Evidence for a direct projection from the superior temporal gyrus to the entorhinal cortex in the monkey

During the course of a larger study of the afferent and efferent connections of the entorhinal cortex in the macaque monkey we have found evidence for a hitherto undescribed projection to the entorhinal cortex from the superior temporal gyrus. The evidence is derived principally from experiments in which small volumes of wheat germ agglutinin-conjugated horseradish peroxidase (WGA-HRP) were injected into different parts of the entorhinal cortex, but has been confirmed by 3H-amino acid autoradiography. After WGA-HRP injections into the entorhinal cortex, retrogradely labeled neurons have been seen mainly in layer III, but also to some extent in layer VI, throughout much of the superior temporal gyrus. The projection appears to be topographically organized in the sense that the ventral insular cortex and the adjoining temporal operculum have been found to project to the periamygdaloid cortex and the lateral division of the entorhinal cortex; the convexity of the superior temporal gyrus and the cortex along the dorsal bank of the superior temporal gyrus project further caudally to the medial division of the entorhinal cortex; and the cortex surrounding the fundus of the superior temporal sulcus projects to the perirhinal cortex. Following an injection of 3H-amino acids into the convexity of the superior temporal gyrus, terminal labeling has been seen over layers I and II of the entorhinal cortex and over layer I in the most lateral portion of the presubiculum. While the distribution of retrogradely labeled cells in our WGA-HRP experiments encompasses several cytoarchitectonically distinguishable areas in the superior temporal gyrus, the most heavily labeled field appears to coincide with what Gross and his colleagues have termed the 'superior temporal polysensory area' on the dorsal bank of the superior temporal sulcus.     

Complementary circuits connecting the orbital and medial prefrontal networks with the temporal, insular, and opercular cortex in the macaque monkey

The origin and termination of axonal connections between the orbital and medial prefrontal cortex (OMPFC) and the temporal, insular, and opercular cortex have been analyzed with anterograde and retrograde axonal tracers, injected in the OMPFC or temporal cortex. The results show that there are two distinct, complementary, and reciprocal neural systems, related to the previously defined "orbital" and "medial" prefrontal networks. The orbital prefrontal network, which includes areas in the central and lateral part of the orbital cortex, is connected with vision-related areas in the inferior temporal cortex (especially area TEav) and the fundus and ventral bank of the superior temporal sulcus (STSf/v), and with somatic sensory-related areas in the frontal operculum (OPf) and dysgranular insular area (Id). No connections were found between the orbital network and auditory areas. The orbital network is also connected with taste and olfactory cortical areas and the perirhinal cortex and appears to be involved in assessment of sensory objects, especially food. The medial prefrontal network includes areas on the medial surface of the frontal lobe, medial orbital areas, and two caudolateral orbital areas. It is connected with the rostral superior temporal gyrus (STGr) and the dorsal bank of the superior temporal sulcus (STSd). This region is rostral to the auditory parabelt areas, and there are only relatively light connections between the auditory areas and the medial network. This system, which is also connected with the entorhinal, parahippocampal, and cingulate/retrosplenial cortex, may be involved in emotion and other self-referential processes.     

Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent areas

The association and commissural fiber systems arising in the olfactory cortical areas caudal to the olfactory peduncle (the piriform cortex, nucleus of the lateral olfactory tract, anterior cortical nucleus of the amygdala, periamygdaloid cortex and entorhinal cortex) have been studied utilizing horseradish peroxidase as both an anterograde and a retrograde axonal tracer. In the piriform cortex two sublaminae within layer II (IIa and IIb) and layer III have been found to give rise to distinctly different projections. Retrograde cell labeling experiments indicate that the association fiber projection from layer IIb is predominantly caudally directed, while the projection from layer III is predominantly rostrally directed. Cells in layer IIa project heavily to areas both caudal and rostral to the piriform cortex. The commissural fibers from the piriform cortex are largely restricted in their origin to layer IIb of the anterior part of the piriform cortex and in their termination on the contralateral side to the posterior part of the piriform cortex and adjacent olfactory cortical areas. A projection to the olfactory bulb has also been found to arise from cells in layers IIb and III of the ipsilateral piriform cortex, but not in layer IIa. In addition to those from the piriform cortex, association projections have also been found from other olfactory cortical areas. The nucleus of the lateral olfactory tract has a heavy bilateral projection to the medial part of the anterior piriform cortex and the lateral part of the olfactory tubercle (as well as a lighter projection to the olfactory bulb); both the anterior cortical nucleus of the amygdala and the periamygdaloid cortex project ipsilaterally to several olfactory cortical areas. The entorhinal cortex has been found to project to the medial parts of the olfactory tubercle and the olfactory peduncle. The olfactory tubercle is the only olfactory cortical area from which no association fiber systems (instrinsic or extrinsic) have been found to originate. A broad topographic organization exists in the distribution of the fibers from several of the olfactory areas. This is most obvious in the anterior part of the olfactory cortex, in which fibers from the more rostral areas (the anterior olfactory nucleus and the anterior piriform cortex) terminate in regions near the lateral olfactory tract, while those from more caudal areas (the posterior piriform cortex and the entorhinal cortex) terminate in areas further removed, both laterally and medially, from the tract. Projections to olfactory areas from the hypothalamus, thalamus, diagonal band, and biogenic amine cell groups have been briefly described.     

Perirhinal cortex projections to the amygdaloid complex and hippocampal formation in the rat

The differential efferent projections of the perirhinal cortex were traced by using anterograde and retrograde tracing techniques. The dorsal bank cortex (area 36) projected lightly to the lateral entorhinal cortex and more strongly to the lateral, posterolateral cortical, and posterior basomedial amygdaloid nuclei and amygdalostriatal transition zone. The ventral bank (dorsolateral entorhinal cortex) projected to the lateral entorhinal cortex, dorsal subiculum, and subfield CA1 and mainly targeted the basolateral amygdaloid nucleus. Corticocortical projections from the dorsal and ventral banks targeted different cortical areas. The fundus of the rhinal sulcus (area 35) projected to both lateral and medial entorhinal cortices, ventral subiculum, lateral and basolateral nuclei, and amygdalostriatal transition zone. Corticocortical projections targeted areas projected to by both dorsal and ventral banks and also by second somatosensory area, first temporal cortical area, and striate cortex. Neurons projecting to the lateral nucleus were distributed in all layers of the dorsal bank, wheras those projecting to CA1 and subiculum were found in superfical layers (mostly layer III) of the ventral bank. Projections to the basolateral nucleus arose from superfical layers (mostly layer II) of the fundus and deep layers of the ventral bank. Furthermore, projections to the amygdala mostly arose from rostral levels, whereas hippocampal projections primarily originated caudally. The rat perirhinal cortex is heterogeneous in its efferent connectivity, and distinct projections arise from the dorsal and ventral banks and fundus of the rhinal sulcus. The widespread cortical connectivity of the fundus suggests that only this part of the perirhinal cortex is similar to area 35 of the primate brain.     

Cortical connections of the inferior arcuate sulcus cortex in the macaque brain

Injections of the retrograde/anterograde tracers Wheat Germ Agglutinin-Horseradish peroxidase (WGA-HRP) into the cortex along the banks of the inferior limb of the arcuate sulcus in the cortex of 4 macaque monkeys (Macaca fascicularis) were used to investigate its cortico-cortical connections. All injections produced transported label within the sulcus principalis, the ventral lateral prefrontal cortex, the anterior cingulate sulcus and the dorsal insular cortex. The distribution of label within each of these areas differed slightly depending on the injection site. Injections along the caudal bank of the inferior arcuate sulcus label premotor, supplementary motor, and precentral motor areas but produce relatively sparse prefrontal labeling. Posteriorly label is transported to the inferior parietal cortex and the dorsal opercular bank of the Sylvian fissure. Injections along the rostral bank of the sulcus do not label motor areas but produce labeling in dorsal, lateral and orbital prefrontal areas, and in cortex along the ventral bank of the superior branch of the arcuate sulcus. Posteriorly label is transported to cortical areas in the superior temporal gyrus including the dorsal bank of the superior temporal sulcus. The more dorsal rostral bank injection produced both superior temporal and some sparse inferior parietal labeling and the more ventral rostral bank injection produced extensive superior temporal labeling but no parietal labeling. No labeling was ever seen in cortex ventral to the fundus of the superior temporal sulcus. Although other auditory recipient prefrontal areas have been reported, this is the first demonstration of a region chiefly devoted to auditory connections within the ventral frontal cortex. Its adjacency to areas associated with vocal muscle movement, and its connections to midline cortical areas associated with vocal functions in both primates and humans may provide important clues to the organization of Broca's language area.     

