Corticocortical connections of area 2 of somatosensory cortex in macaque monkeys: a correlative anatomical and electrophysiological study

The cortical connections of electrophysiologically identified locations in the body representations in somatosensory cortex of macaque monkeys were investigated after injections of horseradish peroxidase, wheat germ agglutinin (WGA) conjugated with horseradish peroxidase, tritiated WGA, or tritiated proline. After extensive microelectrode mapping of portions of the body representations in areas 3b, 1, 2, and 5 and careful determinations of electrophysiological borders between areas, restricted injections of tracers were placed, usually into the representation of the hand in area 2. Other injections were placed in the foot representation in area 2 or in area 1, in the wrist representation in area 1, and in the forearm and wrist representation in area 5. Connection patterns were related to the physiological mapping results and to cortical cytoarchitecture. Injections confined to a lateral portion of area 2 representing the glabrous digits of the hand revealed reciprocal connections with the digit representations in areas 1 and 3b. Projections to area 2 were largely from layer III neurons in both of these fields, and return projections terminated largely in supragranular layers. Other inputs were from layer III cells in one or more separate locations in area 5 and in one or more closely spaced foci in the expected location of S-II in the lateral sulcus. These connections were also reciprocal with terminations apparent in layers IV and III. A few neurons in area 4 were labeled in some of these cases. Results were similar after an injection in the foot representation in area 2 with the differences that infragranular neurons, in addition to supragranular neurons, formed a substantial part of the projection to area 2, terminations as well as projections were noted from area 4, interconnections were found more rostrally in area 6, and a dense focus of label was apparent in the dorsal bank of cingulate sulcus in the apparent location of the supplementary motor area. Injections in the foot representation in area 1 revealed dense layer IV terminations in the foot representation in area 2, as well as connections with area 3b, the S-II region, and areas 5 and 7. The injection in the wrist representation in area 1 resulted in dense terminations in the portion of area 5 responsive to the distal forearm and hand, sparser connections with a lateral location in part of area 2 related to the hand, and interconnections with 3b and S-II.(ABSTRACT TRUNCATED AT 400 WORDS)     

Thalamic connections of three representations of the body surface in somatosensory cortex of gray squirrels

The anatomical tracer, wheat germ agglutinin, was used to determine the connections of electrophysiologically identified locations in three architectonically distinct representations of the body surface in the somatosensory cortex of gray squirrels. Injections in the first somatosensory area, S-I, revealed reciprocal connections with the ventroposterior nucleus (VP), a portion of the thalamus just dorsomedial to VP, the posterior medial nucleus, Pom, and sometimes the ventroposterior inferior nucleus (VPI). As expected, injections in the representation of the face in S-I resulted in label in ventroposterior medial (VPM), the medial subnucleus of VP, whereas injections in the representation of the body labeled ventroposterior lateral (VPL), the lateral subnucleus of VP. Furthermore, there was evidence from connections that the caudal face and head are represented dorsolaterally in VPM, and the forelimb is represented centrally and medially in VPL. The results also support the conclusion that a representation paralleling that in VP exists in Pom, so that the ventrolateral part of Pom represents the face and the dorsomedial part of Pom is devoted to the body. Because connections with VPI were not consistently revealed, the possibility exists that only some parts or functional modules of S-I are interconnected with VPI. Two separate small representations of the body surface adjoin the caudoventral border of S-I. Both resemble the second somatosensory area, S-II, enough to be identified as S-II in the absence of evidence for the other. We term the more dorsal of the two fields S-II because it was previously defined as S-II in squirrels (Nelson et al., '79), and because it more closely resembles the S-II identified in most other mammals. We refer to the other field as the parietal ventral area, PV (Krubitzer et al, '86). Injections in S-II revealed reciprocal connections with VP, Pom, and a thalamic region lateral and caudal to Pom and dorsal to VP, the posterior lateral nucleus, Pol. Whereas major interconnections between S-II and VPI have been reported for cats, raccoons, and monkeys, no such interconnections were found for S-II in squirrels. The parietal ventral area, PV, was found to have prominent reciprocal interconnections with VP, VPI, and the internal (magnocellular) division of the medial geniculate complex (MGi). The pattern of connections conforms to the established somatotopic organization of VP and suggests a crude parallel somatotopic organization in VPI. Less prominent interconnections were with Pol.(ABSTRACT TRUNCATED AT 400 WORDS)     

