Connections of inferior temporal areas TE and TEO with medial temporal-lobe structures in infant and adult monkeys

As part of a long-term study designed to examine the ontogeny of visual memory in monkeys and its underlying neural circuitry, we have examined the connections between inferior temporal cortex and medial temporal-lobe structures in infant and adult monkeys. Inferior temporal cortical areas TEO and TE were injected with WGA conjugated to HRP and tritiated amino acids, respectively, or vice versa, in 1-week-old and 3-4-yr-old Macaca mulatta, and the distributions of labeled cells and terminals were examined in both limbic structures and temporal-lobe cortical areas. In adult monkeys, inferior temporal-limbic connections included projections from area TEO to the dorsal portion of the lateral nucleus of the amygdala and from area TE to the lateral and lateral basal nuclei; inputs to both areas TEO and TE included those from the lateral, lateral basal, and medial basal nuclei of the amygdala and to area TE from the accessory basal nucleus. Additional limbic inputs to both areas TEO and TE arose from the posterior portion of the presubiculum. In infant monkeys, we found, in addition to these adultlike connections, a projection from area TEO to the lateral basal nucleus of the amygdala. Inferior temporal cortical connections in adult monkeys included projections from area TEO to area TE and, in turn, from area TE to area TG and perirhinal area 36, as well as from area TE back to area TEO; inputs to both areas TEO and TE included those from area TG, perirhinal areas 35 and 36, and parahippocampal areas TF and TH. All of these adultlike connections were also observed in infant monkeys, but, in addition, the infants showed projections from area TE to perirhinal area 35 as well as to parahippocampal areas TF and TH, and from area TEO to area TF. Moreover, in infants, the projection from area TE to perirhinal area 36 was considerably more widespread than in adults, both in areal extent and in laminar distribution. The results therefore indicate the existence of projections in infant monkeys from inferior temporal areas to the amygdala, perirhinal cortex, and parahippocampal cortex that are either totally eliminated in adults or more refined in their distribution. Both elimination and refinement of projections thus appear to characterize the maturation of axonal pathways between the inferior temporal cortex and medial temporal-lobe structures in monkeys.     

Cortical connections of inferior temporal area TEO in macaque monkeys

In macaque monkeys, lesions involving the posterior portion of the inferior temporal cortex, cytoarchitectonic area TEO, produce a severe impairment in visual pattern discrimination. Recently, this area has been shown to contain a complete, though coarse, representation of the contralateral visual field (Boussaoud, Desimone, and Ungerleider: J. Comp. Neurol. 306:554–575, '91). Because the inputs and outputs of area TEO have not yet been fully described, we injected a variety of retrograde and anterograde tracers into 11 physiologically identified sites within TEO of seven rhesus monkeys and analyzed the areal and laminar distribution of its cortical connections. Our results show that TEO receives feedforward, topographically organized inputs from prestriate areas V2, V3, and V4. Additional sparser feedforward inputs arise from areas V3A, V4t, and MT. Each of these inputs is reciprocated by a feedback projection from TEO. TEO was also found to have reciprocal intermediate-type connections with the fundus of the superior temporal area (area FST), cortex in the most posteromedial portion of the superior temporal sulcus (the posterior parietal sulcal zone [area PP]), cortex in the intraparietal sulcus (including the lateral intraparietal area [area LIP]), the frontal eye field, and area TF on the parahippocampal gyrus. The connections with V3A, V4t, and PP were found only after injections in the peripheral field representations of TEO. Finally, TEO was found to project in a feedforward pattern to area TE and to areas anterior to FST on the lateral bank and floor of the superior temporal sulcus (areas TEm, TEa, and IPa, Seltzer and Pandya: Brain Res. 149:1–24, '78), all of which send feedback projections to TEO. Feedback projections also arise from parahippocampal area TH, and areas TG, 36, and possibly 35. These are complemented by only sparse feedforward projections to TG from central field representations in TEO and to TH from peripheral field representations. The results thus indicate that TEO forms an important link in the occipitotemporal pathway for object recognition, sending visual information forward from V1 and prestriate relays in V2–V4 to anterior inferior temporal area TE. © 1993 Wiley-Liss, Inc.