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.     

Entorhinal cortex of the monkey: IV. Topographical and laminar organization of cortical afferents

The nonhuman primate entorhinal cortex is the primary interface for information flow between the neocortex and the hippocampal formation. Based on previous retrograde tracer studies, neocortical afferents to the macaque monkey entorhinal cortex originate largely in polysensory cortical association areas. However, the topographical and laminar distributions of cortical inputs to the entorhinal cortex have not yet been comprehensively described. The present study examines the regional and laminar termination of projections within the entorhinal cortex arising from different cortical areas. The study is based on a library of 51 (3)H-amino acid injections that involve most of the afferent regions of the entorhinal cortex. The range of termination patterns was broad. Some areas, such as the medial portion of orbitofrontal area 13 and parahippocampal areas TF and TH, project widely within the entorhinal cortex. Other areas have a more focal and regionally selective termination. The lateral orbitofrontal, insular, anterior cingulate, and perirhinal cortices, for example, project only to rostral levels of the entorhinal cortex. The upper bank of the superior temporal sulcus projects mainly to intermediate levels of the entorhinal cortex, and the parietal and retrosplenial cortices project to caudal levels. The projections from some of these cortical regions preferentially terminate in the superficial layers (I-III) of the entorhinal cortex, whereas others project more heavily to the deep layers (V-VI). Thus, some of the cortical inputs may be more influential on the cortically directed outputs of the hippocampal formation or on gating neocortical information flow into the other fields of the hippocampal formation rather than contributing to the perforant path inputs to other hippocampal fields.     

Posterior parietal cortex in rhesus monkey: II. Evidence for segregated corticocortical networks linking sensory and limbic areas with the frontal lobe

We have examined the circuitry connecting the posterior parietal cortex with the frontal lobe of rhesus monkeys. HRP-WGA and tritiated amino acids were injected into subdivisions 7m, 7a, 7b, and 7ip of the posterior parietal cortex, and anterograde and retrograde label was recorded within the frontal motor and association cortices. Our main finding is that each subdivision of parietal cortex is connected with a unique set of frontal areas. Thus, area 7m, on the medial parietal surface, is interconnected with the dorsal premotor cortex and the supplementary motor area, including the supplementary eye field. Within the prefrontal cortex, area 7m's connections are with the rostral sector of the frontal eye field (FEF), the dorsal bank of the principal sulcus, and the anterior bank of the inferior arcuate sulcus (Walker's area 45). In contrast, area 7a, on the posterior parietal convexity, is not linked with premotor regions but is heavily interconnected with the rostral FEF in the anterior bank of the superior arcuate sulcus, the dorsolateral prefrontal convexity, the rostral orbitofrontal cortex, area 45, and the fundus and adjacent cortex of the dorsal and ventral banks of the principal sulcus. Area 7b, in the anterior part of the posterior parietal lobule, is interconnected with still a different set of frontal areas, which include the ventral premotor cortex and supplementary motor area, area 45, and the external part of the ventral bank of the principal sulcus. The prominent connections of area 7ip, in the posterior bank of the intraparietal sulcus, are with the supplementary eye field and restricted portions of the ventral premotor cortex, with a wide area of the FEF that includes both its rostral and caudal sectors, and with area 45. All frontoparietal connections are reciprocal, and although they are most prominent within a hemisphere, notable interhemispheric connections are also present. These findings provide a basis for a parcellation of the classically considered association cortex of the frontal lobe, particularly the cortex of the principal sulcus, into sectors defined by their specific connections with the posterior parietal subdivisions. Moreover, the present findings, together with those of a companion study (Cavada and Goldman-Rakic: J. Comp. Neurol. this issue) have allowed us to establish multiple linkages between frontal areas and specific limbic and sensory cortices through the posterior parietal cortex. The networks thus defined may form part of the neural substrate of parallel distributed processing in the cerebral cortex.     