Somatotopic organization of the lateral sulcus of owl monkeys: area 3b, S-II, and a ventral somatosensory area

Multiunit microelectrode recordings and injections of horseradish peroxidase (HRP) were used to reveal neuron response properties, somatotopic organization, and interconnections of somatosensory cortex in the lateral sulcus (sylvian fissure) of New World owl monkeys. There were a number of main findings. 1) Representations of the face and head in areas 3b, 1, and S-II are found on the upper bank of the lateral sulcus. Most of the mouth and lip representations of area 3b were found in a rostral extension along the lip of the lateral sulcus. Adjacent cortex deeper in the lateral sulcus represented the nose, eye, ear, and scalp. 2) S-II was located on the upper bank of the lateral sulcus and extended past the fundus onto the deepest part of the lower bank. The face was represented most superficially in the sulcus, with the hand, foot, and trunk located in a rostrocaudal sequence deeper in the sulcus. The orientation of S-II is "erect," with the limbs pointing away from area 3b. 3) Neurons in S-II were activated by light tactile stimulation of the contralateral body surface. Receptive fields were several times larger than for area 3b neurons. 4) A 1-2-mm strip of cortex separating the face and hand representations in S-II was consistently responsive to the stimulation of deep receptors but was unresponsive to light cutaneous stimulation. 5) Injections of horseradish peroxidase in the electrophysiologically identified hand or foot representations of area 3b revealed somatotopically matched interconnections with mapped hand and foot representations in S-II. 6) A systematic representation of the body, termed the "ventral somatic" area, VS, was found extending laterally from S-II on the lower bank of the lateral sulcus. Within VS, the hand and foot were represented deep in the sulcus along the hand and foot regions of S-II, and the face was lateral near the ventral lip of the sulcus. 7) Neurons at most recording sites in the VS region were activated by contralateral cutaneous stimuli. However, a few sites had neurons with bilateral receptive fields. Receptive field sizes were comparable to those in S-II. In addition, neurons in islands of cortex in the VS region had properties that suggested that they were activated by pacinian receptors, while other regions were difficult to activate by light tactile stimuli but responded to stimuli that would activate deep receptors. 8) A few recording sites caudal to S-II on the upper bank of the lateral sulcus were responsive to somatic stimuli.(ABSTRACT TRUNCATED AT 400 WORDS)     

Cortical and thalamic connections of the parietal ventral somatosensory area in marmoset monkeys (Callithrix jacchus).

Microelectrode mapping methods were used to define the parietal ventral somatosensory area (PV) on the upper bank of the lateral sulcus in five marmosets (Callithrix jacchus). In the same animals, neuroanatomical tracers were placed into electrophysiologically identified sites in PV and/or the second somatosensory area (S2). Foci of anterograde and retrograde label were related to electrophysiological maps of cortical areas and cortical and thalamic architecture. The results lead to the following conclusions: (1) Multiunit recordings from cortex on the upper bank of the lateral sulcus demonstrate that PV is somatotopically organized, with the face representation adjoining area 3b and the hindlimb and tail representations away from this border in cortex deep on the upper bank of the lateral sulcus. The forelimb representation is caudal in PV adjacent to the S2 forelimb representation. The body surface representation in PV approximates a mirror image of that in S2; (2) Areas PV and S2 are less myelinated and have less cytochrome oxidase enzyme activity than area 3b; (3) The ventroposterior inferior nucleus (VPI) of the thalamus provides the major somatosensory projections to PV. PV is reciprocally connected with VPI and anterior pulvinar; (4) PV has ipsilateral cortical connections with areas 3a, 3b, 1, and M1 and higher order somatosensory fields, and at least most of these connections are somatotopically matched; and (5) Callosal connections of PV are with S2 and PV of the other cerebral hemisphere. These results further establish PV as one of at least four somatosensory areas of the lateral sulcus of primates.     

