrast, the list method employs the forgetting instruction after a whole list—generally, the first list—has been presented. The main result of these procedures shows contrasting memory performance for the to-be-forgotten items vs. the to-be-remembered items: lower recall is observed for the to-be-forgotten items in comparison with the recall level of the to-be-remembered items.

Sahakyan and Kelley (2002) developed the diversion paradigm to explain how participants in a directed forgetting paradigm with the list method comply with the instruction to forget some recently presented material. In this paradigm, after learning the first list, the participants are instructed to engage in diversionary thought (e.g., thinking about their parents' home or imagining being invisible). With these instruction modifications that explicitly command the mind's focus to another mental context, it was observed that both younger and older adults showed significant forgetting (Sahakyan et al., 2008). One explanation for the diversion paradigm effect (the impaired ability to retain the information acquired immediately before the diversionary thought) claims that diversionary thought begins a new mental context in which the items on the second list are encoded and that, in this way, the context of the first list study becomes quite different from the context of the memory test (Sahakyan and Delaney, 2005; Delaney et al., 2010). It is also important to observe that accepting the contextual account does not necessarily imply discarding the possibility of the inhibition intervention. The contextual mental shifts (diversionary thought) might be followed by the inhibition of the unwanted context in which events were encoded (Anderson, 2009).

According to Delaney et al. (2010), it is important not only to study how diversionary thought contributes to forgetting information—which the authors call the amnesic effect of diversionary thought—but also to estimate the magnitude of the diversionary thought effect depending on the mental distance (temporal, circumstantial, spatial) from the current moment. With this aim, the authors conducted two experiments with undergraduate students that included different diversionary thoughts about autobiographical memories: the students' parents' home vs. their current home (Experiment 1) and international vs. domestic vacations (Experiment 2). The study results showed worse recall of the first word list when the diversionary thought condition differed greatly from the participants' real situations in both space and time (long-distance vacations; their parents' home) in comparison with the condition in which participants thought about events that were current or nearer in space.

The present study employed the diversion paradigm developed by Delaney et al. (2010) in a sample of healthy older adults. The study has two aims: to determine whether thinking about an autobiographical memory interferes with the recall of recently encoded information and to explore whether the temporal distance implied by diversionary thought has an effect on the level of forgetting, specifically, with older thought events leading to more forgetting. We were specifically interested in learning whether thinking about autobiographical memories related to recent events (the last party the participant had attended) triggered less forgetting than did personal memories concerning a distant event (the participants' childhood home).

#### Materials and Methods

#### Subjects

Ninety community-dwelling older adults have voluntarily participated in this study. They were recruited through snowball sampling. The participants were assigned to one of the following conditions: experimental (two diversionary thought tasks, N = 30 each) or control (speed reading task, N = 30). Participants living in their childhood home were excluded from this study, as were those with a performance of more than 1 SD below the normal score on the Mini–Mental State Examination (MMSE; Folstein et al., 1975; Portuguese norms by Morgado et al., 2009) and the Vocabulary subtest of the Wechsler Adult Intelligence Scale 3rd edition; Wechsler, 2008). To rule out the presence of depressive symptomatology, participants with a score above 10 points on the Geriatric Depression Scale (GDS 30 item version; Yesavage et al., 1983; Portuguese adaptation and norms by Barreto et al., 2008) were excluded from the study. This study was approved by the Scientific Council of the Faculty of Psychology and Educational Sciences of the University of Coimbra, and verbal informed consent was obtained from participants prior to the session.

#### Materials

Delaney et al. (2010) diversion paradigm was adapted to Portuguese older adults. Two lists were created, each with 16 unrelated concrete Portuguese nouns selected from the Corpus for European Portuguese norms (Nascimento et al., 2009). Written frequency of the stimuli was medium to high according to the same norms. The words were read sequentially, keeping a card with the word visible, at a rate of 5 s per word. Each list served as List 1 and List 2 an equal number of times. The experimental condition concerning the diversion paradigm included two diversionary thought tasks: the participants' childhood home (old event condition) and the last party they had attended (recent event condition). The design of this experiment was a between-subjects design.

#### Procedure

The experiment began with the administration of the diversion paradigm (Delaney et al., 2010). All participants were tested individually and instructed to study two word lists (List 1 and List 2) for a later memory test. After studying List 1, the participants in each experimental group were asked to perform, within 45 s, one of the two diversionary thought tasks, whereas those in the control group performed a speed reading task (reading an excerpt about a collage technique aloud as quickly as possible while ignoring its content). The text selected for the reading control task did not include any of the words on the word lists. In the diversionary thought task, participants were asked to remember their childhood home, imagining themselves there and describing their home aloud (old event condition) or doing the same for the last party they had attended (recent event condition) in accordance with their condition assignments. Then, all participants studied the second list of words followed by an arithmetic filler task of backwards counting for 90 s. At the end, the participants were asked to freely recall the maximum number of words from each list on separate sheets of paper. First, they recalled the words from List 1 and then the words from List 2. The amount of time allotted for each list recall was 80 s. A post-experiment questionnaire concerning the diversionary thought (e.g., How often do you remember/think about your childhood home? Apart from the current situation, how much time had elapsed since the last time you had thought about or remembered your childhood home?) was applied. Later, the participants were also administered the MMSE to screen for their general cognitive functioning, the Vocabulary subtest of the Wechsler Adult Intelligence Scale 3rd edition to briefly assess their verbal skills, and the GDS 30 to evaluate the presence of depressive symptomatology. As the exclusion criteria were also based on the results on these tests, 9 subjects were eliminated from the present study. This procedure left a total of 90 participants.

#### Statistical Analysis

Statistical analysis was performed using the Statistical Package for the Social Sciences (SPSS) Version 18 for Windows (IBM, New York, USA). The level of significance adopted for all the statistical comparisons reported was set at p < 0.05. We computed a oneway analysis of variance (ANOVA) for unrelated samples for the comparisons between the control and experimental conditions concerning the results on the MMSE, GDS 30 and Vocabulary test, and the same statistical test was calculated with condition (diversionary thought about an old event, diversionary thought about a recent event, and no diversionary thought) as the independent variable for the comparison concerning the words recalled from List 1 and List 2 in each experimental condition and control condition.

