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The superior occipital gyrus is always well defined, and is continuous an anterior and a posterior part. The parieto-occipital and calcarine sulci
along the superomedial margin of the hemisphere with the cuneus. appear continuous on the surface, but when their borders are retracted
Superiorly, it is delimited by the depth of the parieto-occipital fissure it becomes obvious that they are separated by one or more small gyri.
on the superolateral hemispheric surface. It is continuous with the The anterior part of the calcarine sulcus is classified as a complete sulcus
superior parietal lobule through the parieto-occipital arcus (corre- because its depth creates an elevation (calcar avis) in the medial wall
sponding to the first or superior parieto-occipital ‘pli de passage’ of of the occipital horn of the lateral ventricle. The posterior part of the
Gratiolet). Laterally, the superior occipital gyrus may be delimited by calcarine sulcus is considered an axial sulcus, given that its axis runs
either the intra-occipital, transverse occipital or superior occipital along the visual cortex. Only the posterior part includes the primary
sulcus. visual cortical areas, which are located on its superior (cuneal) and
The inferior occipital gyrus lies horizontally along the inferolateral inferior (lingual) surfaces. This part of the calcarine sulcus frequently
margin of the hemisphere, with its base lying over the tentorium cere- harbours the cuneolingual gyrus that links both gyri.
belli. Anteriorly, it is usually continuous with the inferior temporal At the level of the occipital pole, the calcarine sulcus usually branches
gyrus; posteriorly, it extends medially around the occipital pole, becom- in a T or Y shape as the retrocalcarine sulcus. The gyrus descendens of
ing continuous with the lingual gyrus on the medial surface of the Ecker lies posterior to and along the retrocalcarine sulcus and is occa-


hemisphere. Superiorly, the inferior occipital gyrus is delimited by the sionally bounded posteriorly by the occipitopolar sulcus. The retrocal-
lateral or inferior occipital sulcus. carine sulcus and its variations are sometimes referred to as external
The lateral occipital sulcus is a very evident horizontal sulcus. Ante- calcarine sulci.
riorly, it is frequently connected to the inferior temporal sulcus; inferi- Given the anatomical constancy of the calcarine and parieto-occipital
orly, it may be accompanied by a shorter accessory lateral occipital fissures on the medial occipital surface, the cuneus (O) is always a
6
sulcus. Both of these sulci may be connected with a sulcal complex well-defined wedge-like convolution. The real anterior border of the
known as the anterior occipital sulcus, which, when present, lies along cuneus is the cuneal limiting sulcus within the parieto-occipital fissure.
the anterior aspect of the middle occipital gyrus. The inferior occipital Posteriorly, the cuneus rests over the posterior part of the calcarine
sulcus is sometimes described as a distinct and very small sulcus located sulcus and over the posterior aspect of the lingual gyrus. Superior to the
near the inferior margin of the inferior occipital gyrus, but here the posterior part of the calcarine sulcus, the cuneus harbours the paracal-
lateral and inferior occipital sulci are considered to be part of the same carine or cuneal sulcus (the inferior sagittal sulcus of the cuneus of
structure. Retzius) and, further dorsally, the occipital paramedial sulcus (the para-
The intraparietal sulcus extends longitudinally and inferiorly into mesial sulcus of Elliot Smith or superior sagittal sulcus of Retzius).
the occipital lobe, where it becomes the intra-occipital sulcus. The latter The basal or inferior surface of the occipital lobe is continuous with
may occasionally descend to the occipital pole but it usually terminates the basal surface of the temporal lobe. It is formed, from medial to


on reaching the transverse occipital sulcus, dividing it into lateral and lateral, by the lingual, fusiform and inferior occipital gyri respectively
medial parts that penetrate the superior occipital gyrus (see Fig. 25.17). (see Fig. 25.10B; Fig. 25.18). For details of the sulcal and gyral anatomy
Since the lateral (inferior) occipital sulcus is always present and clearly of the basal occipital-temporal lobe, see Chau et al (2014).
divides the superolateral occipital surface into an inferior part, consti- The lingual gyrus (medial temporo-occipital gyrus, O) lies inferiorly
5
tuted by the inferior occipital gyrus, and a superior part, it has been along the entire length of the calcarine sulcus, forming the mediobasal
suggested that the gyral pattern of the superior part depends mainly on portion of the occipital lobe. It is continuous anteriorly with the para-
the morphology of the lateral aspect of the transverse occipital sulcus. hippocampal gyrus and its basal surface rests on the tentorium cerebelli.
When this sulcal segment descends towards the occipital pole as an Posteriorly, it is frequently divided into a superior and inferior part by
inferior extension of the intra-occipital sulcus, it divides the upper an intralingual sulcus, which may be a posteromedial ramus of the
occipital convexity into superior and middle occipital gyri. The lunate collateral sulcus.
sulcus, although conspicuous in monkeys and apes, is only sometimes
identifiable in human brains, when it appears as a well-defined vertical
and backward-curved sulcus anterior to the occipital pole.
Despite significant anatomical variation, the superolateral occipital
Un
convolutions are connected to the parietal and temporal convolutions RhiS
by consistent cortical folds. According to the classic description by
Gratiolet, four folds connect the parietal and temporal lobes with the ITG
occipital lobe: the superior parieto-occipital fold (parieto-occipital
arcus) connects the superior parietal lobule with the superior occipital ColS


gyrus; the inferior parieto-occipital fold, a posterior extension of the
angular gyrus, connects with the middle occipital gyrus and occasion- FuG
ally also with the superior occipital gyrus; the first temporo-occipital PHG OTS
fold is the continuation of the middle temporal gyrus with the inferior
occipital gyrus; and the second temporo-occipital fold is the continua-
tion of the inferior temporal gyrus with the inferior occipital gyrus.
The medial surface of the occipital lobe shows less morphological
variation than the superolateral surface. It is separated from the parietal
IOG
lobe by the parieto-occipital sulcus and dominated by the calcarine ColS
sulcus. The dorsal part of this region, above the calcarine sulcus and
LiG
posterior to the parieto-occipital fissure, is the cuneus. The ventral part
of this region, lying below the calcarine sulcus and extending as far as
the occipital extension of the collateral fissure, is the lingual gyrus (see
Fig. 25.10B). The calcarine sulcus starts anteriorly underneath the sple- Fig. 25.18 The basal temporo-occipital surface. Abbreviations: ColS,
nium of the corpus callosum, delineating the inferior aspect of the collateral sulcus; FuG, fusiform gyrus; IOG, inferior occipital gyrus; ITG,
isthmus of the cingulate gyrus, and runs posteriorly just above the inferior temporal gyrus; LiG, lingual gyrus; OTS, occipitotemporal sulcus;
inferomedial margin of the hemisphere. The parieto-occipital fissure PHG, parahippocampal gyri; RhiS, rhinal sulcus; Un, uncus. (Adapted with
emerges superiorly from the calcarine sulcus, separates the cuneus from permission from Ribas GC. The cerebral sulci and gyri. Neurosurg Focus
the precuneus of the parietal lobe, and divides the calcarine sulcus into 2010, 28(2):E2.)


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matter, encounters neurones that all respond preferentially to either a surface lies over the floor of the middle cranial fossa posterior to the
stationary or a moving straight line of a given orientation within the greater wing of the sphenoid bone. The opercular surface lies inside the
visual field. Cells with simple, complex and hypercomplex receptive lateral fissure (see Figs 25.1, 25.9). Along the superolateral surface of
fields occur in area 17. Simple cells respond optimally to lines in a the hemisphere, the posterior limit of the temporal lobe is arbitrarily
narrowly defined position. Complex cells respond to a line anywhere defined by imaginary lines that run from the superomedial part of the
within a receptive field, but with a specific orientation. Hypercomplex parieto-occipital sulcus to the preoccipital notch or incisure, and by a
cells are similar to complex cells except that the length of the line or posterior prolongation of the lateral fissure. Functionally, the temporal
bar stimulus is also critical for an optimal response. There is a relation- lobe is bilaterally related with auditory functions and in the dominant
ship between the complexity of response and the position of cells in hemisphere mostly with the comprehension of language. (For further
relation to the cortical laminae. Simple cells are mainly in layer IV, and reading on the microsurgical anatomy of the temporal lobe, see Kucuky-
complex and hypercomplex cells predominate in either layers II and III uruk et al (2012).)
or layers V and VI.
The second visual area (V2) occupies much of area 18 but is not
Temporal lobe sulci and gyri
coextensive with it. It contains a complete retinotopic representation of
the visual hemifield, which is a mirror image of that in area 17, with
the vertical meridian represented most posteriorly along the border The lateral surface is composed of superior, middle and inferior tem-
between areas 17 and 18. The major ipsilateral corticocortical feed- poral gyri (T1, T2 and T3 respectively), separated by the superior and
forward projection to V2 comes from V1. Feed-forward projections from inferior temporal sulci and all lying parallel to the lateral fissure (see


V2 pass to several other visual areas (and are reciprocated by feedback Figs 25.1, 25.8). Anteriorly, the middle temporal gyrus is generally
connections), including the third visual area (V3) and its various sub- shorter; when this occurs, the superior and inferior gyri come together
divisions (V3/V3d; VP/V3v; V3a); the fourth visual area (V4); areas in to form the temporal pole (see Fig. 25.9B; Fig. 25.20A).
the temporal and parietal association cortices; and the frontal eye field.
Thalamic afferents to V2 come from the lateral geniculate nucleus, the
Temporal lobe internal structure
inferior and lateral pulvinar nuclei and parts of the intralaminar group
and connectivity
of nuclei. Additional subcortical afferents are as for cortical areas in
general. Subcortical efferents arise predominantly in layers V and VI.
They pass to the thalamus, claustrum, superior colliculus, pretectum, The superior, middle and inferior temporal gyri correspond to Brod-
brainstem reticular formation, striatum and pons. As for area 17, the mann’s areas 22, 21 and 20 respectively, and the temporal pole corre-
callosal connections of V2 are restricted predominantly to the cortex, sponds to area 38. The anterior transverse temporal gyrus and adjoining
which contains the representation of the vertical meridian. part of the superior temporal gyrus are auditory in function, and are
The third visual area (V3) is a narrow strip adjoining the anterior considered to be Brodmann’s area 42. The anterior gyrus is approxi-
margin of V2, probably still within area 18 of Brodmann. V3 has been mately area 41.
subdivided into dorsal (V3/V3d) and ventral (VP/V3v) regions on the The temporal operculum houses the primary auditory cortex, AI.
basis of its afferents from area V1, myeloarchitecture, callosal and asso- This is coextensive with the granular area 41 in the transverse temporal
ciation connections, and receptive field properties. The dorsal subdivi- gyri. Surrounding areas constitute auditory association cortex. The