The entorhinal cortex of the monkey: II. Cortical afferents

The entorhinal cortex of the monkey is commonly viewed as the major link between the cerebral cortex and the other fields of the hippocampal formation. Until recently, however, little was known about the origins of the cortical projections to the entorhinal cortex, and most of the available information is still based on degeneration studies. We have carried out a systematic analysis of these connections by placing small injections of the retrograde tracer wheat germ agglutinin conjugated to horseradish peroxidase into each of the fields of the entorhinal cortex of the Macaca fascicularis monkey. Retrogradely labeled cells were observed in several areas of the frontal and temporal lobes, the insula, and the cingulate cortex. In the frontal lobe, the greatest number of labeled cells were observed in the orbital region and specifically in areas 13 and 13a: labeled cells were also seen in areas 14, 11, and 12. In the dorsolateral frontal cortex, labeled cells were observed mainly in the rostral half of area 46; occasionally cells were also seen in areas 9, 8, and 6. In the cingulate cortex, labeled cells were observed in area 25, area 32, and rostral levels of area 24; fewer cells were observed at caudal levels of area 24 or in area 23. The retrosplenial region (areas 30 and 29), including its caudal extension along the rostral calcarine sulcus and its ventral extension into the temporal lobe, contained numerous labeled cells. In the temporal lobe, retrogradely labeled cells were arranged in two rostrocaudally oriented bands. Rostral to the hippocampal formation, the first band encompassed the piriform and periamygdaloid cortices and areas 35 and 36; the labeling in area 36 was continuous to the temporal pole. At more caudal levels this band was located immediately lateral to the hippocampal formation and included areas 35 and 36 rostrally and areas TH and TF caudally. The second band was situated in the superior temporal gyrus where labeled cells were observed in several distinct cytoarchitectonic fields, including the parainsular cortex in the fundus of the inferior limiting sulcus. In the insula proper, retrogradely labeled cells were seen mainly in the rostral or agranular division; far fewer were observed in the dysgranular and granular insula. Whereas there is little available physiological information concerning many of the cortical regions that project to the entorhinal cortex, on anatomical grounds they may be generally characterized as polysensory associational regions.     

Auditory belt and parabelt projections to the prefrontal cortex in the Rhesus monkey

Recent anatomical and electrophysiological studies have expanded our knowledge of the auditory cortical system in primates and have described its organization as a series of concentric circles with a central or primary auditory core, surrounded by a lateral and medial belt of secondary auditory cortex with a tertiary parabelt cortex just lateral to this belt. Because recent studies have shown that rostral and caudal belt and parabelt cortices have distinct patterns of connections and acoustic responsivity, we hypothesized that these divergent auditory regions might have distinct targets in the frontal lobe. We, therefore, placed discrete injections of wheat germ agglutinin-horseradish peroxidase or fluorescent retrograde tracers into the prefrontal cortex of macaque monkeys and analyzed the anterograde and retrograde labeling in the aforementioned auditory areas. Injections that included rostral and orbital prefrontal areas (10, 46 rostral, 12) labeled the rostral belt and parabelt most heavily, whereas injections including the caudal principal sulcus (area 46), periarcuate cortex (area 8a), and ventrolateral prefrontal cortex (area12vl) labeled the caudal belt and parabelt. Projections originating in the parabelt cortex were denser than those arising from the lateral or medial belt cortices in most cases. In addition, the anterior third of the superior temporal gyrus and the dorsal bank of the superior temporal sulcus were also labeled after prefrontal injections, confirming previous studies. The present topographical results suggest that acoustic information diverges into separate streams that target distinct rostral and caudal domains of the prefrontal cortex, which may serve different acoustic functions. J. Comp. Neurol. 403:141–157, 1999. © 1999 Wiley-Liss, Inc.     