#### Results

Ninety non-institutionalized healthy older adults (47 females and 43 males) aged 65–69 years (M = 66.90, SD = 1.53), with education levels between 3 and 6 years, participated in this study.

TABLE 1 | Cognitive status, depressive symptomatology and vocabulary scores of the participants in the experimental and control conditions.

The scores on the tests that were administered to assess the exclusion criteria for participants in this study are displayed in **Table 1**. The participants in the experimental conditions and in the control condition did not differ: F(2,87) = 2.74, MSE = 4.900, p = 0.070, η 2 p = 3.195 for the MMSE; F(2,87) = 1.60, MSE = 13.756, p = 0.208, η 2 p = 0.059 for the GDS 30 items; and F(2,87) = 0.57, MSE = 46.344, p = 0.568, η 2 p = 0.013 for the Vocabulary test.

The mean proportions of words recalled from List 1 and List 2 in each experimental condition (old event: the childhood home, recent event: the last party) and control (no diversionary thought) are presented in **Table 2**.

The ANOVA results indicated that condition significantly influenced the level of recall for List 1, F(2,87) = 6.44, MSE = 0.045, p = 0.003, η 2 p = 0.124. Games-Howell post hoc tests revealed significant differences between the old event (childhood home) condition and the control condition (p = 0.020) and between the recent event (last party) condition and the control condition (p = 0.008) but not between the old event condition and the recent event condition (p = 0.978). Thus, the amnesic effect of the diversionary thought was achieved. However, we did not find an effect of the event temporal distance produced by the diversionary thought, as the recall between the two experimental conditions did not differ. Concerning the List 2 recall, the ANOVA result was not statistically significant, F(2,87) = 1.65, MSE = 0.023, p = 0.198, η 2 p = 0.037, suggesting that the participants' recall levels were equal in the three conditions.

#### Discussion

In this study, the participants in both diversionary thought conditions recalled fewer words from List 1 than did participants in the condition with a reading speed task (control condition). Thus, remembering a personal past event produced recall impairment with the first studied word list, i.e., the expected amnesic effect of diversionary thought was achieved. The

temporal distance of the diversionary thought (old event vsrecent event conditions) did not influence recall; that is, the difference in List 1 recall levels between the two diversionary thought conditions did not reach statistical significance.

The first result concerning the amnesic effect of diversionary thought is in accordance with a previous study of the diversion paradigm in a sample of undergraduate students (Delaney et al., 2010) and with a directed forgetting paradigm employing the list method (Sahakyan et al., 2008) in a sample of younger and older adults. The explanation for this amnesic effect was not addressed in the present study, although context change (i.e., due to the contextual change induced by the diversionary thought, the context of encoding List 1 differed from the context of the memory test) has emerged in the literature as the strongest explanation (Sahakyan and Kelley, 2002; Sahakyan and Delaney, 2005; Delaney et al., 2010). The temporal distance of the diversionary thought (old event: the childhood home vs recent event: the last party) does not appear to differentially influence the recall of previously encoded information. To the best of our knowledge, there is no published study on whether the temporal distance created by a diversionary thought influences older adults' forgetting. The result obtained differs from research with undergraduate students that suggests that diversionary thoughts affect the degree of forgetting information (Delaney et al., 2010): when the distance between the present moment and the past remembered event is longer, more

#### References

forgetting occurs. The analysis of the participants' responses to the post-experiment questionnaire, specifically the responses to the question about the last time they had thought about their childhood home/the last party that they had attended, indicated that the participants in the old event condition had retrieved memories of their childhood home more recently than the participants in the recent event condition had remembered the last party that they had attended. In future studies, the temporal distance of the diversionary thought should be further controlled. The study of these issues will be useful from a practical perspective to promote strategies that enable older adults to better remember important information and more effectively forget irrelevant information, at least immediately after encoding this information. The assessment of executive functions constitutes another limitation of this study, as these functions are strongly related to memory functioning and its decline occurs frequently in older people (e.g., Schaie and Willis, 2009).

The amnesic effect of diversionary thought that was achieved in the present study suggests that this effect is also found in normal aging. Given that remembering a past personal event can have a negative impact on the recall of recently encoded information, training that improves older adults' attentional strategies becomes relevant. This training could help older people remember relevant information and forget unimportant information.

**Conflict of Interest Statement**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2015 Alves, Resende and Pinho. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and 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.

## Speaking in Alzheimer's disease, is that an early sign? importance of changes in language abilities in Alzheimer's disease

*Greta Szatloczki1 \*, Ildiko Hoffmann2,3 , Veronika Vincze4 , Janos Kalman1 and Magdolna Pakaski1*

*1Research Institute for Linguistics, Hungarian Academy of Sciences, Szeged, Hungary, 2Research Institute for Linguistics, Hungarian Academy of Sciences, Budapest, Hungary, 3Department of Linguistics, University of Szeged, Szeged, Hungary, 4MTA-SZTE Research Group on Artificial Intelligence, University of Szeged, Szeged, Hungary*

It is known that Alzheimer's disease (AD) influences the temporal characteristics of spontaneous speech. These phonetical changes are present even in mild AD. Based on this, the question arises whether an examination based on language analysis could help the early diagnosis of AD and if so, which language and speech characteristics can identify AD in its early stage. The purpose of this article is to summarize the relation between prodromal and manifest AD and language functions and language domains. Based on our research, we are inclined to claim that AD can be more sensitively detected with the help of a linguistic analysis than with other cognitive examinations. The temporal characteristics of spontaneous speech, such as speech tempo, number of pauses in speech, and their length are sensitive detectors of the early stage of the disease, which enables an early simple linguistic screening for AD. However, knowledge about the unique features of the language problems associated with different dementia variants still has to be improved and refined.