sion receives from V1, whereas the ventral does not. Functionally, the primary auditory cortex is reciprocally connected with all subdivisions
dorsal part shows less wavelength selectivity, greater direction selectivity of the medial geniculate nucleus, and may receive additional thalamo-
and smaller receptive fields than does the ventral subdivision. Both cortical projections from the medial pulvinar. The geniculocortical
areas receive a feed-forward projection from V2 and are interconnected fibres terminate densely in layer IV. AI contains a tonotopic representa-
by association fibres. A further visual area, area V3a, lies anterior to the tion of the cochlea in which high frequencies are represented posteri-
dorsal subdivision of V3. It receives afferent association connections orly and low frequencies anteriorly. Single-cell responses are to single
from V1, V2, V3/V3d and VP/V3v, and has a complex and irregular tones of a narrow frequency band. Cells in single vertical electrode
topographic organization. All subdivisions project to diverse visual penetrations share an optimum frequency response.
areas in the parietal, occipital and temporal cortices, including V4, and The auditory cortex interconnects with prefrontal cortex, though the
to the frontal eye fields. projections from AI are small. In general, posterior parts of the opercu-
The fourth visual area, V4, lies within area 19 anterior to the V3 lum project to areas 8 and 9. Central parts project to areas 8, 9 and 46.
complex. It receives a major ipsilateral feed-forward projection from V2. More anterior regions project to areas 9 and 46, to area 12 on the orbital
Colour selectivity as well as orientation selectivity may be transmitted surface of the hemisphere, and to the anterior cingulate gyrus on the
to V4 and bilateral damage causes achromatopsia. V4 is more complex medial surface. Contralateral corticocortical connections are with the
than a simple colour discrimination area because it is also involved in same and adjacent regions in the other hemisphere. Onward connec-
the discrimination of orientation, form and movement. It sends a feed- tions of the auditory association pathway converge with those of the
forward projection to the inferior temporal cortex and receives a feed- other sensory association pathways in cortical regions within the supe-


back projection. It also connects with other visual areas that lie more rior temporal sulcus.
dorsally in the temporal lobe, and in the parietal lobe. Thalamocortical The posterior cortical area of the dominant hemisphere, Wernicke’s
connections are with the lateral and inferior pulvinar and the intra- area, is intrinsically related to the auditory cortex. It is particularly
laminar nuclei. Other subcortical connections conform to the general responsible for the comprehension of language but its stimulation
pattern for all cortical areas. Callosal connections are with the contra- causes speech arrest. Wernicke’s area is not well defined anatomically
lateral V4 and other occipital visual areas. but occupies mainly the posterior aspect of the superior temporal gyrus
Visual processing in inferior temporal and temporoparietal cortices and the basal aspect of the supramarginal gyrus. It may extend inferiorly
involves two parallel pathways (dorsal and ventral visual streams) that along the middle temporal gyrus and anteriorly to within 3 cm of the
emanate from the occipital lobe and are specialized for action and temporal pole (Ojemann et al 1989).
perception respectively (Goodale and Milner 1992, Goodale et al Evidence suggests that area 21, the middle temporal cortex, is
2005). The dorsal pathway, concerned primarily with visuospatial dis- polysensory in humans, and that it connects with auditory, somatosen-
crimination, projects from V1 and V2 to the superior temporal and sory and visual cortical association pathways. The auditory association
surrounding parietotemporal areas, and ultimately to area 7a of the areas of the superior temporal gyrus project in a complex ordered
parietal cortex; it mediates the sensory-motor transformations required fashion to the middle temporal gyrus, as does the parietal cortex. The
to enable visually guided actions directed at an object. The fourth visual middle temporal gyrus connects with the frontal lobe: the most poste-
area, V4, is a key relay station for the ventral stream of projections, rior parts project to posterior prefrontal cortex, areas 8 and 9, while
which is related to the perceptual identification of objects. Its connec- intermediate regions connect more anteriorly with areas 19 and 46.


tions pass sequentially along the inferior temporal gyrus in a feed- Further forwards, the middle temporal region has connections with
forward manner, from V4 to posterior, intermediate and then anterior, anterior prefrontal areas 10 and 46, and with anterior orbitofrontal
inferior temporal cortices. Ultimately, they feed into the temporal polar areas 11 and 14. The most anterior middle temporal cortex is connected
and medial temporal areas and so interface with the limbic system. with the posterior orbitofrontal cortex, area 12, and with the medial
surface of the frontal pole. Further forwards, this middle temporal
region projects to the temporal pole and the entorhinal cortex. Tha-
TEMPORAL LOBE lamic connections are with the pulvinar nuclei and the intralaminar
group. Other subcortical connections follow the general pattern for all
The lateral surface of the temporal lobe is inferior to the lateral fissure, cortical areas. Some projections (e.g. to the pons), particularly from
and lies beneath the squamous portion of the temporal bone. The basal anteriorly in the temporal lobe, are minimal. Physiological responses


Cerebral hemispheres
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SFS MeFS IHF SFG The superior temporal sulcus is well defined and deep. Typically, it
is interrupted and composed of up to four segments but it may be
continuous (Ochiai et al 2004). It terminates within the inferior pari-
etal lobule, posterior to the end of the lateral fissure, by trifurcating into
an ascending sulcal segment and an inferior branch that runs towards
MFG the occipital lobe. The superior temporal gyrus always continues poste-
MFS riorly to the supramarginal gyrus encircling the terminal portion of the
lateral fissure. The middle temporal gyrus is always connected to the
IFS angular gyrus beneath the distal and horizontal portion of the superior
FMaS IFG temporal sulcus. The inferior temporal gyrus is continuous posteriorly
Orb with the inferior occipital gyrus over the preoccipital notch. The inferior
temporal sulcus is usually discontinuous. Both superior and inferior
temporal sulci start at the most anterior aspect of the temporal pole
ARSyF and end posterior to the arbitrary border of the temporal lobe; both of
STG them have their depths directed towards the inferior or temporal horn
STS
of the lateral ventricle. Topographically, the depth of the posterior part
MTG of the superior temporal sulcus is particularly related to the ventricular
atrium.
ITS ITG
The basal surface of the temporal lobe is composed laterally by the
inferior surface of the inferior temporal gyrus and medially by the
anterior or temporal portion of the fusiform or lateral temporo-occipital
gyrus; the gyri are separated by the temporo-occipital sulcus. Medially,
A RhiS OrbS Un OrbGi TePo the fusiform gyrus is delimited by the collateral sulcus (inferior longi-
tudinal sulcus of Huschke), which separates it from the parahippocam-
OlfTr OlfBu IHF OlfS PostMedOrbLob pal gyrus of the limbic lobe (see Fig. 25.18). Short and secondary sulci
(fusiform sulci) are found within its surface. Although not extensive,
AntOrbG the fusiform gyrus has an anterior or temporal part, T (between the


4
LatOrbG OrbS inferior and parahippocampal gyri), and a posterior or occipital part,
PostOrbG O 4 (between the inferior occipital and lingual gyri). The anterior part
MedOrbG of the fusiform gyrus is typically curved or pointed, resembling an
TePo arrow; its anterior border usually lies close to the level of the cerebral
LG aR tOe lfStr ON peduncle. The temporal portion of the fusiform gyrus lies over the
posterior aspect of the floor of the middle fossa and the upper surface
AntPerfSubst HySta
MedOlfStr RhiS of the petrous part of the temporal bone. The occipital part of the fusi-
OptTr ITG form gyrus lies underneath the ventricular atrium.
MaBo PostPerfSubst Anterior to the fusiform gyrus, the collateral sulcus may be continu-
Un
OTS ous with the rhinal sulcus. Alternatively, and more frequently, these
OcN sulci are separated by the so-called temporolimbic passage. The rhinal
sulcus separates the entorhinal cortex of the uncus medially from the
neocortex of the temporal pole laterally.
FuG
The superior or opercular surface of the temporal lobe is formed by
the superior surface of the superior temporal gyrus, which lies within
the lateral fissure and is composed of multiple transverse gyri. One
B PHG IstSplBrSt ColS of these is the voluminous transverse gyrus. It originates around the
Fig. 25.20 A, An anterior view of cerebral hemispheres. B, A view of the midpoint of the superior temporal gyrus and is orientated diagonally
basal frontotemporal surface. Abbreviations: AntOrbG, anterior orbital towards the posterior vertex of the floor of the lateral fissure, with its
gyrus; AntPerfSubst, anterior perforated substance; ARSyF, anterior longest axis orientated towards the ventricular atrium. This gyrus, which
ramus or stem of lateral or Sylvian fissure; BrSt, brainstem (pons); ColS, may be single or double, is Heschl’s gyrus; it is bounded anteriorly by


collateral sulcus; FMaS, frontomarginal sulcus; FuG, fusiform gyrus; GRe, the first transverse sulcus and posteriorly by the more defined sulcus of
gyrus rectus; HySta, hypophysial stalk; IFG, inferior frontal gyrus; IFS, Heschl, and divides the temporal opercular surface into an anterior,
inferior frontal sulcus; IHF, interhemispheric fissure; Ist, isthmus of polar plane and a posterior, temporal plane. The sulcus acusticus, an
cingulate gyrus; ITG, inferior temporal gyrus; ITS, inferior temporal sulcus; infrequent, small superior extension of the superior temporal sulcus
LatOlfStr, lateral olfactory striae; LatOrbG, lateral orbital gyrus; MaBo, anterior to Heschl’s gyrus, indicates the anterior aspect of Heschl’s gyrus
mammillary body; MedOlfStr, medial olfactory striae; MedOrbG, medial on the superolateral surface of the temporal lobe. If the transverse
orbital gyrus; MeFS, medial frontal sulcus; MFG, middle frontal gyrus; temporal sulcus, which lies posterior to Heschl’s sulcus within the
MFS, middle frontal sulcus; MTG, middle temporal gyrus; OcN, temporal plane, reaches the lateral surface of the superior temporal
oculomotor nerve; OlfBu, olfactory bulb; OlfS, olfactory sulcus; OlfTr,
gyrus, it indicates the posterior aspect of Heschl’s gyrus. The transverse
olfactory tract; ON, optic nerve; OptTr, optic tract; Orb, orbital part of
gyrus of Heschl and the most posterior aspect of the superior temporal
inferior frontal gyrus; OrbGi, orbital gyri; OrbS, orbital sulcus; OTS,
gyrus correspond to the primary auditory cortex.
occipitotemporal sulcus; PHG, parahippocampal gyri; PostMedOrbLob,
The surface of the polar plane is composed of multiple transverse
posteromedial orbital lobule; PostOrbG, posterior orbital gyrus;
gyri directed obliquely towards the inferior part of the insular circular


PostPerfSubst, posterior perforated substance; RhiS, rhinal sulcus; SFG,
sulcus (inferior limiting sulcus) (Fig. 25.21A). The temporal plane is
superior frontal gyrus; SFS, superior frontal sulcus; Spl, splenium of
flat, perpendicular to the brain surface, and triangular in shape. Its
corpus callosum; STG, superior temporal gyrus; STS, superior temporal
sulcus; TePo, temporal pole; Un, uncus. (Adapted with permission from internal vertex corresponds to the posterior vertex of the base of the
Ribas GC. The cerebral sulci and gyri. Neurosurg Focus 2010, 28(2):E2.) lateral (Sylvian) fissure, at the point where the superior part of the
insular circular sulcus (superior limiting sulcus) meets the inferior part
of the insular circular sulcus (inferior limiting sulcus), lying immedi-
Ipsilateral corticocortical fibres pass from area 17 to a variety of ately over the atrium. The temporal plane is usually larger in the domi-
functional areas in areas 18 and 19 and in the parietal and temporal nant hemisphere, supposedly reflecting its association with language
cortices. Fibres from area 17 pass to area 18 (which contains visual areas functions (Geschwind and Levitsky 1968). Topographically, the oblique
V2, V3 and V3a); area 19 (which contains V4); the posterior intrapari- polar plane covers the insular surface, Heschl’s gyrus underlies the
etal and the parieto-occipital areas; and to parts of the posterior tem- opercular surface of the postcentral gyrus, and the flat surface of the
poral lobe, the middle temporal area and the medial superior temporal temporal plane underlies the opercular surface of the supramarginal
area. Subcortical efferents of the striate cortex pass to the superior col- gyrus.
liculus, pretectum and parts of the brainstem reticular formation. Pro-
jections to the striatum (notably the tail of the caudate nucleus) and to
the pontine nuclei are sparse. Geniculo- and claustrocortical projections


are reciprocated by prominent descending projections, which arise in
layer VI.


