Intrinsic connections and architectonics of the superior temporal sulcus in the rhesus monkey

The intrinsic connections of the superior temporal sulcus (STS) in the rhesus monkey were studied by anterograde and retrograde tracer techniques and correlated with a reevaluation of cortical cytoarchitecture. The polymodal region in the upper bank (area TPO) is divisible into four rostral-to-caudal architectonic sectors, exhibiting increasing degrees of laminar differentiation and cellularity as one proceeds caudally. These sectors, including the sulcal proisocortex (area Pro), are tied together in a sequence of reciprocal connections. Each rostrocaudal sector of area TPO also has reciprocal connections with the laterally adjacent area TAa, at the upper rim of the sulcus, and medially adjacent areas PGa and IPa, near the depth. A similar arachitectonic/connectional organization exists for unimodal vision-related cortex in the lower bank of the STS. Here a rostrocaudal sequence of reciprocal connections unites area Pro, rostral and caudal divisions of area TEa, and the extrastriate visual area OAa (MT). Area TEa also has reciprocal connections with adjacent segments of area TEm laterally, at the lower rim of the sulcus, and area IPa, medially, in the depth. In both upper and lower banks, caudal-to-rostral "forwardgoing" connections begin in supragranular layers of cortex and terminate in and around layer IV. Reciprocal, "backgoing" connections take origin from cells in infragranular layers and terminate mainly over the first layer of the caudally adjacent target zone. Orthogonally directed, "side-to-side" projections originate in both supra- and infragranular layers and terminate diffusely over all layers of cortex.     

Post-rolandic cortical projections of the superior temporal sulcus in the rhesus monkey.

The efferent connections of different cytoarchitectonic areas of the superior temporal sulcus (STS) in the rhesus monkey with parieto-temporo-occipital cortex were investigated using autoradiographic methods. Four rostral-to-caudal subdivisions of cortex (area TPO) in the upper bank of the STS have distinct projection patterns. Rostral sectors (areas TPO-1 and -2) project to the rostral superior temporal gyrus (areas Ts1, Ts2, and Ts3), insula of the Sylvian fissure, and parahippocampal gyrus (perirhinal and prorhinal cortexes, areas TF, TH, and TL); caudal sectors (TPO-3 and -4) project to the caudal superior temporal gyrus (areas paAlt and Tpt), supratemporal plane (area paAc), circular sulcus of the Sylvian fissure (area reIt), as well as medial paralimbic (areas 23, 24, and retrosplenial cortex) and extrastriate (areas 18 and 19) cortexes. Area TPO-1 does not project to the parietal lobe; area TPO-2 projects to the inferior parietal lobule; area TPO-3 to the lower bank of the intraparietal sulcus (IPS) (area POa); and area TPO-4 to medial parietal cortex (area PGm). Vision-related cortex (area TEa) in the rostral lower bank of the STS sends fibers to the rostral inferotemporal region (areas TE1, -2, and -3) and parahippocampal gyrus (perirhinal cortex, areas TF and TL). Visual zones in the caudal lower bank and depth of the sulcus (area OAa, or MT and FST) project to the caudal inferotemporal region (areas TE3 and TEO), lateral preoccipital region (area V4), and lower bank of the IPS (area POa). A zone in the rostral depth of the STS (area IPa) projects to the rostral inferotemporal region, parahippocampal gyrus, insula of the Sylvian fissure, parietal operculum, and lower rim of the IPS (area PG). STS projections to parieto-temporo-occipital cortex have "feedforward," "feedbackward," and "side-to-side" laminar patterns of termination similar to those of other cortical sensory systems. The differential connectivity supports the cytoarchitectonic parcellation of the STS and suggests functional heterogeneity.     