1 This article is a US Goveriiment work and, as such, is in the public domain in the United States of America.

     

Organization of the amygdalopetal projections from modality-specific cortical association areas in the monkey

As part of an attempt to understand how sensory stimuli influence emotional processes we examined all of the telencephalic sensory systems of the rhesus monkey for efferents to the amygdala and immediately surrounding structures, using primarily the Fink-Heimer technique. The results support the following conclusions. 1. All sensory systems contain areas that project to the amygdaloid complex (the somatosensory system, tentatively so), but not to more central limbic structures in the basal forebrain and hypothalamus. Consequently, whatever influence the sensory systems have on emotional processes mediated by these more central limbic structures is likely to depend largely on relays through the amygdala. 2. Except for the olfactory system, the amygdalopetal projections arise only from the later stages of cortical processing within each sensory system, i.e., from the modality-specific association areas one or more steps removed from the primary sensory areas. Thus, the modality-specific cortical sources of the amygdalopetal projections, like their amygdaloid targets, are important links in the sensory-limbic pathways. These sources are: for vision, areas TE and ventral TG; for audition, anterior TA and dorsal TG; for taste, area IA; and for somesthesis, possibly areas IA or IB. The amygdalopetal sources thus occupy a limited territory that begins dorsally in the anterior insula and extends ventrally across the anterior temporal neocortex as far as the rhinal fissure. 3. Within the visual system, progressively heavier and more widespread efferents arise from successively later stages of the amygdalopetal sources. The posterior half of TE sends a moderate projection to the dorsal part of the lateral nucleus, the anterior half of TE sends a heavy projection to the dorsal parts of both the lateral and basal nuclei, and the ventral part of TG sends a heavy projection to the dorsal and medial parts of the lateral and basal nuclei and to the dorsal part of the basal accessory nucleus. This pattern of progressive intensification and spread of the amygdalopetal projections applies also to the auditory system and probably to the other cortical sensory systems as well. The pattern suggests that a progressively greater influence on amygdaloid activity is exerted by successively more highly processed sensory information. 4. The efferents to the amygdaloid complex from the different sensory systems terminate in a dovetailed pattern. The major amygdaloid targets are: for vision, the anterodorsal parts of the lateral, basal, and basal accessory nuclei; for audition, the posterior parts of the lateral and basal accessory nuclei; for taste, the medial parts of the lateral and basal nuclei; and for olfaction, the cortical and medial nuclei. This pattern implies that each part of the amygdala is under the major influence of a particular sensory system. 5. The same cortical areas that give rise to separate sensory channels to the amygdala send efferents that converge upon the perirhinal and prorhinal cortices, areas known to be a major source of input to the hippocampus. Consequently, both the amygdala and hippocampus can be activated by the same highly processed sensory information, a conclusion that may help to account for a recent finding that these two structures can substitute for each other in a mechanism for recognition memory.     

Intrinsic connections of the rat amygdaloid complex: Projections originating in the accessory basal nucleus

The amygdaloid complex plays an important role in the detection of emotional stimuli, the generation of emotional responses, the formation of emotional memories, and perhaps other complex associational processes. These functions depend upon the flow of information through intricate and poorly understood circuitries within the amygdala. As part of an ongoing project aimed at further elucidating these circuits, we examined the intra-amygdaloid connections of the acessory basal nucleus in the rat. In addition, we examined connections of the anterior cortical nucleus and amygdalahippocampal area to determine whether portions of these nuclei should be included in the accessory basal nucleus (as some earlier studies suggest). Phaseolus vulgaris leucoagglutinin was injected into different rostrocaudal levels of the accessory basal nucleus (n = 12) or into the anterior cortical nucleus (n = 3) or amygdalahippocampal area (n = 2). The major intra-amygdaloid projections from the accessory basal nucleus were directed to the medial and capsular divisions of the central nucleus, the medial division of the amygdalohippocampal area, the medial division of the lateral nucleus, the central division of the medial nucleus, and the posterior cortical nucleus. The projections originating in the anterior cortical nucleus and the lateral division of the amygdalohippocampal area differed from those originating in the accessory basal nucleus, which suggests that these areas are not part of the deep amygdaloid nuclei have different intra-amygdaloid connections. The pattern of these various connections suggests that information entering the amygdala from different sources can be integrated only in certain amygdaloid regions. © 1996 Wiley-Liss, Inc.     

Lesions of inferior temporal area TE in infant monkeys alter cortico-amygdalar projections.

When inferior temporal area TE is removed bilaterally in infant monkeys, the normally transient projection from area TEO to the lateral basal nucleus of the amygdala is maintained, and the normally limited projection from area TEO to the dorsal part of the lateral nucleus of the amygdala expands to invade the terminal space in the lateral nucleus that is normally occupied by terminals from area TE. The maintenance and sprouting of these projections from area TEO could play a role in the permanent preservation of visual memory ability in monkeys that have received bilateral removal of area TE in infancy.     

