Topographical organization of cortical afferents to extrastriate visual area PO in the macaque: a dual tracer study

We have examined the origin and topography of cortical projections to area PO, an extrastriate visual area located in the parieto-occipital sulcus of the macaque. Distinguishable retrograde fluorescent tracers were injected into area PO at separate retinotopic loci identified by single-neuron recording. The results indicate that area PO receives retinotopically organized inputs from visual areas V1, V2, V3, V4, and MT. In each of these areas the projection to PO arises from the representation of the periphery of the visual field. This finding is consistent with neurophysiological data indicating that the representation of the periphery is emphasized in PO. Additional projections arise from area MST, the frontal eye fields, and several divisions of parietal cortex, including four zones within the intraparietal sulcus and a region on the medial dorsal surface of the hemisphere (MDP). On the basis of the laminar distribution of labeled cells we conclude that area PO receives an ascending input from V1, V2, and V3 and receives descending or lateral inputs from all other areas. Thus, area PO is at approximately the same level in the hierarchy of visual areas as areas V4 and MT. Area PO is connected both directly and indirectly, via MT and MST, to parietal cortex. Within parietal cortex, area PO is linked to particular regions of the intraparietal sulcus including VIP and LIP and two newly recognized zones termed here MIP and PIP. The wealth of connections with parietal cortex suggests that area PO provides a relatively direct route over which information concerning the visual field periphery can be transmitted from striate and prestriate cortex to parietal cortex. In contrast, area PO has few links with areas projecting to inferior temporal cortex. The pattern of connections revealed in this study is consistent with the view that area PO is primarily involved in visuospatial functioning.     

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.     

Response latencies of neurons in visual areas MT and MST of monkeys with striate cortex lesions

Cortical area, MT (middle temporal area) is specialized for the visual analysis of stimulus motion in the brain. It has been suggested [Brain 118 (1995) 1375] that motion signals reach area MT via two dissociable routes, namely a 'direct' route which bypasses primary visual cortex (area, striate cortex (V1)) and is specialized for processing 'fast' motion (defined as faster than 6 degrees/s) with a relatively short latency, and an 'indirect' route via area V1 for processing 'slow' motion (slower than 6 degrees/s) with a relatively long latency. We tested this proposal by measuring the effects of unilateral V1 lesions on the magnitudes and latencies of responses to fast- and slow-motion (depicted by random dot kinematograms (RDK) ) of single neurons in areas MT and medial superior temporal area (MST) of anaesthetized macaque monkeys. In the unlesioned hemisphere contralateral to a V1 lesion, response magnitudes and latencies of MT neurons were similar to those previously reported from MT neurons in normal monkeys, and there was no significant association between slow movement and long response latency (>100 ms), or between fast movement and short latency (< or =100 ms). V1 lesions led to diminished response magnitudes and increased latencies in area MT of the lesioned hemisphere, but did not selectively abolish MT responses to slow moving stimuli, or abolish long-latency responses to either slow- or fast-moving stimuli. Response magnitudes and latencies in area MST, which receives visual inputs directly from area MT and is also specialized for visual analysis of motion, were unaffected by V1 lesions (though we have shown elsewhere that directionally-selective responses in both areas were impaired by V1 lesions). Overall, the results are incompatible with the hypothesis that there are dissociable routes to MT specialized for processing separately fast and slow motion.     

Projections to the superior temporal sulcus from the central and peripheral field representations of V1 and V2

In a series of three studies, we have begun to explore the sequence of visual information processing along the pathway from striate cortex (V1), through MT, into the parietal lobe. In this first study, we sought to establish the relationships among MT, the heavily myelinated zone of the superior temporal sulcus (STS), and the V1 and V2 projection fields in the STS. Autoradiographic material from seven hemispheres of six macaques injected with tritiated amino acids into either V1 or V2 was analyzed in detail, and the results were plotted onto two-dimensional reconstructions of the STS. Autoradiographic material from eight additional macaques with V2 injections was also examined. The results indicate that the central visual field representations of both V1 and V2 project into the heavily myelinated zone in the lower bank and floor of the STS, confirming prior studies, whereas the far peripheral representations of both V1 and V2 project into the cortex medial to this zone on the upper bank of the sulcus. There is no evidence that this medial cortex is a separate area that receives projections from V1 and V2 in parallel with the projections these areas send to the heavily myelinated zone. Rather, there seems to be a single projection field of V1 and V2 whose central representation lies within the heavily myelinated zone and whose most peripheral representation lies medial to it. Because of the difference in myelination between the central and peripheral field representations as well as visuotopic anomalies between them, we retain the term "MT" for the heavily myelinated zone and apply the term "MTp" to the far peripheral projection zone. Both MT and MTp are required to process the complete outputs of V1 and V2 within the STS and thus should probably be regarded as two distinctive parts of a single visual area. The difference in myelination between MT and MTp suggests that there is a difference in visual processing between the central and peripheral visual fields. The average size of MT is estimated to be 62 mm2, and the average size of MT and MTp combined to be 76 mm2, which is consistent with estimates derived from several other studies.     