#### *Edited by:*

*Lia Fernandes, University of Porto, Portugal*

#### *Reviewed by:*

*Valentina Echeverria Moran, Bay Pines VA Medical Center, USA Johannes Schröder, University of Heidelberg, Germany*

#### *\*Correspondence:*

*Greta Szatloczki<EMAIL_ADDRESS>
*Received: 29 June 2015 Accepted: 28 September 2015 Published: 20 October 2015*

#### *Citation:*

*Szatloczki G, Hoffmann I, Vincze V, Kalman J and Pakaski M (2015) Speaking in Alzheimer's disease, is that an early sign? Importance of changes in language abilities in Alzheimer's disease. Front. Aging Neurosci. 7:195. doi: 10.3389/fnagi.2015.00195*

Keywords: screening, mild cognitive impairment, Alzheimer's disease, language domain, systematic review

#### INTRODUCTION

Despite great efforts concentrated on disease modifying therapies of Alzheimer's disease (AD), halting the degenerative process has not been possible. For this reason, early diagnosis of AD became crucial in the management of the disease. Current pharmacological agents available for AD are more effective in the mild cases, even in the cases of mild cognitive impairments (MCI). It is welldocumented that manifest AD patients show markers of language deficit long before their diagnosis is confirmed (Mesulam et al., 2008) and this tendency is especially useful for detecting mild cognitive decline, the prodromal stage of AD (Garrard et al., 2005).

Diagnostic procedures of language functions play a major role in the detection process of the cognitive deficits with different stages. Questions nevertheless remain whether the characterization of the linguistic profiles of MCI/AD cases is useful or not in the detection procedure. The purpose of this review is to summarize the main language deficits in relation to prodromal and manifest AD, focusing on the changes of different language domains (semantic, pragmatic, syntactic, and phonologic ones) during the course of the disease. Additionally, the relationship between language and other cognitive functions in AD will be discussed.

#### ALZHEIMER'S DISEASE AND LANGUAGE

Cognitive deficits involve executive function, reasoning, visuoconstructive, and language abilities. Language deficits typically become noticeable from the early stage of the disease (Morris, 1996). Naming disorders, impaired auditory and written comprehension, fluent but empty speech, and semantic paraphasia are typical language deficits in AD, however, repetition abilities and articulation remain relatively intact (Appell et al., 1982; Bayles et al., 1992; Croot et al., 2000). The different stages of the disease exhibit specific patterns of linguistic difficulties in a given domain. The following five domains of language are known: phonetics and phonology, morphology, lexicon and semantics, syntax, and pragmatics. These language domains are affected in different ways in AD (Bayles and Boone, 1982).

In the **Table 1**, we are going to summarize the language function measurements of MCI and different stages in AD. As the disease progresses (from MCI to severe AD), a continuous decline in language can be observed in AD patients (Kempler, 2004).

### THE RELATIONSHIP BETWEEN LANGUAGE AND COGNITIVE FUNCTIONS IN ALZHEIMER'S DISEASE

In AD, language and memory functions are closely related since linguistic functioning requires memory functions. Difficulties in productive speech, speech comprehension, and memory functions overlap. Senile changes in language comprehension and expression entail the decline of global speech performance, and a lapse in evocative memory puts constraints on the active vocabulary (Kempler, 2004).

In a summative work, the relationship between simple language measures and cognitive impairment in AD was estimated by the mini-mental state examination (MMSE) and the clinical dementia rating scale (CDR), respectively. Language measures included articulation, fluency (word-finding ability, hypofluency, hyperfluency), semantic fluency, repetition, and confrontational naming. A significant relationship was found between CDR and MMSE scores and all language measures apart from hyperfluency. Impairment in language fluency, animal naming, and confrontational naming are common, especially in the case of impaired cognitive and global performance (Weiner et al., 2008).

It has also been shown that patients with AD show difficulties in performing tasks that tap semantic knowledge, such as naming, verbal fluency, or object recognition. These symptoms occur early and they increase during the course of the illness, suggesting early and progressive impairment of the semantic memory of these patients (Nebes et al., 1989). Briefly, semantic memory can be defined as the capacity to acquire and retain general knowledge about the world, containing basic facts and meanings, as well as words and their meanings. Several approaches have been put forward in order to test semantic memory, such as priming tests, category fluency, and object or picture naming (Hodges, 1994).

Another stream of research aims at the examination of lexical semantic memory (Balthazar et al., 2007). According to these results, the three groups (control, amnestic MCI, mild AD) showed a continuum of decreasing cognitive ability in all cognitive tests. In semantic memory tests, the performance of amnestic MCI patients was similar to that of controls, but showed worse results on verbal fluency task, which involves semantic knowledge, as well as language use, executive function, and short-term memory. Thus, verbal fluency might have been influenced by short-term memory. As the disease progresses, other areas including the temporal cortex are involved, which can explain the difficulties with

*AD, Alzheimer's disease; MCI, mild cognitive impairment; CTRL, healthy controls.*

semantic knowledge in mild AD. It has been shown that amnestic MCI impairs episodic memory while the lexical semantic system is spared, which can be affected in the early phase of AD.

In summary, deficits in language and memory functions, especially in semantic memory are commonly found in patients with AD, even in the early phase. Therefore, the need can arise for developing a purely language-based screening test, which can serve as an early diagnostic tool for MCI.

#### NEURAL BASES OF LANGUAGE DEFICITS IN ALZHEIMER'S DISEASE

Considering the cognitive impairments in AD, the neural basis of episodic memory has been primarily investigated by the anatomical and functional neuroimaging techniques, such as functional magnetic resonance imaging (fMRI), diffusion tensor imaging (DTI), or positron emission tomography (PET). So far, only a limited number of publications are available, which focus on the detection of organic or functional changes in the central nervous system underlying language impairments. For example, a recent investigation of healthy subjects and individuals with amnestic mild cognitive impairment (aMCI) demonstrated a difference in the neuroanatomical bases of episodic and semantic performance (Hirni et al., 2013). Specifically, region of interest (ROI) analyses showed that episodic memory performance was associated with the bilateral entorhinal cortex/hippocampus (ERC/HP) head, whereas semantic memory performance was associated with left medial perirhinal cortex (mPRC) and bilateral ERC/HP head integrity suggesting that mPRC damage in very early AD may be detectable with common clinical tests of semantic memory if episodic memory performance is controlled (Hirni et al., 2013).