Some observations on cortical inputs to the macaque monkey amygdala: an anterograde tracing study

We have previously described the origins of neocortical inputs to the lateral nucleus of the macaque monkey amygdala based on retrograde tracing studies. Here we report results from studies that have attempted to confirm the projections from several candidate afferent regions using (3)H-amino acid autoradiography as an anterograde tracer. We have charted, based on the results of 33 separate injections, the topographic distribution of cortical projections throughout the amygdala. Areas TE and TEO of the inferotemporal cortex, portions of the superior temporal gyrus, and the granular region of the insula project primarily to the lateral nucleus, with little or no innervation of other amygdaloid nuclei. In contrast, orbitofrontal, medial prefrontal, and anterior cingulate regions project primarily to the basal and accessory basal nuclei and provide little innervation to the lateral nucleus. The orbitofrontal and medial prefrontal cortices, but not the anterior cingulate cortex, project to medially situated amygdaloid areas such as the cortical and medial nuclei and to the periamygdaloid cortex. The agranular and dysgranular insula, the parainsula, and rostral portions of the superior temporal gyrus project both to the lateral, basal, and accessory basal nuclei and to the medially situated nuclei. Projections to the central nucleus are particularly prominent from these regions. These data are discussed in relation to the hierarchical processing of sensory information that occurs within the amygdaloid complex.     

The organization of projections from the amygdala to visual cortical areas TE and V1 in the macaque monkey

We examined the organization of amygdaloid projections to visual cortical areas TE and V1 by injecting anterograde tracers into the amygdaloid complex of Macaca fascicularis monkeys. The magnocellular and intermediate divisions of the basal nucleus of the amygdala gave rise to heavy projections to both superficial layers (border of I/II) and deep layers (V/VI) throughout the rostrocaudal extent of area TE. Although most of the injections led to heavier fiber and terminal labeling in the superficial layers of area TE, the most dorsal injections in the basal nucleus produced denser labeled fibers and terminals in the deep layers of area TE. Area V1 received projections primarily from the magnocellular division of the basal nucleus, and these terminated exclusively in the superficial layers. As in area TE, projections from the amygdala to area V1 were distributed throughout its rostrocaudal and transverse extents. Labeled axons demonstrated 11.67 varicosities/100 microm on average in the superficial layers of area TE and 8.74 varicosities/100 microm in the deep layers. In area V1 we observed 8.24 varicosities/100 microm. Using confocal microscopy, we determined that at least 55% of the tracer-labeled varicosities in areas TE and V1 colocalized synaptophysin, a marker of synaptic vesicles, indicating that they are probably synaptic boutons. Electron microscopic examination of a sample of these varicosities confirmed that labeled boutons formed synapses in areas TE and V1. These feedback-like projections from the amygdala have the potential of modulating key areas of the visual processing system.     

Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque

To identify the cortical connections of the medial superior temporal (MST) and fundus of the superior temporal (FST) visual areas in the extrastriate cortex of the macaque, we injected multiple tracers, both anterograde and retrograde, in each of seven macaques under physiological control. We found that, in addition to connections with each other, both MST and FST have widespread connections with visual and polysensory areas in posterior prestriate, parietal, temporal, and frontal cortex. In prestriate cortex, both areas have connections with area V3A. MST alone has connections with the far peripheral field representations of V1 and V2, the parieto-occipital (PO) visual area, and the dorsal prelunate area (DP), whereas FST alone has connections with area V4 and the dorsal portion of area V3. Within the caudal superior temporal sulcus, both areas have extensive connections with the middle temporal area (MT), MST alone has connections with area PP, and FST alone has connections with area V4t. In the rostral superior temporal sulcus, both areas have extensive connections with the superior temporal polysensory area (STP) in the upper bank of the sulcus and with area IPa in the sulcal floor. FST also has connections with the cortex in the lower bank of the sulcus, involving area TEa. In the parietal cortex, both the central field representation of MST and FST have connections with the ventral intraparietal (VIP) and lateral intraparietal (LIP) areas, whereas MST alone has connections with the inferior parietal gyrus. In the temporal cortex, the central field representation of MST as well as FST has connections with visual area TEO and cytoarchitectonic area TF. In the frontal cortex, both MST and FST have connections with the frontal eye field. On the basis of the laminar pattern of anterograde and retrograde label, it was possible to classify connections as forward, backward, or intermediate and thereby place visual areas into a cortical hierarchy. In general, MST and FST receive forward inputs from prestriate visual areas, have intermediate connections with parietal areas, and project forward to the frontal eye field and areas in the rostral superior temporal sulcus. Because of the strong inputs to MST and FST from area MT, an area known to play a role in the analysis of visual motion, and because MST and FST themselves have high proportions of directionally selective cells, they appear to be important stations in a cortical motion processing system.     