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reTpahC
SupLimS CInsS CS Fig. 25.21 The lateral (A) and anterior (B) surfaces
of the insula. Abbreviations: AntLimS, anterior
limiting sulcus; Ap, insular apex; CInsS, central
insular sulcus; CS, central sulcus; IFG, inferior
frontal gyrus; InfLimS, inferior limiting sulcus; ITG,
inferior temporal gyrus; LIG, long insular gyri;
MedOrbG, medial orbital gyrus; MFG, middle
frontal gyrus; MTG, middle temporal gyrus; PoPl,
polar plane of the opercular temporal surface;
PostOrbG, posterior orbital gyrus; SFG, superior
frontal gyrus; ShIG, short insular gyri; STG,
superior temporal gyrus; SupLimS, superior
limiting sulcus of insula; SyF, lateral or Sylvian
fissure; TrInsG, transverse insular gyrus. (Adapted
with permission from Ribas GC. The cerebral sulci
and gyri. Neurosurg Focus 2010, 28(2):E2.)
A AntLimS ShIG Ap InfLimS LIG
SFG
MFG
IFG
SyF
STG
MTG
ITG
B PostOrbG MedOrbG TrInsG PoPI AntLimS
of cells in this middle temporal region show convergence of different input from the anterior part of the superior temporal gyrus. The inferior
sensory modalities, and many neurones respond to faces. part receives visual input from the anterior area of the inferior temporal
The inferior temporal cortex, area 20, is a higher visual association cortex. Other ipsilateral connections are with the anterior insular, the
area. The posterior inferior temporal cortex receives major ipsilateral posterior and medial orbitofrontal, and the medial prefrontal cortices.
corticocortical fibres from occipitotemporal visual areas, notably V4. It The temporal pole projects onwards into limbic and paralimbic areas.
contains a coarse retinotopic representation of the contralateral visual Thalamic connections are mainly with the medial pulvinar nucleus and


field, and sends a major feed-forward pathway to the anterior part of with intralaminar and midline nuclei. Other subcortical connections
the inferior temporal cortex. The anterior inferior temporal cortex are as for the cortex in general, although some projections, such as that
projects on to the temporal pole and to paralimbic areas on the medial to the pontine nuclei, are very small. Physiological responses of cells in
surface of the temporal lobe. Additional ipsilateral association connec- this and more medial temporal cortex correspond particularly to behav-
tions of the inferior temporal cortex are with the anterior middle tem- ioural performance and to the recognition of high-level aspects of social
poral cortex, in the walls of the superior temporal gyrus, and with visual stimuli.
areas of the parietotemporal cortex. Frontal lobe connections are with The cortex of the medial temporal lobe includes major subdivisions
area 46 in the dorsolateral prefrontal cortex (posterior inferior tempo- of the limbic system, such as the hippocampus and entorhinal cortex.
ral) and with the orbitofrontal cortex (anterior inferior temporal). The Areas of neocortex adjacent to these limbic regions are grouped together
posterior area also connects with the frontal eye field. Reciprocal tha- as medial temporal association cortex.
lamic connections are with the pulvinar nuclei; the posterior part is Nuclei of the amygdala project to, and receive fibres from, neocorti-
related mainly to the inferior and lateral nuclei, and the anterior part cal areas, predominantly of the temporal lobe, and possibly inferior
to the medial and adjacent lateral pulvinar. Intralaminar connections parietal cortex. The density of these pathways increases towards the
are with the paracentral and central medial nuclei. Other subcortical temporal pole.
connections conform to the general pattern of all cortical regions. Cal-
losal connections are between corresponding areas and the adjacent
visual association areas of each hemisphere. INSULAR LOBE
The cortex of the temporal pole receives feed-forward projections
from widespread areas of temporal association cortex that are immedi- The insula forms the base of the Sylvian cistern and lies between the
ately posterior to it. The dorsal part receives predominantly auditory frontal and temporal lobes (see Fig. 25.21; Fig. 25.22).


Cerebral hemispheres
383.e1
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reTpahC
BoFo
AntLimS
Orb
CaN
Cl
IntCap
CS Ins
PoPl
Put
Tha
SupLimS
HeG
TePl
Atr
PaCLob
A
Fi
Ins
Tail Body Head
B Hippoc TempSt
Fig. 25.22 The temporal opercular surface, the insula and the temporal
stem, right side. A, View from above: the right frontal and occipital lobes
have been sectioned horizontally and their superior parts removed. B, The
hippocampus (Hippoc) lying along the temporal horn. Other abbreviations:
AntLimS, anterior limiting sulcus; Atr, atrium of lateral ventricle; BoFo,
body of fornix; CaN, caudate nucleus; Cl, claustrum; CS, central sulcus;
Fi, fimbria; HeG, Heschl gyrus; IntCap, internal capsule; Ins, insula; Orb,
orbital part of inferior frontal gyrus; PaCLob, paracentral lobule; PoPl,
polar plane of the opercular temporal surface; Put, putamen; SupLimS,
superior limiting sulcus of insula; TempSt, temporal stem; TePl, temporal
plane; Tha, thalamus. (Adapted with permission from Ribas GC. The
cerebral sulci and gyri. Neurosurg Focus 2010, 28(2):E2.)


Cerebral hemispheres
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Insular lobe sulci and gyri corpus callosum, frequently connecting with the medial aspect of the
superior frontal gyrus in its course. It is connected to the paracentral
lobule as it lies over the body of the corpus callosum; more posteriorly,
The insula has both lateral and anterior surfaces. The superior and
it is connected to the precuneus. Posterior to the splenium of the corpus
inferior limiting sulci are morphologically true sulci that delineate the
callosum, it narrows to become the isthmus, and continues to the
lateral insular surface from the frontoparietal operculum, the lateral
parahippocampal gyrus. Anteriorly and basally, the cingulate sulcus
insular surface and the temporal operculum (Türe et al 1999). The
may be continuous with the anterior paraolfactory sulcus under the
anterior limit of the insula is considerably deeper and morphologically
rostrum of the corpus callosum; when this occurs, the cingulate gyrus
characteristic of a true fissure or space and separates the anterior surface
is continuous with the paraolfactory or subcallosal gyri. The cingulate
of the insula from the fronto-orbital operculum. The upper half of the
sulcus may be double and parallel; the additional superior fold is the
fundus of the anterior limiting sulcus is separated from a true anterior
paracingulate sulcus.
recess of the lateral ventricle, anterior to the head of the caudate nucleus,
Anteriorly, the parahippocampal gyrus folds back on itself medially
by the fibres of the thin anterior limb of the internal capsule, whereas
to form the uncus, which is incorporated superiorly into the most
the fundus of the lower half continues to the ventral striatopallidal or
lateral aspect of the frontobasal region via a well-defined neural pedun-
anterior perforated substance region (Heimer 2003).
cle anterior to the inferior horn of the lateral ventricle (see Figs 25.18
and 25.20B). Along its axial extension, the basal and medial surface of


Insular lobe internal structure the parahippocampal gyrus curves laterally, forming a flat superior
and connectivity surface, the subiculum. The latter is slightly triangular with an anterior
vertex; it corresponds to the floor of the lateral part of the transverse
fissure. This portion of the transverse fissure harbours the so-called
Cytoarchitectonically, three zones are recognized within the insula.
lateral wing of the ambient cistern. Laterally, the parahippocampal
Anteriorly, and extending caudally into the central insula, the cortex is
gyrus is contiguous with the fusiform gyrus underneath the depths
agranular. It is surrounded by a belt of dysgranular cortex, in which
of the collateral sulcus. Posteriorly, it is continuous with the lingual
laminae II and III can be recognized, and this in turn is surrounded by
gyrus and the cingulate gyrus along its isthmus. Medially, it lies under
an outer zone of homotypical granular cortex that extends to the caudal
the thalamus along the choroidal fissure. Superiorly, it is attached
limit of the insula.
along the inferior aspect of the insular lobe via fibres that cover the
Thalamic afferents to the insula come from subdivisions of the
inferior horn.
ventral posterior nucleus and of the medial geniculate body, from the
The indusium griseum is a thin layer of grey matter lying over the
oral and medial parts of the pulvinar, the suprageniculate/nucleus limi-
corpus callosum and covered by medial and lateral longitudinal striae
tans complex, the mediodorsal nucleus and the nuclei of the intralami-
running within the callosal sulcus beneath each cingulate gyrus. Ante-
nar and midline groups. It appears that the anterior (agranular) cortex
riorly, the indusium griseum is connected to the paraterminal gyrus
is connected predominantly with the mediodorsal and ventroposterior
via the prehippocampal rudiment. Posteriorly, it circles the splenium
nuclei, while the posterior (granular) cortex is connected predomi-
of the corpus callosum and runs along the fasciolar gyrus on each


nantly with the pulvinar and the ventral posterior nuclei. The other
side.
nuclear groups appear to connect with all areas.
In the subcallosal area, the anterior and posterior paraolfactory gyri
Ipsilateral cortical connections of the insula are diverse. Somatosen-
lie anterior to the paraterminal gyrus, separated by the anterior paraol-
sory connections are with SI, SII and surrounding areas, and areas 5
factory sulcus. Anteriorly, a consistent fold connects the most basal
and 7b of the parietal lobe. The insular cortex also has connections with
portion of the cingulate gyrus with the gyrus rectus, encircling the pos-
the orbitofrontal cortex. Several auditory regions in the temporal lobe
terior end of the superior rostral sulcus, called the cingulate pole
interconnect with the posterior granular insula and the dysgranular
(Yasargil 1994). The paraterminal gyrus lies on the medial wall of the
cortex more anteriorly. Connections with visual areas are virtually
cerebral hemisphere posterior to the paraolfactory gyri, immediately
absent. The anterior agranular cortex of the insula appears to have con-
facing the lamina terminalis, and delineated anteriorly by the short,
nections primarily with olfactory, limbic and paralimbic structures,
vertical posterior olfactory sulcus. Inferiorly, the paraterminal gyrus
including, most prominently, the amygdala.
extends along the diagonal band of Broca and the lateral olfactory
The insula receives somatosensory, viscerosensory, homeostatic and
stria.
nociceptive information from the entire body. (For a discussion of the
The choroidal fissure extends between the entire fornix and thala-
role of the operculo-insular region in the processing of somatosensory
mus, from the inferior choroidal point between the head and the body
inputs, see Mazzola et al (2012).)
of the hippocampus to the interventricular foramen. Anterior to the
inferior choroidal point (the point at which the anterior choroidal
artery enters the temporal pole of the lateral ventricle (Tubbs et al


