Comprehensive Physiology Wiley Online Library

Memory: Anatomical Organization of Candidate Brain Regions

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Abstract

The sections in this article are:

1 Relationship Between Association Cortices and Medial Temporal Lobe
2 Anatomy of Hippocampal Formation
2.1 Species Differences
2.2 Nomenclature
2.3 Subdivisions
2.4 Intrinsic Circuitry
2.5 Hippocampal Topography
2.6 Extrinsic Connections
2.7 Immunohistochemical Studies of Neuroactive Substances
3 Anatomy of Mamillary Complex
3.1 Intrinsic Organization
3.2 Afferents
3.3 Efferents
3.4 Connections of Associated Nuclei
4 Anatomy of Amygdaloid Complex
4.1 Nomenclature and Subdivisions
4.2 Intrinsic Circuitry
4.3 Extrinsic Connections
4.4 Neuroactive Substances
5 Comparison of Organization of Amygdaloid Complex and Hippocampal Formation
6 Anatomy of Mediodorsal Nucleus of Thalamus
6.1 Intrinsic Organization
6.2 Cortical Connections
6.3 Subcortical Connections
7 Neuropathology of Memory‐Related Structures in Alzheimer's Disease
7.1 Hippocampal Formation
7.2 Amygdaloid Complex
7.3 Mamillary Complex and Mediodorsal Thalamus
7.4 Loss of Neuroactive Substances in Alzheimer‐Affected Hippocampal Formation
8 Temporal Stem Hypothesis Revisited
9 Are There Additional Candidate Structures?
Figure 1. Figure 1.

Outlines of surface of macaque monkey brain show positions of major primary sensory cortices and of unimodal and polymodal association areas. Right: medial (top) and lateral (bottom) view of monkey brain. Primary visual cortex (VI), primary auditory cortex (AI), and primary somatosensory cortex (SI) are labeled, as is primary motor cortex (MI). Small numbers designate cortical fields as defined by Brodmann . AMG, amygdala; HIP, hippocampus, IPS, intraparietal sulcus; LF, lateral fissure; STS, superior temporal sulcus; TH and TF, fields of parahippocampal gyrus; TPO and PGa, polysensory fields on dorsal bank of superior temporal sulcus. Left: medial (top), lateral (middle), and ventral (bottom) surfaces of monkey brain. Approximate extents of primary (stippling) and secondary (vertical lines) unimodal association cortices are labeled. Positions of certain polysensory cortical regions (dotted shading) are also shown.

From Pandya and Seltzer
Figure 2. Figure 2.

Summary diagram showing progression of connections from primary sensory cortices to unimodal association cortices and finally to polymodal association areas. In each, dotted pattern shows projection origins and horizontal lines delimit termination regions. In somatosensory system, for example, primary somatosensory cortex (S) gives rise to projections to motor cortex (4) and to somatosensory association cortex (5). Area 5, in turn, gives rise to projections to premotor cortex (6) and to posterior parietal cortex (7). This latter region projects to polysensory zones in superior temporal sulcus (STS), cingulate gyrus (CG), and perirhinal cortex . A, primary auditory cortex; Am, amygdala; SM, supplementary motor cortex; STP, supratemporal plane; TG, temporal polar cortex.

Adapted from Jones and Powell
Figure 3. Figure 3.

Diagram illustrating progression of sensory information in visual system from primary visual cortex (OC) through successive association cortices (OB, OA, TEO, and TE) to amygdaloid complex. Unimodal visual input to amygdala arises from highest levels of hierarchy of cortical processing.

Adapted from Mishkin
Figure 4. Figure 4.

Four coronal sections through temporal lobe of macaque monkey brain (rostral to caudal) showing position of amygdaloid complex (A) and hippocampal formation (H) relative to other temporal lobe structures. Fibers that form portion of “temporal stem” (TS) are marked in B. Calibration marker, 5 mm. amts, Anterior middle temporal sulcus; f, fimbria; 51, piriform and periamygdaloid cortex; la, Id, Ig, insula cortex; ITG, inferior temporal gyrus; las, lateral sulcus; or, optic radiations; ots, occipitotemporal sulcus; pmts, posterior middle temporal sulcus; PU, putamen; PUL, pulvinar; rs, rhinal sulcus; STG, superior temporal gyrus; sts, superior temporal sulcus; TA, TE, TEO, TF, TG, TH, OA, OB, fields of temporal and occipital lobes according to Bailey and Bonin ; 35/36, perirhinal cortex. For other abbreviations see Fig. legend, p. 251.

Figure 5. Figure 5.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained human hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; EC, entorhinal cortex; f, fimbria; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum.

Figure 6. Figure 6.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained macaque monkey hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum; TE, visual association isocortex; TF/TH, polymodal association cortex of parahippocampal gyrus. For other abbreviations see Fig. legend, p. 251.

Figure 7. Figure 7.

Surface maps showing demarcation, based on cytoarchitectonic criteria, of entorhinal cortex of humans (A) and macaque monkey (B) proposed by Rose . Similar map for monkey by Sgonina is shown in C, and subdivisions of entorhinal cortex by Van Hoesen and Pandya are illustrated in D. In each map, rostral is to left and mediodorsal is at top. Entorhinal cortex is differentiated along mediolateral and rostrocaudal gradients.

Figure 8. Figure 8.

Illustration of Golgi preparation from Lorente de Nó shows principal cell types in dentate gyrus (fascia dentata) and CA1 hippocampal field (cornu ammonis). Main cell type in dentate gyrus is granule cell (cells 7–12), which has unipolar dendritic tree that extends into molecular layer. A second class of neurons, basket pyramidal cells (cell 13), gives rise to GABAergic basket plexus that terminates around the granule cell bodies. Principal cell in hippocampus is pyramidal cell (cells 1–5), which has apical dendritic plexus that extends into overlying strata radiatum and lacunosum‐moleculare, and basal dendritic plume that extends into subjacent stratum oriens. There are also several classes of inhibitory interneurons in hippocampus, some of which are located in pyramidal cell layer (cell 6) and in other strata as well.

From Lorente de Nó
Figure 9. Figure 9.

Illustration of Golgi‐stained neurons in mouse hippocampus from Lorente de Nó . Large cells of polymorphic region of dentate gyrus (cells 21 and 22, “mossy cells”) and pyramidal cells of the CA3 region (cells 8 and 10–19) have specialized spines (thorny excrescences) on their proximal dendrites, which are primary termination of mossy fibers from dentate gyrus. Interneuron of basket type is pictured as cell 9. Note that the pyramidal cells of CA2 region do not have large spines on their proximal dendrites and do not receive mossy fiber input. They are, however, much larger than adjoining pyramidal cells of CA1 region.

From Lorente de Nó
Figure 10. Figure 10.