Parietal,temporal, and occipita projections to cortex of the superior temporal sulcus in the rhesus monkey: A retrograde tracer study

The afferent cortical connections of individual cytoarchitectonic areas within the superior temporal sucus (STS) of the rhesus monkey were studied by retrograde tracer techniques, including double tracer experiments. Rostral superior temporal polysensory (STP) cortex (area TPO-1) receives input from the rostral superior temporal gyrus (STG), cortex of the circular sulcus, and parahippocampal gyrus (PHG) (areas 35, TF, and TL). Mid-STP cortex (areas TPO-2 and -3) has input from the mid-STG, cortex of the mid-circular sulcus, caudal inferior parietal lodule (IPL), cingulate gyrus (areas, 23, 24, retrosplenial cortex), and mid-PHG (areas 28, TF, TH, and TL). Caudal STP cortex (area TPO-4) has afferent connections with the caudal STG, cortex of the cauda insula and caudal circular sulcus, caudal IPL, lower bank of the intraparietal sulcus (IPS), medial parietal lobe, cingulate gyrus, and mid- and caudal PHG (areas TF, TH, TL; prostriate area). The most rostral cortex of the lower bank of the STS (areasTEa and TEm), a presumed visual association area, receives input from the rostal inferotemporal (IT) region; more cauda portions of areas TEa and TEm have afferent connections with the caudal IT region, PHG, preoccipital gyrus, and cortex of the lower bank of the IPS. © 1994 Wiley-Liss, Inc.

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

     

Converging visual and somatic sensory cortical input to the intraparietal sulcus of the rhesus monkey

A cyto- and myeloarchitectonic study reveals the presence of a distinct cortical zone ("area POa") in the lower bank of the intraparietal sulcus of the rhesus monkey. Using both autoradiographic and silver impregnation techniques, an analysis of cortical connections shows two overlapping projections to this sulcal zone. These come from (1) the middle portion of the preoccipital gyrus (area OA) and (2) the rostral inferior parietal lobule (area PF).     

Cingulate cortex of the rhesus monkey: II. Cortical afferents

Cortical projections to subdivisions of the cingulate cortex in the rhesus monkey were analyzed with horseradish peroxidase and tritiated amino acid tracers. These projections were evaluated in terms of an expanded cytoarchitectural scheme in which areas 24 and 23 were divided into three ventrodorsal parts, i.e., areas 24a-c and 23a-c. Most cortical input to area 25 originated in the frontal lobe in lateral areas 46 and 9 and orbitofrontal areas 11 and 14. Area 25 also received afferents from cingulate areas 24b, 24c, and 23b, from rostral auditory association areas TS2 and TS3, from the subiculum and CA1 sector of the hippocampus, and from the lateral and accessory basal nuclei of the amygdala (LB and AB, respectively). Areas 24a and 24b received afferents from areas 25 and 23b of cingulate cortex, but most were from frontal and temporal cortices. These included the following areas: frontal areas 9, 11, 12, 13, and 46; temporal polar area TG as well as LB and AB; superior temporal sulcus area TPO; agranular insular cortex; posterior parahippocampal cortex including areas TF, TL, and TH and the subiculum. Autoradiographic cases indicated that area 24c received input from the insula, parietal areas PG and PGm, area TG of the temporal pole, and frontal areas 12 and 46. Additionally, caudal area 24 was the recipient of area PG input but not amygdalar afferents. It was also the primary site of areas TF, TL, and TH projections. The following projections were observed both to and within posterior cingulate cortex. Area 29a-c received inputs from area 46 of the frontal lobe and the subiculum and in turn it projected to area 30. Area 30 had afferents from the posterior parietal cortex (area Opt) and temporal area TF. Areas 23a and 23b received inputs mainly from frontal areas 46, 9, 11, and 14, parietal areas Opt and PGm, area TPO of superior temporal cortex, and areas TH, TL, and TF. Anterior cingulate areas 24a and 24b and posterior areas 29d and 30 projected to area 23. Finally, a rostromedial part of visual association area 19 also projected to area 23. The origin and termination of these connections were expressed in a number of different laminar patterns. Most corticocortical connections arose in layer III and to a lesser extent layer V, while others, e.g., those from the cortex of the superior temporal sulcus, had an equal density of cells in both layers III and V.(ABSTRACT TRUNCATED AT 400 WORDS)     