LIMBIC LOBE 2010)), the anterior and mesial parts of the temporal lobe and the
parahippocampal gyrus merge with the basal and lateral aspect of the
Limbus means edge or border; the descriptive term limbic was first used frontal lobe through a neural peduncle that constitutes the so-called
in the sixteenth century (Morgane and Mokler 2006), but is more temporal stem (see below). Posterior to the inferior choroidal point,
usually associated with Broca, who described the cingulate and parahip- the choroidal fissure lies within the inferior horn between the fimbria
pocampal gyri as the greater limbic lobe, and considered the different of the fornix and the inferior aspect of the thalamus, along the parape-
sulci that limited these two gyri as parts of a single sulcus that he called duncular space that harbours the ambient cistern. More posteriorly, the
the limbic sulcus (Broca 1877). On phylogenetic grounds, Broca con- choroidal fissure within the atrium lies between the crura and the pul-
sidered that these structures might be associated with olfaction and for vinar, lateral to the quadrigeminal or pineal cistern. More superiorly
many years the term rhinencephalon (‘smell brain’) was used synony- and anteriorly, the choroidal fissure lies between the body of the fornix
mously with limbic lobe; the term is no longer used. and the superior surface of the thalamus.
The limbic lobe contains the cortical structures on the most medial The collateral sulcus is a long, deep sulcus that extends along the
edge of the hemisphere and includes the cingulate, parahippocampal basal temporal and occipital surface, with multiple side branches. Its
and dentate gyri, the cingulate isthmus, the subcallosal area (paraolfac- temporal segment bulges into the ventricular floor as the collateral
tory and paraterminal gyri), the collateral and rhinal sulci, the uncus eminence, located lateral to the hippocampus. Its occipital segment
and the hippocampal formation. (The Terminologia Anatomica restricts corresponds to the collateral trigone that forms the triangular, flat


the hippocampal representation in the limbic lobe to the fimbria of the surface of the ventricular atrium and posterior horn. The rhinal sulcus,
hippocampus; other authors include the hippocampal formation (e.g. which is not always readily identifiable, separates the uncus from the
Chronister and Hardy 2006).) rest of the temporal pole. The subcallosal, cingulate, subparietal, ante-
rior calcarine, collateral and rhinal sulci are frequently considered to
form the limbic fissure.
Limbic lobe sulci and gyri
Uncus
Within the inner aspect of the medial surface of each cerebral hemi- The uncus is triangular. It has a medial vertex; its anteromedial surface
sphere, the cingulate gyrus wraps around the corpus callosum and faces the carotid cistern and its posteromedial surface faces and encir-
continues posteriorly and inferiorly to the parahippocampal gyrus (see cles the mesencephalic peduncle (see Fig. 25.18). The semilunar gyrus,
Fig. 25.10B). Lying above the callosal sulcus and below the cingulate a lateral extension of the lateral olfactory stria, and the ambient gyrus
sulcus, the cingulate gyrus starts within the subcallosal area below form two small prominences on its medial and anterior surface. Both
the rostrum of the corpus callosum and ascends around the genu of the gyri cover the amygdala and are separated by the semi-annular sulcus,


Cerebral hemispheres
384.e1
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The anterior surface of the insula is covered by the fronto-orbital
operculum (the posterior portion of the posterior orbital gyrus and the
orbital part of the inferior frontal gyrus). Its lateral surface is covered
superiorly by the frontoparietal operculum (triangular and opercular
parts of the inferior frontal gyrus, subcentral gyrus, and anterior and
basal part of the supramarginal gyrus) and inferiorly by the temporal
operculum (polar plane of the superior temporal gyrus; see Fig. 25.14).
The lateral surface of the insula may be conceptualized as a pyramid
with a triangular base; its anteroinferior vertex is the limen insulae and
its summit is the insular apex. The limen insulae consists of a narrow
strip of olfactory cortex that extends along the lateral aspect of the
lateral olfactory stria, conjoining the insular cortex and anterior perfo-
rated substance. The surface of the insula is divided into anterior and
posterior parts by a deep central sulcus that courses obliquely from the
limen insulae towards the central sulcus of the cerebral hemisphere. The
anterior part of the insular surface is composed of transverse, accessory
and short insular gyri (anterior, middle and posterior short insular gyri),
all arising from the region of the insular apex. The middle and posterior
short insular gyri are separated by the precentral insular sulcus.
The transverse insular gyrus runs along the limen insulae, connecting
the anterior insula with the posteromedial orbital lobule. The latter is
the connection between the posterior portion of the medial orbital
gyrus and the posterior orbital gyrus, and is located anterior to and
along the lateral olfactory stria. The accessory gyrus extends from the
anterior portion of the anterior short gyrus superiorly to the transverse
insular gyrus, beneath the fronto-orbital operculum. Both gyri consti-
tute the insular pole within the anterior aspect of the insula (Türe et al
1999, Türe et al 2000). The posterior part of the insula is located behind


its central sulcus and is composed of anterior and posterior insular long
gyri. Both of these gyri are separated by the postcentral insular sulcus;
the anterior long gyrus is usually larger, and may be single and divided
at its upper end.
The insular surface is delineated peripherally by the peri-insular
sulcus (circular sulcus of Reil), which is interrupted by the transverse
insular gyrus running across the limen insulae. Given the triangular
shape of the insula, the peri-insular sulcus is usually divided into three
parts, variously named either as the anterior, superior and inferior peri-
insular sulci (Türe et al 1999), or the anterior, superior and inferior
limiting sulci of the insula (Rhoton 2003).


Cerebral lobes
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52
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which harbours the anterior choroidal artery. Inferiorly, the free edge the fornix by the fimbriodentate sulcus lying parallel to the hippocam-
of the tentorium cerebelli is frequently associated with another depres- pal sulcus (Fig. 25.26).
sion. The most rostral and anterior aspects of the uncus correspond to The main outflow bundle of the hippocampus, the fornix, wraps
the entorhinal cortex. The posterior half of the uncus contains the head round the thalamus, from which it is separated by the choroidal fissure
of the hippocampus and is separated inferiorly from the parahippo- and the choroid plexus (see Fig. 25.3). It has several named parts:
campal gyrus by the uncal sulcus. The medial surface of the uncus faces fimbria, crus, body and column (pillar). The fibres of the alveus con-
the crural cistern. Its inferior surface is hidden inside the uncal sulcus, verge to form the fimbria along the medial portion of the floor of the
in which the posterior half of the uncus harbours the uncinate gyrus inferior horn of the lateral ventricle. At a point beneath the splenium
anteriorly and the uncal apex (intralimbic gyrus, hippocampus inver- of the corpus callosum, the white matter of the fimbria separates from
sus) posteriorly, separated by the band of Giacomini. Collectively, these the hippocampus to become the crus of the ipsilateral fornix. The two
structures correspond to the extraventricular part of the head of the crura pass upwards and forwards beneath the corpus callosum, mirror-
hippocampus. The band of Giacomini corresponds to the tail of the ing its arch but with a tighter curve. They are joined via fibres that cross
dentate gyrus, which vanishes on the medial aspect of the uncus. Along in the commissure of the fornix (hippocampal commissure). Beyond
the cerebral base, the parahippocampal gyrus is delineated laterally by this point, the crura merge to become the body of the fornix, which


the collateral sulcus, separating it from the fusiform gyrus, and more continues anteriorly within the roof of the third ventricle, below the
anteriorly by the rhinal sulcus, which is occasionally continuous with lower border of the septum pellucidum and near the midline (Figs
the collateral sulcus. 25.27–25.28). At the level of the interventricular foramen (foramen of
Munro) and the anterior commissure, the most anterior segment of the
Hippocampus
body diverges from its contralateral counterpart, and passes in an ante-
The hippocampus (hippocampus proper, cornu ammonis, Ammon’s rior, lateral and inferior direction as the column (pillar) of the fornix
horn) is a convex elevation, approximately 5 cm long, within the para- to penetrate the hypothalamic parenchyma towards the ipsilateral
hippocampal gyrus inside the inferior (temporal) horn of the lateral mammillary body. As they separate from the underlying thalamus, the
ventricle (Duvernoy 1998) (Figs 25.23–25.24). Macroscopically, it can columns of the fornix form the anterior margins of the interventricular
be divided into a head, a body and a tail (see Fig. 25.22B). Anteriorly, foramen.
the head is expanded and bears two or three shallow grooves (pes hip-
pocampi). The surface of the hippocampus, the alveus, is covered by Limbic lobe internal structure
the ependyma inside the ventricular cavity.
and connectivity
The dentate gyrus consists of small cortical prominences that form
a chain along the medial aspect of the hippocampus (Fig. 25.25). Along
Cingulate and parahippocampal cortex
its medial margin, it is separated from the subiculum of the parahip-
pocampal gyrus by the hippocampal sulcus, usually a shallow sulcus The cingulate gyrus may be divided rostrocaudally into several cytoar-
that terminates anteriorly within the uncus (see Fig. 25.23). More supe- chitectonically discrete areas: prelimbic (area 32) and infralimbic


riorly and medially, the dentate gyrus is separated from the fimbria of (area 25) cortices, anterior cingulate cortex (areas 23, 24, 32 and 33)
A B C
Hippocampal sulcus Fimbria
Dentate gyrus
Hippocampus
(cornu ammonis)
Subiculum
Parahippocampal
gyrus
Collateral sulcus Inferior horn of lateral ventricle
Fig. 25.23 A series of coronal sections of the temporal lobe and inferior horn of the lateral ventricle illustrating the relationships between the components
of the hippocampal formation.
Fig. 25.24 A dissection of the left cerebral
hemisphere demonstrating components of the
limbic system. The body of the corpus callosum
has been divided sagittally; the left frontal,
temporal and occipital lobes have been sectioned
horizontally and their superior parts removed. The
left lentiform complex and thalamus have been
Corpus callosum removed and the floor of the inferior horn of the
lateral ventricle opened. (Dissection by AM Seal;
Caudate nucleus photograph by Kevin Fitzpatrick on behalf of GKT
Fornix
School of Medicine, London; figure enhanced by
Anterior perforated Thalamus B Crossman.)
substance
Fimbria
Anterior commissure
Mammillary body
Pes hippocampi Hippocampus


Cerebral hemispheres
385.e1
52
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CiG StTerm Fo AntCom
A Tha Hypothal MaThTr MaBo
CI Put AntCom CC Fo SeptPell Ro Ge Sept
B VeStrPa LamTer ON
Fig. 25.27 The fornix and related structures, right side of the brain.
A, Medial structures after the removal of the corpus callosum, disclosing
neural structures related to limbic circuits. B, The ventral striatopallidal
region (VeStrPa) inferior and anterior to the anterior commissure
(AntCom). The septal region (Sept) lies anterior to the anterior commissure
and posterior to the cingulate pole. The column of the fornix (Fo) runs
posterior to the anterior commissure. Other abbreviations: CC, corpus
callosum; CiG, cingulate gyrus; Cl, claustrum; Ge, genu of corpus
callosum; Hypothal, hypothalamus; LamTer, lamina terminalis; MaBo,
mammillary body; MaThTr, mammillothalamic tract; ON, optic nerve; Put,
putamen; SeptPell, septum pellucidum; Ro, rostrum of corpus callosum;
StTerm, stria terminalis; Tha, thalamus. (Dissection courtesy of Professor
Guilherme Ribas.)