In another study, a 2-back versus 1-back letter recognition task was performed by MCI and AD patients, using DTI and fMRI. Significant hypoactivation was found in posterior brain areas and relative hyperactivation in anterior brain areas during working memory in AD/MCI subjects compared to controls. In MCI/AD subjects, impairments of structural fiber tract integrity co-occur with breakdown of posterior and relatively preserved anterior cortical activation during working memory performance (Teipel et al., 2014).

Posterior corpus callosum connects superior parietal, posterior temporal, and occipital cortical areas (De Lacoste et al., 1985), which include key nodes of working memory activation. The superior longitudinal fasciculus forms a large arc superior and lateral to the putamen connecting all four cerebral lobes, which has a main role in language processing in the human brain (Bernal and Altman, 2010; Axer et al., 2013). This area is known to be impaired in MCI and mild AD (Liu et al., 2011; Zhang et al., 2013) and is a possible reason for functional uncoupling of prefrontal and posterior brain areas during verbal working memory performance (Teipel et al., 2014).

#### LANGUAGE FUNCTIONS DURING THE COURSE OF ALZHEIMER'S DISEASE

The impairment of the language functions in the course of AD may be characteristic not only for the given stage of the disease but also for its prodroma, MCI. During the total course of the disease, language seems to be impaired disproportionally, meaning that the semantic and pragmatic language systems are more impaired than syntax (Bayles and Boone, 1982). Impairments in the lexical, semantic, and pragmatic language functions are typically present in mild AD since they depend on cognition to a greater extent (Taler and Phillips, 2008; Tsantali et al., 2013). Articulatory and syntactic domains of language production remain intact until late stages of the disease (Croot et al., 2000).

In the following sections, relevant studies will be discussed and summarized in order to investigate language functioning during the course of AD, considering the most extensively researched language domains (**Table 2**).

#### Phonetics and Phonology in Alzheimer's Disease

Temporal parameters of speech can be investigated in the language domains phonetics and phonology, more precisely, in spontaneous speech (Hoffmann et al., 2010; López-de-Ipiña et al., 2013), in a reading aloud task (Martínez-Sánchez et al., 2013), and in spoken tasks (Satt et al., 2014).

In the MCI phase, the most characteristic linguistic changes are longer hesitations and a lower speech rate in spontaneous speech (Hoffmann et al., 2010; Roark et al., 2011; Jarrold et al., 2014; Satt et al., 2014). The manually extracted acoustic features of spontaneous speech and an automatizing biomarker extraction process using automatic speech recognition (ASR) have been recently compared in MCI patients and control subjects (Tóth et al., 2015). The classification results provided by ASR-based feature extraction were just slightly worse than those of the manual method (Tóth et al., 2015).

The temporal parameters of spontaneous speech have also been investigated in mild AD and control subjects (Hoffmann et al., 2010). This study aimed to identify a speech parameter that might distinguish mild AD patients from normal individuals. The following aspects of spontaneous speech were included in the analysis: articulation rate, speech tempo, hesitation ratio, and grammatical error ratio. Results showed that articulation rate in mild and severe AD patients was significantly different from normal controls; furthermore, a difference among mild, moderate, and severe AD patients was also reported. Significant differences in speech tempo and hesitation ratio were found between all experimental groups, apart from moderate and severe AD patients, who performed similarly on both tasks. Grammatical error analysis showed significant difference between moderate and severe AD groups; however, this was not found when comparing normal subjects and mild AD groups (Hoffmann et al., 2010).

In another study, an automatic spontaneous speech analysis was also carried out to identify mild AD. It was suggested that shorter recording times reflect that for AD patients, speech requires more efforts than for healthy individuals: patients speak more slowly with longer pauses, as well as they spend more time to find the correct word, which in turn leads to speech disfluency or break messages (López-de-Ipiña et al., 2013).

A similar research studied the temporal organization of speech in AD patients and matched healthy controls with an oral reading

*AD, Alzheimer's disease; MCI, mild cognitive impairment.*

*The scale of MMSE scores is as follows: MCI: 28–26 points (Roalf et al., 2013), mild AD: 25–20 points, moderate AD: 19–10 points, and severe AD: 9–0 points (Vertesi et al., 2001).* +*, degree of involvement;* −*, intact; ?, no data.*

task. The following indices were analyzed: total duration of the reading task, number of pauses, pause proportion, phonation time, phonation – time ratio, speech rate, and articulation rate. The AD group showed impairment in all of these variables. Reduced speech and articulation rates, low effectiveness of phonation time, as well as increased number and proportion of pauses characterized their reading. The two temporal parameters with the greatest discriminatory capacity were speech rate and articulation rate. In sum, signal processing algorithms applied to reading fluency recordings were capable of differentiating between AD patients and controls with an accuracy of 80% based on speech rate. Thus, analyzing temporal parameters for reading fluency, especially speech and articulation rates, allowed to distinguish between asymptomatic subjects and patients in mild AD (Martínez-Sánchez et al., 2013).

Although examining the temporal parameters of spontaneous speech, it is not clear which variables are capable of separating the mild AD group from the control group. Some researchers divided the mild AD group from the control group based on the articulation rate, speech tempo, and hesitation ratio variables (Hoffmann et al., 2010), whereas others suggested that speech rate and articulation rate are the best discriminating variables (Martínez-Sánchez et al., 2013). Furthermore, some researchers emphasize the importance of break analysis as well (López-de-Ipiña et al., 2013). However, there is an agreement that the temporal analysis of spontaneous speech is proven to be an effective method for spotting mild AD.

In moderate or severe AD, there are more and more serious temporal changes in spontaneous speech: hesitation number and time increase, compared to mild AD, and the mental lexicon is even more difficult to access (Hoffmann et al., 2010).