Architectonics and cortical connections of the upper bank of the superior temporal sulcus in the rhesus monkey: an analysis in the tangential plane

Area TPO in the upper bank of the superior temporal sulcus (STS) of macaque monkeys is thought to correspond to the superior temporal polysensory (STP) cortex, but has been shown to have neurochemical/connectional subdivisions. To examine directly the relationship between chemoarchitecture and cortical connections of area TPO, the upper bank of the STS was sectioned tangential to the cortical surface. Three subdivisions of area TPO (TPOr, TPOi, and TPOc) were examined with cytochrome oxidase (CO) histochemistry and neurofilament protein (NF) immunoreactivity and architectonic patterns were compared with connections on the same or adjacent sections. Area TPOc, which may partly overlap with the location of the medial superior temporal area MST, exhibited regular patchy staining for CO in layers III/IV and a complementary pattern in the NF stain. Area TPOr, but not TPOi, also had a patchy pattern of complementary staining in CO and neurofilament similar to TPOc, although not as distinct. Tracer injections within cortex including the frontal eye fields (areas 46 and 8) labeled areas TPOc, TPOi, and TPOr. The caudal inferior parietal lobule (IPL) projected to all three areas. The projections from prearcuate and posterior parietal cortices showed both overlap and nonoverlap with each other within TPOc, TPOi, and TPOr. Projections were to all neurochemical components within the subdivisions of TPO. The findings support the parcellation of area TPO into three subdivisions and extend findings of chemoarchitectonic modules within high-order association cortices.     

Corticothalamic connections of the posterior parietal cortex in the rhesus monkey

Corticothalamic connections of posterior parietal regions were studied in the rhesus monkey by using the autoradiographic technique. Our observations indicate that the rostral superior parietal lobule (SPL) is connected with the ventroposterolateral (VPL) thalamic nucleus. In addition, whereas the rostral SPL is connected with the ventrolateral (VL) and lateral posterior (LP) thalamic nuclei, the rostral IPL has connections with the ventroposteroinferior (VPI), ventroposteromedial parvicellular (VPMpc), and suprageniculate (SG) nuclei as well as the VL nucleus. The caudal SPL and the midportion of IPL show projections mainly to the lateral posterior (LP) and oral pulvinar (PO) nuclei, respectively. These areas also have minor projections to the medial pulvinar (PM) nucleus. Finally, the medial SPL and the caudal IPL project heavily to the PM nucleus, dorsally and ventrally, respectively. In addition, the medial SPL has some connections with the LP nucleus, whereas the caudal IPL has projections to the lateral dorsal (LD) nucleus. Furthermore, the caudal and medial SPL and the caudal IPL regions have additional projections to the reticular and intralaminar nuclei-the caudal SPL predominantly to the reticular, and the caudal IPL mainly to the intralaminar nuclei. These results indicate that the rostral-to-caudal flow of cortical connectivity within the superior and inferior parietal lobules is paralleled by a rostral-to-caudal progression of thalamic connectivity. That is, rostral parietal association cortices project primarily to modality-specific thalamic nuclei, whereas more caudal regions project most strongly to associative thalamic nuclei.     