Fiber pathways and cortical connections of preoccipital areas in rhesus monkeys

An understanding of visual function at the cerebral cortical level requires detailed knowledge of anatomical connectivity. Cortical association pathways and terminations of preoccipital visual areas were investigated in rhesus monkeys by using the autoradiographic tracing technique. Medial and adjacent dorsomedial preoccipital regions project via the occipitofrontal fascicle to the frontal lobe (dorsal area 6, and areas 8Ad, 8B, and 46); via the dorsal portion of the superior longitudinal fascicle (SLF) to dorsal area 6, area 9, and the supplementary motor area; and via the cingulate fascicle to area 24. In addition, medial and dorsomedial preoccipital areas send projections to parietal (areas PGm, PEa, PG‐Opt, and POa) and superior temporal (areas MST and MT) regions. In contrast, connections from the dorsolateral, annectant, and ventral preoccipital regions are conveyed via the inferior longitudinal fascicle (ILF) to the parietal lobe (areas POa and IPd), superior temporal sulcus (areas MT, MST, FST, V4t, and IPa), inferotemporal region (areas TEO and TE1–TE3), and parahippocampal gyrus (areas TF, TH, and TL). The central‐lateral preoccipital region projects via an ILF‐SLF pathway to frontal area 8Av. The preoccipital areas also have caudal connections to occipital areas V1, V2, and V3. Finally, preoccipital regions are interconnected via different intrinsic pathways. These findings provide further insight into the nature of preoccipital fiber pathways and the connectional organization of the visual system. J. Comp. Neurol. 518:3725–3751, 2010. © 2010 Wiley‐Liss, Inc.     

Comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: II. Reciprocal and non-reciprocal connections

The pattern of direct connections between the amygdala and the hippocampal formation in the rhesus monkey (Macaca mulatta) was delineated by using both anterograde and retrograde tract-tracing techniques. From the amygdala the accessory basal, medial basal, and the cortical nuclei and the cortical amygdaloid transition area send projections to the hippocampal formation. The efferents from the magnocellular part of the accessory basal nucleus and the cortical nuclei terminate in the molecular layer of subfields CA3, CA2, and CA1', and to a lesser extent in the molecular layer and the superficial part of the pyramidal cell layers of the prosubiculum. In contrast, the projections from the medial basal nucleus and the cortical amygdaloid transition area terminate in the molecular layer and the superficial part of the pyramidal cell layers of the prosubiculum only. From the hippocampal formation, subfield CA1' and the prosubiculum send efferents that terminate in the medial basal nucleus, the cortical transition area, and the ventral part of the cortical nuclei. In addition, the CA1' subfield projects to the ventral, parvicellular part of the accessory basal nucleus. The present data emphasize an important role for the prosubiculum and the CA1' subfield in medial temporal lobe area connections. Both regions, in addition to supporting direct connections between the amygdala and the hippocampal formation, also have extensive connections with the entorhinal cortex. As for the amygdala, the accessory basal nucleus sends efferents to both the hippocampal formation and the entorhinal cortex. The data demonstrate an anatomical means by which the amygdala, hippocampal formation, and the entorhinal cortex may interact. It is proposed that these connections may be important in the limbic memory system.     

Organization of connections between the amygdaloid complex and the perirhinal and parahippocampal cortices in macaque monkeys

Neuroanatomical studies in macaque monkeys have demonstrated that the perirhinal and parahippocampal (PRPH) cortices are strongly interconnected with the hippocampal formation. Recent behavioral evidence indicates that these cortical regions are importantly involved in normal recognition memory function. The PRPH cortices are also interconnected with the amygdaloid complex, although comparatively little is known about the precise topography of these connections. We investigated the topographic organization of reciprocal connections between the amygdala and the PRPH cortices by placing anterograde and retrograde tracers throughout these three regions. We found that there was an organized arrangement of connections between the amygdala and the PRPH cortices and that the deep (lateral, basal, and accessory basal) nuclei of the amygdaloid complex were the source of most connections between the amygdala and the PRPH cortices. The temporal polar regions of the perirhinal cortex had the strongest and most widespread interconnections with the amygdala. Connections from more caudal levels of the perirhinal cortex had a more discrete pattern of termination. Perirhinal inputs to the amygdala terminated primarily in the lateral nucleus, the magnocellular and parvicellular divisions of the basal nucleus, and the magnocellular division of the accessory basal nucleus. Return projections originated predominately in the lateral nucleus, the intermediate and parvicellular divisions of the basal nucleus, and the magnocellular division of the accessory basal nucleus. The interconnections between the amygdala and the parahippocampal cortex were substantially less robust than those with the perirhinal cortex and mainly involved the basal nucleus. Area TF was more strongly interconnected with the amygdala than was area TH. Input from the parahippocampal cortex terminated predominantly in the lateral half of the parvicellular division of the basal nucleus but also to a lesser extent in the magnocellular division of the basal nucleus and the lateral nucleus. Return projections originated predominantly in the magnocellular division of the basal nucleus and were directed almost exclusively to area TF. © 1996 Wiley-Liss, Inc.     