#### Lexical, Semantic, and Pragmatic Domains of Language in Alzheimer's Disease

Mild cognitive impairment patients usually have trouble with finding the right word (Fraser et al., 2014; Garrard et al., 2014). As regards semantics and syntax, both seem to be impaired since fluency tasks and naming tasks show deficits; moreover, comprehension of sentences and texts and production of narrative speech are also impaired, concerning the semantic content and syntactic structures of speech (Juncos-Rabadán et al., 2010).

Alzheimer's disease patients lack the distinctive semantic attributes of concepts: there is strong evidence that dysfunction in linguistic tasks is caused by the general cognitive impairment in AD (Feinberg and Farah, 1997). The most common and obvious language errors made by AD patients are semantic errors (Croot et al., 2000), namely that they use superordinate category names instead of the target name (Saito and Takeda, 2001) or circumlocutory speech with progressively impaired naming (Emery, 2000).

The semantic association test (SAT) is a tool for detecting disorders in verbal and visual semantic processing (Visch-Brink and Denes, 1993). In general, AD patients had significantly lower scores on SAT than controls. However, their data expose an incoherent relation between naming and semantic processing in AD. In contrast to semantic processing, the performance of AD patients on naming fell within the normal range, implying that naming is independent of semantic processing in AD (Visch-Brink et al., 2004).

Alzheimer's disease patients typically have difficulties in tasks of confrontational naming and verbal fluency (Appell et al., 1982; Bayles et al., 1987). Semantic verbal fluency and phonological verbal fluency tests are widely used in diagnosis of AD and they are reliable indicators of language deterioration in the early detection of AD (Laws et al., 2010). Difficulties in word finding are one of the earliest manifestations of language breakdown in AD. This pattern of impairment has been implicated as the loss of semantic knowledge in AD (Hodges et al., 1992). Results from language tests and priming experiments clearly suggest altered intentional and automatic semantic processes in AD. However, the order in which these processes are impaired during the course of the disease is unclear (Duong et al., 2006).

Lexico-semantic impairments in AD have been attributed to abnormalities in intentional and automatic access to semantic memory. In a study, MCI, pre-AD, and normal elderly people were tested with intentional access tasks (picture naming and semantic probes), automatic access tasks (lexical decision and priming), and executive function tasks (Stroop and Strooppicture naming). Results indicated that the MCI group was only impaired in tasks of intentional access relative to the AD group, which showed impairment in all tasks. Since most MCI subjects eventually develop AD, the results suggest that the intentional access to semantic memory is impaired earlier compared to the automatic access. The AD individuals performed significantly different from normal controls in all four semantic tasks (Duong et al., 2006). AD subjects demonstrated slowing in lexical decision as well as increase in semantic priming, termed hyperpriming (Giffard et al., 2001, 2002), which speaks for abnormal automatic semantic processing. Abnormal performance has also been found in picture naming and semantic probe questions which require effortful semantic processing and search. The results confirmed the observation that subtle cognitive impairments, such as language impairment, may co-occur with the readily observed memory impairments (Petersen et al., 1999, 2001; Ritchie et al., 2001).

Alterations in productive and receptive discourse-level processing have also been reported in MCI and mild AD. AD individuals generally produce shorter texts than the normal controls with less relevant information and multiple error types (incoherent/indefinite phrases, semantic and graphemic paraphasia, and inability to abstract) and describe all pictorial themes (Taler and Phillips, 2008).

To sum up, we can say that the performance of AD patients is different compared to the control group in most of the semantic tasks. Changes in semantic processing (Petersen et al., 1999, 2001;

#### REFERENCES

Ritchie et al., 2001; Duong et al., 2006) trigger semantic errors in AD patients (Croot et al., 2000). Furthermore, impaired naming (Emery, 2000) and picture naming (Petersen et al., 1999, 2001; Ritchie et al., 2001), word finding difficulties, and abnormal verbal fluency are also present in this group (Appell et al., 1982; Bayles et al., 1987). Slow lexical decision could be one of the reasons behind all of these (Giffard et al., 2001, 2002). However, it should be noted that although lexico-semantic changes in AD have been intensively studied, research on pragmatics has rarely been carried out among AD patients, thus it constitutes a potential field for future investigations.

#### CONCLUSION

On the basis of the existing research findings, we can state that the language deficit in AD is present in the early stage of the disease; therefore, the objective measures of the different language domains are very important in the recognition of these patients. However, up to now, very few linguistic methods have been published, which are suitable for the early diagnosis of AD.

The disproportional impairments of language functions in the course of the disease have been proven by almost cohort studies. Large scale prospective longitudinal studies would be more beneficial; however, they have been also missing. Additionally, more extensive use of functional neuroimaging techniques based on linguistic tasks in MCI or mild AD could lead to a more informed picture of the neural bases of language functions in the different stages of the disease.

In the future, additional work needs to be done to validate new methods across different settings (such as population-based, primary care, and memory clinics), age, and ethnic groups. Since the earliest measurable language domain is the temporal parameter of speech, the computerized analysis of spontaneous speech developed recently may be a promising approach in the early detection of AD. The combined use of the measurement of linguistic parameters and telemedicine technologies might permit the screening of MCI or mild AD by an interactive test using a software package or mobile application. Having an accurate method to assess for dementia and predict risk in routine clinical care will aid decision-making and can ultimately lead to disease prevention.

#### ACKNOWLEDGMENTS

This work was supported by the Hungarian National Research Funds: TÁMOP-4.2.2.A-11/1/KONV-2012-0073 and Bolyai János Research Scholarship and the A/2-11-1-2012-0001 "National Excellence Program."

**Conflict of Interest Statement:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

*Copyright © 2015 Szatloczki, Hoffmann, Vincze, Kalman and Pakaski. 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.*

## The neural mechanisms underlying the aging-related enhancement of positive affects: electrophysiological evidences

*Xianxin Meng1, Jiemin Yang2, AYan Cai2, XinSheng Ding1, Wenwen Liu1, Hong Li3 and JiaJin Yuan2\**

*1 School of Education, Nanyang Normal College, Nanyang, China, 2 Faculty of Psychology, Southwest University, Chongqing, China, 3 Research Centre for Brain Function and Psychological Science, Shenzhen University, Shenzhen, China*

Background: Previous studies reported that old adults, relative to young adults, showed improvement of emotional stability and increased experiences of positive affects.