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)     

Cortical connections of inferior temporal area TEO in macaque monkeys

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

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

     

Organization of visual inputs to the inferior temporal and posterior parietal cortex in macaques.

It has been proposed that visual information in the extrastriate cortex is conveyed along 2 major processing pathways, a "dorsal" pathway directed to the posterior parietal cortex, underlying spatial vision, and a "ventral" pathway directed to the inferior temporal cortex, underlying object vision. To determine the relative distributions of cells projecting to the 2 pathways, we injected the posterior parietal and inferior temporal cortex with different fluorescent tracers in 5 rhesus monkeys. The parietal injections included the ventral intraparietal (VIP) and lateral intraparietal (LIP) areas, and the temporal injections included the lateral portions of cytoarchitectonic areas TE and TEO. There was a remarkable segregation of cells projecting to the 2 systems. Inputs to the parietal cortex tended to arise either from areas that have been implicated in spatial or motion analysis or from peripheral field representations in the prestriate cortex. By contrast, inputs to the temporal cortex tended to arise from areas that have been implicated in form and color analysis or from central field representations. Cells projecting to the parietal cortex were found in visual area 2 (V2), but only in the far peripheral representations of both the upper and lower visual field. Likewise, labeled cells found in visual areas 3 (V3) and 4 (V4) were densest in their peripheral representations. Heavy accumulations of labeled cells were found in the dorsal parieto-occipital cortex, including the parieto-occipital (PO) area, part A of V3 (V3A), and the dorsal prelunate area (DP). In the superior temporal sulcus, cells were found within several motion-sensitive areas, including the middle temporal area (MT), the medial superior temporal area (MST), the fundus of the superior temporal area (FST), and the superior temporal polysensory area (STP), as well as within anterior portions of the sulcus whose organization is as yet poorly defined. Cells projecting to areas TE and TEO in the temporal cortex were located within cytoarchitectonic area TG at the temporal pole and cytoarchitectonic areas TF and TH on the parahippocampal gyrus, as well as in noninjected portions of area TE buried within the superior temporal sulcus. In the prestriate cortex, labeled cells were found in V2, V3, and V4, but, in contrast to the loci labeled after parietal injections, those labeled after temporal injections were concentrated in the foveal or central field representations. Although few double-labeled cells were seen, 2 regions containing intermingled parietal- and temporal-projection cells were area V4 and the cortex at the bottom of the anterior superior temporal sulcus.(ABSTRACT TRUNCATED AT 400 WORDS)     

Cortical connections of the caudal subdivision of the dorsolateral area (V4) in monkeys.