Topographic organization of orbitofrontal projections to the parahippocampal region in rats

The parahippocampal region, which comprises the perirhinal, postrhinal, and entorhinal cortices, as well as the pre‐ and parasubiculum, receives inputs from several association cortices and provides the major cortical input to the hippocampus. This study examined the topographic organization of projections from the orbitofrontal cortex (OFC) to the parahippocampal region in rats by injecting anterograde tracers, biotinylated dextran amine (BDA) and Phaseolus vulgaris‐leucoagglutinin (PHA‐L), into four subdivisions of OFC. The rostral portion of the perirhinal cortex receives strong projections from the medial (MO), ventral (VO), and ventrolateral (VLO) orbitofrontal areas and the caudal portion of lateral orbitofrontal area (LO). These projections terminate in the dorsal bank and fundus of the rhinal sulcus. In contrast, the postrhinal cortex receives a strong projection specifically from VO. All four subdivisions of OFC give rise to projections to the dorsolateral parts of the lateral entorhinal cortex (LEC), preferentially distributing to more caudal levels of LEC. The medial entorhinal cortex (MEC) receives moderate input from VO and weak projections from MO, VLO, and LO. The presubiculum receives strong projections from caudal VO but only weak projections from other OFC regions. As for the laminar distribution of projections, axons originating from OFC terminate more densely in upper layers (layers I–III) than in deep layers in the parahippocampal region. These results thus show a striking topographic organization of OFC‐to‐parahippocampal connectivity. Whereas LO, VLO, VO, and MO interact with perirhinal–LEC circuits, the interactions with postrhinal cortex, presubiculum, and MEC are mediated predominantly through the projections of VO. J. Comp. Neurol. 522:772–793, 2014. © 2013 Wiley Periodicals, Inc.     

Projections from the superior temporal sulcus to the agranular frontal cortex in the macaque

The aim of this study was to investigate the organization of the projections from the superior temporal sulcus (STS) to the various areas forming the agranular frontal cortex. Injections of retrograde neuronal tracers were made in the various agranular areas, in nine macaque monkeys. The results showed that two rostral premotor areas, F6 (pre-SMA) and F7, and the ventrorostral part of area F2 (F2vr) are targets of projections from the upper bank of the STS (uSTS). F6 and the dorsorostral part of F7 (supplementary eye field, SEF) are targets of projections from the rostral part of the uSTS, corresponding to the so-called 'superior temporal polysensory area' (STP). In contrast, the ventral part of area F7 (not including the SEF) and F2vr are targets of afferents from the caudal part of the uSTS. Ventral F7 is the target of weak afferents from the caudalmost and dorsalmost part of the uSTS (area 7a), whilst F2vr is the target of projections from a relatively more rostral and ventral sector of the uSTS, close to the fundus of the sulcus. This sector should correspond to area MST. In conclusion, F6 and SEF receive high order information from STP, whereas ventral F7 and F2vr receive information from areas of the dorsal visual stream.     

Topographical organization of the cortical afferent connections of the prefrontal cortex in the cat

The topographical distribution of the cortical afferent connections of the prefrontal cortex (PFC) in adult cats was studied by using the retrograde axonal transport of horseradish peroxidase technique. Small single injections of the enzyme were made in different locations of the PFC, and the areal location and density of the subsequent neuronal labeling in neocortex and allocortex were evaluated in each case. The comparison of the results obtained in the various cases revealed that four prefrontal sectors (rostral, dorsolateral, ventral, and dorsomedial) can be distinguished, each exhibiting a particular pattern of cortical afferents. All PFC sectors receive projections from the ipsilateral insular (agranular and granular subdivisions) and limbic (infralimbic, prelimbic, anterior limbic, cingular, and retrosplenial areas) cortices. These cortices provide the most abundant cortical projections to the PFC, and their various subdivisions have different preferential targets within the PFC. The premotor cortex and the following neocortical sensory association areas project differentially upon the various ipsilateral PFC sectors: the portion of the somatosensory area SIV in the upper bank of the anterior ectosylvian sulcus, the visual area in the lower bank of the same sulcus, the auditory area AII, the temporal area, the perirhinal cortex, the posterior suprasylvian area, area 20, the posterior ectosylvian area, the suprasylvian fringe, the lateral suprasylvian area (anterolateral and posterolateral subdivisions), area 5, and area 7. The olfactory peduncle, the prepiriform cortex, the cortico-amygdaloid transition area, the entorhinal cortex, the subiculum (ventral, posteroventral, and posterodorsal sectors), the caudomedial band of the hippocampal formation and the postsubiculum are the allocortical sources of afferents to the PFC. The dorsolateral PFC sector is the target of the largest insular, limbic, and neocortical sensory association projections. The dorsomedial and rostral sectors receive notably less abundant cortical afferents than the dorsolateral sector. Those to the dorsomedial sector arise from the same areas that project to the dorsolateral sector and are more abundant to the dorsal part, where the medial frontal eye field cortex is located. The rostral sector receives projections principally from all other PFC sectors, and from the limbic and insular cortices. The projections from the allocortex reach preferentially the ventral PFC sector. Intraprefrontal connections are most abundant within each PFC sector. Commissural interprefrontal connections are largest from the site homotopic to the HRP injection.(ABSTRACT TRUNCATED AT 400 WORDS)     