Chemoarchitectonics and corticocortical terminations within the superior temporal sulcus of the rhesus monkey: Evidence for subdivisions of superior temporal polysensory cortex

Cortex of the upper bank of the superior temporal sulcus (STS) in macaque monkeys, termed the superior temporal polysensory (STP) region, corresponds largely to architectonic area TPO and is connectionally distinct from adjacent visual areas. To investigate whether or not the STP region contains separate subdivisions, immunostaining for parvalbumin and neurofilament protein (using the SMI-32 antibody) was compared with patterns of corticocortical terminations in the STS. Chemoarchitectonic results provided evidence for three caudal-to rostral subdivisions: TPOc, TPOi, and TPOr. Area TPOc was characterized by patchy staining for parvalbumin and SMI-32 in cortical layers IV/III and III, respectively. Area TPOi had more uniform chemoarchitectonic staining, whereas area TPOr had a thicker layer IV than TPOi. The connectional results showed prefrontal cortex in the location of the frontal eye fields (area8) and dorsal area 46 projected in a columnar pattern to all cortical layers of area TPOc, to layer IV of TPOi, and in a columanr fashion, with a moderate increase in density in layer IV, to TPOr. In TPOc, columns of frontal connections showed a peridicity similar to that of the SMI-32 staining. The caudal inferior parietal lobule (area 7a) and superior temporal gyrus projected to each subdivision of area TPO, displaying either panlaminar or fourth-layer terminations. In addition to STP cortex, parvalbumin and SMI-32 immunostaining allowed identification of caudal visual areas of the STS, including MT, MST, FST, and V4t. These areas received first and sixth-layer projections from prefrontal cortex and area 7a. © 1995 Wiley-Liss, Inc.     

Reciprocal connections between olfactory structures and the cortex of the rostral superior temporal sulcus in the Macaca fascicularis monkey

Convergence of sensory modalities in the nonhuman primate cerebral cortex is still poorly understood. We present an anatomical tracing study in which polysensory association cortex located at the fundus and upper bank of the rostral superior temporal sulcus presents reciprocal connections with primary olfactory structures. At the same time, projections from this polysensory area reach multiple primary olfactory centres. Retrograde (Fast Blue) and anterograde (biotinylated dextran-amine and 3H-amino acids) tracers were injected into primary olfactory structures and rostral superior temporal sulcus. Retrograde tracers restricted to the anterior olfactory nucleus resulted in labelled neurons in the rostral portion of the upper bank and fundus of superior temporal sulcus. Injections of biotinylated dextran-amine at the fundus and upper bank of the superior temporal sulcus confirmed this projection by labelling axons in the dorsal and lateral portions of the anterior olfactory nucleus, as well as piriform, periamygdaloid and entorhinal cortices. Retrograde tracer injections at the rostral superior temporal sulcus resulted in neuronal labelling in the anterior olfactory nucleus, piriform, periamygdaloid and entorhinal cortices, thus providing confirmation of the reciprocity between primary olfactory structures and the cortex at the rostral superior temporal sulcus. The reciprocal connections between the rostral part of superior temporal sulcus and primary olfactory structures represent a convergence for olfactory and other sensory modalities at the cortex of the rostral temporal lobe.     

Thalamic connections of the cortex of the superior temporal sulcus in the rhesus monkey

The thalamocortical connections of the superior temporal sulcus (STS) were studied by means of the WGA-HRP retrograde tracing technique. The results indicate that the distribution of thalamic projections varies along the rostral-caudal dimension of the STS. Thus the rostral portion of the upper bank receives input primarily from the medialmost portion of the medial pulvinar (PM) nucleus. The middle region of the upper bank receives projections from medial and central portions of the PM nucleus, and also from the oral pulvinar, limitans, suprageniculate, medial geniculate, and dorsomedial nuclei. The cortex of the caudal portion of the upper bank has basically similar thalamic input; however, the projections from the PM nucleus originate in central and lateral portions. Additionally, there are projections from the lateral pulvinar (PL), ventroposterolateral, central lateral, parafascicular, and paracentral nuclei. In contrast to the dorsal bank, the cortex of the ventral bank of the STS receives somewhat different and less extensive thalamic input. The rostral portion of the lower bank receives projections only from the ventromedial sector of the PM nucleus, whereas the middle portion of the lower bank receives projections from the PL and the inferior pulvinar nuclei as well as from the PM nucleus. The upper bank of the STS, on the basis of physiological and anatomical studies (Jones and Powell, '70; Seltzer and Pandya, '78; Gross et al., '81; Baylis et al., '87), has been shown to contain multimodal areas. The present data indicate that the multimodal region of the STS has a preferential relationship with the central sector of the PM nucleus.     