Simplified circuit diagram demonstrating fundamental “trisynaptic” circuit of rat hippocampus. Fibers originating in entorhinal cortex (perforant path, pp) travel through subiculum and terminate on dendrites of granule cells in outer two‐thirds of molecular layer of dentate gyrus. Granule cells give rise to axons (mossy fibers, mf), which terminate on CA3 pyramidal cells. CA3 pyramidal cells project to CA1 region (Schaffer collaterals, sc). Because of “lamellar organization” of hippocampus, slices cut perpendicular to its long axis contain an intact chain of these connections.

Figure 11. Figure 11.

Line drawings of coronal section through monkey hippocampal formation on which major intrinsic and extrinsic efferent projections are plotted. A: various fields that comprise hippocampal formation are labeled and fundamental trisynaptic circuit is drawn [entorhinal cortex to dentate gyrus (1), dentate gyrus to hippocampal field CA3 (2), field CA3 to field CA1 (3)]. B: in addition to projecting to field CA3 (1), mossy fibers arising from dentate granule cells terminate on polymorphic cells of hilar region (2); these cells give rise to ipsilateral associational and commissural projections that terminate in molecular layer (3). CA3 pyramidal cells give rise to associational projections to other levels of field CA3 (5, 6) in addition to their projection to field CA1 (4). CA1 pyramidal cells project to subiculum (7), presubiculum (8), and entorhinal cortex (9). Cells in subiculum, presubiculum, and parasubiculum send a major projection to entorhinal cortex (10, 11, and 12, respectively). C: Projections to septal nuclei are diagramed. Field CA3 of hippocampus projects bilaterally to lateral septum (1) and field CA1 projects ipsilaterally (2). Subiculum also projects to lateral septum (3) and to nucleus accumbens (4). Entorhinal cortex projects to nucleus accumbens (5) and caudate nucleus and putamen (6). D: projections to diencephalon. Subiculum projects bilaterally to medial mamillary nucleus (1), whereas presubiculum projects primarily to lateral mamillary nucleus (2). Presubiculum also projects lightly to medial mamillary nucleus as does entorhinal cortex (3). Projection to anterior thalamus originates primarily in presubiculum and it terminates bilaterally (4). E: projections to amygdaloid complex. Both subiculum (1) and entorhinal cortex (2) project to parvicellular portion of basal nucleus; entorhinal cortex also projects to lateral nucleus (3). F: projections to neocortex. Although corticopetal projections of hippocampal formation are relatively unstudied, there is evidence for projections from both subicular complex and entorhinal cortex to cortical fields listed. AT, anterior thalamic nuclei; B, basal nucleus of amygdala; CA1, CA3, fields of hippocampus; DG, dentate gyrus; f, fornix; LM, lateral mamillary nucleus; LS, lateral septal nucleus; MM, medial mamillary nucleus; NA, nucleus accumbens; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. legend, p. 251.

Figure 12. Figure 12.

Distribution of preterminal axons in entorhinal cortex arising from subfields of subicular complex. Projections from subiculum terminate in deep layers, whereas those from presubiculum end mainly in layer III and those from parasubiculum end in layer I.

From Köhler
Figure 13. Figure 13.

Summary diagram of commissural connections of monkey hippocampal formation. Top: extent of commissural fiber system is plotted (dotted lines) on lateral (left) and dorsal (right) views of brain. A: commissural projections of presubiculum and entorhinal cortex. Presubiculum (PrS) projects through hippocampal commissure (hc) to all levels of contralateral caudal entorhinal cortex (ECc). The ECc [but not rostral entorhinal cortex (ECr)] projects weakly to contralateral ECc and very lightly to posterior dentate gyrus (AD) and CA1 hippocampal field. B: rostral dentate gyrus and CA3 hippocampal field (H + AD) project to homotopic region of contralateral side. ab, Angular bundle; f, fimbria.

From Amaral et al.
Figure 14. Figure 14.

Ventromedial views of human (A) and macaque monkey (B) brains showing region of parahippocampal gyrus. cf, Calcarine fissure; cgs, cingulate sulcus; cos, collateral sulcus; ots, occipital temporal sulcus; rs, rhinal sulcus.

Courtesy of G. W. Van Hoesen
Figure 15. Figure 15.

Efferent projections of parahippocampal gyrus plotted on lateral (top) and medial (bottom) surfaces of macaque monkey brain. Numbers indicate cortical fields from nomenclature of Brodmann . Rsp, retrosplenial cortex.

Courtesy of G. W. Van Hoesen
Figure 16. Figure 16.

Photomicrographs of adjacent coronal sections through rostral hippocampal formation of monkey stained by Nissl method (A, bright field) or by immunohistochemical procedure for demonstration of somatostatin‐like immunoreactivity (B, dark‐field photomicrograph with immunoreactivity seen as light regions). Note particularly dense staining of molecular layer of dentate gyrus. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus (pl, polymorphic layer; ml, molecular layer); EC, entorhinal cortex; PaS, parasubiculum; PrS, presubiculum; rs, rhinal sulcus; S, subiculum. Small lettering in field CA1 indicates names of hippocampal laminae (a, alveus; o, stratum oriens; p, pyramidal cell layer; r, stratum radiatum; lm, stratum lacunosum‐moleculare). Calibration marker, 500 μm.

Figure 17. Figure 17.

Photomicrographs of coronal sections through macaque monkey mamillary complex arranged from rostral (A) to caudal (D). Each panel shows adjacent sections stained by Nissl method (top) or by reduced silver method for fibers (bottom). Calibration marker, 500 μm. f, Fornix; IC, intercalated nucleus; LMN, lateral mamillary nucleus; MMN, medial mamillary nucleus (MMNm pars medialis; MMNl, pars lateralis; MMNb, pars basalis); mp, mamillary peduncle; mtg, mamillotegmental tract; NG, nucleus gemini; PHN, posterior hypothalamic nucleus; pmt, principal mamillary tract; smc, supramamillary commissure; SUM, supramamillary area; TB, tuberomamillary nucleus. For other abbreviations see Fig. legend, p. 251.

Figure 18. Figure 18.

Photomicrographs of adjacent sections through monkey mamillary complex stained as in Fig. . Main component of mamillary complex is medial nucleus (MMN), which can be divided into medial (M), lateral (L), and basal (MMNb) divisions. Other major component is lateral mamillary nucleus (LMN). Associated with mamillary complex are tuberomamillary nucleus (TB) and paramamillary nucleus (PM). Note in B the dense plexus of fibers that invest LMN. Principal mamillary tract (pmt) arises from dorsal surface of medial mamillary nucleus.

Figure 19. Figure 19.

Summary diagram of efferent connections of primate mamillary complex. Medial nucleus (MM) projects ipsilaterally via principal mamillary tract (pmt) and mamillothalamic tract (mth) to anteromedial (AM) and anteroventral (AV) subdivisions of anterior thalamus and also to ventral tegmental nucleus (VT) via mamillotegmental tract (mtg). Fibers from lateral mamillary nucleus (LM) use same pathways to project bilaterally to anterodorsal nucleus of thalamus (AD) and to dorsal tegmental nucleus (DT).