Evidence suggests that all primates have rostral and caudal subdivisions in the region of visual cortex identified as the dorsolateral area (DL) or V4. However, the connections of DL/V4 have not been examined in terms of these subdivisions. To determine the cortical connections of the caudal subdivision of DL (DLC) in squirrel monkeys, injections of the neuroanatomical tracers wheat germ agglutinin conjugated to horseradish peroxidase, Diamidino Yellow, and Fluoro-Gold were made in cortex rostral to V II. To aid in delineating the borders of DLC, cortex was also evaluated architectonically. Based on similar patterns of connections, DLC extends from dorsolateral to ventrolateral cortex. DLC receives strong, feedforward input from V II and projects in a feedforward fashion to the rostral subdivision of DL (DLR) and caudal inferior temporal (IT) cortex, including a separate location in the inferior temporal sulcus. DLC has weaker connections with V I, the middle temporal area (MT), cortex rostral to MT in the location of the fundal superior temporal area (FST), cortex dorsal to DLC, ventral cortex rostral to V II, and cortex in the frontal lobe, lateral to the inferior arcuate sulcus. Only lateral DLC has connections with V I, and only dorsolateral DLC has connections with cortex dorsal to DLC. The topographic organization of DLC was inferred from its connections with V II. Thus, dorsolateral DLC represents the lower field, lateral DLC represents central vision, and ventrolateral DLC represents the upper field. Limited observations were made on DLR. Confirming earlier observations (Cusick and Kaas: Visual Neurosci. 1:211, 1988), DLR is paler than DLC myeloarchitectonically. DLR receives only sparse feedforward input from V II, but stronger input from DLC. DLR has strong connections with cortex just rostral to dorsal V II, ventral posterior parietal cortex in the sylvian fissure, MT, the medial superior temporal area, FST, and the inferior temporal sulcus. DLR also shares connections with IT cortex. Thus, while both DLC and DLR are involved in the pathway relaying visual information to IT cortex, an area specialized for object vision, DLR also projects densely to areas such as MT involved in the pathway relaying to posterior parietal cortex, a region specialized for spatial localization and motion perception.     

Afferent basis of visual response properties in area MT of the macaque. I. Effects of striate cortex removal

The middle temporal area (MT) of the macaque monkey is a region of extrastriate cortex involved in the analysis of visual motion. MT receives strong projections from striate cortex and from area V2, which is dependent on striate for visual responsiveness. Accordingly, the visual properties of MT neurons have been thought to reflect the further processing of its input from striate cortex. We examined the dependence of MT activity on pathways deriving from striate cortex by recording from MT neurons following removal of their striate input. Repeated recordings in area MT were made in 4 hemispheres of anesthetized macaques following either partial or total ablations of striate cortex. Cells in MT were tested for responsiveness, selectivity for direction of motion and direction tuning, and ocular dominance. Receptive fields were also plotted. In an additional animal, we recorded from MT neurons during reversible cooling of the central representation in striate cortex. We found that striate cortex removal or inactivation did not abolish the visual responsiveness of the majority of MT cells. Although the residual responses were generally much weaker than in the intact animal, direction selectivity and binocularity were still present. Moreover, receptive field size and overall topography appeared unaltered.     

Multiple visual areas in the caudal superior temporal sulcus of the macaque

Anatomical and physiological evidence indicates that, in addition to area MT, much of the cortex in the caudal superior temporal sulcus (STS) of the macaque has visual functions. Yet the organization of areas outside of MT remains unclear, and there are even conflicting data on the boundaries of MT itself. To examine these issues, we recorded form neurons throughout this region in three monkeys. Anterograde or retrograde tracers were injected into MT at the conclusion of recording to identify its projection fields. Based on differences in their visuotopic organization, neuronal properties, receptive field size, myeloarchitecture, and pattern of connections with MT, several visual areas were distinguished within the caudal STS. Area MT, defined as the heavily myelinated portion of the striate (VI) projection zone in STS, contained a systematic representation of only about the central 30 degrees--40 degrees of the contralateral field. The far peripheral field was represented medial to MT in MTp, which we had previously found receives projections from far peripheral V1 and V2 (Ungerleider and Desimone: J. Comp. Neurol. 248:147-163, 1986). Like MT, MTp contained a high proportion of directionally selective cells, and receptive field size in MTp was the size expected of MT fields if the latter were to extend into the periphery. Areas MST (medial superior temporal) and PP (posterior parietal) were found medial to MT and MTp. Both MST and PP had a high proportion of directionally selective cells, but only MST received a direct projection from MT. Cells in MST had larger receptive fields than those in either MT or MTp but nonetheless displayed a crude visuotopic organization. Receptive fields of cells in PP were even larger, some including the entire contralateral visual field. Furthermore, unlike cells in MST, some in PP responded to auditory or somesthetic stimuli in addition to visual stimuli. Area FST, which has a distinctive myeloarchitecture, was found anterior to MT in the fundus of the STS, for which it is named. FST received a direct projection from MT, but only about a third of its cells were directionally selective. Receptive fields of cells in FST were large, often included the center of gaze, and often crossed into the ipsilateral visual field. Area V4t (transitional V4) and a portion of V4 were found lateral to MT within the STS, and both received direct projections from MT. V4t has a distinctive, light myelination. Both areas had a low incidence of directionally selective cells, and both contained coarse representations of the lower visual field.(ABSTRACT TRUNCATED AT 400 WORDS)     