Overlapping and nonoverlapping cortical projections to cortex of the superior temporal sulcus in the rhesus monkey: Double anterograde tracer studies

To examine how fibers from functionally distinct cortical zones interrelate within their target areas of the superior temporal sulcus (STS) in the rhesus monkey, separate anterograde tracers were injected in two different regions of the same hemisphere known to project to the STS. Paired injections were placed in dorsal prearcuate cortex and the caudal inferior parietal lobule (IPL), interconnected regions that are part of a hypothesized distributed network concerned with visuospatial analysis or directed attention; in a presumed auditory region of the superior temporal gyrus (STG) and in extrastriate visual cortex, the caudal IPL and lower rim of the intraparietal sulcus; and in dorsal prearcuate cortex and the STG. Overlapping and nonoverlapping projections were then examined in STS visual and polysensory areas. Prefrontal and parietal fibers directly overlapped extensively in area MST and all subdivisions of presumed polysensory cortex (areas TPOc, TPOi, and TPOr), although nonoverlapping connections were also found. Although STG and IPL fibers targeted all TPO subdivisions, connections were to nonoverlapping, but often adjacent, columns. Paired prefrontal and STG injections revealed largely nonoverlapping vertical columns of connections but substantial overlap within layers VI and I of areas TPOc and TPOi. The findings suggest that area TPO contains differently connected modules that may maintain at least initial segregation of visual versus auditory inputs. Other modules within area TPO receive directly converging input from the posterior parietal and the prefrontal cortices and may participate in a distributed cortical network concerned with visuospatial functions. © 1996 Wiley-Liss, Inc.     

Projections to the basis pontis from the superior temporal sulcus and superior temporal region in the rhesus monkey.

The present investigation was designed to determine the origins in the temporal lobe, and terminations in the pons, of the temporopontine pathway. Injections of tritiated amino acids were placed in multimodal regions in the upper bank of the superior temporal sulcus (STS), and in unimodal visual, somatosensory, and auditory areas in different sectors of the lower bank of the STS, the superior temporal gyrus (STG), and the supratemporal plane (STP). The distribution of terminal label in the nuclei of the basis pontis was studied using the autoradiographic technique. Following injections of isotope into the multimodal areas (TPO and PGa) in the upper bank of the STS, intense aggregations of label were observed in the extreme dorsolateral, dorsolateral, and lateral nuclei of the pons, and modest amounts of label were seen in the peripeduncular nucleus. The caudalmost area TPO projected in addition to the ventral and intrapeduncular pontine nuclei. The second auditory area, AII, and the adjacent auditory association areas of the STG and STP contributed modest projections to the dorsolateral, lateral, and peripedunuclar nuclei, but generally spared the extreme dorsolateral nucleus. The lower bank of the STS, which subserves central vision, the somatosensory associated region at the fundus of the rostral STS, and the primary auditory area did not project to the pons. The higher order, multimodal STS contribution to the corticopontocerebellar circuit may provide a partial anatomical substrate for the hypothesis that the cerebellum contributes to the modulation of nonmotor functions.     