Projections from the amygdaloid complex to the claustrum and the endopiriform nucleus: a Phaseolus vulgaris leucoagglutinin study in the rat

The claustrum and the endopiriform nucleus contribute to the spread of epileptiform activity from the amygdala to other brain areas. Data of the distribution of pathways underlying the information flow between these regions are, however, incomplete and controversial. To investigate the projections from the amygdala to the claustrum and the endopiriform nucleus, we injected the anterograde tracer Phaseolus vulgaris leucoagglutinin into various divisions of the amygdaloid complex, including the lateral, basal, accessory basal, central, anterior cortical and posterior cortical nuclei, the periamygdaloid cortex, and the amygdalohippocampal area in the rat. Analysis of immunohistochemically processed sections reveal that the heaviest projections to the claustrum originate in the magnocellular division of the basal nucleus. The projection is moderate in density and mainly terminates in the dorsal aspect of the anterior part of the claustrum. Light projections from the parvicellular and intermediate divisions of the basal nucleus terminate in the same region, whereas light projections from the accessory basal nucleus and the lateral division of the amygdalohippocampal area innervate the caudal part of the claustrum. The most substantial projections from the amygdala to the endopiriform nucleus originate in the lateral division of the amygdalohippocampal area. These projections terminate in the central and caudal parts of the endopiriform nucleus. Lighter projections originate in the anterior and posterior cortical nuclei, the periamygdaloid cortex, the medial division of the amygdalohippocampal area, and the accessory basal nucleus. These data provide an anatomic basis for recent functional studies demonstrating that the claustrum and the endopiriform nucleus are strategically located to synchronize and spread epileptiform activity from the amygdala to the other brain regions. These topographically organized pathways also provide a route by means of which the claustrum and the endopiriform nucleus have access to inputs from the amygdaloid networks that process emotionally significant information.     

Thalamoamygdaloid projections in the rat: a test of the amygdala's role in sensory processing.

We used the autoradiographic tract-tracing method to define the amygdaloid projection fields after injecting 3H-amino acids into individual thalamic nuclei in the rat. The parvicellular division of the ventroposterior nucleus, the thalamic taste relay, projected lightly to the central and lateral amygdaloid nuclei. The central medial, interanteromedial, and paraventricular thalamic nuclei, viscerosensory relays of the thorax and abdomen, projected heavily to the amygdala. All projected to the basolateral amygdaloid nucleus, the paraventricular nucleus in addition having terminations in the central nucleus, the amygdaloid portion of the nucleus of the stria terminalis, and the amygdalohippocampal transition area. The magnocellular division of the medial geniculate, a thalamic auditory (and, to a moderate degree, a spinothalamic) relay, sent heavy projections to the central, accessory basal, lateral, and anterior cortical nuclei, and to the anterior amygdaloid area and the nucleus of the accessory olfactory tract. Other thalamic nuclei projecting to the amygdala, for which functions could not be associated, were the paratenial and subparafascicular nuclei. The former projected to the lateral, basal, and posterolateral cortical nuclei; the latter projected very lightly to the central, medial, and basal accessory nuclei. These results show that, like the cortical amygdaloid nuclei, which are sensory (olfactory) in nature, the subcortical amygdaloid nuclei must have major sensory functions. These thalamic afferents, when correlated with cortical and brainstem data from the literature, suggested that the amygdala is in receipt of sensory information from many modalities. To uncover the manner by which such information is processed by the amygdala and relayed to effector areas of the brain, six hypothetical mechanisms relating to modality specificity and convergence were posited. By charting sensory-related afferents to all subdivisions of the amygdala, each nucleus was characterized as to its mechanism of information processing. Four proposed amygdaloid systems emerged from this analysis. A unimodal corticomedial amygdaloid system relays pheromonal information from the accessory olfactory bulb to medial basal forebrain and hypothalamic areas. A second system--the lateral-basomedial--collects and combines input from a number of sensory modalities and distributes it to the same basal forebrain and hypothalamic areas as the corticomedial. The central system appears to concentrate the effect of viscerosensory information arriving from multiple brainstem, thalamic, cortical, and amygdaloid sources; this information is combined with significant auditory and spinothalamic inputs from the thalamus and cortex. The central system projects to lateral nuclei in the basal forebrain, hypothalamus, and brainstem.(ABSTRACT TRUNCATED AT 400 WORDS)     