Interhemispheric connections of somatosensory cortex in the flying fox

The interhemispheric connections of somatosensory cortex in the gray-headed flying fox (Pteropus poliocephalus) were examined. Injections of anatomical tracers were placed into five electrophysiologically identified somatosensory areas: the primary somatosensory area (SI or area 3b), the anterior parietal areas 3a and 1/2, and the lateral somatosensory areas SII (the secondary somatosensory area) and PV (pairetal ventral area). In two animals, the hemisphere opposite to that containing the injection sites was explored electrophysiologically to allow the details of the topography of interconnections to be assessed. Examination of the areal distribution of labeled cell bodies and/or axon terminals in cortex sectioned tangential to the pial surface revealed several consistent findings. First, the density of connections varied as a function of the body part representation injected. For example, the area 3b representation of the trunk and structures of the face are more densely interconnected than the representation of distal body parts (e.g., digit 1, D1). Second, callosal connections appear to be both matched and mismatched to the body part representations injected in the opposite hemisphere. For example, an injection of retrograde tracer into the trunk representation of area 3b revealed connections from the trunk representation in the opposite hemisphere, as well as from shoulder and forelimb/wing representations. Third, the same body part is differentially connected in different fields via the corpus callosum. For example, the D1 representation in area 3b in one hemisphere had no connections with the area 3b D1 representation in the opposite hemisphere, whereas the D1 representation in area 1/2 had relatively dense reciprocal connections with area 1/2 in the opposite hemisphere. Finally, there are callosal projections to fields other than the homotopic, contralateral field. For example, the D1 representation in area 1/2 projects to contralateral area 1/2, and also to area 3b and SII. J. Comp. Neurol. 402:538–559, 1998. © 1998 Wiley-Liss, Inc.     

Somatosensory cortex of prosimian Galagos: physiological recording,cytoarchitecture, and corticocortical connections of anterior parietal cortex and cortex of the lateral sulcus

Compared with our growing understanding of the organization of somatosensory cortex in monkeys, little is known about prosimian primates, a major branch of primate evolution that diverged from anthropoid primates some 60 million years ago. Here we describe extensive results obtained from an African prosimian, Galago garnetti. Microelectrodes were used to record from large numbers of cortical sites in order to reveal regions of responsiveness to cutaneous stimuli and patterns of somatotopic organization. Injections of one to several distinguishable tracers were placed at physiologically identified sites in four different cortical areas to label corticortical connections. Both types of results were related to cortical architecture. Three systematic representations of cutaneous receptors were revealed by the microelectrode recordings, S1 proper or area 3b, S2, and the parietal ventral area (PV), as described in monkeys. Strips of cortex rostral (presumptive area 3a) and caudal (presumptive area 1-2) to area 3b responded poorly to tactile stimuli in anesthetized galagos, but connection patterns with area 3b indicated that parallel somatosensory representations exist in both of these regions. Area 3b also interconnected somatotopically with areas S2 and PV. Areas S2 and PV had connections with areas 3a, 3b, 1-2, each other, other regions of the lateral sulcus, motor cortex (M1), cingulate cortex, frontal cortex, orbital cortex, and inferior parietal cortex. Connection patterns and recordings provided evidence for several additional fields in the lateral sulcus, including a retroinsular area (Ri), a parietal rostral area (PR), and a ventral somatosensory area (VS). Galagos appear to have retained an ancestral preprimate arrangement of five basic areas (S1 proper, 3a, 1-2, S2, and PV). Some of the additional areas suggested for lateral parietal cortex may be primate specializations.     

Ipsilateral cortical connections of motor, premotor, frontal eye, and posterior parietal fields in a prosimian primate, Otolemur garnetti

The ipsilateral connections of motor areas of galagos were determined by injecting tracers into primary motor cortex (M1), dorsal premotor area (PMD), ventral premotor area (PMV), supplementary motor area (SMA), and frontal eye field (FEF). Other injections were placed in frontal cortex and in posterior parietal cortex to define the connections of motor areas further. Intracortical microstimulation was used to identify injection sites and map motor areas in the same cases. The major connections of M1 were with premotor cortex, SMA, cingulate motor cortex, somatosensory areas 3a and 1, and the rostral half of posterior parietal cortex. Less dense connections were with the second (S2) and parietal ventral (PV) somatosensory areas. Injections in PMD labeled neurons across a mediolateral belt of posterior parietal cortex extending from the medial wall to lateral to the intraparietal sulcus. Other inputs came from SMA, M1, PMV, and adjoining frontal cortex. PMV injections labeled neurons across a large zone of posterior parietal cortex, overlapping the region projecting to PMD but centered more laterally. Other connections were with M1, PMD, and frontal cortex and sparsely with somatosensory areas 3a, 1-2, S2, and PV. SMA connections were with medial posterior parietal cortex, cingulate motor cortex, PMD, and PMV. An FEF injection labeled neurons in the intraparietal sulcus. Injections in posterior parietal cortex revealed that the rostral half receives somatosensory inputs, whereas the caudal half receives visual inputs. Thus, posterior parietal cortex links visual and somatosensory areas with motor fields of frontal cortex.     