#### *Edited by:*

*Constança Paúl, Coral do Instituto de Ciências Biomédicas Abel Salazar – University of Porto, Portugal*

#### *Reviewed by:*

*Manuel De Vega, Universidad de La Laguna, Spain Ramesh Kandimalla, Texas Tech University, USA*

#### *\*Correspondence:*

*Jiajin Yuan, Faculty of Psychology, Southwest University, Beibei, Chongqing 400715, China<EMAIL_ADDRESS><EMAIL_ADDRESS>
*Received: 28 April 2015 Accepted: 10 July 2015 Published: 06 August 2015*

#### *Citation:*

*Meng X, Yang J, Cai A, Ding X, Liu W, Li H and Yuan J (2015) The neural mechanisms underlying the aging-related enhancement of positive affects: electrophysiological evidences. Front. Aging Neurosci. 7:143. doi: 10.3389/fnagi.2015.00143* Methods: In order to better understand the neural underpinnings behind the agingrelated enhancement of positive affects, it is necessary to investigate whether old and young adults differ in the threshold of eliciting positive or negative emotional reactions. However, no studies have examined emotional reaction differences between old and young adults by manipulating the intensity of emotional stimuli to date. To clarify this issue, the present study examined the impact of aging on the brain's susceptibility to affective pictures of varying emotional intensities. We recorded event-related potentials (ERP) for highly negative (HN), mildly negative (MN) and neutral pictures in the negative experimental block; and for highly positive (HP), mildly positive (MP) and neutral pictures in the positive experimental block, when young and old adults were required to count the number of pictures, irrespective of the emotionality of the pictures.

Results: Event-related potentials results showed that LPP (late positive potentials) amplitudes were larger for HN and MN stimuli compared to neutral stimuli in young adults, but not in old adults. By contrast, old adults displayed larger LPP amplitudes for HP and MP relative to neutral stimuli, while these effects were absent for young adults. In addition, old adults reported more frequent perception of positive stimuli and less frequent perception of negative stimuli than young adults. The post-experiment stimulus assessment showed more positive ratings of Neutral and MP stimuli, and reduced arousal ratings of HN stimuli in old compared to young adults.

Conclusion: These results suggest that old adults are more resistant to the impact of negative stimuli, while they are equipped with enhanced attentional bias for positive stimuli. The implications of these results to the aging-related enhancement of positive affects were discussed.

Keywords: aging, event-related potentials, positive affects, late positive potentials, attention

### Introduction

Although human aging is associated with reductions of physical and cognitive abilities, many studies indicate that emotional stability and positive affects may enhance with normal aging (Mroczek and Kolarz, 1998; Ehrlich and Isaacowitz, 2002; Clark and Oswald, 2007). In an early study, Mroczek and Kolarz (1998) observed that old adults tend to report less negative experience and more positive experience than young adults. Consistent with this aging-related enhancement of emotional stability, a number of studies have demonstrated that relative to young adults, old adults showed preferential processing of positive information over negative information (Williams et al., 2006; Wood and Kisley, 2006; Kisley et al., 2007; Leclerc and Kensinger, 2008a; Feng et al., 2011), which is known as the agingrelated positivity effect. Allard and Isaacowitz (2008) observed that old adults fixated more toward positive and neutral than negative pictures in both full and divided attention conditions. By recording eyeblink startle responses, Feng et al. (2011) reported that old adults showed potentiated responses when viewing positive pictures in comparison to negative pictures, whereas this was not the case for young adults. Socioemotional selectivity theory (SST) provides a framework for understanding the aging-related enhancement of positive affects. This theory states that motivation and goal preferences are influenced by time perspective (Carstensen et al., 1999). Young adults perceive their time remaining in life to be expansive and are more motivated to acquire knowledge whereas old adults perceive their time left in life as limited and would prioritize present-oriented goals of emotional meaning (Carstensen et al., 1999). This motivational shift leads to that old adults focus more attention on positive aspect of life.

A number of studies have investigated neural underpinnings of the aging-related enhancement of positive affects (Williams et al., 2006; Wood and Kisley, 2006; Kisley et al., 2007; Leclerc and Kensinger, 2008a). Using both event-related potential (ERP) and functional MRI methods, Williams et al. (2006) found that aging was associated with enhanced medial prefrontal activation for fearful faces and smaller activation for happy faces. The enhanced prefrontal control of negative and smaller control of positive information with aging has been considered as an important explanation for this phenomenon (Williams et al., 2006). In addition, several studies reported that the aging-related enhancement of positive affects is driven primarily by decreased neural responding to negative materials (Wood and Kisley, 2006; Kisley et al., 2007). For example, using an emotional categorization task and ERP technique, Kisley et al. (2007) observed age-related reductions in neural reactivity to negative pictures, but little age-related changes in neural reactivity to positive pictures. However, other studies demonstrated that this phenomenon is driven primarily by increased brain reactions to positive materials (Mather et al., 2004; Leclerc and Kensinger, 2008a). For example, by requiring subjects to identify the uses of emotional objects, Leclerc and Kensinger (2008a) observed greater activations of ventromedial prefrontal cortex for positive than for negative pictures in old adults, whereas young adults showed enhanced activations for negative than for positive pictures in this region.