Prenatal specification of callosal connections in rhesus monkey

Anatomical tracing and quantitative techniques were used to examine the tempo and pattern of maturation for callosal projection neurons in the monkey prefrontal cortex (PFC) during fetal and postnatal development. Nineteen monkeys were injected with retrograde tracers (fluorescent dyes, horseradish peroxidase conjugated to wheat germ agglutinin [WGA-HRP] or HRP crystals) at various ages between embryonic day 82 (E82) and adulthood. The size of injection sites was varied in fetal, newborn, and adult cases. In adults, labeled neurons were found in greatest density in the homotopic cortex of the opposite hemisphere and considerable numbers were also observed in a constellation of heterotopic areas including the medial and lateral orbital cortex, the dorsomedial convexity, and the pregenual cortex. The majority of labeled neurons were consistently concentrated in the lower half of layer III in all areas. In cases with large injection sites, callosal neurons of layer III formed a continuous and uninterrupted band that extended over the entire lateral surface of the prefrontal cortex spanning both homotopic and heterotopic areas. In contrast, in cases with small injection sites, the labeling of layer III neurons exhibited discontinuities. Between embryonic ages E82 and E89, injections limited to the cortical layers labeled only a small number of neurons in the opposite hemisphere, indicating that few callosal axons have invaded the cortex by this age. However, by E111 comparable injections labeled a large number of callosal neurons and many features of their distribution were adult-like. The number and constellation of cytoarchitectonic areas that were labeled in the frontal cortex of the opposite hemisphere were the same as in adults and the majority of callosal neurons were found in supragranular layer III. Finally, in fetal animals beyond E111, labeled neurons extended as a nearly unbroken band over a wide expanse of the dorsolateral PFC, resembling the pattern seen in adult monkeys with large injections. The conclusion we draw from these results, together with our earlier findings (Schwartz and Goldman-Rakic: Nature 299:154, 1982), is that callosal neurons whose axons enter the cortical layers of the primate prefrontal cortex achieve their mature laminar and areal distribution prior to birth and do so largely by cumulative processes.     

Intrinsic connections of the macaque monkey hippocampal formation: II. CA3 connections

We examined the topographic organization of the connections of the CA3 field of the macaque monkey hippocampus. Discrete anterograde and retrograde tracer injections were made at various positions within CA3 and CA1. The projections from CA3 to CA1 (Schaffer collaterals), which terminate in the strata radiatum, pyramidale, and oriens, are present throughout the entire transverse extent of CA1. Projections extend both rostrally and caudally from the injection site for as much as three‐fourths of the longitudinal extent of the hippocampus. The associational projections from CA3 to CA3 also travel extensively along the longitudinal axis. CA3 gives rise to more substantial projections to CA1 than to CA3. CA3 projections that originate at the level of the uncus tend to be more restricted to the rostral portions of CA1 and CA3. As in the rodent brain, projections from CA3 to CA1 are distributed along a radial gradient, depending on the transverse location of the cells of origin. CA3 cells located near the dentate gyrus generate projections that more densely terminate superficially in the terminal zone of CA1, whereas CA3 cells located closer to CA1 give rise to projections that more heavily terminate deeply in the terminal zone of CA1. The present results indicate that in the monkey, as in the rat, CA3 cells give rise to extensive projections to CA1 and CA3. Interestingly, radial, transverse, and longitudinal gradients of CA3 fiber distribution, so clear in the rat, are much more subtle in the nonhuman primate brain. J. Comp. Neurol. 515:349–377, 2009. © 2009 Wiley‐Liss, Inc.     

Selectivity between faces in the responses of a population of neurons in the cortex in the superior temporal sulcus of the monkey

There is a population of neurons in the cortex in the middle and anterior part of the superior temporal sulcus (STS) of the monkey with responses which are selective for faces. If, consistent with the effects of damage to the temporal lobe, these neurons are involved in face recognition or in making appropriate social responses to different individuals, then it might be expected that at least some of these neurons might respond differently to different faces. To investigate whether at least some of these neurons do respond differently to different faces, their responses were measured to a standard set of faces, presented in random sequence using a video framestore. It was found that a considerable proportion of the neurons with face selective responses tested (34/44 or 77%) responded differently to different faces, as shown by analyses of variance. An index of the discriminability of the most and least effective face stimulus (d') ranged between 0.2 and 5.0 for the different neurons. Although these neurons often responded differently to different faces, they did not usually respond to only one of the faces in the set, so that information that a particular face had been shown was present across an ensemble of neurons, rather than in the responses of an individual neuron. These findings indicate that the responses of these neurons would be useful in providing information on which different behavioral responses made to different faces could be based. These neurons could thus be filters, the output of which could be used for recognition of different individuals and in emotional responses made to different individuals.     