Projections from the amygdaloid complex to the piriform cortex: A PHA-L study in the rat

Projections from the amygdala to the piriform cortex are proposed to provide a pathway via which the emotional system can modulate the processing of olfactory information as well as mediate the spread of seizure activity in epilepsy. To understand the details of the distribution and topography of these projections, we injected the anterograde tracer Phaseolus vulgaris-leucoagglutinin into different nuclear divisions of the amygdaloid complex in 101 rats and analyzed the distribution and density of projections in immunohistochemically processed preparations. The heaviest projections from the amygdala to the piriform cortex originated in the medial division of the lateral nucleus, the periamygdaloid and sulcal subfields of the periamygdaloid cortex, and the posterior cortical nucleus. The heaviest terminal labeling was observed in layers Ib and III of the medial aspect of the posterior piriform cortex. Lighter projections to the posterior piriform cortex originated in the dorsolateral division of the lateral nucleus, the magnocellular and parvicellular divisions of the basal and accessory basal nuclei, and the anterior cortical nucleus. The projections to the anterior piriform cortex were light and originated in the dorsolateral and medial divisions of the lateral nucleus, the magnocellular division of the basal and accessory basal nuclei, the anterior and posterior cortical nuclei, and the periamygdaloid subfield of the periamygdaloid cortex. The results indicate that only selective amygdaloid nuclei or their subdivisions project to the piriform cortex. In addition, substantial projections from several amygdaloid nuclei converge in the medial aspect of the posterior piriform cortex. Via these projections, the amygdaloid complex can modulate the processing of olfactory information in the piriform cortex. In pathologic conditions such as epilepsy, these connections might provide pathways for the spread of seizure activity from the amygdala to extra-amygdaloid regions.     

Connections of the amygdala of the rat. IV: Corticoamygdaloid and intraamygdaloid connections as studied with axonal transport of horseradish peroxidase

The corticoamygdaloid and intraamygdaloid projections of the rat were studied by the use of retrograde transport of horseradish peroxidase (HRP). Observations based on anterograde transport of the enzyme were exploited to determine the course of the intrinsic connections. The HRP was injected stereotactically by means of iontophoresis. Most of the amygdaloid nuclei were selectively injected, and all but a few were reached by more than one approach. The vast majority of corticoamygdaloid fibers was found to originate in cortical areas defined as allocortical (Stephan, 1975). From the medial frontal cortex the central amygdaloid nucleus (AC) receives a hitherto undescribed projection originating in the tenia tecta; and both the AC and the lateral amygdaloid nucleus (AL) receive fibers from the prelimbic and infralimbic areas. The anterior cingulate area entertains a weak connection with the basolateral amygdaloid nucleus (BL). As to the insular cortex, the posterior agranular insular area projects to all amygdaloid subdivisions; the BL, AC, and the anterior cortical nucleus (COa) receive, in addition, fibers from the ventral agranular area. The prepyriform cortex connects with the entire amygdala except the medial nucleus (Am) The amygdala receives afferents from a transitional area between the amygdala and the entorhinal area. The entorhinal area proper is related to the amygdala via projections from the ventral part of the lateral entorhinal area to the AL and from the dorsal part of the lateral entorhinal area to the BL. The former nucleus also receives fibers from the perirhinal region. Additional amygdalopetal connections from the hippocampal region include a previously undescribed projection from the temporal two-thirds of CA1 to the AL and BL and to the posterior cortical nucleus (COp) with the adjacent periamygdaloid cortex (PAC). The subiculum projects to the AL, and more modestly to other amygdaloid nuclei There is an extensive network of intraamygdaloid connections, the Am and AC being the only nuclei not giving rise to intrinsic fibers.     

A comparison of the efferents of the amygdala and the hippocampal formation in the rhesus monkey: I. Convergence in the entorhinal, prorhinal, and perirhinal cortices