Cerebral hemispheres
386
3
NOiTCes
and part of the posterior cingulate or retrosplenial cortex (area 29) nections with the entorhinal cortex. Projections between the paralimbic
(Commentary 3.1). area 32 and the limbic cortex (anterior, retrosplenial and entorhinal
The cingulate gyrus contains specific motor areas and has extensive cortex) are somewhat less prominent. Areas 24 and 29 are connected
connections with neocortical areas of the frontal lobe and with soma- with the paralimbic posterior cingulate area 23. In primates, the para-
tosensory and visual association areas of the parietal, occipital and hippocampal gyrus projects to virtually all association areas of the
temporal lobes. The afferents to the cingulate gyrus are predominantly cortex; it also provides the major funnel through which polymodal
from neocortical areas on the lateral surface of the hemisphere. Within sensory inputs converge on the hippocampus.
the cingulate cortex, most projections pass caudally, ultimately into the
Hippocampal cortex
parahippocampal gyrus. Through this system, afferents from wide-
spread areas of association cortex converge on the medial temporal lobe The hippocampus is composed of trilaminar archicortex: a single
and hippocampal formation. There are parallel stepwise routes to these layer of pyramidal cells sandwiched between plexiform layers. It is
targets through cortical areas on the lateral surface. The anterior cingu- divided into three distinct fields: CA1, CA2 and CA3 (see Fig. 25.26;
late gyrus appears to be a component of a functional circuit that medi- Fig. 25.29).
ates pain perception and processing. The cingulate motor cortex Field CA3 borders the hilus of the dentate gyrus at one end, and field
subregion of the anterior cingulate gyrus is one of the first cortical brain CA2 at the other. Field CA3 pyramidal cells are the largest in the hip-
regions activated in pain processing; its probable function is to mediate pocampus and receive the mossy fibre input from dentate granule cells


withdrawal actions and so minimize further injury. (For further reading, on their proximal dendrites. The whole pyramidal cell layer in this field
see Weston (2012).) The insula has strong functional connections with is about 10 cells thick. The border between CA3 and CA2 is not well
anterior and dorsal subregions of the anterior cingulate gyrus (areas 24 marked. The CA2 field has the most compact layer of pyramidal cells.
and 32),
The parahippocampal gyrus includes areas 27, 28 (entorhinal
cortex), 35, 36, 48 and 49, and temporal cortical fields. It has complex
Fimbria Alveus
interconnections with the cingulate cortex and with the hippocampal
formation. In monkeys, the infralimbic cortex (area 25) has been
shown to project to areas 24a and 24b. Area 25 also has reciprocal con- Fimbriodentate Cornu Stratum oriens
sulcus a m
CA2
monis Stratum pyramidalis
CA3 Stratum radiatum
Olfactory tract
CA4 CA1 Stratum lacunosum
Tail of dentate
Hippoc sa um lcp ua sl Dentategyrus
Infundibulum gyrus Stratum moleculare
Oculomotor nerve I on ft r ua nli cm ub sic gyrus
mulucibuS
Mammillary bodies Dentate gyrus P
re
s
u
Fimbria
biculu
m
Midbrain ML ba
o
et
d
de
y
ir aa ll gg ee nn ii cc uu ll aa tt ee Parasubiculum
Parahippocampalgyrus
body
Tela choroidea Pulvinar
Splenium of corpus Dentate gyrus Entorhinal cortex
callosum
Hippocampus (cornu ammonis) Parahippocampal gyrus
Fig. 25.25 The basal aspect of the brain dissected to display the dentate Fig. 25.26 The hippocampal formation showing the disposition of the
gyrus, uncus and fimbria on the left. various cell fields.
Stria medullaris thalami Cingulate gyrus and cingulum Fig. 25.28 Components of the limbic system


(yellow). The medial aspect of the left cerebral
Indusium griseum and hemisphere. The approximate locations of some
Body of fornix longitudinal striae Brodmann’s areas are indicated.
Septum pellucidum
Dorsal fornix 24 (supracommissural
septum)
23
Mammillothalamic Anterior nuclear
tract group of thalamus
Mammillotegmental 32
tract Anterior commissure
29
Isthmus 25 Paraterminal gyrus
(precommissural
Gyrus fasciolaris septum)
Prehippocampal
Fimbria of fornix
rudiment
Stria terminalis 28 Paraolfactory area
Hippocampus Olfactory bulb
Dentate gyrus
Column of fornix
(postcommissural
Amygdala Uncus fornix)
Brainstem Parahippocampal Mammillary body
gyrus


limbic system
387
52
reTpahC
CA2
d
e
CA3 f
fim g
CA1
DG c
a b
PrS
PaS S
PRC
EC
2 mm
Fig. 25.29 A coronal, thionin-stained section of the human hippocampal
formation. Abbreviations: a, molecular layer of the dentate gyrus; b,
granule cell layer of the dentate gyrus; c, plexiform layer of the dentate
gyrus; CA1–3, fields of the hippocampus; d, stratum oriens layer of
Pyramidal neurones of the cornu ammonis and their axons, which
the hippocampus; DG, dentate gyrus; e, pyramidal cell layer of the
form the efferent hippocampal fibres of the alveus and fimbria
hippocampus; EC, entorhinal cortex; f, stratum radiatum of the
hippocampus; fim, fimbria; g, stratum lacunosum-moleculare of Afferent fibres to the cornu ammonis from the fimbria
the hippocampus; PaS, parasubiculum; PRC, perirhinal cortex;
PrS, presubiculum; S, subiculum. (Courtesy of D Amaral.) Afferent fibres from the entorhinal cortex via the perforant path
Basket neurones
It completely lacks a mossy fibre input from dentate granule cells Neurones of the dentate gyrus and their axons,
and receives a major input from the supramammillary region of the which form the mossy fibres of the hippocampus
hypothalamus. Field CA1 is usually described as the most complex of
Subicular efferent fibres to the fornix via the alveus
the hippocampal subdivisions and its appearance varies along its trans-
verse and rostrocaudal axes. The CA1/CA2 border is not sharp, and at Fig. 25.30 The neuronal organization and connections of the dentate
its other end CA1 overlaps the subiculum for some distance. Approxi- gyrus, hippocampus (cornu ammonis), subiculum and parahippocampal
mately 10% of neurones in this field are interneurones. gyrus.


It is common to describe several strata within the layers of the hip-
pocampus. Working from the ventricular aspect, these are the alveus
(contains subicular and hippocampal pyramidal cell axons converging
components has always rendered it anatomically and functionally dif-
on the fimbria of the fornix); stratum oriens (mainly the basal dendrites
ficult to dissect. Although much of the earliest research was necessarily
of pyramidal cells and some interneurones); stratum pyramidalis;
undertaken in non-human primates, cats and rodents, the use of non-
stratum lucidum (contains mossy fibres that make contact with the
invasive imaging, deep-brain stimulation and clinical behavioural
proximal dendrites of pyramidal cells in field CA3); stratum radiatum;
studies is enabling detailed analyses of the human limbic system in
and stratum lacunosum-moleculare. The stratum lucidum is not as
both normal and pathological states.
prominent in humans as it is in other primates, and is not present in
Most descriptions of the limbic system include the structures within
fields CA1 and CA2.
the limbic lobe; the amygdaloid nuclear complex; various nuclei of the
In the stratum radiatum and stratum oriens, CA3 and CA2 cells
hypothalamus, particularly those associated with the mammillary
receive associational connections from other rostrocaudal levels of the
body; the septal nuclei; nucleus accumbens; cingulate cortex; major
hippocampus, as well as afferents from subcortical structures, such as
areas of the prefrontal cortex habenula; anterior thalamic nuclei; parts
the septal nuclei and supramammillary region. The projections from
of the basal ganglia; ventral tegmental area; and limbic midbrain areas,
pyramidal cells of fields CA3 and CA2 to CA1, often called Schaffer
including the periaqueductal grey (Morgane and Mokler 2006). The
collaterals, also terminate in the stratum radiatum and stratum oriens.
term ‘limbic brain’ encompasses all of these structures and their projec-
The projections from the entorhinal cortex to the dentate gyrus (the


tions to forebrain, midbrain, lower brainstem and spinal cord limbic
perforant pathway) travel in the stratum lacunosum-moleculare, where
systems, principally via the fornix, stria terminalis, ventral amygdalo-
they make synaptic contact en passant with the distal apical dendrites
fugal pathway and the mammillothalamic tract. The appropriateness of
of hippocampal pyramidal cells.
continuing to regard the limbic system as the sole theoretical framework
The trilaminar cortex of the dentate gyrus is the least complex of the
for emotional functions has been questioned (Heimer and van Hoesen
hippocampal fields (see Fig. 25.29). Its major cell type is the granule
2006, Heimer 2008). (Seminal studies by Papez (1937), Klüver and
cell, found in the dense granule cell layer. Granule cells have unipolar
Bucy (1937) and Nauta (1958) document the development of ideas
dendrites that extend into the overlying molecular layer. The latter
about the limbic system.)
receives most of the afferent projections to the dentate gyrus, primarily
from the entorhinal cortex (Fig. 25.30). The granule cell and molecular
Hippocampal formation
layers are sometimes referred to as the fascia dentata. The polymorphic
layer, or hilus of the dentate gyrus, contains cells that give rise primarily
to ipsilateral association fibres. They remain within the dentate gyrus The hippocampal formation includes the dentate gyrus, hippocampus
and do not extend into other hippocampal fields. proper, subicular complex (subiculum, presubiculum, parasubiculum)
and entorhinal cortex (area 28). Passing medially from the collateral
sulcus, the neocortex of the parahippocampal gyrus merges with the
LIMBIC SYSTEM
transitional juxtallocortex of the subiculum (see Fig. 25.23). The latter
curves superomedially to the inferior surface of the dentate gyrus, then
The limbic system is an extended neural network that is concerned with laterally to the laminae of the hippocampus. This curvature continues,


emotional and motivational activity and other basic psychological func- first superiorly, then medially above the dentate gyrus, and ends point-
tions such as memory and learning. The complex connectivity of its ing towards the centre of the superior surface of the dentate gyrus.