Visuotopic organisation and neuronal response selectivity for direction of motion in visual areas of the caudal temporal lobe of the marmoset monkey (Callithrix jacchus): Middle temporal area,middle temporal crescent,and surrounding cortex

On the basis of extracellular recordings in marmoset monkeys, we report on the organisation of the middle temporal area (MT) and the surrounding middle temporal crescent (MTc). Area MT is approximately 5-mm long and 2-mm wide, whereas the MTc forms a crescent-shaped band of cortex 1-mm wide. Neurones in area MT form a first-order representation of the contralateral hemifield, whereas those in the MTc form a second-order representation with a field discontinuity near the horizontal meridian. The representation of the vertical meridian forms the border between area MT and the MTc. In both areas, the fovea is represented ventrocaudally, and the visual field periphery is represented dorsorostrally. Analysis of single units revealed that 86% of cells in area MT show a strong selectivity for the direction of motion of visual stimuli. The proportion of direction-selective cells in the MTc (53%), whereas lower than that in area MT, is much higher than that observed in most other visual areas. Neurones in the cortex immediately rostral to area MT and the MTc are direction selective, with receptive fields predominantly located in the visual field periphery. In contrast, only a minority of the cells in the cortex ventral to the MTc are direction selective, and their receptive fields emphasise central vision. The results suggest that the MTc is functionally closely related to area MT, and distinct from the areas forming the dorsolateral complex. The MTc may have a role in combining information about motion in the visual field, processed by area MT, with information about stimulus shape, processed by the dorsolateral complex. J. Comp. Neurol. 393:505–527, 1998. © 1998 Wiley-Liss, Inc.     

Cortical connections of visual area MT in the macaque

We have identified the cortical connections of area MT and determined their topographic organization and relationship to myeloarchitectural fields. Efferents of MT were examined in seven macaques that had received injections of tritiated amino acids, and afferents were examined in one macaque that had received injections of two fluorescent dyes. The injection sites formed an orderly sequence from the representation of central to that of peripheral vision in the upper and lower visual fields. In addition to connections with the striate cortex (V1), connections were found between MT and a variety of extrastriate areas, including V2, V3, V3A, V4, V4t, VIP, MST, FST, possibly PO, and, finally, the frontal eye field. The connections of MT with V1, V2, and the dorsal and ventral portions of V3 were topographically organized and consistent with the visuotopic arrangement reported previously in these areas. V2 could be distinguished from V3 by the distinctive myeloarchitectural appearance of the former. Connections with areas V4 and V4t also displayed at least a coarse visuotopic organization, in that the central representation of MT projected laterally in these areas and the peripheral representation projected medially. The lower visual field representation of V4 was located dorsally, on the prelunate convexity, while the upper field representation was located primarily on the ventral aspect of the hemisphere. V4t had a distinctively light myeloarchitecture and received projections from only the lower field representation of MT. The remaining connections of MT were with areas located entirely in the dorsal half of the hemisphere. There were widespread connections with areas MST and FST in the superior temporal sulcus, with some evidence for a crude visuotopic organization in MST. Connections were also found with area VIP in the intraparietal sulcus, with area V3A on the annectent gyrus, possibly with area PO in the dorsomedial prestriate cortex, and, finally, with the frontal eye field on the anterior bank of the lower limb of the arcuate sulcus. Area FST and parts of both MST and VIP had a distinctive myeloarchitecture. The pattern of laminar connections with V1, V2, and V3 indicated that MT projects "back" to these areas and they project "forward" to MT. That is, the projections to these areas from MT terminated in both the supragranular and infragranular layers and the projections to MT from these areas originated predominantly from cells located above granular layer IV (above layer IVC in V1).(ABSTRACT TRUNCATED AT 400 WORDS)     

Spatial and temporal frequency tuning in striate cortex: functional uniformity and specializations related to receptive field eccentricity