Cytoarchitecture and cortical connections of the posterior cingulate and adjacent somatosensory fields in the rhesus monkey

The cytoarchitecture and connections of the caudal cingulate and medial somatosensory areas were investigated in the rhesus monkey. There is a stepwise laminar differentiation starting from retrosplenial area 30 towards the isocortical regions of the medial parietal cortex. This includes a gradational emphasis on supragranular laminar organization and general reduction of the infragranular neurons as one proceeds from area 30 toward the medial parietal regions, including areas 3, 1, 2, 5, 31, and the supplementary sensory area (SSA). This trend includes a progressive increase in layer IV neurons. Area 23c in the lower bank and transitional somatosensory area (TSA) in the upper bank of the cingulate sulcus appear as nodal points. From area 23c and TSA the architectonic progression can be traced in three directions: one culminates in areas 3a and 3b (core line), the second in areas 1, 2, and 5 (belt line), and the third in areas 31 and SSA (root line). These architectonic gradients are reflected in the connections of these regions. Thus, cingulate areas (30, 23a, and 23b) are connected with area 23c and TSA on the one hand and have widespread connections with parieto-temporal, frontal, and parahippocampal (limbic) regions on the other. Area 23c has connections with areas 30, 23a and b, and TSA as well as with medial somatosensory areas 3, 1, 2, 5, and SSA. Area 23c also has connections with parietotemporal, frontal, and limbic areas similar to areas 30, 23a, and 23b. Area TSA, like area 23c, has connections with areas 3, 1, 2, 5, and SSA. However, it has only limited connections with the parietotemporal and frontal regions and none with the parahippocampal gyrus. Medial area 3 is mainly connected to medial and dorsal sensory areas 3, 1, 2, 5, and SSA and to areas 4 and 6 as well as to supplementary (M2 or area 6m), rostral cingulate (M3 or areas 24c and d), and caudal cingulate (M4 or areas 23c and d) motor cortices. Thus, in parallel with the architectonic gradient of laminar differentiation, there is also a progressive shift in the pattern of corticocortical connections. Cingulate areas have widespread connections with limbic, parietotemporal, and frontal association areas, whereas parietal area 3 has more restricted connections with adjacent somatosensory and motor cortices. TSA is primarily related to the somatosensory-motor areas and has limited connections with the parietotemporal and frontal association cortices.     

Organization of direct hippocampal efferent projections to the cerebral cortex of the rhesus monkey: Projections from CA1, prosubiculum,and subiculum to the temporal lobe

This study investigates direct hippocampal efferent projections to the temporal lobe of the rhesus monkey. Tritiated amino acid injections were placed into the hippocampal formation to identify terminal fields, and complementary fluorescent retrograde tracer injections were placed into the cortex to identify the cells of origin. Tritiated amino acid injections into CA1, prosubicular, or subicular subfields produced anterograde label over parts of the parahippocampal gyrus and temporal pole. Injections of fluorescent retrograde tracers demonstrated that these projections originate from longitudinal strips of neurons that occupy part of the CA1 subfield as well as from strips of neurons in adjacent prosubicular and subicular subfields. Thus, an injection into area TH of the posterior parahippocampal gyrus labeled neurons in a longitudinal strip of proximal CA1 (i.e., near CA2) as well as a strip in the subiculum; injections into areas TF, TL, 35, or Pro labeled neurons in a longitudinal strip of distal CA1 (i.e., near the prosubiculum) as well as one in the prosubiculum; and an injection into area TFO labeled neurons in a longitudinal strip in the middle of CA1. These strips of neurons extended longitudinally throughout the entire rostrocaudal length of the hippocampus. These results demonstrate that, in the monkey, CA1 projections to cortex arise topographically from longitudinally oriented strips of neurons that occupy only a part of the transverse extent of CA1 but that cover most of the anteroposterior extent of the hippocampus. Thus, in the monkey, CA1 is not a single uniform entity and may have a unique role as a source of direct hippocampal projections to the cerebral cortex. J. Comp. Neurol. 392:92–114, 1998. © 1998 Wiley-Liss, Inc.     