Figure 20. Figure 20.

Diagram of efferent connections of the 2 major subdivisions (areas 23 and 24) of cingulate cortex. Note that anterior cingulate (area 24) projects heavily to amygdaloid complex and to perirhinal and entorhinal cortices. Posterior cingulate cortex (area 23) has prominent projections to parahippocampal gyrus (TH‐TF) and presubiculum. AMG, amygdala; AS, arcuate sulcus; CC, corpus callosum; CF, calcarine fissure; CING S, cingulate sulcus; CS, central sulcus; IOS, inferior occipital sulcus; IPS, intraparietal sulcus; LB, basal nucleus of amygdala; LF, lateral fissure; LS, lunate sulcus; OS, orbital sulcus; OTS, occipital temporal sulcus; PAR HIPP, parahippocampal gyrus; POMS, parieto‐occipital medial sulcus; Presub, presubiculum; PS, principal sulcus; RS, rhinal sulcus; rspl c, retrosplenial cortex; STS, superior temporal sulcus.

From Pandya et al.
Figure 21. Figure 21.

Coronal section through the Nissl‐stained amygdaloid complex of macaque monkey. Major subdivisions of amygdala include lateral nucleus (L); basal nucleus, which has magnocellular (Bmg), parvicellular (Bpc), and paralaminar (Bpl) subdivisions; accessory basal nucleus, which has magnocellular (ABmg) and parvicellular (ABpc) divisions; central nucleus, which has medial (Cm) and lateral (Cl) divisions; medial nucleus (M); cortical area (CO); and periamygdaloid cortex (PAC). Entorhinal cortex (EC), bounded laterally by rhinal sulcus (rs), is also shown; the 6 principal laminae are numbered.

Figure 22. Figure 22.

Amygdaloid complex of shrew in its normal orientation (A) and after being rotated ventrolaterally (B). In B, positions of major nuclei closely resemble those of human amygdala. ABa, accessory basal nucleus, magnocellular division; ABb, accessory basal nucleus, parvicellular division; Ba, basal nucleus, magnocellular division; Bb, basal nucleus, parvicellular division; C, cortical area; CE, central nucleus; I, intercalated nucleus; L, lateral nucleus; M, medial nucleus; O, nucleus of lateral olfactory tract.

From Crosby and Humphrey
Figure 23. Figure 23.

Intrinsic connections of monkey amygdaloid complex. Local projections of lateral nucleus (A), basal nucleus (B), accessory basal nucleus (C), and central and medial nuclei and periamygdaloid cortex (D) are indicated. Arrows ending within origin nucleus indicate associational projections. Note tendency for laterally placed nuclei to project to central and medial nuclei. AB, accessory basal nucleus; Bmg, magnocellular division of basal nucleus; Bp, parvicellular division of basal nucleus; CI, lateral division of central nucleus; Cm, medial division of central nucleus. For other abbreviations see Fig. legend, p. 251.

Figure 24. Figure 24.

Representative coronal sections through brain of macaque monkey, arranged from rostral (A) to caudal (L), showing distribution pattern of anterogradely labeled projections resulting from injection of tritiated amino acids into central nucleus of amygdala. Injection site is shown as blackened area in B and C. Labeled fibers are represented as dashed lines and terminal fields as dots. On left side of each section, triangles mark location of pigment‐containing, presumably monoaminergic neurons. ac, Anterior commissure; ACA, amygdaloclaustral area; AHA, amygdalohippocampal area; AM, anteromedial nucleus (thalamus); AN, arcuate nucleus (hypothalamus); AV, anteroventral nucleus (thalamus); BA, accessory basal nucleus (amygdala); BAm, accessory basal nucleus pars magnocellularis (amygdala); BAp, accessory basal nucleus pars parvocellularis (amygdala); bc, brachium conjunctivum; BL, basal nucleus (amygdala); BLm, basal nucleus pars magnocellularis (amygdala); BLp, basal nucleus pars parvicellularis (amygdala); BNM, basal nucleus of Meynert; BNST, bed nucleus of stria terminalis; bp, brachium pontis; C, central nucleus (amygdala); CBL, cerebellum; CD, caudate nucleus; Cde, nucleus centralis pars densocellularis (thalamus); CG, central gray; Cif, nucleus centralis inferior (thalamus); Cim, nucleus centralis intermedius (thalamus); CL, claustrum; Cl, nucleus centralis lateralis (thalamus); Clc, nucleus centralis pars laterocellularis (thalamus); CM, nucleus centralis medialis (thalamus); COa, anterior cortical nucleus (amygdala); COp, posterior cortical nucleus (amygdala); cp, cerebral peduncle; Cs, nucleus centralis superior (thalamus); CS, central superior raphe nucleus; DK, nucleus of Darkschewitsch; DM, dorsomedial nucleus (hypothalamus); DMN, dorsal motor nucleus of the vagus nerve; DR, dorsal raphe nucleus; EC, entorhinal cortex; EN, endopiriform nucleus; flm, medial longitudinal fasciculus; fm, fimbria; fx, fornix; GP, globus pallidus; GPe, globus pallidus (external); GPi, globus pallidus (internal); H, hippocampal formation; HB, habenular nuclei; HDB, horizontal limb of the nucleus of the diagonal band; IC, inferior colliculus; ic, internal capsule; IO, inferior olive; IP, interpeduncular nucleus; IS, interstitial nucleus; L, lateral nucleus (amygdala); LCd, nucleus locus coeruleus pars dorsalis; LCN, lateral cuneate nucleus; LCv, nucleus locus coeruleus pars ventralis; LD, laterodorsal nucleus (thalamus); If, lenticular fasciculus; LGN, lateral geniculate nucleus (thalamus); LH, lateral hypothalamus; LP, lateroposterior nucleus (thalamus); LR, lateral reticular nucleus; LT, lateral tuberal nucleus (hypothalamus); M, medial nucleus (amygdala); MD, mediodorsal nucleus (thalamus); MGN, medial geniculate nucleus (thalamus); Ml, lateral mamillary nucleus; ml, medial lemniscus; Mm, medial mamillary nucleus; NC, nucleus cuneiformis; NPC, nucleus of posterior commissure; NST, nucleus of solitary tract; NSTp, nucleus of solitary tract pars parvocellularis; oc, optic chiasm; ot, optic tract; P, putamen; PAC, periamygdaloid cortex; Pbl, lateral parabrachial nucleus; Pbm, medial parabrachial nucleus; pc, posterior commissure; PF, parafascicular nucleus; PH, nucleus prepositus hypoglossi; Pm, medial preoptic nucleus; PM, paramamillary nucleus; PN, pontine nuclei; PP, peripeduncular nucleus; PR, paramedian reticular nucleus; PRF, pontine reticular formation; PS, parasolitary nucleus; pt, pyramidal tract; PTA, pretectal area; PU, pulvinar nucleus; PUi, pulvinar nucleus pars inferior; PUl, pulvinar nucleus pars lateralis; PUm, pulvinar nucleus pars medialis; PV, periventricular nucleus (hypothalamus); Pv, ventral putamen; R, nucleus reticularis (thalamus); RE, nucleus reuniens (thalamus); RF, reticular formation; RM, nucleus raphe magnus; RN, red nucleus; RP, nucleus raphe pallidus; RTP, nucleus reticularis tegmenti pontis; SC, superior colliculus; SI, substantia innominata; sm, stria medullaris; SNc, substantia nigra pars compacta; SNr, substantia nigra pars reticulata; SO, superior olive; SON, supraoptic nucleus; ST, subthalamic nucleus; st, stria terminalis; tb, trapezoid body; TRF, tegmental reticular field; ts, solitary tract; V, ventricle; VA, nucleus ventralis anterior (thalamus); VDB, vertical limb of nucleus of diagonal band; Vl, inferior vestibular nucleus; VL, nucleus ventralis lateralis (thalamus); Vl, lateral vestibular nucleus; VM, ventromedial nucleus (hypothalamus); Vm, medial vestibular nucleus; VPL, nucleus ventralis posterolateralis (thalamus); VPM, nucleus ventralis posteromedialis (thalamus); Vs, superior vestibular nucleus; VTA, ventral tegmental area; ZI, zona incerta; 3, oculomotor nucleus; 4, trochlear nucleus; 6, abducens nucleus; 7, facial nucleus; 12, hypoglossal nucleus; M5, motor nucleus of trigeminal nerve; Me5, mesencephalic nucleus of trigeminal nerve; P5, principal nucleus of trigeminal nerve; S5, spinal nucleus of trigeminal nerve.