In light of anatomical evidence suggesting differential connection patterns in central vs. peripheral representations of cortical areas, we investigated the extent to which the response properties of cells in the primary visual area (V1) of the marmoset change as a function of eccentricity. Responses to combinations of the spatial and temporal frequencies of visual stimuli were quantified for neurons with receptive fields ranging from 3° to 70° eccentricity. Optimal spatial frequencies and stimulus speeds reflected the expectation that the responses of cells throughout V1 are essentially uniform, once scaled according to the cortical magnification factor. In addition, temporal frequency tuning was similar throughout V1. However, spatial frequency tuning curves depended both on the cell’s optimal spatial frequency and on the receptive field eccentricity: cells with peripheral receptive fields showed narrower bandwidths than cells with central receptive fields that were sensitive to the same optimal spatial frequency. Although most V1 cells had separable spatial and temporal frequency tuning, the proportion of neurons displaying significant spatiotemporal interactions increased in the representation of far peripheral vision (> 50°). In addition, of the fewer than 5% of V1 cells that showed robust (spatial frequency independent) selectivity to stimulus speed, most were concentrated in the representation of the far periphery. Spatiotemporal interactions in the responses of many cells in the peripheral representation of V1 reduced the ambiguity of responses to high‐speed (> 30°/s) signals. These results support the notion of a relative specialization for motion processing in the far peripheral representations of cortical areas, including V1.     

The cortical connections of area V6: an occipito-parietal network processing visual information

The aim of this work was to study the cortical connections of area V6 by injecting neuronal tracers into different retinotopic representations of this area. To this purpose, we first functionally recognized V6 by recording from neurons of the parieto-occipital cortex in awake macaque monkeys. Penetrations with recording syringes were performed in the behaving animals in order to inject tracers exactly at the recording sites. The tracers were injected into the central or peripheral field representation of V6 in different hemispheres. Irrespective of whether injections were made in the centre or periphery, area V6 showed reciprocal connections with areas V1, V2, V3, V3A, V4T, the middle temporal area /V5 (MT/V5), the medial superior temporal area (MST), the medial intraparietal area (MIP), the ventral intraparietal area (VIP), the ventral part of the lateral intraparietal area and the ventral part of area V6A (V6AV). No labelled cells or terminals were found in the inferior temporal, mesial and frontal cortices. The connections of V6 with V1, and with all the retinotopically organized prestriate areas, were organized retinotopically. The connection of V6 with MIP suggests a visuotopic organization for this latter. Labelling in V6A and VIP after either central or peripheral V6 injections was very similar in location and extent, as expected on the basis of the nonretinotopic organization of these areas. We suggest that V6 plays a pivotal role in the dorsal visual stream, by distributing the visual information coming from the occipital lobe to the sensorimotor areas of the parietal cortex. Given the functional characteristics of the cells of this network, we suggest that it could perform the fast form and motion analyses needed for the visual guiding of arm movements as well as their coordination with the eyes and the head.     

Visual topography of area TEO in the macaque.

Previous studies have mapped the visuotopic organization of visual areas from V1 through V4 in the occipital cortex and of area TE in the temporal cortex, but the cortex in between, at the occipito-temporal junction, has remained relatively unexplored. To determine the visuotopic organization of this region, receptive fields were mapped at 1,200 visually responsive sites on 370 penetrations in the ventral occipital and temporal cortex of five macaques. We identified a new visual area, roughly corresponding to cytoarchitectonic area TEO, located between the ventral portion of V4 and area TE. Receptive fields in TEO are intermediate in size between those in V4 and TE and have a coarse visuotopic organization. Collectively, receptive fields in TEO appear to cover nearly the entire contralateral visual field. The foveal and parafoveal representation of TEO is located laterally on the convexity of the inferior temporal gyrus, and the peripheral field is represented medially on the ventral surface of the hemisphere, within and medial to the occipitotemporal sulcus. Beyond the medial border of TEO, within cyteoarchitectonic area TF, is another visually responsive region, which we have termed VTF; this region may also have some crude visual topography. Bands of constant eccentricity in TEO appear to be continuous with those in V2, V3v, and V4. The upper field representation in TEO is located adjacent to that in ventral V4, with a representation of the horizontal meridian forming the boundary between the two areas. The lower field representation in TEO is located just anterior to the upper field but is smaller. In contrast to the orderly representation of eccentricity in TEO, we found little consistent representation of polar angle, other than the separation of upper and lower fields. The results of injecting anatomical tracers in two animals suggest that TEO is an important link in the pathway that relays visual information from V1 to the inferior temporal cortex. TEO is thus likely to play an important role in pattern perception.     