Association fiber pathways to the frontal cortex from the superior temporal region in the rhesus monkey

The projections to the frontal cortex that originate from the various areas of the superior temporal region of the rhesus monkey were investigated with the autoradiographic technique. The results demonstrated that the rostral part of the superior temporal gyrus (areas Pro, Ts1, and Ts2) projects to the proisocortical areas of the orbital and medial frontal cortex, as well as to the nearby orbital areas 13, 12, and 11, and to medial areas 9, 10, and 14. These fibers travel to the frontal lobe as part of the uncinate fascicle. The middle part of the superior temporal gyrus (areas Ts3 and paAlt) projects predominantly to the lateral frontal cortex (areas 12, upper 46, and 9) and to the dorsal aspect of the medial frontal lobe (areas 9 and 10). Only a small number of these fibers terminated within the orbitofrontal cortex. The temporofrontal fibers originating from the middle part of the superior temporal gyrus occupy the lower portion of the extreme capsule and lie just dorsal to the fibers of the uncinate fascicle. The posterior part of the superior temporal gyrus projects to the lateral frontal cortex (area 46, dorsal area 8, and the rostralmost part of dorsal area 6). Some of the fibers from the posterior superior temporal gyrus run initially through the extreme capsule and then cross the claustrum as they ascend to enter the external capsule before continuing their course to the frontal lobe. A larger group of fibers curves round the caudalmost Sylvian fissure and travels to the frontal cortex occupying a position just above and medial to the upper branch of the circular sulcus. This latter pathway constitutes a part of the classically described arcuate fasciculus.     

The intrinsic architectonic and connectional organization of the superior temporal region of the rhesus monkey

The superior temporal region (STR) in the rhesus monkey includes the circular sulcus (Cis), the supratemporal plane (STP), and the superior temporal gyrus (STG). Rostrally the STR is continuous with the periallocortices of the prepyriform and anterior insular regions; caudally it borders the isocortices of the inferior parietal lobule and the superior temporal sulcus. The STR contains 12 cytoarchitectonic areas: four fields on the Cis, four on the STP, and four on the STG. The sulcal fields (root fields) are adjacent to the insula and resemble it in the possession of a relatively strong layer V; the STP fields (core fields) are characterized by well-developed layer IV; and the STG fields (belt fields) exhibit strong differentiation of layer III. In each line of fields the more rostral ones show relative prominence of the deeper layers, with increasing prominence of the superficial layers occurring caudad in a stepwise fashion. Analysis of the connectional organization of the fields within the STR suggests an assembly of four rostrocaudal stages, each composed of one field from each line–a root, a core, and a belt field. There is a specific arrangement of connections among the fields of a given stage and between fields in adjacent stages. Projections directed caudally from one field to another field in the adjacent stage arise in layers V and VI and terminate in the superficial layers (mainly layer I). Projections directed to a field in a rostrally adjacent stage arise from layer III neurons and terminate in layers III and IV, usually in columns. There is also a laminar specificity between fields lying within a given stage.     

The organization of the cortico-cortical connections between the walls of the lower part of the superior temporal sulcus and the inferior parietal lobule in the monkey

After injections of HRP into area 7a, PG, in the monkey labelled cells have been found in the walls and floor of the lower part of the superior temporal sulcus; the part of area 7a, PG, in the posterior wall of the intraparietal sulcus is connected with the floor and posterior wall of the superior temporal sulcus, and the part of 7a, PG on the surface of the inferior parietal lobule with the floor and anterior wall. Area 7b, PF is related to a restricted part of the floor of the superior temporal sulcus.