This is the first in a series of papers investigating the neuroanatomical basis for the interaction of the amygdala and the hippocampal formation in the rhesus monkey. The present report focuses on the complementary and convergent projections of the amygdala and hippocampal formation to the entorhinal and perirhinal cortices. These results were obtained from complementary experiments using injections of radioactively labeled amino acids to identify the anterograde projection patterns and injections of horseradish peroxidase and fluorescent retrograde tracers to confirm the cytoarchitectonic location of the neurons of origin for each projection. The results of this investigation demonstrate that both the hippocampal formation and the amygdala project to the entorhinal and perirhinal cortices where, with a few exceptions, the major projections of each structure generally are found in different layers of the same cytoarchitecture subdivisions of the entorhinal cortex but overlap in the same layers of the perirhinal cortex. Thus, the lateral and accessory basal nuclei of the amygdala project to layer 3 of areas Pr1, 28I, 28L, and 28S, and the accessory basal nucleus projects strongly to layer 1 of these same areas. In contrast, the subiculum, prosubiculum, and subfield CA1 of the of the hippocampal formation all have a projection to layer 5 of these same areas. In area 28M, the accessory basal nucleus of the amygdala projects to layer 1, while the subiculum, prosubiculum, and subfield CA1 of the hippocampal formation all project to layer 5, and the presubiculum projects to layer 3. In addition to these complementary laminar projections, there are a few areas of laminar overlap. Thus in area 28S, both the presubiculum and the CA1 subfield project to layer 3, where the lateral and accessory basal amygdaloid nuclei also project. Similarly, in 28I there is a major projection from the presubiculum and a lighter projection from the subiculum and CA1 to layer 3, where the lateral and accessory basal nuclei also project. There is also extensive laminar overlap in the perirhinal cortex. From the amygdala, the accessory basal nucleus projects to layers 1 and 3 and the lateral basal nucleus to layers 3, 5, and 6, while from the hippocampal formation, the prosubiculum projects to layers 3, 5, and 6, and the CA1 subfield projects to layer 5. This pattern of hippocampal and amygdaloid projections to the entorhinal and perirhinal cortices indicates that these cortices constitute a region of potentially extensive interaction between the amygdala and the hippocampus.     

Projections from visual cortical areas of the superior temporal sulcus to the lateral terminal nucleus of the accessory optic system in macaque monkeys

Tritiated amino acids were injected into the striate area and in single visual areas of the superior temporal sulcus (STS) of 7 cynomolgus monkeys, in order to trace visual cortical projections to the nuclei of the accessory optic system (AOS). Injections in STS separately involved the areas MT and MST, and resulted in labels within the lateral terminal nucleus of the AOS. In no case were labels found within the AOS nuclei in the brains injected in the striate area, or within the contralateral AOS. It seems likely that the areas MT and MST contribute signals--selectively related to visual motion processing--to the AOS, which is probably involved in the neuronal pathway subserving the optokinetic reflex.     

The organization of the thalamocortical connections of the mediodorsal thalamic nucleus in the rat, related to the ventral forebrain-prefrontal cortex topography.

The medial and central segments of the mediodorsal nucleus of the thalamus (MD) receive afferents from the ventral forebrain, including the piriform cortex, the ventral pallidum, and the amygdaloid complex. Because MD is reciprocally interconnected with prefrontal and agranular insular cortical areas, it provides a relay of ventral forebrain activity to these cortical areas. However, there are also direct projections from the piriform cortex and the amygdala to the prefrontal and agranular insular cortices. This study addresses whether this system has a "triangular" organization, such that structures in the ventral forebrain project to interconnected areas in MD and the prefrontal/insular cortex. The thalamocortical projections of MD have been studied in experiments with injections of retrograde tracers into prefrontal or agranular insular cortical areas. In many of the same experiments, projections from the ventral forebrain to MD and to the prefrontal/insular cortex have been demonstrated with anterograde axonal tracers. The connections of the piriform cortex (PC) with MD and the prefrontal/insular cortex form an organized triangular system. The PC projections to the central and medial segments of MD and to the lateral orbital cortex (LO) and the ventral and posterior agranular insular cortices (AIv and AIp) are topographically organized, such that more caudal parts of PC tend to project more medially in MD and more caudally within the orbital/insular cortex. The central and medial portions of MD also send matching, topographically organized projections to LO, AIv and AIp, with more medial parts of MD projecting further caudally. The anterior cortical nucleus of the amygdala (COa) also projects to the dorsal part of the medial segment of MD and to its cortical targets, the medial orbital area (MO) and AIp. The projections of the basal/accessory basal amygdaloid nuclei to MD and to prefrontal cortex, and from MD to amygdaloceptive parts of prefrontal cortex, are not as tightly organized. Amygdalothalamic afferents in MD are concentrated in the dorsal half of the medial segment. Cells in this part of the nucleus project to the amygdaloceptive prelimbic area (PL) and AIp. However, other amygdaloceptive prefrontal areas are connected to parts of MD that do not receive fibers from the amygdala. Ventral pallidal afferents are distributed to all parts of the central and medial segments of MD, overlapping with the fibers from the amygdala and piriform cortex. Fibers from other parts of the pallidum, or related areas such as the substantia nigra, pars reticulata, terminate in the lateral and ventral parts of MD, where they overlap with inputs from the superior colliculus and other brainstem structures.(ABSTRACT TRUNCATED AT 400 WORDS)     