Efferent projections of the anterior perirhinal cortex in the rat

Because convulsive seizures develop very rapidly from kindling sites in the anterior perirhinal cortex, we studied perirhinal efferents by using the anterograde tracer Phaseolus vulgaris leucoagglutinin (PhAL). PhAL injections into the anterior perirhinal cortex labelled a prominent network of fibers within the frontal cortex that was most dense within layers I and II and layer VI. As individual PhAL injection sites within the perirhinal cortex were restricted to one or two adjacent laminae, we were able to determine that layer V was the main source of the perirhinofrontal projection. This was confirmed by frontal cortex injections of the retrograde tracer Fluorogold (FG). Other cortical areas with densely labelled fibers following perirhinal PhAL injections included the agranular insular, infralimbic, orbital, parietal, and entorhinal cortices. Moderate to mild fiber labelling was also noted in the posterior piriform, temporal and occipital cortices, and the claustrum. Subcortical labelling was seen in the nucleus accumbens; fundus striati; basal and lateral amygdala nuclei; thalamic nuclei, including the reuniens, posterior and ventral posteromedial nuclei; the “acoustic thalamus”; and the central grey. Several of these cortical and subcortical projections were bilateral. The different laminar origin of these perirhinal efferents is discussed. These results confirmed our prediction of extensive direct projections from the anterior perirhinal cortex to the frontal cortex in the rat. The significance of this projection is discussed with special reference to the anatomical basis of convulsive limbic seizures. © 1996 Wiley-Liss, Inc.     

Posterior parietal cortex in rhesus monkey: I. Parcellation of areas based on distinctive limbic and sensory corticocortical connections

Injections of HRP-WGA in four cytoarchitectonic subdivisions of the posterior parietal cortex in rhesus monkeys allowed us to examine the major limbic and sensory afferent and efferent connections of each area. Area 7a (the caudal part of the posterior parietal lobe) is reciprocally interconnected with multiple visual-related areas: the superior temporal polysensory area (STP) in the upper bank of the superior temporal sulcus (STS), visual motion areas in the upper bank of STS, the dorsal prelunate gyrus, and portions of V2 and the parieto-occipital (PO) area. Area 7a is also heavily interconnected with limbic areas: the ventral posterior cingulate cortex, agranular retrosplenial cortex, caudomedial lobule, the parahippocampal gyrus, and the presubiculum. By contrast, the adjacent subdivision, area 7ip (within the posterior bank of the intraparietal sulcus), has few limbic connections but projects to and receives projections from widespread visual areas different than those that are connected with area 7a: the ventral bank and fundus of the STS including part of the STP cortex and the inferotemporal cortex (IT), areas MT (middle temporal) and possibly MTp (MT peripheral) and FST (fundal superior temporal) and portions of V2, V3v, V3d, V3A, V4, PO, and the inferior temporal (IT) convexity cortex. The connections between posterior parietal areas and visual areas located on the medial surface of the occipital and parieto-occipital cortex, containing peripheral representations of the visual field (V2, V3, PO), represent a major previously unrecognized source of visual inputs to the parietal association cortex. Area 7b (the rostral part of the posterior parietal lobe) was distinctive among parietal areas in its selective association with somatosensory-related areas: S1, S2, 5, the vestibular cortex, the insular cortex, and the supplementary somatosensory area (SSA). Like 7ip, area 7b had few limbic associations. Area 7m (on the medial posterior parietal cortex) has its own topographically distinct connections with the limbic (the posterior ventral bank of the cingulate sulcus, granular retrosplenial cortex, and presubiculum), visual (V2, PO, and the visual motion cortex in the upper bank of the STS), and somatosensory (SSA, and area 5) cortical areas. Each parietal subdivision is extensively interconnected with areas of the contralateral hemisphere, including both the homotopic cortex and widespread heterotopic areas. Indeed, each area is interconnected with as many areas of the contralateral hemisphere as it is within the ipsilateral one, though less intensively. This pattern of distribution allows for a remarkable degree of interhemispheric integration.(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.     