Corticocortical projections to representations of the teeth,tongue, and face in somatosensory area 3b of macaques

We placed injections of anatomical tracers into representations of the tongue, teeth, and face in the primary somatosensory cortex (area 3b) of macaque monkeys. Our injections revealed strong projections to representations of the tongue and teeth from other parts of the oral cavity responsive region in 3b. The 3b face also provided input to the representations of the intraoral structures. The primary representation of the face showed a pattern of intrinsic connections similar to that of the mouth. The area 3b hand representation provided little to no input to either the mouth or the face representations. The mouth and face representations of area 3b received projections from the presumptive oral cavity and face regions of other somatosensory areas in the anterior parietal cortex and the lateral sulcus, including areas 3a, 1, 2, the second somatosensory area (S2), the parietal ventral area (PV), and cortex that may include the parietal rostral (PR) and ventral somatosensory (VS) areas. Additional inputs came from primary motor (M1) and ventral premotor (PMv) areas. This areal pattern of projections is similar to the well‐studied pattern revealed by tracer injections in regions of 3b representing the hand. The tongue representation appeared to be unique in area 3b in that it also received inputs from areas in the anterior upper bank of the lateral sulcus and anterior insula that may include the primary gustatory area (area G) and other cortical taste‐processing areas, as well as a region of lateral prefrontal cortex (LPFC) lining the principal sulcus. J. Comp. Neurol. 522:546–572, 2014. © 2013 Wiley Periodicals, Inc.     

Cortical connections of areas 17 (V-I) and 18 (V-II) of squirrels

Connections of visual cortex in squirrels were investigated by placing WGA-HRP injections, and in some cases fluorescent dyes, into area 17 (V-I) or area 18 (V-II). Results were related to architectonic fields determined in brain sections cut parallel to the surface of manually flattened cortex and to limited microelectrode mapping data. Injections in area 17 provided evidence for 1) a patchy pattern of horizontal intrinsic connections extending 1-2 mm from the injection site; 2) uneven, widely distributed connections with area 18 (V-II) and adjoining occipital-temporal (OT) cortex; and 3) callosal connections of large portions of area 17 with the 17/18 border zone. While restricted locations in area 17 had uneven interconnections over several mm of area 18, more rostral locations in area 17 related to more rostral locations in area 18, demonstrating a topographic tendency. Injections in area 18 revealed 1) zones of discontinuous connections with area 17 that followed a topographic pattern, 2) patches of intrinsic connections that spread over distances of up to 6-8 mm from the injection site; 3) two zones of uneven connections with OT cortex suggesting the locations of at least two visual areas, OTr and OTc; 4) connections with limbic cortex rostromedial to areas 17 and 18; 5) sparse connections with regions of temporal cortex lateral to OT; and 6) uneven callosal connections with area 18 and OT cortex. The widespread and unevenly distributed intrinsic callosal interconnection patterns of areas 17 and 18 contrast with the restricted excitatory receptive fields of neurons and the retinotopic patterns of representation in these fields. Although physiological evidence is presently lacking, the patchy connections suggest that areas 17 and 18 in squirrels are modularly organized.     