Cerebral hemispheres
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Glutamate and/or aspartate appears to be the major excitatory trans- The entorhinal cortex is divisible into six layers and is quite distinct
mitter in three pathways in the hippocampal formation: namely, the from other neocortical regions. Layer I is acellular and plexiform. Layer
perforant pathway, which arises in the entorhinal cortex and terminates II is a narrow cellular layer, which consists of islands of large pyramidal
primarily in the dentate gyrus; the mossy fibres, which run from the and stellate cells. These cell islands are a distinguishing feature of the
dentate granule cells to the pyramidal cells of the CA3 field; and in the entorhinal cortex. They form small bumps on the surface of the brain
Schaffer collaterals of CA3 pyramidal cells, which terminate on CA1 that can be seen by the naked eye (verrucae hippocampi) and provide
pyramidal cells. GABAergic neurones are found in the deep portions of an indication of the boundaries of the entorhinal cortex. Layer III con-
the granule cell layer in the dentate gyrus (basket cells). sists of medium-sized pyramidal cells. There is no internal granular
The highest concentration of GABA receptors is found in the molecu- layer (another classic feature of entorhinal cortex); in its place is an
lar layer of the dentate gyrus. In the hippocampus proper, GABAergic acellular region of dense fibres called the lamina dissecans, which is
cells are found mostly in the stratum oriens, but also in the pyramidal sometimes called layer IV. Layers III and V are apposed in regions where
cell layer and stratum radiatum. the lamina dissecans is absent. Layer V consists of large pyramidal cells
There are many peptide-containing neurones in the hippocampal five or six deep. Layer VI is only readily distinguishable from layer V
formation. Granule cells in the dentate gyrus appear to contain the close to the border with the perirhinal cortex. Its cells continue around
opioid peptide dynorphin, which is also present in mossy fibres running the angular bundle (subcortical white matter deep to the subicular


to the CA3 field. Enkephalin, or a related peptide, may be present in complex made up largely of perforant path axons) to lie beneath the
fibres arising in the entorhinal cortex. There is a dense plexus of pre- and parasubiculum.
somatostatin-immunoreactive fibres in the molecular layer of the The entorhinal cortex has reciprocal connections with the hippo-
dentate gyrus and also in the stratum lacunosum-moleculare of the campus and neocortical regions. It receives afferents from many areas,
hippocampus. The polymorphic layer of the dentate gyrus, stratum including the parahippocampal gyrus and dorsal bank of the superior
oriens of the hippocampus and the deep layers of the entorhinal temporal gyrus, and perirhinal (Brodmann’s area 35), temporal polar,
cortex all contain somatostatin-immunoreactive neurones. VIP- agranular insular, posterior orbitofrontal, dorsolateral prefrontal
immunoreactive neurones are plentiful in many hippocampal fields, (Brodmann’s areas 9, 10, 46), medial frontal (Brodmann’s areas 25, 32),
especially in the superficial layers of the entorhinal cortex. Cells con- cingulate (Brodmann’s areas 23, 24) and retrosplenial cortices. It
taining CCK immunoreactivity are found in the hilar region of the projects to the perirhinal and temporal polar cortices and the caudal
dentate gyrus, in all layers of the hippocampus, especially in the pyrami- parahippocampal and cingulate gyri. Evidence from clinical and animal
dal cell layer, and also throughout the subicular complex and entorhi- studies suggests that the entorhinal cortex plays an essential role within
nal cortex. There are also substantial plexuses of CCK-immunoreactive a frontotemporal cortical memory network (Takehara-Nishiuchi 2014).
fibres in the stratum lacunosum-moleculare, subicular complex and
entorhinal cortex. Hippocampal CCK-immunoreactive cells may give Septum
rise to extrinsic projections, e.g. to the lateral septum and medial mam-


millary nucleus, because CCK-immunoreactive fibres are found in the
The septum is a midline and paramedian structure (see Fig. 24.6). Its
fimbria/fornix.
upper portion corresponds largely to the bilateral laminae of fibres,
The medial septal complex and the supramammillary area of the
sparse grey matter and neuroglia known as the septum pellucidum,
posterior hypothalamus are the two major sources of subcortical affer-
which separates the lateral ventricles (see Fig. 25.28). Below this, the
ents to the hippocampal formation. There are also projections from the
septal region is made up of four main nuclear groups: dorsal, ventral,
amygdaloid complex and claustrum (to the subicular complex and
medial and caudal. The dorsal group is essentially the dorsal septal
entorhinal cortex), as well as monoaminergic projections from the
nucleus, the ventral group consists of the lateral septal nucleus, the
ventral tegmental area, the mesencephalic raphe nuclei and the locus
medial group contains the medial septal nucleus and the nucleus of the
coeruleus. The noradrenergic and serotoninergic projections reach all
diagonal band of Broca, and the caudal group contains the fimbrial and
hippocampal fields but are especially dense in the dentate gyrus. Neu-
triangular septal nuclei.
rones in the supramammillary area project to the hippocampal forma-
The major afferents to the region terminate primarily in the lateral
tion via the fornix and a ventral route; they terminate most heavily in
septal nucleus. They include fibres carried in the fornix that arise from
the dentate gyrus and fields CA2 and CA3 of the cornu ammonis. All
hippocampal fields CA3 and CA1 and the subiculum, and afferents
divisions of the anterior thalamic nuclear complex and associated
arising from the preoptic area, anterior, paraventricular and ventrome-
lateral dorsal nucleus project to the hippocampal formation, predomi-
dial hypothalamic nuclei, and the lateral hypothalamic area. The lateral
nantly to the subicular complex. Some midline thalamic nuclei, particu-


septum receives a rich monoaminergic innervation, including noradren-
larly the parataenial, central medial and reuniens nuclei, project
ergic afferents from the locus coeruleus and medullary cell groups (A1,
especially to the entorhinal cortex.
A2), serotoninergic afferents from the midbrain raphe nuclei, and
dopaminergic afferents from the ventral tegmental area (A10).
Subicular complex Efferents from the lateral septum project to the medial and lateral
The subicular complex is generally subdivided into subiculum, pre- preoptic areas, anterior hypothalamus, supramammillary and midbrain
subiculum and parasubiculum. The subiculum consists of a superficial ventral tegmental area, via the medial forebrain bundle, and to the
molecular layer containing apical dendrites of subicular pyramidal cells, medial habenular nucleus and some midline thalamic nuclei via
a pyramidal cell layer and a deep polymorphic layer. The presubiculum, the stria medullaris thalami. The projections from the habenula via the
lying medial to the subiculum, is distinguished by a densely packed fasciculus retroflexus to the interpeduncular nucleus and adjacent
superficial layer of pyramidal cells and forms the boundary between the ventral tegmental area in the midbrain provide a route through which
subicular complex and the entorhinal cortex. The cell layers deep to forebrain limbic structures influence midbrain nuclear groups.
the parasubiculum are indistinguishable from the deep layers of the Efferents from the medial septal and vertical limb nuclei of the
entorhinal cortex. diagonal band travel via the dorsal fornix, fimbria, supracallosal striae
The major subcortical projections of the hippocampal formation, to and a ventral route through the amygdaloid complex. While these pro-
the septal nucleus, lateral and medial mammillary nuclei, nucleus jections reach all hippocampal fields, the most prominent terminations
accumbens, anterior thalamus and entorhinal cortex, all arise from are in the dentate gyrus, field CA3, presubiculum, parasubiculum and


pyramidal neurones of the subicular complex. The presubiculum, in entorhinal cortex. Many are GABAergic or cholinergic.
particular, projects to the anterior thalamic nuclear complex (antero-
medial, anteroventral and laterodorsal nuclei). The subicular complex Amygdala
receives numerous direct cortical inputs, e.g. from the temporal polar,
perirhinal and dorsolateral cortices and the parahippocampal and supe-
The amygdala (amygdaloid nuclear complex) consists of lateral, central
rior temporal gyri.
and basal nuclei lying in the dorsomedial temporal pole, anterior to
the hippocampus, close to the tail of the caudate nucleus and partly
Entorhinal cortex
deep to the gyrus semilunaris, gyrus ambiens and uncinate gyrus (Figs
The entorhinal cortex is the most posterior part of the piriform cortex 25.31–25.32; see Fig. 25.28). Collectively, the nuclei form the ventral,
and is divided into medial and lateral areas (Brodmann’s areas 28a and superior and medial walls of the tip of the inferior horn of the lateral
28b). It extends rostrally to the anterior limit of the amygdala and ventricle. The amygdala is partly continuous above with the infero-
caudally it overlaps a portion of the hippocampal fields. The lateral medial margin of the claustrum. Fibres of the external capsule and
areas receive fibres from the olfactory bulb and the piriform and peri- substriatal grey matter, including the cholinergic magnocellular nucleus
amygdaloid cortices; more caudal regions do not generally receive basalis of Meynert, partially separate it from the putamen and globus
primary olfactory inputs. pallidus. Laterally, the amygdala lies close to the optic tract.


limbic system
389
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CaN IntCap GloPa CoRa SupLongFasc Fig. 25.31 The uncinate fasciculus has been
removed to expose the anterior commissure and
the lateral fibres of the anterior commissure have
been removed to expose the optic radiation.
Abbreviations: AntCom, anterior commissure;
AnsaPed, ansa peduncularis; CaN, caudate
nucleus; CoRa, corona radiata; GloPa, globus
pallidus; IntCap, internal capsule; OptRad, optic
radiation; SupLongFasc, superior longitudinal
fasciculus. (Courtesy of Richard Gonczalo Párraga.
Adapted from: Párraga RG, Ribas GC, Welling LC,
Alves RV, de Oliveira E. Microsurgical anatomy of
the optic radiation and related fibres in
3-dimensional images. Neurosurgery 2012,
71[ONS Suppl 1]:ons160–ons172.)
OptRad
AnsaPed
AntCom Amygdala Meyer’s loop
dala appear to utilize, at least in part, the excitatory amino acids gluta-
mate or aspartate as a transmitter. Moreover, they project to the ventral
striatum rather than to hypothalamic and brainstem sites. Thus, it may
be appropriate to consider this part of the amygdaloid complex as a
Olfactory bulb polymodal cortex-like area, separated from the cerebral cortex by fibres
Olfactory tract of the external capsule.
Olfactory Medial olfactory The central nucleus is present through the caudal half of the amyg-
trigone stria daloid complex. It lies dorsomedial to the basal nucleus and is divided
Diagonal band into medial and lateral parts. The medial part, which contains larger
Lateral of Broca cells than the lateral part, resembles the adjacent putamen. The medial
olfactory stria APS Cortical amygdaloid and central nuclei appear to have an extension across the basal fore-
Amygdalar GA GS nucleus brain, as well as within the stria terminalis, which merges with the bed
sulcus EA UG Uncus: see nucleus of the stria terminalis. This extensive nuclear complex is some-
contralateral