From Price and Amaral
Figure 25. Figure 25.

Representative coronal sections through forebrain of macaque monkey showing pattern of anterograde labeling after injection of amino acids into amygdaloid complex. Heaviest labeling is in nucleus accumbens (Ac), but there is also patchy labeling in caudate nucleus (Ca) and ventral portion of putamen (Pu). Labeling is particularly heavy in tail of caudate nucleus. Am, amygdala; Ca, caudate nucleus; CGL, lateral geniculate nucleus; Ch, cholinergic cell groups; GPv, globus pallidus, ventral division; OT, olfactory tubercle; ot, optic tract; PC, piriform cortex; Pu, putamen; Pul, pulvinar; R, red nucleus; S, septal nuclei. For other abbreviations see Fig. legend, p. 251.

From Russchen et al.
Figure 26. Figure 26.

Illustration of amygdalohippocampal projections in monkey brain. Representative coronal section through amygdala is shown at left and coronal section through hippocampal formation is shown at right. ABmg, accessory basal nucleus, magnocellular division; ABpc, accessory basal nucleus, parvicellular division; Bmg, basal nucleus, magnocellular division; Bpc, basal nucleus, parvicellular division; CA1, CA3, hippocampal fields; CEl, central nucleus, lateral division; CEm, central nucleus, medial division; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. legend, p. 251.

Figure 27. Figure 27.

A: illustrations of lateral, ventral, and medial surfaces of macaque monkey brain. Cortical fields indicated with nomenclature of Walker , Brodmann , and Bailey and Bonin . Insular cortex [dashed line surrounding lateral sulcus (Is)] is divided into agranular (la), dysgranular (Id), and granular (Ig) regions. B: shaded areas represent cortical regions that send direct projections to amygdala. C: shaded areas represent cortical regions that receive projections from amygdaloid complex. Question marks indicate that full extent of amygdaloid projections to these regions is not yet determined.

Figure 28. Figure 28.

Diagrams of lateral (left) and medial (right) surfaces of monkey, cat, and rat brains. Areas that project directly to amygdaloid complex are indicated by shading. Route by which sensory information attains these areas is also indicated (dashed arrows).

From Russchen
Figure 29. Figure 29.

Summary diagram showing topographic distribution of sensory projections to amygdaloid complex. Distribution of projections from sensory cortical areas (top panel) is indicated (with same stippling patterns) on 4 representative coronal sections through macaque monkey amygdala. a, Amygdaloid sulcus; AAA, anterior area of amygdala; AB, basal nucleus of amygdala; ABA, accessory basal nucleus of amygdala; AC, cortical nucleus of amygdala; ACA, claustral area of amygdala; ACe, central nucleus of amygdala; AL, lateral nucleus of amygdala; AM, medial nucleus of amygdala; C Ant, anterior commissure; Cd, caudate nucleus; CI, claustrum; Ea, entorhinal cortex, anterior part; En, endopiriform nucleus; erh, endorhinal sulcus; H, hippocampal formation; h, hippocampal sulcus; IA, insula cortex, anterior part; IB, insula cortex, posterior part; Pe, perirhinal cortex; Pi f, piriform cortex, frontal part; Pi t, piriform cortex; temporal part; Pr, prorhinal cortex; Put, putamen; rh, rhinal sulcus; SI‐B, substantia innominata—basal nucleus of Meynert; SI‐DB, substantia innominata—diagonal band; SOL, lateral olfactory stria; TA, superior temporal cortex; TE, inferior temporal cortex; TEO, inferior temporal cortex, posterior part; TG, temporal polar cortex; T Opt, optic tract; Tr, transition area; V Lat, lateral ventricle.

From Turner et al.
Figure 30. Figure 30.

Coronal section through macaque monkey thalamus. Mediodorsal nucleus is divided into magnocellular (or medial) (MDmc), parvicellular (or lateral) (MDpc), and multiform or paralaminar (MDmf) divisions.

From Olszewski
Figure 31. Figure 31.

Summary diagram of thalamic projections to monkey frontal cortex. Injections of retrograde tracers into regions (different shading patterns, top right) result in retrograde labeling of neurons in bands indicated in representative coronal sections of monkey thalamus at left. Panels (lower right) show same bands of labeling in horizontal sections through thalamus. A, anterior thalamus; CE, midline nuclei; CL, central lateral nucleus; CM‐PF, centromedian‐parafascicular complex; MGB, medial geniculate body; PCN, paracentral nucleus; PUL, pulvinar; VIM, ventral intermediate nucleus. For other abbreviations see Fig. legend, p. 251.

From Kievit and Kuypers
Figure 32. Figure 32.

Diagrammatic summary of distribution of projections from various regions of frontal cortex to mediodorsal thalamus of macaque monkey. CM‐Pf, centromedian‐parafascicular complex; Cif, nucleus centralis, inferior division; MD, mediodorsal nucleus (mc, magnocellular division; pc, parvicellular division; mf, multiform or paralaminar division; de, densocellular division).

From Akert and Hartmann‐von Monakow
Figure 33. Figure 33.

Distribution of labeled cells after injection of retrograde tracer into magnocellular division of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al.
Figure 34. Figure 34.

Distribution of labeled cells after injection of retrograde tracer into parvicellular portion of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al.
Figure 35. Figure 35.