Anatomical and functional organization of somatosensory areas of the lateral fissure of the New World titi monkey (Callicebus moloch)

The organization of anterior and lateral somatosensory cortex was investigated in titi monkeys (Callicebus moloch). Multiunit microelectrode recordings were used to identify multiple representations of the body, and anatomical tracer injections were used to reveal connections. (1) Representations of the face were identified in areas 3a, 3b, 1, S2, and the parietal ventral area (PV). In area 3b, the face was represented from chin/lower lip to upper lip and neck/upper face in a rostrocaudal sequence. The representation of the face in area 1 mirrored that of area 3b. Another face representation was located in area 3a. Adjoining face representations in S2 and PV exhibited mirror-image patterns to those of areas 3b and 1. (2) Two representations of the body, the rostral and caudal ventral somatosensory areas (VSr and VSc), were found in the dorsal part of the insula. VSc was roughly a reversal image of the S2 body representation, and VSr was roughly a reversal of PV. (3) Neurons in the insula next to VSr and VSc responded to auditory stimuli or to both auditory and somatosensory stimuli. (4) Injections of tracers within the hand representations in areas 3b, 1, and S2 revealed reciprocal connections between these three areas. Injections in areas 3b and 1 labeled the ventroposterior nucleus, whereas injections in S2 labeled the inferior ventroposterior nucleus. The present study demonstrates features of somatosensory cortex of other monkeys in titi monkeys, while revealing additional features that likely apply to other primates.     

Connections of somatosensory cortex in megachiropteran bats: The evolution of cortical fields in mammals

The cortical connections of the primary somatosensory area (SI or 3b), a caudal somatosensory field (area 1/2), the second somatosensory area (SII), the parietal ventral area (PV), the ventral somatosensory area (VS), and the lateral parietal area (LP) were investigated in grey headed flying foxes by injecting anatomical tracers into electrophysiologically identified locations in these fields. The receptive fields for clusters of neurons were mapped with sufficient density for injection sites to be related to the boundaries of fields, and to representations of specific body parts within the fields. In all cases, cortex was flattened and sectioned parallel to the cortical surface. Sections were stained for myelin and architectonic features of cortex were related to physiological mapping and connection patterns. We found patterns of topographic and montopographic connections between 3b and adjacent anterior parietal fields 3a and 1/2, and fields caudolateral to 3b (SII and PV). Area 1/2 had both topographic and nontopographic connections with 3b, PP, and SII. Connections of SII and PV with areas 3b, 3a, and 1/2 were roughly topographic, although there was clear evidence for nontopographic connections between these fields. SII was most densely connected with area 1/2, while PV was most densely connected with 3b. SII had additional connections with fields in lateral parietal cortex and with subdivisions of motor cortex. Other connections of PV were with subdivisions of motor cortex and pyriform cortex. Laminar differences in connection patterns of SII and PV with surrounding cortex were also observed. Injections in the ventral somatosensory area revealed connections with SII, PV, area 1/2, auditory cortex, entorhinal cortex, and pyriform cortex. Finally, the lateral parietal field had very dense connections with posterior parietal cortex, caudal temporal cortex, and with subdivisions of motor cortex. Our results indicate that the 3b region is not homogeneous, but is composed of myelin dense and light regions, associated with 3b proper and invaginations of area 1/2, respectively. Connections of myelin dense 3b were different from invaginating portions of myelin light area 1/2. Our findings that 3b is densely interconnected with PV and moderately to lightly interconnected with SII supports the notion that SII and PV have been confused across mammals and across studies. Our connectional evidence provides further support for our hypothesis that area 1/2 is partially incorporated in 3b and has led to theories of the evolution of cortical fields in mammals. © 1993 Wiley-Liss, Inc.     

Cortical connections of the second somatosensory area and the parietal ventral area in macaque monkeys

To gain insight into how cortical fields process somatic inputs and ultimately contribute to complex abilities such as tactile object perception, we examined the pattern of connections of two areas in the lateral sulcus of macaque monkeys: the second somatosensory area (S2), and the parietal ventral area (PV). Neuroanatomical tracers were injected into electrophysiologically and/or architectonically defined locations, and labeled cell bodies were identified in cortex ipsilateral and contralateral to the injection site. Transported tracer was related to architectonically defined boundaries so that the full complement of connections of S2 and PV could be appreciated. Our results indicate that S2 is densely interconnected with the primary somatosensory area (3b), PV, and area 7b of the ipsilateral hemisphere, and with S2, 7b, and 3b in the opposite hemisphere. PV is interconnected with areas 3b and 7b, with the parietal rostroventral area, premotor cortex, posterior parietal cortex, and with the medial auditory belt areas. Contralateral connections were restricted to PV in the opposite hemisphere. These data indicate that S2 and PV have unique and overlapping patterns of connections, and that they comprise part of a network that processes both cutaneous and proprioceptive inputs necessary for tactile discrimination and recognition. Although more data are needed, these patterns of interconnections of cortical fields and thalamic nuclei suggest that the somatosensory system may not be segregated into two separate streams of information processing, as has been hypothesized for the visual system. Rather, some fields may be involved in a variety of functions that require motor and sensory integration.     