Differences in spatial and temporal frequency interactions between central and peripheral parts of the feline area 18

The visual system demonstrates significant differences in information processing abilities between the central and peripheral parts of the visual field. Optical imaging based on intrinsic signals was used to investigate the difference in stimulus spatial and temporal frequency interactions related to receptive field eccentricity in the cat area 18. Changing either the spatial or the temporal frequency of grating stimuli had a significant impact on responses in the cortical areas corresponding to the centre of the visual field and more peripheral parts at 10 degrees eccentricity. The cortical region corresponding to the centre of the gaze was tuned to 0.4 cycles per degree (c/deg) for spatial frequency and 2 Hz for temporal frequency. In contrast, the cortical region corresponding to the periphery of the visual field was tuned to a lower spatial frequency of 0.15 c/deg and a higher temporal frequency of 4 Hz. Interestingly, when we simultaneously changed both the spatial frequency and the temporal frequency of the grating stimuli, the responses were significantly different from those estimated with an assumption of independence between the spatial and temporal frequency in the cortical region corresponding to the periphery of the visual field. However, in the cortical area corresponding to the centre of the gaze, spatial frequency showed significant independence from temporal frequency. These properties support the notion of relative specialization of visual information processing for peripheral representations in cortical areas.     

The middle temporal visual area in the macaque: Myeloarchitecture,connections, functional properties and topographic organization

The location, topographic organization, and function of the middle temporal visual area (MT) in the macaque monkey was studied using anatomical and physiological techniques. MT is a small, elliptically shaped area on the posterior bank of the superior temporal sulcus which can be identified by its direct inputs from striate cortex and by its distinctive pattern of heavy myelination. Its average surface area is 33 mm², which is less than 3% of the size of striate cortex. It contains a complete, topographically organized representation of the contralateral visual hemifield. There are substantial irregularities in the detailed pattern of topographic organization, however, and the representation is significantly more complex than that found for MT in other primates. Much of MT is devoted to the representation of central visual fields, with the emphasis on central vision being similar to that found in striate cortex. Electrophysiological recordings have confirmed previous reports of a high incidence of direction selective cells in MT. The transition in functional properties, from cells lacking direction selectivity outside MT to direction selective cells within, occurs over a distance of 0.1–0.2 mm or less along the lateral border of MT. Such a transition does not occur along the medial border, however, as the cortex medial to MT contains many cells with strong direction selectivity. Nevertheless, this region differs from MT in its myeloarchitecture, its lack of inputs from striate cortex, and the large size of its receptive fields. These results demonstrate the existence of three distinct visual areas on the posterior bank of the superior temporal sulcus which can be distinguished on the basis of both physiological and anatomical criteria.     

Differential dependency on motion coherence in subregions of the human MT+ complex

The detection of coherent motion embedded in noise has been widely used as a measure of global visual motion processing. Animal studies have demonstrated that this performance is closely linked to the responses of direction-sensitive neurons in the macaque middle temporal (MT) and medial superior temporal (MST) areas. Despite the strong similarities between the visual cortex of human and that of non-human primates, the human middle temporal complex (area MT+), located in the posterior part of the inferior temporal sulcus and presumably comprising both area MT and area MST, has not consistently been found to share the functional hallmark of MT and MST neurons, i.e. their preference for coherent rather than incoherent visual motion. In order to search for such preferences in human area MT+, blood oxygen level-dependent responses to random dot kinematograms presented in the right visual hemifield were studied here as a function of stimulus size and dot density. The stimulus extensions were varied in such a way as to cover an area either equaling, exceeding or falling below the mean receptive field size of macaque area MT. Unlike the posterior part of human area MT+, the anterior part and its right-hemisphere homolog showed significantly stronger responses to coherent than to incoherent motion. These differences were only present for large stimuli that presumably exceeded the receptive field size of neurons in area MT. Our results suggest that functional magnetic resonance imaging may reveal stronger responses to coherent visual motion in human area MST, provided that the stimulus allows for sufficient summation within the receptive fields. In contrast, functional magnetic resonance imaging may fail to reveal the same dependency for human area MT.     