Rhinal fissure times referred to as the ‘extended amygdala’ (Fig. 25.33). It is formed
side for
subdivisions by the centromedial amygdaloid complex (medial nucleus, medial and
Hippocampal lateral parts of the central nucleus), the medial bed nucleus of the stria
fissure Parahippocampal
gyrus terminalis, and the cell columns that traverse the sublenticular substan-
Collateral
tia innominata, which lies between them. Developmental and cyto- and
fissure Structures related to the
chemoarchitectonic studies suggest that the subnuclei of the bed
olfactory and limbic systems
nucleus of the stria terminalis are aligned along an anterior to posterior
Fig. 25.32 The inferior aspect of the brain. The brainstem has been
rather than a medial to lateral gradient (Crestani et al 2013). Portions
removed and the right temporal pole has been displaced laterally to
of the medial nucleus accumbens may also be included in the extended
expose underlying structures. Abbreviations: APS, anterior perforated
amygdala.
substance; EA, entorhinal area; GA, gyrus ambiens; GS, gyrus
A consistent feature of the intrinsic connections among amygdaloid
semilunaris; UG, uncinate gyrus.
nuclei is that they arise primarily in the lateral and basal nuclei, and
terminate in the central and medial nuclei, suggesting a largely unidi-
The lateral nucleus has dorsomedial and ventrolateral subnuclei. The rectional flow of information. In brief, the lateral nucleus projects to
basal nucleus is commonly divided into dorsal magnocellular and all divisions of the basal nucleus, accessory basal nucleus, paralaminar
intermediate parvicellular basal nuclei and a ventral band of darkly and anterior cortical nuclei, and less heavily to the central nucleus; it
staining cells, the paralaminar basal nucleus, so called because it receives few afferents from other nuclei. The magnocellular, parvicel-
borders the white matter ventral to the amygdaloid complex. The acces- lular and intermediate parts of the basal nucleus project to the accessory


sory basal nucleus lies medial to the basal nuclear divisions and may basal, central (especially the medial part) and medial nuclei, as well as
be divided into dorsal, magnocellular and ventral, parvicellular parts. to the periamygdaloid cortex and the amygdalohippocampal area. The
The lateral and basal nuclei are often referred to collectively as the accessory basal nucleus projects densely to the central nucleus, espe-
basolateral area (nuclear group) of the amygdaloid complex. It has been cially its medial division, as well as to the medial and cortical nuclei.
suggested that the basolateral nuclear complex (lateral, basal, accessory Its major intra-amygdaloid afferents arise from the lateral nucleus. The
basal) should be considered as a quasicortical structure because it shares medial nucleus projects to the accessory basal, anterior cortical and
several characteristics with the cortex. Although it lacks a laminar struc- central nuclei, as well as to the periamygdaloid cortex and amygdalo-
ture, it has direct, often reciprocal, connections with adjacent temporal hippocampal area, while afferents arise especially from the lateral
and other areas of cortex, and it projects to the motor or premotor nucleus. The intrinsic connections of the cortical nucleus are not well
cortex. It receives a direct cholinergic and non-cholinergic input from understood. The posterior part of the cortical nucleus projects to the
the magnocellular corticopetal system in the basal forebrain, and has medial nucleus but it has been difficult to differentiate this projection
reciprocal connections with the mediodorsal thalamus. The distribu- from that arising in the amygdalohippocampal area. The central nucleus
tion of small peptidergic neurones in the basolateral nuclear complex, projects to the anterior cortical nucleus and the various cortical transi-
e.g. those containing neuropeptide Y (NY), somatostatin (SOM) and tion zones. It forms an important focus for afferents from many of the
CCK, are also similar in form and density to those found in the adjacent amygdaloid nuclei, especially the basal and accessory basal nuclei, and
temporal lobe cortex. Projection neurones from this part of the amyg- it has major extrinsic connections.


Cerebral hemispheres
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The amygdaloid complex has particularly extensive and rich connec- olfactory cortex in the orbitofrontal region of prefrontal cortex, bypass-
tions with many areas of the neocortex in unimodal and polymodal ing the thalamus; many of their terminal fields are primitive cortical
regions of the frontal, cingulate, insular and temporal neocortices. It areas that are considered to be parts of the limbic system, an arrange-
receives numerous projections from the brainstem, including the ment that underscores the ability of odours to modulate emotional
peripeduncular and parabrachial nuclei. The amygdala receives a rich processing and behaviour (Gottfried 2006).
monoaminergic innervation. The noradrenergic projection arises pri- The olfactory nerves arise from olfactory receptor neurones in the
marily from the locus coeruleus, serotoninergic fibres arise from the olfactory mucosa. The axons collect into numerous small bundles
dorsal and, to some extent the median, raphe nuclei, and the dopamin- ensheathed by a population of unique glia and surrounded by layers of
ergic innervation arises primarily in the midbrain ventral tegmental area meninges, and enter the anterior cranial fossa by passing through the
(A10). The basal and parvicellular accessory basal nuclei, the amygdalo- foramina in the cribriform plate of the ethmoid bone. They attach to
hippocampal area and nucleus of the lateral olfactory tract receive a the inferior surface of the olfactory bulb, which is situated at the ante-
very dense cholinergic innervation arising from the magnocellular rior end of the olfactory sulcus on the orbital surface of the frontal lobe,
nucleus basalis of Meynert. and terminate in the bulb.
Olfactory bulb
OLFACTORY PATHWAYS
The olfactory bulb is continuous posteriorly with the olfactory tract,
The organization of the olfactory system reflects its phylogenetically through which the output of the bulb passes directly to the ipsilateral
ancient lineage. Afferent olfactory pathways proceed directly to the piriform cortex, amygdala and rostral entorhinal cortex. There is a clear


laminar structure in the olfactory bulb (Fig. 25.34). From the surface
inwards, the laminae are the olfactory nerve layer, glomerular layer,
external plexiform layer, mitral cell layer, internal plexiform layer and
granule cell layer. The olfactory nerve layer consists of the unmyelinated
axons of the olfactory neurones. The continuous turnover of receptor
GP
cells means that axons in this layer are at different stages of growth,
maturity or degeneration. The glomerular layer consists of a thin sheet
of glomeruli where the incoming olfactory axons divide and synapse
VP
on terminal dendrites of secondary olfactory neurones, i.e. mitral,
tufted and periglomerular cells. The external plexiform layer contains
the principal and secondary dendrites of mitral and tufted cells. The
mitral cell layer is a thin sheet composed of the cell bodies of mitral
Anterior commissure cells, each of which sends a single principal dendrite to a glomerulus,
secondary dendrites to the external plexiform layer, and a single axon
Internal capsule to the olfactory tract. It also contains a few granule cell bodies. The
internal plexiform layer contains axons, recurrent and deep collaterals
GP
of mitral and tufted cells, and granule cell bodies. The granule cell layer
Anterior commissure contains the majority of the granule cells and their superficial and deep
processes, together with numerous centripetal and centrifugal nerve
fibres that pass through the layer.
Different odour molecules are represented by different patterns of
spatial activity in the olfactory bulb (Shepherd 2006). The principal
neurones in the olfactory bulb are the mitral and tufted cells; their
axons form its output via the olfactory tract.
Temporal lobe The granule cell layer of the bulb is extended into the olfactory tract
as scattered medium-sized multipolar neurones that constitute the ante-
rior olfactory nucleus. Many centripetal axons from mitral and tufted
Striatum cells relay in, or give collaterals to, the anterior olfactory nucleus; the
axons from the nucleus continue with the remaining direct fibres from
Globus pallidus (GP) and ventral pallidum (VP) the bulb into the olfactory striae.


Afferent inputs to the olfactory bulb arise from a variety of central
Extended amygdala
sites. Neurones of the anterior olfactory nucleus and collaterals of
Nucleus accumbens pyramidal neurones in the olfactory cortex project to the granule cells
of the olfactory bulb. Cholinergic neurones in the horizontal limb
Magnocellular basal forebrain
nucleus of the diagonal band of Broca, part of the basal forebrain
Fig. 25.33 A coronal section through the basal forebrain and temporal cholinergic system, project to the granule cell layer and also to the
pole, illustrating the relationship between the striatum, nucleus glomerular layer. Other afferents to the granule cell layer and the
accumbens, globus pallidus, ventral pallidum, extended amygdala and glomeruli arise from the pontine locus coeruleus and the mesencephalic
magnocellular basal forebrain system. raphe nucleus.
Fig. 25.34 Organization of the olfactory bulb.
Centrifugal axon
Nerve fibres of olfactory tract
Internal granule neurone
Granule cell layer and internal plexiform layer
Mitral neurone
Mitral cell layer
External plexiform layer
Layer of synaptic glomeruli
and interglomerular spaces
Olfactory nerve fibre layer
Dopaminergic periglomerular neurone
Olfactory receptor cell Tufted cell Anterior olfactory nucleus


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The amygdaloid nuclear complex has rich interconnections with tromedial and premammillary nuclei. The amygdala projects to the
allocortical, juxtallocortical and, especially, neocortical areas. It projects rostrocaudal extent of the lateral hypothalamus. The majority of the
to widely dispersed neocortical fields, principally from the basal fibres originate in the central nucleus and run principally in the ventral
nucleus. The complex projects to virtually all levels of the visual cortex amygdalofugal pathway and medial forebrain bundle. There is a rich
in both temporal and occipital lobes; the largest component of these projection to the medial, magnocellular part of the mediodorsal
projections arises from the magnocellular basal nucleus. It has been nucleus of the thalamus, particularly from the lateral, basal and acces-
suggested that a direct pathway to the amygdala that bypasses the sory basal nuclei and the periamygdaloid cortex. The central and
primary sensory cortices and relies on crude sensory input in the visual medial nuclei project to the midline nuclei, especially the nucleus cen-
domain may represent a neural ‘alarm’ system for rapid alerting to tralis and nucleus reuniens. The parvicellular division of the basal
sources of threat, without the need for conscious appraisal (Liddell et al nucleus, magnocellular accessory basal nucleus (but not the magnocel-
2005). The amygdala also reciprocates projections to the auditory cortex lular basal nucleus) and the central nucleus all project to basal fore-
in the rostral half of the superior temporal gyrus. Projections to the brain cholinergic cell groups, notably the nucleus basalis of Meynert
polymodal sensory areas of the temporal lobe generally reciprocate the and the horizontal limb nucleus of the diagonal band. The striatum,
amygdalopetal projections. Efferents from the lateral and accessory and particularly the nucleus accumbens, receives prominent projec-
basal nuclei are directed to the temporal pole, particularly the medial tions from the amygdaloid complex, predominantly from the basal and
perirhinal area. The insular cortex is heavily innervated by the amyg- accessory basal nuclei. The ventral striatum sends many fibres to the


daloid medial and anterior cortical nuclei. The orbital cortex and ventral pallidum, which in its turn projects to the mediodorsal nucleus
medial frontal cortical areas 24, 25 and 32, including parts of the ante- of the thalamus. The ventral striatopallidal system thus provides an
rior cingulate gyrus, receive a heavy projection, whereas areas 8, 9, 45 additional route by which the amygdala can influence mediodorsal
and 46 of the dorsolateral prefrontal cortex, as well as the premotor thalamic–prefrontal cortical processes. The lateral, magnocellular
cortex (area 6), are reported to receive a patchy innervation. The basal accessory basal and parvicellular basal nuclei contribute the largest
nucleus is an important source of these projections, which are aug- proportion of efferents to the hippocampal formation. The main pro-
mented by contributions from the accessory basal (magnocellular and jection is from the lateral nucleus to the rostral entorhinal cortex, but
parvicellular divisions) and lateral nuclei. many fibres also terminate in the hippocampus proper and the subicu-
In addition to direct projections from the olfactory bulb to the lum. There appears to be marked polarity in amygdalohippocampal
nucleus of the lateral olfactory tract, anterior cortical nucleus and the connections in that the amygdala has a greater influence on hippocam-
periamygdaloid cortex (piriform cortex), there are also associational pal processes than vice versa. Amygdala–cortical functional connectiv-
connections between all parts of the primary olfactory cortex and these ity underlies a range of cognitive and affective processes. The appropriate
same superficial amygdaloid structures. The anterior temporal lobe pro- development of these functional connections has been correlated with
vides the largest proportion of the cortical input to the amygdala, the emotional behaviour of adults; extensive and specific changes
predominantly to the lateral nucleus. Rostral parts of the superior tem- in these connections emerge between childhood and adolescence
poral gyrus, which may represent unimodal auditory association cortex, (Gabard-Durnam et al 2014). Atypical functional connectivity patterns