Thus, there exist disagreements concerning the neural mechanisms behind the aging-related enhancement of positive affects. Though Williams et al. (2006) suggest that the agingrelated shift in prefrontal control of negative and positive stimuli contributes to this phenomenon, this inference was based on a face perception task, instead of a direct emotional control task. Of particular importance, it needs to be elucidated whether this phenomenon is driven solely by decreased brain reactions to negative materials or by enhanced reactions to positive materials, or by both. It is worth noting that most of the prior studies which addressed neural mechanisms of this phenomenon required subjects to assess the emotionality of the stimuli explicitly (Mather et al., 2004; Williams et al., 2006; Wood and Kisley, 2006; Kisley et al., 2007; Leclerc and Kensinger, 2008a). It has been indicated that emotional effects are susceptible to the contamination of the explicit categorization of emotional stimuli, which is known as the "relevance-for-task effect" that is most pronounced in ERP experiment (Carretié et al., 1996, 2001). Thus, it is necessary to design a covert emotional task to control this confound. On the other hand, in order to obtain a clean emotional effect, it is necessary to set non-emotional, neutral stimuli as a baseline for positive or negative stimuli, and then to compute the emotion effect based on the emotional-neutral differences in dependent variables (Meng et al., 2009; Yuan et al., 2009), rather than simply comparing positive with negative stimuli.

Furthermore, in order to better understand the neural underpinnings behind the aging-related enhancement of positive affects, it is necessary to investigate whether old and young adults differ in the threshold of eliciting positive or negative emotional reactions. Specifically, because it is well established that aging is linked with better emotional stability and increased positive affects, it is possible that old adults are reactive to positive stimuli of low emotional intensity, which may not be the case for young adults. Similarly, given the robustness of this agingrelated phenomenon, old adults are also likely to elicit emotional reactions to negative stimuli at a higher threshold than young adults. However, no studies have examined emotional reaction differences between old and young adults by manipulating the intensity of emotional stimuli to date. In fact, a great number of prior studies confirmed that the intensity of emotional stimuli is important (Leppanen et al., 2007 ˇ ; Yuan et al., 2007; Meng et al., 2009; Schaefer et al., 2009), and emotions of diverse intensities modulate cognitive activities differently (Yuan et al., 2008, 2012; Schaefer et al., 2009, 2011). Without manipulation of the emotional intensity of positive and negative stimuli, it is difficult to reveal the difference in the threshold of emotion elicitation across age groups.

In addition, a number of studies have indicated that the impact of aging on processing of emotional stimuli is clearly observed in controlled processing tasks which involve prefrontal cortex activity (Carstensen et al., 1999; Leclerc and Kensinger, 2008a); while this impact is not observed in tasks involving automatic processing (Hahn et al., 2006; Mather and Knight, 2006; Leclerc and Kensinger, 2008b; Mickley Steinmetz et al., 2010). For example, using eye-tracking method, Rosler et al. (2005) reported that when a negative–neutral picture pair was presented, young adults maintained attention longer toward negative pictures than old adults did, but young and old adults showed similar initial attentional orienting for the negative pictures. Using a spatialcueing task, Brassen et al. (2011) reported that relative to young adults, old adults showed increased distractibility by happy faces in the high attention to faces condition. However, this age difference vanished when attention was low to faces (Brassen et al., 2011). Although these studies imply that the impact of aging on emotional processing entails the access of controlled processing resources (Leclerc and Kensinger, 2008a; Mickley Steinmetz et al., 2010; Sasse et al., 2014), how emotion-related aging effect varies with the information processing stages has yet to be directly investigated.

Based on the above considerations, the present study aimed to address the impact of aging on automatic and controlled processing of positive and negative stimuli of varying emotional intensity, by using ERP measures and a block-design covertemotional task. We used ERP technique as it is helpful in depicting the timing features, specifically, the automatic and controlled processing of emotional stimuli and their modulation by aging. Previous studies used two ERP components, P1 and late positive potential (LPP), to reflect automatic and controlled processing, respectively (Wood and Kisley, 2006; Kisley et al., 2007; Olofsson et al., 2008; Langeslag and Van Strien, 2010). P1 component is an early component peaking about 100 ms post stimulus and has been accepted to reflect exogenous, automatic sensory processing (Scott et al., 2009; Dan and Raz, 2012). P1 amplitudes are thought to be sensitive to attention allocation (Luck et al., 1994; Smith et al., 2003; Brown et al., 2010), and be heightened for emotional stimuli compared to neutral stimuli (Scott et al., 2009; Dan and Raz, 2012). By contrast, LPP, which is also named late positive component (LPC) by some researchers (Ashley et al., 2004; Langeslag et al., 2007), starts around 400 ms and lasts for 700 ms. LPP reflects consciously controlled processing that involves continued voluntary attention toward emotional stimuli (Hajcak and Dennis, 2009; Langeslag and Van Strien, 2010). The LPP amplitudes increased with the enhancement of experienced emotion, and decreased with the reduction of experienced emotion (Flaisch et al., 2008; MacNamara et al., 2011). Based on previous studies (Carstensen et al., 1999; Hahn et al., 2006; Mather and Knight, 2006; Leclerc and Kensinger, 2008a,b; Mickley Steinmetz et al., 2010), we predict that the impact of aging on brain processing of emotional stimuli may occur at voluntary attention stage, instead of early automatic attention stage. Specifically, young and old adults may display similar emotional reactivity to emotional pictures in early P1 component whereas the two groups may display different emotional reactivity to pictures in LPP component.

In addition, considerable studies with young adults indicate that LPP elicited by negative pictures are largest over the parietal scalp (Cuthbert et al., 2000; Hajcak and Olvet, 2008; Yuan et al., 2014a,b). Based on these evidences, if old adults relative to young adults show decreased negative emotional reactivity, it is likely to observe decreased LPP amplitudes for negative pictures at parietal scalp, in old compared to young adults. On the other hand, functional MRI studies have indicated that the processing bias of old adults for positive stimuli is mainly manifested by the greater neural activity for positive relative to negative stimuli in prefrontal cortical regions (e.g., ventromedial or dorsolateral PFC; Leclerc and Kensinger, 2008a; Ritchey et al., 2011). However, the covert emotional task is associated with similar late potentials for positive and neutral stimuli in young adults (Yuan et al., 2007, 2009). Based on these evidences, we hypothesize to observe enhanced LPP amplitudes for positive compared to neutral pictures at prefrontal scalp, in old adults but not in young adults.