Topographic organisation of extrastriate areas in the flying fox: implications for the evolution of mammalian visual cortex.

The organisation of extrastriate cortex was studied in anaesthetised flying foxes (Pteropus poliocephalus) by using multiunit recording techniques. Based on the visuotopic organisation and response characteristics, the cortex immediately rostral to the second visual area (V2) was subdivided into two fields: visual area 3 (V3) laterally and the occipitoparietal area (OP) medially. Area V3 is a 1.0-1.5 mm wide strip of cortex that represents the entire contralateral hemifield as a mirror image of the representation found in V2. The representation of the vertical meridian and the area centralis form the rostral border of V3. In area OP, receptive fields are much larger than those of V3 and form a separate visuotopic map, with the upper quadrant represented rostral to the lower quadrant. Multiunit clusters in the cortex rostral to area OP (posterior parietal area) respond to both visual and somatosensory stimuli. Farther laterally, in the cortex rostral to V3, the occipitotemporal area (OT) was found to form yet another map of the visual field. Similar to the middle temporal area in primates, area OT in the flying fox forms a first-order representation of the visual field, with the lower quadrant represented medially, the upper quadrant represented laterally, the area centralis represented caudally, and the visual field periphery represented rostrally. The cortex surrounding area OT rostrally and ventrally is also visually responsive but could not be subdivided due to the large receptive fields. Finally, visual responses were elicited from an area adjacent to the peripheral representation in the first visual area (V1) in the splenial sulcus. These results demonstrate that nearly half of the flying fox cortex is related to vision, which contrasts with that of microchiropteran bats, in which auditory areas predominate. A comparison of the flying fox with other mammals suggests that several areas, including homologues of V1, V2, V3, OT, and the splenial area, may have originated early in mammalian evolution and have been inherited by most present-day eutherians. However, studies in other species will be needed to distinguish patterns of common ancestry from parallel evolution.     

Topographic patterns of V2 cortical connections in macaque monkeys

Patterns of connections of dorsal and ventral portions of the second visual area (V2) were used to evaluate and extend current theories of cortical organization and processing streams in macaque monkeys. Injections of wheat germ agglutinin-horseradish peroxidase (WGA-HRP) and up to four different fluorochromes in V2 labeled neurons and terminations in V2 and in 1) caudal (DLc) and rostral (DLr) subdivisions of dorsolateral cortex between V2 and the middle temporal area (MT); 2) regions we define as dorsomedial (DM) and dorsointermediate (DI) areas; 3) MT, medial superior temporal area (MST), and fundal superior temporal area (FST); 4) the dorsal part of inferior temporal (TEO) cortex; and 5) two locations in posterior parietal cortex. The largest extrastriate connection zone was DLc, which occupied the caudal one-third to one-half of the fourth visual area (V4) region of other proposals. Based on the connection pattern, foveal vision in DLc is represented adjacent to foveal vision in V2, with the lower quadrant represented dorsally and the upper quadrant ventrally, as in V2, but within a much less extensive region of cortex. The sparser connections of DLr formed a more compressed but parallel visuotopic pattern. A third visuotopic pattern of connections was located in a moderately myelinated region of cortex just rostral to dorsomedial V2. Whereas the region would include parts of dorsal visual area 3 (V3), V3a, and possibly other areas of other proposals, we interpret the connection pattern as reflecting a dorsomedial visual area, DM, with foveal vision represented caudolaterally and other parts of the lower and upper quadrants represented more medially and rostrally. A fourth pattern of label in dorsointermediate cortex suggested the location and organization of another visual area (DI). Most of a fifth connection pattern with MT was congruent with the known visuotopic organization of MT area, but visuotopically mismatched foci of connections were observed as well. Sparser foci of label in MST suggested a rostrodorsal representation of foveal vision, with paracentral vision represented more caudally. Separate dorsal and ventral foci of label in FST were consistent with previous evidence for dorsal (FSTd) and ventral (FSTv) visual areas. Finally, connections with TEO and posterior parietal cortex were sparse. Our results suggest that much of visual cortex organization is similar in New and Old World monkeys. © 1996 Wiley-Liss, Inc.