project to the lateral nucleus. There are also projections from polymo- have been implicated in conditions including depression, schizophre-
dal sensory association cortices of the temporal lobe, including perirhi- nia and bipolar disorder.
nal cortex (areas 35 and 36), the caudal half of the parahippocampal The central nucleus is also the major relay for projections from the
gyrus, the dorsal bank of the superior temporal sulcus, and both the amygdala to the brainstem and receives many reciprocal projections. It
medial and lateral areas of the cortex of the temporal pole. The CA1 projects to the periaqueductal grey matter, ventral tegmental area, sub-
field of the hippocampus and adjacent subiculum, and possibly the stantia nigra pars compacta, peripeduncular nucleus, mesencephalic
entorhinal cortex, project to the amygdala, mainly to the parvicellular tegmental reticular formation, parabrachial nucleus, nucleus of the soli-
basal nucleus. The rostral insula projects heavily to the lateral, parvicel- tary tract and the dorsal motor nucleus of the vagus.
lular basal and medial nuclei. The caudal insula, which is reciprocally These cells are morphologically similar and most use an excitatory
connected with the second somatosensory cortex, also projects to the amino acid, probably glutamate or aspartate, as their neurotransmitter.
lateral nucleus, thus providing a route by which somatosensory infor- The mitral cell spans the layers of the bulb and receives the sensory
mation reaches the amygdala. The caudal orbital cortex projects to the input superficially at its glomerular tuft. The axons of mitral and tufted
basal, magnocellular accessory basal and lateral nuclei. The medial cells appear to be parallel output pathways from the olfactory bulb. The
prefrontal cortex projects to the magnocellular divisions of the acces- main types of interneurones in the olfactory bulb are the periglomerular
sory and basal nuclei. cells and granule cells. The majority of periglomerular cells are dopamin-
The central nucleus is the major relay for amygdaloid projections to ergic (cell group A15) but some are GABAergic; their axons are distrib-


the hypothalamus. Amygdaloid fibres reach the bed nucleus of the stria uted laterally and terminate within extraglomerular regions. Granule
terminalis primarily via the stria terminalis, but also via the ventral cells are similar in size to periglomerular cells. Their most characteristic
amygdalofugal pathway. In general, central and basal nuclei project to feature is the absence of an axon and they therefore resemble amacrine
the lateral bed nucleus, and medial and posterior cortical nuclei project cells in the retina. Granule cells have two principal spine-bearing den-
to the medial bed nucleus. Anterior cortical and medial nuclei project drites that pass radially in the bulb; they appear to be GABAergic. The
largely to the medial preoptic area and anterior medial hypothalamus granule cell is likely to be a powerful inhibitory influence on the output
(including the paraventricular and supraoptic nuclei) and to the ven- neurones of the olfactory bulb.


White matter of the cerebral hemispheres
391
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Olfactory tract and anterior areas in the same hemisphere; commissural fibres link corresponding
perforated substance cortical areas in the two hemispheres; and projection fibres connect the
cerebral cortex with the corpus striatum, diencephalon, brainstem and
spinal cord.
As the olfactory tract approaches the anterior perforated substance
(ventral striatopallidal region), it flattens and splays out as the olfactory
trigone. Fibres of the tract continue from the caudal angles of the
ASSOCIATION FIBRES
trigone as diverging medial and lateral olfactory striae, which border
the anterior perforated substance (see Figs 25.20B, 25.32). The lateral
Association fibres may be either short or long. They serve to connect
olfactory stria follows the anterolateral margin of the anterior perfo-
regions of grey matter reciprocally, establishing spatially defined net-
rated substance to the limen insulae, where it bends posteromedially
works that determine function. Short association fibres (arcuate or
to merge with an elevated region, the gyrus semilunaris, at the rostral
U-fibres) may be entirely intracortical, passing between the walls of a
margin of the uncus in the temporal lobe. The lateral olfactory gyrus
sulcus, or they may pass subcortically between adjacent gyri. They
forms a tenuous grey layer covering the lateral olfactory stria; it merges
connect clusters of cortical areas subserving similar functions, e.g. in the
laterally with the gyrus ambiens, part of the limen insulae. Together,
frontal lobe, short intralobar tracts connect the supplementary motor
the lateral olfactory gyrus and gyrus ambiens form the prepiriform
area and presupplementary motor area with posterior Broca’s region
region of the cortex, which passes caudally into the entorhinal area of
(frontal ‘aslant’ tract); posterior orbitofrontal cortex with the anterior
the parahippocampal gyrus. The prepiriform and periamygdaloid
polar region (fronto-orbitopolar tract); and the posterior precentral


regions and the entorhinal area (area 28) together make up the piriform
cortex with anterior prefrontal cortex (frontal superior longitudinal
cortex, the largest cortical olfactory area. The medial olfactory stria
fasciculus) (Catani et al 2012).
passes medially along the rostral boundary of the anterior perforated
Fasciculi (bundles, tracts) of long association fibres connect ana-
substance towards the medial continuation of the diagonal band of
tomically distant yet functionally highly integrated areas of the ipsilat-
Broca and together they curve up on the medial aspect of the hemi-
eral cortex. It is assumed that they enable rapid feed-forward propagation
sphere, anterior to the attachment of the lamina terminalis. The anterior
of sensory input to the cortical circuitry responsible for the performance
perforated substance is continuous laterally with the peduncle of the
of complex behavioural and cognitive functions. They include the supe-
temporal stem and the amygdaloid complex, and medially with the
rior, middle and inferior longitudinal fasciculi, inferior fronto-occipital
septal region.
fasciculus, uncinate fasciculus, cingulum and fornix (Martino and de
The main targets of the lateral olfactory tract are the piriform cortex,
Lucas 2014). Individual variability in both the three-dimensional
amygdala and rostral entorhinal cortex (Gottfried 2006). Neurones in
topography and size of these tracts has been reported.
the piriform cortex project widely to targets that include the neocortex
(especially the orbitofrontal cortex), agranular insula, thalamus (espe-
cially the medial dorsal thalamic nucleus), hypothalamus, amygdala Superior longitudinal fasciculus
and hippocampal formation.
The superior longitudinal fasciculus (SLF) is composed of three subsets
WHITE MATTER OF THE CEREBRAL of fibres: a frontoparietal or horizontal segment; a temporoparietal or
vertical segment; and a temporofrontal segment or arcuate fasciculus
HEMISPHERES
(Catani et al 2005, Fernández-Miranda et al 2008a, Martino and Brogna


2011) (Figs 25.35–25.37; see Fig. 25.41).
The use of diffusion tensor imaging (DTI) as a tool with which to
explore gross fibre architecture non-invasively has enabled the virtual
Inferior longitudinal fasciculus
dissection and visualization of those tracts in the living human brain;
the impact of this technology, e.g. in neurosurgery, has been dramatic
(Fernández-Miranda et al 2008a, Martino et al 2011). The extensive The inferior longitudinal fasciculus connects the anterior aspect of
tractography literature should be consulted not only for anatomical the temporal lobe with the posterior aspect of the occipital lobe and
details that are beyond the scope of this book but also for critical analy- runs predominantly within the depth of the fusiform gyrus (see
ses of the methodological issues that compromise interpretation of Fig. 25.35). It consists of a direct and a more lateral indirect pathway.
image reconstructions, particularly where fibres change direction The direct pathway connects with the anterior portions of the temporal
abruptly or bundles cross or ‘kiss’ each other. While an undoubtedly gyri, fusiform and parahippocampal gyri and with the amygdala and
powerful tool, DTI does not provide information about functional or hippocampus (Catani and Thiebaut de Schotten 2008). The indirect,
synaptic connections. occipitotemporal pathway consists of short U-shaped bundles connect-
The white matter of the cerebral hemispheres is composed of three ing adjacent gyri in the inferior temporal and occipital convexities.
categories of myelinated axons. Association fibres link different cortical The function of the inferior longitudinal fasciculus has not been
Fig. 25.35 A diffusion tensor imaging tractography
reconstruction of the association bundles of a left
hemisphere. Key: 1, inferior fronto-occipital
fasciculus; 2, inferior longitudinal fasciculus; 3,
uncinate fasciculus; 4, arcuate fasciculus; 5,
horizontal segment of the superior longitudinal
fasciculus; 6, vertical segment of the superior
longitudinal fasciculus. Ant, anterior; Post,
posterior. (With permission from Martino J, De Witt
5 Hamer PC, Vergani F, et al, Cortex-sparing fiber


dissection: an improved method for the study of
white matter anatomy in the human brain, J Anat
6 2011 Oct;219(4):531–41).
4
Ant Post
3 1
2


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391.e1
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CoRa GloPa SupLongFasc SagStr Fig. 25.36 A progressive fibre dissection of the
lateral aspect of the left cerebral hemisphere.
Parts of the superior longitudinal fasciculus
(SupLongFasc) have been removed to expose the
corona radiata, and the sagittal stratum (SagStr),
inferior fronto-occipital fasciculus (IFOF) and
uncinate fasciculus (UncFasc) can be identified
passing along the basal portion of the insular
cortex. Other abbreviations: AntCom, anterior
commissure; CoRa, corona radiata; GloPa, globus
pallidus. (Courtesy of Richard Gonczalo Párraga.
Adapted from: Párraga RG, Ribas GC, Welling LC,
Alves RV, de Oliveira E. Microsurgical anatomy of
the optic radiation and related fibres in
3-dimensional images. Neurosurgery 2012,
71[ONS Suppl 1]:ons160–ons172.)
UncFasc IFOF AntCom
SupLF FPSeg TPSeg Frontoparietal fibres run deeply underneath the frontoparietal oper-
(Horizontal) (Vertical) culum, connecting the posterior aspect of the inferior frontal gyrus
(Broca’s area) with the inferior parietal lobule (supramarginal and
angular gyri). This frontoparietal portion of the superior longitudinal
fasciculus appears to consist of three components: SLF I connects the
superior parietal lobule and the precuneus with the premotor and pre-
frontal cortex (areas 6, 8 and 9, and the supplementary motor area);
SLF II runs above the superior limiting sulcus of the insula and connects
the angular gyrus with the dorsal premotor and prefrontal areas; and
SLF III connects the supramarginal gyrus with the ventral premotor and
prefrontal cortex (Broca’s area) and corresponds to the horizontal
segment itself (Makris et al 2005).
Temporal-parietal fibres connect the posterior portions of the supe-
rior and middle temporal gyri (Wernicke’s area) with the inferior pari-


etal lobule (Catani et al 2005, Fernández-Miranda et al 2008a, Martino
and Brogna 2011). The temporal-frontal segment connects more diffuse
areas of the posterior aspect of the temporal lobe with the posterior
aspect of the frontal lobe and corresponds to the arcuate fasciculus. This
longer portion of the superior longitudinal fasciculus is anatomically
more defined posteriorly where it arches around the distal aspect of the
lateral fissure (Bernal and Altman 2010, Bernal and Ardila 2009, Glasser
and Rilling 2008, Martino and Brogna 2011). The superior longitudinal
fasciculus thus forms an indirect pathway that links Broca’s area with
Wernicke’s area through the inferior parietal lobule and by a direct and
TFSeg
deeper pathway corresponding to the arcuate fasciculus.
Fig. 25.37 A diffusion tensor imaging reconstruction of the superior
longitudinal fasciculus (SupLF). Abbreviations: FPSeg, frontoparietal
or horizontal segment; TFSeg, temporal-frontal segment; TPSeg,
temporoparietal or vertical segment. (Courtesy of Prof. Edson Amaro
Jr MD, Department of Radiology, University of São Paulo Medical School.)