Distribution of neurofibrillary tangles (NFT) plotted onto coronal section of hippocampal formation from brain of patient with Alzheimer's disease. Each dot represents one neurofibrillary tangle. CA1, CA2–3, hippocampal fields; CA4, hilar region of dentate gyrus; NEO, neocortex; PRE, presubiculum; Pr2, prorhinal cortex; SUB, subiculum; 35, perirhinal cortex; 28, entorhinal cortex.

From Kemper
Figure 36. Figure 36.

Top: line drawings of coronal sections of human brain at levels through amygdaloid complex (left) and hippocampal formation (right); temporal stem (TEMP STEM) is labeled in each. Bottom: illustration showing dissection of left temporal lobe of human brain, which reveals fibers of temporal stem.

From Penfield


Figure 1.

Outlines of surface of macaque monkey brain show positions of major primary sensory cortices and of unimodal and polymodal association areas. Right: medial (top) and lateral (bottom) view of monkey brain. Primary visual cortex (VI), primary auditory cortex (AI), and primary somatosensory cortex (SI) are labeled, as is primary motor cortex (MI). Small numbers designate cortical fields as defined by Brodmann . AMG, amygdala; HIP, hippocampus, IPS, intraparietal sulcus; LF, lateral fissure; STS, superior temporal sulcus; TH and TF, fields of parahippocampal gyrus; TPO and PGa, polysensory fields on dorsal bank of superior temporal sulcus. Left: medial (top), lateral (middle), and ventral (bottom) surfaces of monkey brain. Approximate extents of primary (stippling) and secondary (vertical lines) unimodal association cortices are labeled. Positions of certain polysensory cortical regions (dotted shading) are also shown.

From Pandya and Seltzer


Figure 2.

Summary diagram showing progression of connections from primary sensory cortices to unimodal association cortices and finally to polymodal association areas. In each, dotted pattern shows projection origins and horizontal lines delimit termination regions. In somatosensory system, for example, primary somatosensory cortex (S) gives rise to projections to motor cortex (4) and to somatosensory association cortex (5). Area 5, in turn, gives rise to projections to premotor cortex (6) and to posterior parietal cortex (7). This latter region projects to polysensory zones in superior temporal sulcus (STS), cingulate gyrus (CG), and perirhinal cortex . A, primary auditory cortex; Am, amygdala; SM, supplementary motor cortex; STP, supratemporal plane; TG, temporal polar cortex.

Adapted from Jones and Powell


Figure 3.

Diagram illustrating progression of sensory information in visual system from primary visual cortex (OC) through successive association cortices (OB, OA, TEO, and TE) to amygdaloid complex. Unimodal visual input to amygdala arises from highest levels of hierarchy of cortical processing.

Adapted from Mishkin


Figure 4.

Four coronal sections through temporal lobe of macaque monkey brain (rostral to caudal) showing position of amygdaloid complex (A) and hippocampal formation (H) relative to other temporal lobe structures. Fibers that form portion of “temporal stem” (TS) are marked in B. Calibration marker, 5 mm. amts, Anterior middle temporal sulcus; f, fimbria; 51, piriform and periamygdaloid cortex; la, Id, Ig, insula cortex; ITG, inferior temporal gyrus; las, lateral sulcus; or, optic radiations; ots, occipitotemporal sulcus; pmts, posterior middle temporal sulcus; PU, putamen; PUL, pulvinar; rs, rhinal sulcus; STG, superior temporal gyrus; sts, superior temporal sulcus; TA, TE, TEO, TF, TG, TH, OA, OB, fields of temporal and occipital lobes according to Bailey and Bonin ; 35/36, perirhinal cortex. For other abbreviations see Fig. legend, p. 251.



Figure 5.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained human hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; EC, entorhinal cortex; f, fimbria; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum.



Figure 6.

Coronal sections through rostral (A) and caudal (B) portions of Nissl‐stained macaque monkey hippocampal formation. Calibration marker, 2 mm. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; PRC, perirhinal cortex; S, subiculum; TE, visual association isocortex; TF/TH, polymodal association cortex of parahippocampal gyrus. For other abbreviations see Fig. legend, p. 251.



Figure 7.

Surface maps showing demarcation, based on cytoarchitectonic criteria, of entorhinal cortex of humans (A) and macaque monkey (B) proposed by Rose . Similar map for monkey by Sgonina is shown in C, and subdivisions of entorhinal cortex by Van Hoesen and Pandya are illustrated in D. In each map, rostral is to left and mediodorsal is at top. Entorhinal cortex is differentiated along mediolateral and rostrocaudal gradients.



Figure 8.

Illustration of Golgi preparation from Lorente de Nó shows principal cell types in dentate gyrus (fascia dentata) and CA1 hippocampal field (cornu ammonis). Main cell type in dentate gyrus is granule cell (cells 7–12), which has unipolar dendritic tree that extends into molecular layer. A second class of neurons, basket pyramidal cells (cell 13), gives rise to GABAergic basket plexus that terminates around the granule cell bodies. Principal cell in hippocampus is pyramidal cell (cells 1–5), which has apical dendritic plexus that extends into overlying strata radiatum and lacunosum‐moleculare, and basal dendritic plume that extends into subjacent stratum oriens. There are also several classes of inhibitory interneurons in hippocampus, some of which are located in pyramidal cell layer (cell 6) and in other strata as well.

From Lorente de Nó


Figure 9.

Illustration of Golgi‐stained neurons in mouse hippocampus from Lorente de Nó . Large cells of polymorphic region of dentate gyrus (cells 21 and 22, “mossy cells”) and pyramidal cells of the CA3 region (cells 8 and 10–19) have specialized spines (thorny excrescences) on their proximal dendrites, which are primary termination of mossy fibers from dentate gyrus. Interneuron of basket type is pictured as cell 9. Note that the pyramidal cells of CA2 region do not have large spines on their proximal dendrites and do not receive mossy fiber input. They are, however, much larger than adjoining pyramidal cells of CA1 region.

From Lorente de Nó


Figure 10.

Simplified circuit diagram demonstrating fundamental “trisynaptic” circuit of rat hippocampus. Fibers originating in entorhinal cortex (perforant path, pp) travel through subiculum and terminate on dendrites of granule cells in outer two‐thirds of molecular layer of dentate gyrus. Granule cells give rise to axons (mossy fibers, mf), which terminate on CA3 pyramidal cells. CA3 pyramidal cells project to CA1 region (Schaffer collaterals, sc). Because of “lamellar organization” of hippocampus, slices cut perpendicular to its long axis contain an intact chain of these connections.



Figure 11.