Parcellation of human temporal polar cortex: A combined analysis of multiple cytoarchitectonic,chemoarchitectonic, and pathological markers

Although the human temporal polar cortex (TPC), anterior to the limen insulae, is heavily involved in high‐order brain functions and many neurological diseases, few studies on the parcellation and extent of the human TPC are available that have used modern neuroanatomical techniques. The present study investigated the TPC with combined analysis of several different cellular, neurochemical, and pathological markers and found that this area is not homogenous, as at least six different areas extend into the TPC, with another area being unique to the polar region. Specifically, perirhinal area 35 extends into the posterior TPC, whereas areas 36 and TE extend more anteriorly. Dorsolaterally, an area located anterior to the typical area TA or parabelt auditory cortex is distinguishable from area TA and is defined as area TAr (rostral). The polysensory cortical area located primarily in the dorsal bank of the superior temporal sulcus, separate from area TA, extends for some distance into the TPC and is defined as the TAp (polysensory). Anterior to the limen insulae and the temporal pyriform cortex, a cortical area, characterized by its olfactory fibers in layer Ia and lack of layer IV, was defined as the temporal insular cortex and named as area TI after Beck (J. Psychol. Neurol. 1934;41:129–264). Finally, a dysgranular TPC region that capped the tip with some extension into the dorsal aspect of the TPC is defined as temporopolar area TG. Therefore, the human TPC actually includes areas TAr and TI, anterior parts of areas 35, 36, TE, and TAp, and the unique temporopolar area TG. J. Comp. Neurol. 514:595–623, 2009. © 2009 Wiley‐Liss, Inc.     

Dual olfactory representation in the rat thalamus: an anatomical and electrophysiological study

A combination of electrophysiological and anatomical techniques was used to determine the sites of termination of olfactory projections to the thalamus and the distribution of the cells of origin of these projections within the olfactory cortex. Following electrical stimulation of the olfactory bulb, short-latency unit responses were recorded not only in the central segment of the mediodorsal thalamic nucleus but also in the ventral and anterior parts of the submedial thalamic nucleus. Responses were not obtained in the ventral or lateral parts of the mediodorsal nucleus, in the dorsal part of the submedial nucleus, or in the intralaminar nuclei between the mediodorsal and submedial nuclei. The cells of origin of the projection were identified by making injections of horseradish peroxidase conjugated to wheat germ agglutinin (HRP WGA) into the thalamus and examining the olfactory cortex for retrogradely labeled cells. Following injections into the mediodorsal nucleus, labeled cells were found in the polymorphic cell zone deep to the olfactory tubercle, in the ventral endopiriform nucleus deep to the piriform cortex, and in an equivalent position deep to the periamygdaloid and lateral entorhinal cortices. After injections into the submedial nucleus, a smaller number of labeled cells were found in similar locations, except that they were restricted to the rostral olfactory cortical areas and were not found deep to the lateral part of the piriform cortex. Retrogradely labeled cells and anterogradely labeled axons were also found in the lateral orbital and ventral agranular insular areas of the prefrontal cortex with injections into the mediodorsal nucleus, and in the ventrolateral orbital area with injections into the submedial nucleus. Anterograde tracing experiments, using the autoradiographic method, have confirmed these results. Injections of 3H-leucine deep to the junction between the anterior piriform cortex and the olfactory tubercle label axons in both the central segment of the mediodorsal nucleus and the ventral part of the submedial nucleus, while injections deep to the posterior piriform cortex label axons in the mediodorsal nucleus only. Within the mediodorsal nucleus, the projection also appears to be organized so that fibers which arise more rostrally terminate ventrolaterally in the central segment, while fibers which arise more caudally terminate more dorsomedially. These results indicate that there is a substantial and possibly dual thalamocortical mechanism available for processing of olfactory stimuli.     