On the other hand, previous studies often used a random design, which presented positive, negative and neutral stimuli in a single block, with their order fully randomized (Wood and Kisley, 2006; Kisley et al., 2007). Though these studies observed clear emotion effects in electrophysiological measures, they observed no emotional effect in behavioral measures (Wood and Kisley, 2006; Kisley et al., 2007). A possible reason is that presenting positive to negative (or negative to positive) stimuli across trials may produce inter-trial emotion offset, which prevents the generation of a robust emotion induction effect in behavioral assessment. However, it is important to assess emotion impact from behavioral measures, not only for confirming whether a given type of emotional stimuli effectively elicit the target emotion, but also for verifying what neurophysiologic results truly reflect. For these considerations, the current study used a block design (Rowe et al., 2007; Yuan et al., 2012), with one block presenting highly positive (HP), mildly positive (MP) and neutral pictures while the other block presenting highly negative (HN), mildly negative (MN) and neutral pictures. A neutral baseline condition was used in either block, to isolate the emotional effect for each condition. To investigate the behavioral index of emotion impact and its relation with aging, subjects were asked to report the perceived frequency and the category of emotional images for each block, according to subjective impressions. We used this procedure, rather than direct mood rating, to avoid a potential floor effect in mood data because emotional stimuli were intermixed with neutral stimuli in either block. If old adults truly differ from young adults in susceptibility to positive or negative stimuli, the perceived frequency should be different across age groups. This method has been verified effective in reflecting group differences in susceptibility to emotional stimuli in our prior study (Yuan et al., 2009).

Lastly, in order to avoid cultural bias when International Affective Picture System (IAPS) was used directly in Chinese subjects (Huang and Luo, 2004), the pictures used to elicit emotional responses in the present study were selected from the native Chinese Affective Picture System (CAPS), which was established in a similar way to IAPS (Bai et al., 2005). According to the widely accepted dimensional theory of emotion, the affective significance of a stimulus is organized along the two primary dimensions: valence and arousal (Lang et al., 1997; Bradley et al., 2001). Intense emotional stimuli are normally accompanied by higher arousal in comparison with mildly emotional stimuli, irrespective of whether the stimuli are positive or negative (Bradley et al., 1990; Lang et al., 1997; Cuthbert et al., 2000; Keil et al., 2002; Kuppens et al., 2013). Thus, we predict that HP pictures would be rated more positive and more arousing than MP pictures; and HN pictures be rated more negative and more arousing than MN pictures.

#### Materials and Methods

#### Subjects

As paid volunteers, 17 young adults (age: 18–22; 8 females) and 17 old adults (age: 60–74; 9 females) in local community were randomly sampled for the experiment. The gender composition was not significantly different across the two samples [χ2 (1) = 0.118, *p* = 0.73]. All the subjects were right-handed and had no self-reported visual problems. As a final check of visual function, all the subjects read textual instructions on a computer screen at a distance of 2.5 m easily. In addition, both young and old adults were healthy, reporting no current symptoms and no history of anxious or depressive disorders. No subjects were taking medication that would affect the central nervous system. Each participant signed an informed consent form prior to the experiment. The experimental procedure was in accordance with the ethical principles of the 1964 Declaration of Helsinki (World Medical Organization [WHO], 1996). Prior to the experiment, the life satisfaction (LS) was assessed by the subjects answering "how is your life recently?" ranging from 1: very stressful; 3: ordinary to 5: very good. The scores of young adults were not significantly different from 3 [*t*(16) = 1.098, *p* = 0.289], while old adults' rating was higher than 3 [*t*(16) = 4.243, *p* = 0.001]. The LS was higher for old (4.055) relative to young adults [3.294; *t*(32) = –2.088, *p* = 0.045).

#### Stimulus Materials

The present study included two experimental blocks. Each block consisted of 168 pictures (grouped into three conditions). In the positive block, 168 pictures were grouped as HP, MP, or neutral. Like many other studies using IAPS, the pictures used for this study covered a variety of contents (Cuthbert et al., 2000; Smith et al., 2003), such as highly pleasant, mildly pleasant, or neutral animals (e.g., puppies, pandas, or wolfs), natural scenes (e.g., landscapes, seashores, or mountains) and human activity (e.g., cheers, sports, conversation). In the negative block, 168 pictures were grouped as HN, MN, or neutral; such as HN, MN, or neutral animals (e.g., snakes, bugs, or eagles), natural scenes (e.g., fire disaster, flood, clouds) and human activity (e.g., homicide, violence, or sports). All the 336 pictures were selected from the CAPS. In the positive block, the three sets of pictures differed significantly from one another in both valence [*F*(2,165) = 286.14, *p* < 0.001] and arousal [*F*(2,165) = 290.54, *p* < 0.001]. HP pictures were rated more positive than were MP pictures [*F*(1,110) = 86.62, *p* < 0.001] which, in turn, were rated positive compared with the Neutral pictures [*F*(1,110) = 121.63, *p* < 0.001]. Also, HP pictures were rated more arousing relative to MP pictures [*F*(1,110) = 98.76, *p* < 0.001] which, again, were rated more arousing than were Neutral stimuli [*F*(1,110) = 145.49, *p* < 0.001]. In the negative block, the three sets of pictures differed significantly from one another in valence [*F*(2,165) = 1348.33, *p* < 0.001] and arousal [*F*(2,165) = 615.69, *p* < 0.001]. HN pictures were rated more negative than were MN pictures [*F*(1,110) = 293.65, *p* < 0.001] which, in turn, were rated negative compared with the Neutral pictures [*F*(1,110) = 1337.01, *p* < 0.001]. Also, HN pictures were rated more arousing relative to MN pictures [*F*(1,110) = 273.37, *p* < 0.001] which, again, were rated more arousing than were Neutral pictures [*F*(1,110) = 379.2, *p* < 0.001, see **Figure 1**]. All the pictures were identical in size and resolution (15 cm × 10 cm, 100 pixels per inch). In addition, the luminance level of the pictures was tested prior to experiment, and the luminance level and spatial frequency were matched across the three conditions in each block. The contrast of the monitor was set to a constant value across subjects.

#### Behavioral Procedures