Line drawings of coronal section through monkey hippocampal formation on which major intrinsic and extrinsic efferent projections are plotted. A: various fields that comprise hippocampal formation are labeled and fundamental trisynaptic circuit is drawn [entorhinal cortex to dentate gyrus (1), dentate gyrus to hippocampal field CA3 (2), field CA3 to field CA1 (3)]. B: in addition to projecting to field CA3 (1), mossy fibers arising from dentate granule cells terminate on polymorphic cells of hilar region (2); these cells give rise to ipsilateral associational and commissural projections that terminate in molecular layer (3). CA3 pyramidal cells give rise to associational projections to other levels of field CA3 (5, 6) in addition to their projection to field CA1 (4). CA1 pyramidal cells project to subiculum (7), presubiculum (8), and entorhinal cortex (9). Cells in subiculum, presubiculum, and parasubiculum send a major projection to entorhinal cortex (10, 11, and 12, respectively). C: Projections to septal nuclei are diagramed. Field CA3 of hippocampus projects bilaterally to lateral septum (1) and field CA1 projects ipsilaterally (2). Subiculum also projects to lateral septum (3) and to nucleus accumbens (4). Entorhinal cortex projects to nucleus accumbens (5) and caudate nucleus and putamen (6). D: projections to diencephalon. Subiculum projects bilaterally to medial mamillary nucleus (1), whereas presubiculum projects primarily to lateral mamillary nucleus (2). Presubiculum also projects lightly to medial mamillary nucleus as does entorhinal cortex (3). Projection to anterior thalamus originates primarily in presubiculum and it terminates bilaterally (4). E: projections to amygdaloid complex. Both subiculum (1) and entorhinal cortex (2) project to parvicellular portion of basal nucleus; entorhinal cortex also projects to lateral nucleus (3). F: projections to neocortex. Although corticopetal projections of hippocampal formation are relatively unstudied, there is evidence for projections from both subicular complex and entorhinal cortex to cortical fields listed. AT, anterior thalamic nuclei; B, basal nucleus of amygdala; CA1, CA3, fields of hippocampus; DG, dentate gyrus; f, fornix; LM, lateral mamillary nucleus; LS, lateral septal nucleus; MM, medial mamillary nucleus; NA, nucleus accumbens; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. legend, p. 251.



Figure 12.

Distribution of preterminal axons in entorhinal cortex arising from subfields of subicular complex. Projections from subiculum terminate in deep layers, whereas those from presubiculum end mainly in layer III and those from parasubiculum end in layer I.

From Köhler


Figure 13.

Summary diagram of commissural connections of monkey hippocampal formation. Top: extent of commissural fiber system is plotted (dotted lines) on lateral (left) and dorsal (right) views of brain. A: commissural projections of presubiculum and entorhinal cortex. Presubiculum (PrS) projects through hippocampal commissure (hc) to all levels of contralateral caudal entorhinal cortex (ECc). The ECc [but not rostral entorhinal cortex (ECr)] projects weakly to contralateral ECc and very lightly to posterior dentate gyrus (AD) and CA1 hippocampal field. B: rostral dentate gyrus and CA3 hippocampal field (H + AD) project to homotopic region of contralateral side. ab, Angular bundle; f, fimbria.

From Amaral et al.


Figure 14.

Ventromedial views of human (A) and macaque monkey (B) brains showing region of parahippocampal gyrus. cf, Calcarine fissure; cgs, cingulate sulcus; cos, collateral sulcus; ots, occipital temporal sulcus; rs, rhinal sulcus.

Courtesy of G. W. Van Hoesen


Figure 15.

Efferent projections of parahippocampal gyrus plotted on lateral (top) and medial (bottom) surfaces of macaque monkey brain. Numbers indicate cortical fields from nomenclature of Brodmann . Rsp, retrosplenial cortex.

Courtesy of G. W. Van Hoesen


Figure 16.

Photomicrographs of adjacent coronal sections through rostral hippocampal formation of monkey stained by Nissl method (A, bright field) or by immunohistochemical procedure for demonstration of somatostatin‐like immunoreactivity (B, dark‐field photomicrograph with immunoreactivity seen as light regions). Note particularly dense staining of molecular layer of dentate gyrus. CA1, CA2, CA3, hippocampal fields; DG, dentate gyrus (pl, polymorphic layer; ml, molecular layer); EC, entorhinal cortex; PaS, parasubiculum; PrS, presubiculum; rs, rhinal sulcus; S, subiculum. Small lettering in field CA1 indicates names of hippocampal laminae (a, alveus; o, stratum oriens; p, pyramidal cell layer; r, stratum radiatum; lm, stratum lacunosum‐moleculare). Calibration marker, 500 μm.



Figure 17.

Photomicrographs of coronal sections through macaque monkey mamillary complex arranged from rostral (A) to caudal (D). Each panel shows adjacent sections stained by Nissl method (top) or by reduced silver method for fibers (bottom). Calibration marker, 500 μm. f, Fornix; IC, intercalated nucleus; LMN, lateral mamillary nucleus; MMN, medial mamillary nucleus (MMNm pars medialis; MMNl, pars lateralis; MMNb, pars basalis); mp, mamillary peduncle; mtg, mamillotegmental tract; NG, nucleus gemini; PHN, posterior hypothalamic nucleus; pmt, principal mamillary tract; smc, supramamillary commissure; SUM, supramamillary area; TB, tuberomamillary nucleus. For other abbreviations see Fig. legend, p. 251.



Figure 18.

Photomicrographs of adjacent sections through monkey mamillary complex stained as in Fig. . Main component of mamillary complex is medial nucleus (MMN), which can be divided into medial (M), lateral (L), and basal (MMNb) divisions. Other major component is lateral mamillary nucleus (LMN). Associated with mamillary complex are tuberomamillary nucleus (TB) and paramamillary nucleus (PM). Note in B the dense plexus of fibers that invest LMN. Principal mamillary tract (pmt) arises from dorsal surface of medial mamillary nucleus.



Figure 19.

Summary diagram of efferent connections of primate mamillary complex. Medial nucleus (MM) projects ipsilaterally via principal mamillary tract (pmt) and mamillothalamic tract (mth) to anteromedial (AM) and anteroventral (AV) subdivisions of anterior thalamus and also to ventral tegmental nucleus (VT) via mamillotegmental tract (mtg). Fibers from lateral mamillary nucleus (LM) use same pathways to project bilaterally to anterodorsal nucleus of thalamus (AD) and to dorsal tegmental nucleus (DT).



Figure 20.

Diagram of efferent connections of the 2 major subdivisions (areas 23 and 24) of cingulate cortex. Note that anterior cingulate (area 24) projects heavily to amygdaloid complex and to perirhinal and entorhinal cortices. Posterior cingulate cortex (area 23) has prominent projections to parahippocampal gyrus (TH‐TF) and presubiculum. AMG, amygdala; AS, arcuate sulcus; CC, corpus callosum; CF, calcarine fissure; CING S, cingulate sulcus; CS, central sulcus; IOS, inferior occipital sulcus; IPS, intraparietal sulcus; LB, basal nucleus of amygdala; LF, lateral fissure; LS, lunate sulcus; OS, orbital sulcus; OTS, occipital temporal sulcus; PAR HIPP, parahippocampal gyrus; POMS, parieto‐occipital medial sulcus; Presub, presubiculum; PS, principal sulcus; RS, rhinal sulcus; rspl c, retrosplenial cortex; STS, superior temporal sulcus.