Striatal connections of the parietal association cortices in rhesus monkeys

The corticostriatal connections of the parietal association cortices were examined by the autoradiographic technique in rhesus monkeys. The results show that the rostral portion of the superior parietal lobule projects predominantly to the dorsal portion of the putamen, whereas the caudal portion of the superior parietal lobule and the cortex of the upper bank of the intraparietal sulcus have connections with the caudate nucleus as well as with the dorsal portion of the putamen. The medial parietal convexity cortex projects strongly to the caudate nucleus, and has less extensive projections to the putamen. In contrast, the medial parietal cortex within the caudal portion of the cingulate sulcus projects predominantly to the dorsal portion of the putamen, and has only minor connections with the caudate nucleus. The rostral portion of the inferior parietal lobule projects mainly to the ventral sector of the putamen, and has only minor connections with the caudate nucleus. The middle portion of the inferior parietal lobule has sizable projections to both the putamen and the caudate nucleus. The caudal portion of the inferior parietal lobule as well as the lower bank of the intraparietal sulcus project predominantly to the caudate nucleus, and have relatively minor connections with the putamen. The cortex of the parietal opercular region also shows a specific pattern of corticostriatal projections. Whereas the rostral portion projects exclusively to the ventral sector of the putamen, the caudal portion has connections to the caudate nucleus as well. Thus, it seems that parietostriatal projections show a differential topographic distribution; within both the superior and the inferior parietal region, as one progresses from rostral to caudal, there is a corresponding shift in the predominance of projections from the putamen to the caudate nucleus. In addition, with regard to the projections to the putamen, the superior parietal lobule is related mainly to the dorsal portion, and the inferior parietal lobule to the ventral portion. The striatal projections of the cortex of the caudal portion of the cingulate gyrus (corresponding in part to the supplementary sensory area) and of the rostral parietal opercular region (corresponding in part to the second somatosensory area) are directed almost exclusively to the dorsal and ventral sectors of the putamen, respectively. This pattern resembles that of the primary somatosensory cortex. The results are discussed with regard to the overall architectonic organization of the posterior parietal region. Possible functional aspects of parietostriatal connectivity are considered in the light of physiological and behavioral studies. © 1993 Wiley-Liss, Inc.     

The entorhinal cortex of the monkey: I. Cytoarchitectonic organization

As an essential preliminary to a series of experimental studies of the afferent and efferent connections of the monkey entorhinal cortex, we have carried out a detailed analysis of its cytoarchitectonic organization. Primarily on the basis of features observed in Nissl- and fiber-stained preparations, supplemented with Golgi-stained material and preparations stained for heavy metals by Timm's method and histochemically for acetylcholinesterase, the entorhinal cortex has been divided into seven fields that are named according to their rostrocaudal and mediolateral positions except for one rostrally located field that is named for the prominent input that it receives from the olfactory bulb. At rostral levels, the entorhinal cortex is marked by a number of morphological inhomogeneities. The neurons tend to be organized in patches that are surrounded by large, thick, radially oriented bundles of fibers. At caudal levels, the entorhinal cortex has a more distinctly laminated appearance, reminiscent of that in the neocortex, and most of the neurons and fiber fascicles are arranged in discrete radial columns. The cortical region adjoining the entorhinal cortex laterally, which is commonly known as the "perirhinal cortex," is in fact composed of two separate fields corresponding to areas 35 and 36 of Brodmann. Area 35 occupies the fundus and part of the lateral aspect of the rhinal sulcus. Area 36 extends from the lateral bank of the rhinal sulcus into the inferior temporal gyrus, where it borders fields TA and TE rostrally, and field TF of the parahippocampal gyrus caudally. The surface extents of each of the entorhinal fields have been determined by making "unfolded" two-dimensional maps of the region and measuring the areas with a computerized digitizing system.