Amygdaloid projections to subcortical structures within the basal forebrain and brainstem in the rat and cat

The efferent fiber connections of the nuclei of the amygdaloid complex with subcortical structures in the basal telencephalon, hypothalamus, midbrain, and pons have been studied in the rat and cat, using the autoradiographic method for tracing axonal connections. The cortical and thalamic projections of these nuclei have been described in previous papers (Krettek and Price, ′77b,c). Although the subcortical connections of the amygdaloid nuclei are widespread within the basal forebrain and brain stem, the projections of each nucleus have been found to be well defined, and distinct from those of the other amygdaloid nuclei. The basolateral amygdaloid nucleus projects heavily to the lateral division of the bed nucleus of the stria terminalis (BNST), to the caudal part of the substantia innominata, and to the ventral part of the corpus striatum (nucleus accumbens and ventral putamen) and the olfactory tubercle; it projects more lightly to the lateral hypothalamus. The central nucleus also projects to the lateral division of the BNST and the lateral hypothalamus, but in addition it sends fibers to the lateral part of the substantia nigra and the marginal nucleus of the brachium conjunctivum. The basomedial nucleus has projections to the ventral striatum and olfactory tubercle which are similar to those of the basolateral nucleus, but it also projects to the core of the ventromedial hypothalamic nucleus and the premammillary nucleus, and to a central zone of the BNST which overlaps the medial and lateral divisions. The medial nucleus also projects to the core of the ventromedial nucleus and the premammillary nucleus, but sends fibers to the medial division of the BNST and does not project to the ventral striatum. The posterior cortical nucleus projects to the premammillary nucleus and to the medial division of the BNST, but a projection from this nucleus to the ventromedial nucleus has not been demonstrated. Projections to the “shell” of the ventromedial nucleus have been found only from the ventral part of the subiculum and from a structure at the junction of the amygdala and the hippocampal formation, which has been termed the amygdalo-hippocampal area (AHA). The AHA also sends fibers to the medial part of the BNST and the premammillary nucleus. Virtually no subcortical projections outside the amygdala itself have been demonstrated from the lateral nucleus, or from the olfactory cortical areas around the amygdala (the anterior cortical nucleus, the periamygdaloid cortex, and the posterior prepiriform cortex). However, portions of the endopiriform nucleus deep to the prepiriform cortex project to the ventral putamen, and to the lateral hypothalamus.     

The afferent connections of the substantia innominata in the monkey, Macaca fascicularis

The afferent connections of the substantia innominata and the magnocellular nuclei within it (the nucleus of the horizontal limb of the diagonal band, NHDB, and the nucleus basalis of Meynert, NBM) have been studied with anterograde and retrograde axonal tracing techniques. Prominent inputs arise in the amygdaloid complex, restricted areas of the cerebral cortex, parts of the thalamus and hypothalamus, and nuclei of the lower brainstem. Autoradiographic tracing experiments indicate that the amygdaloid fibers are distributed throughout the NHDB and the NBM, and to a lesser extent to the ventral pallidum. Relatively few fibers innervate the more medially located nucleus of the vertical limb of the diagonal band (NVDB) and the medial septal nucleus. Visualization of the amygdalofugal fibers with the tracer PHA-L (Phaseolus vulgaris leuco-agglutinin) shows that they have varicosities resembling boutons en passant along their length in the substantia innominata. Retrograde tracing experiments using WGA-HRP indicate that the cells of origin of the projection from the amygdala are concentrated in the parvicellular basal nucleus, the caudal part of the magnocellular basal nucleus, the magnocellular accessory basal nucleus, and the central nucleus. Relatively few fibers to the substantia innominata arise in the rostrodorsal part of the magnocellular basal nucleus, or in the lateral or parvicellular accessory basal nuclei. Cortical cells projecting to the substantia innominata were retrogradely labeled in the orbitofrontal cortex (including areas 11-14 and 25), the rostral insula (especially the agranular area), the rostroventral temporal cortex (including areas 35, 36, and parts of TG and TE), and the piriform and entorhinal cortices. The projections from the orbital and rostral temporal cortex were confirmed with anterograde tracers. Projections to the substantia innominata were not found from the more lateral, dorsal or caudal parts of the cerebral cortex, although fibers from temporal area TA may pass through the dendritic field of the most caudal cells of the NBM. Diencephalic cells projecting to the substantia innominata are distributed diffusely throughout the preoptic area and hypothalamus, with higher concentration in the lateral preoptic area and in the pre-, supra-, and tubero-mammillary nuclei. Cells are also found in the midline thalamic nuclei and in the region between the peripeduncular and subparafascicular nuclei.(ABSTRACT TRUNCATED AT 400 WORDS)