From Pandya et al.


Figure 21.

Coronal section through the Nissl‐stained amygdaloid complex of macaque monkey. Major subdivisions of amygdala include lateral nucleus (L); basal nucleus, which has magnocellular (Bmg), parvicellular (Bpc), and paralaminar (Bpl) subdivisions; accessory basal nucleus, which has magnocellular (ABmg) and parvicellular (ABpc) divisions; central nucleus, which has medial (Cm) and lateral (Cl) divisions; medial nucleus (M); cortical area (CO); and periamygdaloid cortex (PAC). Entorhinal cortex (EC), bounded laterally by rhinal sulcus (rs), is also shown; the 6 principal laminae are numbered.



Figure 22.

Amygdaloid complex of shrew in its normal orientation (A) and after being rotated ventrolaterally (B). In B, positions of major nuclei closely resemble those of human amygdala. ABa, accessory basal nucleus, magnocellular division; ABb, accessory basal nucleus, parvicellular division; Ba, basal nucleus, magnocellular division; Bb, basal nucleus, parvicellular division; C, cortical area; CE, central nucleus; I, intercalated nucleus; L, lateral nucleus; M, medial nucleus; O, nucleus of lateral olfactory tract.

From Crosby and Humphrey


Figure 23.

Intrinsic connections of monkey amygdaloid complex. Local projections of lateral nucleus (A), basal nucleus (B), accessory basal nucleus (C), and central and medial nuclei and periamygdaloid cortex (D) are indicated. Arrows ending within origin nucleus indicate associational projections. Note tendency for laterally placed nuclei to project to central and medial nuclei. AB, accessory basal nucleus; Bmg, magnocellular division of basal nucleus; Bp, parvicellular division of basal nucleus; CI, lateral division of central nucleus; Cm, medial division of central nucleus. For other abbreviations see Fig. legend, p. 251.



Figure 24.

Representative coronal sections through brain of macaque monkey, arranged from rostral (A) to caudal (L), showing distribution pattern of anterogradely labeled projections resulting from injection of tritiated amino acids into central nucleus of amygdala. Injection site is shown as blackened area in B and C. Labeled fibers are represented as dashed lines and terminal fields as dots. On left side of each section, triangles mark location of pigment‐containing, presumably monoaminergic neurons. ac, Anterior commissure; ACA, amygdaloclaustral area; AHA, amygdalohippocampal area; AM, anteromedial nucleus (thalamus); AN, arcuate nucleus (hypothalamus); AV, anteroventral nucleus (thalamus); BA, accessory basal nucleus (amygdala); BAm, accessory basal nucleus pars magnocellularis (amygdala); BAp, accessory basal nucleus pars parvocellularis (amygdala); bc, brachium conjunctivum; BL, basal nucleus (amygdala); BLm, basal nucleus pars magnocellularis (amygdala); BLp, basal nucleus pars parvicellularis (amygdala); BNM, basal nucleus of Meynert; BNST, bed nucleus of stria terminalis; bp, brachium pontis; C, central nucleus (amygdala); CBL, cerebellum; CD, caudate nucleus; Cde, nucleus centralis pars densocellularis (thalamus); CG, central gray; Cif, nucleus centralis inferior (thalamus); Cim, nucleus centralis intermedius (thalamus); CL, claustrum; Cl, nucleus centralis lateralis (thalamus); Clc, nucleus centralis pars laterocellularis (thalamus); CM, nucleus centralis medialis (thalamus); COa, anterior cortical nucleus (amygdala); COp, posterior cortical nucleus (amygdala); cp, cerebral peduncle; Cs, nucleus centralis superior (thalamus); CS, central superior raphe nucleus; DK, nucleus of Darkschewitsch; DM, dorsomedial nucleus (hypothalamus); DMN, dorsal motor nucleus of the vagus nerve; DR, dorsal raphe nucleus; EC, entorhinal cortex; EN, endopiriform nucleus; flm, medial longitudinal fasciculus; fm, fimbria; fx, fornix; GP, globus pallidus; GPe, globus pallidus (external); GPi, globus pallidus (internal); H, hippocampal formation; HB, habenular nuclei; HDB, horizontal limb of the nucleus of the diagonal band; IC, inferior colliculus; ic, internal capsule; IO, inferior olive; IP, interpeduncular nucleus; IS, interstitial nucleus; L, lateral nucleus (amygdala); LCd, nucleus locus coeruleus pars dorsalis; LCN, lateral cuneate nucleus; LCv, nucleus locus coeruleus pars ventralis; LD, laterodorsal nucleus (thalamus); If, lenticular fasciculus; LGN, lateral geniculate nucleus (thalamus); LH, lateral hypothalamus; LP, lateroposterior nucleus (thalamus); LR, lateral reticular nucleus; LT, lateral tuberal nucleus (hypothalamus); M, medial nucleus (amygdala); MD, mediodorsal nucleus (thalamus); MGN, medial geniculate nucleus (thalamus); Ml, lateral mamillary nucleus; ml, medial lemniscus; Mm, medial mamillary nucleus; NC, nucleus cuneiformis; NPC, nucleus of posterior commissure; NST, nucleus of solitary tract; NSTp, nucleus of solitary tract pars parvocellularis; oc, optic chiasm; ot, optic tract; P, putamen; PAC, periamygdaloid cortex; Pbl, lateral parabrachial nucleus; Pbm, medial parabrachial nucleus; pc, posterior commissure; PF, parafascicular nucleus; PH, nucleus prepositus hypoglossi; Pm, medial preoptic nucleus; PM, paramamillary nucleus; PN, pontine nuclei; PP, peripeduncular nucleus; PR, paramedian reticular nucleus; PRF, pontine reticular formation; PS, parasolitary nucleus; pt, pyramidal tract; PTA, pretectal area; PU, pulvinar nucleus; PUi, pulvinar nucleus pars inferior; PUl, pulvinar nucleus pars lateralis; PUm, pulvinar nucleus pars medialis; PV, periventricular nucleus (hypothalamus); Pv, ventral putamen; R, nucleus reticularis (thalamus); RE, nucleus reuniens (thalamus); RF, reticular formation; RM, nucleus raphe magnus; RN, red nucleus; RP, nucleus raphe pallidus; RTP, nucleus reticularis tegmenti pontis; SC, superior colliculus; SI, substantia innominata; sm, stria medullaris; SNc, substantia nigra pars compacta; SNr, substantia nigra pars reticulata; SO, superior olive; SON, supraoptic nucleus; ST, subthalamic nucleus; st, stria terminalis; tb, trapezoid body; TRF, tegmental reticular field; ts, solitary tract; V, ventricle; VA, nucleus ventralis anterior (thalamus); VDB, vertical limb of nucleus of diagonal band; Vl, inferior vestibular nucleus; VL, nucleus ventralis lateralis (thalamus); Vl, lateral vestibular nucleus; VM, ventromedial nucleus (hypothalamus); Vm, medial vestibular nucleus; VPL, nucleus ventralis posterolateralis (thalamus); VPM, nucleus ventralis posteromedialis (thalamus); Vs, superior vestibular nucleus; VTA, ventral tegmental area; ZI, zona incerta; 3, oculomotor nucleus; 4, trochlear nucleus; 6, abducens nucleus; 7, facial nucleus; 12, hypoglossal nucleus; M5, motor nucleus of trigeminal nerve; Me5, mesencephalic nucleus of trigeminal nerve; P5, principal nucleus of trigeminal nerve; S5, spinal nucleus of trigeminal nerve.