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.     

The somatosensory thalamus of monkeys: cortical connections and a redefinition of nuclei in marmosets.

Thalamic connections of three subdivisions of somatosensory cortex in marmosets were determined by placing wheatgerm agglutinin conjugated with horseradish peroxidase and fluorescent dyes as tracers into electrophysiologically identified sites in S-I (area 3b), S-II, and the parietal ventral area, PV. The relation of the resulting patterns of transported label to the cytoarchitecture and cytochrome oxidase architecture of the thalamus lead to three major conclusions. 1) The region traditionally described as the ventroposterior nucleus (VP) is a composite of VP proper and parts of the ventroposterior inferior nucleus (VPi). Much of the VP region consists of groups of densely stained, closely packed neurons that project to S-I. VPi includes a ventral oval of pale, less densely packed neurons and finger-like protrusions that extend into VP proper and separate clusters of VP neurons related to different body parts. Neurons in both parts of VPi project to S-II rather than S-I. Connection patterns indicate that the proper and the embedded parts of VPi combine to form a body representation paralleling that in VP. 2) VPi also provides the major thalamic input into PV. 3) In architecture, location, and cortical connections, the region traditionally described as the anterior pulvinar (AP) of monkeys resembles the medial posterior nucleus, Pom, of other mammals and we propose that all or most of AP is homologous to Pom. AP caps VP dorsomedially, has neurons that are moderately dense in Nissl staining, and reacts moderately in CO preparations. AP neurons project to S-I, S-II, and PV in somatotopic patterns.     

Heterotopic and homotopic callosal connections in rat visual cortex

Heterotopic and homotopic callosal projections of rat visual cortex are evaluated. Callosal termination zones in visual cortex are identified with a degeneration technique following complete section of the corpus callosum. The zones which receive callosal afferents are the lateral one-third of area 17, an anteroposterior strip in dorsal and in ventral areas 18a, and 4 patches in area 18b. Following a large injection of lectin-bound horseradish peroxidase (WGA-HRP) into visual cortex, many retrogradely labeled neurons are found in the medial two-thirds of area 17 which does not receive callosal afferents, as well as in the lateral, callosal-recipient zone. These data suggest that heterotopic callosal pathways exist in visual cortex. Injections of tritiated amino acids into restricted parts of visual cortex show the following heterotopic connections: lateral area 17 projects to dorsal area 18a; medial area 17 projects to lateral area 17 and dorsal area 18a; area 18a projects to lateral area 17 and anteromedial area 18b; area 18b projects to lateral area 17, dorsal area 18a, heterotopic sites in area 18b, and to area 29d . Heterotopic connections are generally less dense than homotopic ones. In addition, heterotopic connections are generally less dense than homotopic ones. In addition, heterotopic projections terminate in the supragranular layers. This contrasts with the homotopic afferents of areas 17 and 18a which have additional strong projections to layer V. The distribution of label through the depth of the cortex in some of the callosal recipient zones has been quantified. Injections of WGA-HRP restricted to areas 17, 18a or 18b corroborate the presence of each of the heterotopic connections described above. Heterotopic afferents originate mostly from layer V neurons, whereas homotopic afferents arise from neurons primarily in layers II-V. Like the afferents, the numbers of callosal projection cells in heterotopic regions are substantially less than that in homotopic sites. heterotopic callosal connections may be one factor responsible for binocular vision and also may provide the basis for large, nonoriented receptive fields of units in layer V of rodent visual cortex.     

Corticocortical projections to area 1 in squirrel monkeys (Saimiri sciureus)

Cortical area 1 is a non‐primary somatosensory area in the primate anterior parietal cortex that is critical to tactile discrimination. The corticocortical projections to area 1 in squirrel monkeys were determined by placing multiple injections of anatomical tracers into separate body part representations defined by multiunit microelectrode mapping in area 1. The pattern of labeled cells in the cortex indicated that area 1 has strong intrinsic connections within each body part representation and has inputs from somatotopically matched regions of areas 3b, 3a, 2 and 5. Somatosensory areas in the lateral sulcus, including the second somatosensory area (S2), the parietal ventral area (PV), and the presumptive parietal rostral (PR) and ventral somatosensory (VS) areas, also project to area 1. Topographically organized projections to area 1 also came from the primary motor cortex (M1), the dorsal and ventral premotor areas (PMd and PMv), and the supplementary motor area (SMA). Labeled cells were also found in cingulate motor and sensory areas on the medial wall of the hemisphere. Previous studies revealed a similar pattern of projections to area 1 in Old World macaque monkeys, suggesting a pattern of cortical inputs to area 1 that is common across anthropoid primates.     

A visuo‐somatomotor pathway through superior parietal cortex in the macaque monkey: cortical connections of areas V6 and V6A

This report addresses the connectivity of the cortex occupying middle to dorsal levels of the anterior bank of the parieto-occipital sulcus in the macaque monkey. We have previously referred to this territory, whose perimeter is roughly circumscribed by the distribution of interhemispheric callosal fibres, as area V6, or the ‘V6 complex’. Following injections of wheatgerm agglutinin conjugated to horseradish peroxidase (WGA-HRP) into this region, we examined the laminar organization of labelled cells and axonal terminals to attain indications of relative hierarchical status among the network of connected areas. A notable transition in the laminar patterns of the local, intrinsic connections prompted a sub-designation of the V6 complex itself into two separate areas, V6 and V6A, with area V6A lying dorsal, or dorsomedial to V6 proper. V6 receives ascending input from V2 and V3, ranks equal to V3A and V5, and provides an ascending input to V6A at the level above. V6A is not connected to area V2 and in general is less heavily linked to the earliest visual areas; in other respects, the two parts of the V6 complex share similar spheres of connectivity. These include regions of peripheral representation in prestriate areas V3, V3A and V5, parietal visual areas V5A/MST and 7a, other regions of visuo-somatosensory association cortex within the intraparietal sulcus and on the medial surface of the hemisphere, and the premotor cortex. Subcortical connections include the medial and lateral pulvinar, caudate nucleus, claustrum, middle and deep layers of the superior colliculus and pontine nuclei. From this pattern of connections, it is clear that the V6 complex is heavily engaged in sensory-motor integration. The specific somatotopic locations within sensorimotor cortex that receive this input suggest a role in controlling the trunk and limbs, and outward reaching arm movements. There is a secondary contribution to the brain's complex oculomotor circuitry. That the medial region of the cortex is devoted to tightly interconnected representations of the sensory periphery, both visual and somatotopic—which are routinely stimulated in concert—would appear to be an aspect of the global organization of the cortex which must facilitate multimodal integration.     

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.     

Ipsilateral cortical connections of dorsal and ventral premotor areas in New World owl monkeys

In order to compare connections of premotor cortical areas of New World monkeys with those of Old World macaque monkeys and prosimian galagos, we placed injections of fluorescent tracers and wheat germ agglutinin-horseradish peroxidase (WGA-HRP) in dorsal (PMD) and ventral (PMV) premotor areas of owl monkeys. Motor areas and injection sites were defined by patterns of movements electrically evoked from the cortex with microelectrodes. Labeled neurons and axon terminals were located in brain sections cut either in the coronal plane or parallel to the surface of flattened cortex, and they related to architectonically and electrophysiologically defined cortical areas. Both the PMV and PMD had connections with the primary motor cortex (M1), the supplementary motor area (SMA), cingulate motor areas, somatosensory areas S2 and PV, and the posterior parietal cortex. Only the PMV had connections with somatosensory areas 3a, 1, 2, PR, and PV. The PMD received inputs from more caudal portions of the cortex of the lateral sulcus and more medial portions of the posterior parietal cortex than the PMV. The PMD and PMV were only weakly interconnected. New World owl monkeys, Old World macaque monkeys, and galagos share a number of PMV and PMD connections, suggesting preservation of a common sensorimotor network from early primates. Comparisons of PMD and PMV connectivity with the cortex of the lateral sulcus and posterior parietal cortex of owl monkeys, galagos, and macaques help identify areas that could be homologous.