From Price and Amaral


Figure 25.

Representative coronal sections through forebrain of macaque monkey showing pattern of anterograde labeling after injection of amino acids into amygdaloid complex. Heaviest labeling is in nucleus accumbens (Ac), but there is also patchy labeling in caudate nucleus (Ca) and ventral portion of putamen (Pu). Labeling is particularly heavy in tail of caudate nucleus. Am, amygdala; Ca, caudate nucleus; CGL, lateral geniculate nucleus; Ch, cholinergic cell groups; GPv, globus pallidus, ventral division; OT, olfactory tubercle; ot, optic tract; PC, piriform cortex; Pu, putamen; Pul, pulvinar; R, red nucleus; S, septal nuclei. For other abbreviations see Fig. legend, p. 251.

From Russchen et al.


Figure 26.

Illustration of amygdalohippocampal projections in monkey brain. Representative coronal section through amygdala is shown at left and coronal section through hippocampal formation is shown at right. ABmg, accessory basal nucleus, magnocellular division; ABpc, accessory basal nucleus, parvicellular division; Bmg, basal nucleus, magnocellular division; Bpc, basal nucleus, parvicellular division; CA1, CA3, hippocampal fields; CEl, central nucleus, lateral division; CEm, central nucleus, medial division; DG, dentate gyrus; PaS, parasubiculum; PrS, presubiculum; S, subiculum. For other abbreviations see Fig. legend, p. 251.



Figure 27.

A: illustrations of lateral, ventral, and medial surfaces of macaque monkey brain. Cortical fields indicated with nomenclature of Walker , Brodmann , and Bailey and Bonin . Insular cortex [dashed line surrounding lateral sulcus (Is)] is divided into agranular (la), dysgranular (Id), and granular (Ig) regions. B: shaded areas represent cortical regions that send direct projections to amygdala. C: shaded areas represent cortical regions that receive projections from amygdaloid complex. Question marks indicate that full extent of amygdaloid projections to these regions is not yet determined.



Figure 28.

Diagrams of lateral (left) and medial (right) surfaces of monkey, cat, and rat brains. Areas that project directly to amygdaloid complex are indicated by shading. Route by which sensory information attains these areas is also indicated (dashed arrows).

From Russchen


Figure 29.

Summary diagram showing topographic distribution of sensory projections to amygdaloid complex. Distribution of projections from sensory cortical areas (top panel) is indicated (with same stippling patterns) on 4 representative coronal sections through macaque monkey amygdala. a, Amygdaloid sulcus; AAA, anterior area of amygdala; AB, basal nucleus of amygdala; ABA, accessory basal nucleus of amygdala; AC, cortical nucleus of amygdala; ACA, claustral area of amygdala; ACe, central nucleus of amygdala; AL, lateral nucleus of amygdala; AM, medial nucleus of amygdala; C Ant, anterior commissure; Cd, caudate nucleus; CI, claustrum; Ea, entorhinal cortex, anterior part; En, endopiriform nucleus; erh, endorhinal sulcus; H, hippocampal formation; h, hippocampal sulcus; IA, insula cortex, anterior part; IB, insula cortex, posterior part; Pe, perirhinal cortex; Pi f, piriform cortex, frontal part; Pi t, piriform cortex; temporal part; Pr, prorhinal cortex; Put, putamen; rh, rhinal sulcus; SI‐B, substantia innominata—basal nucleus of Meynert; SI‐DB, substantia innominata—diagonal band; SOL, lateral olfactory stria; TA, superior temporal cortex; TE, inferior temporal cortex; TEO, inferior temporal cortex, posterior part; TG, temporal polar cortex; T Opt, optic tract; Tr, transition area; V Lat, lateral ventricle.

From Turner et al.


Figure 30.

Coronal section through macaque monkey thalamus. Mediodorsal nucleus is divided into magnocellular (or medial) (MDmc), parvicellular (or lateral) (MDpc), and multiform or paralaminar (MDmf) divisions.

From Olszewski


Figure 31.

Summary diagram of thalamic projections to monkey frontal cortex. Injections of retrograde tracers into regions (different shading patterns, top right) result in retrograde labeling of neurons in bands indicated in representative coronal sections of monkey thalamus at left. Panels (lower right) show same bands of labeling in horizontal sections through thalamus. A, anterior thalamus; CE, midline nuclei; CL, central lateral nucleus; CM‐PF, centromedian‐parafascicular complex; MGB, medial geniculate body; PCN, paracentral nucleus; PUL, pulvinar; VIM, ventral intermediate nucleus. For other abbreviations see Fig. legend, p. 251.

From Kievit and Kuypers


Figure 32.

Diagrammatic summary of distribution of projections from various regions of frontal cortex to mediodorsal thalamus of macaque monkey. CM‐Pf, centromedian‐parafascicular complex; Cif, nucleus centralis, inferior division; MD, mediodorsal nucleus (mc, magnocellular division; pc, parvicellular division; mf, multiform or paralaminar division; de, densocellular division).

From Akert and Hartmann‐von Monakow


Figure 33.

Distribution of labeled cells after injection of retrograde tracer into magnocellular division of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al.


Figure 34.

Distribution of labeled cells after injection of retrograde tracer into parvicellular portion of mediodorsal nucleus of thalamus. Each dot represents one retrogradely labeled cell.

From Russchen et al.


Figure 35.

Distribution of neurofibrillary tangles (NFT) plotted onto coronal section of hippocampal formation from brain of patient with Alzheimer's disease. Each dot represents one neurofibrillary tangle. CA1, CA2–3, hippocampal fields; CA4, hilar region of dentate gyrus; NEO, neocortex; PRE, presubiculum; Pr2, prorhinal cortex; SUB, subiculum; 35, perirhinal cortex; 28, entorhinal cortex.

From Kemper


Figure 36.

Top: line drawings of coronal sections of human brain at levels through amygdaloid complex (left) and hippocampal formation (right); temporal stem (TEMP STEM) is labeled in each. Bottom: illustration showing dissection of left temporal lobe of human brain, which reveals fibers of temporal stem.

From Penfield
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David G. Amaral. Memory: Anatomical Organization of Candidate Brain Regions. Compr Physiol 2011, Supplement 5: Handbook of Physiology, The Nervous System, Higher Functions of the Brain: 211-294. First published in print 1987. doi: 10.1002/cphy.cp010507