Ventral visual cortex in humans: cytoarchitectonic mapping of two extrastriate areas

The extrastriate visual cortex forms a complex system enabling the analysis of visually presented objects. To gain deeper insight into the anatomical basis of this system, we cytoarchitectonically mapped the ventral occipital cortex lateral to BA 18/V2 in 10 human postmortem brains. The anatomical characterization of this part of the ventral stream was performed by examination of cell-body-stained histological sections using quantitative cytoarchitectonic analysis. First, the gray level index (GLI) was measured in the ventral occipital lobe. Cytoarchitectonic borders, i.e., significant changes in the cortical lamination pattern, were then identified using an observer-independent algorithm based on multivariate analysis of GLI profiles. Two distinct cytoarchitectonic areas (hOC3v, hOC4v) were characterized in the ventral extrastriate cortex lateral to BA 18/V2. Area hOC3v was found in the collateral sulcus. hOC4v was located in this sulcus and also covered the fusiform gyrus in more occipital sections. Topographically, these areas thus seem to represent the anatomical substrates of functionally defined areas, VP/V3v and V4/V4v. Following histological analysis, the delineated cytoarchitectonic areas were transferred to 3D reconstructions of the respective postmortem brains, which in turn were spatially normalized to the Montreal Neurological Institute reference space. A probabilistic map was generated for each area which describes how many brains had a representation of this area in a particular voxel. These maps can now be used to identify the anatomical correlates of functional activations observed in neuroimaging experiments to enable a more informed investigation into the many open questions regarding the organization of the human visual cortex.     

Pattern of extrastriate visual areas connecting reciprocally with striate cortex in the mouse

Several areas reciprocally connected to striate cortex were found in the extrastriate cortex of the mouse after small single injections of horseradish peroxidase into the striate cortex. By showing that the arrangement of these labeled extrastriate areas resembles closely the physiologic and anatomic subdivision of the extrastriate cortex reported previously in several rodent species, this study supports the hypothesis that there exists a common pattern of visual cortical organization in rodents.     

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.     

Reciprocal connections between the striate cortex and extrastriate cortical visual areas in the rat

Following injections of horseradish peroxidase (HRP) in the striate cortex of rats, a precise topographical correspondence between extrastriate cortical fields of anterograde and retrograde label was observed. The arrangement of these extrastriate labeled fields corresponds closely to the previously reported division of the peristriate cortex into multiple visual areas, suggesting that each of these areas is reciprocally connected to striate cortex. Cortical layers II–VI participate in this reciprocal connection.     

Topographic organization of human visual areas in the absence of input from primary cortex.

Recently, there has been evidence for considerable plasticity in primary sensory areas of adult cortex. In this study, we asked to what extent topographical maps in human extrastriate areas reorganize after damage to a portion of primary visual (striate) cortex, V1. Functional magnetic resonance imaging signals were measured in a subject (G.Y.) with a large calcarine lesion that includes most of primary visual cortex but spares the foveal representation. When foveal stimulation was present, intact cortex in the lesioned occipital lobe exhibited conventional retinotopic organization. Several visual areas could be identified (V1, V2, V3, V3 accessory, and V4 ventral). However, when stimuli were restricted to the blind portion of the visual field, responses were found primarily in dorsal extrastriate areas. Furthermore, cortex that had formerly shown normal topography now represented only the visual field around the lower vertical meridian. Several possible sources for this reorganized activity are considered, including transcallosal connections, direct subcortical projections to extrastriate cortex, and residual inputs from V1 near the margin of the lesion. A scheme is described to explain how the reorganized signals could occur based on changes in the local neural connections.     

Cortical connections of areas V3 and VP of macaque monkey extrastriate visual cortex

The cortical connections of visual area 3 (V3) and the ventral posterior area (VP) in the macaque monkey were studied by using combinations of retrograde and anterograde tracers. Tracer injections were made into V3 or VP following electrophysiological recording in and near the target area. The pattern of ipsilateral cortical connections was analyzed in relation to the pattern of interhemispheric connections identified after transection of the corpus callosum. Both V3 and VP have major connections with areas V2, V3A, posterior intraparietal area (PIP), V4, middle temporal area (MT), medial superior temporal area (dorsal) (MSTd), and ventral intraparietal area (VIP). Their connections differ in several respects. Specifically, V3 has connections with areas V1 and V4 transitional area (V4t) that are absent for VP; VP has connections with areas ventral occipitotemporal area (VOT), dorsal prelunate area (DP), and visually responsive portion of temporal visual area F (VTF) that are absent or occur only rarely for V3. The laminar pattern of labeled terminals and retrogradely labeled cell bodies allowed assessment of the hierarchical relationships between areas V3 and VP and their various targets. Areas V1 and V2 are at a lower hierarchical level than V3 and VP; all of the remaining areas are at a higher level. V3 receives major inputs from layer 4B of V1, suggesting an association with the magnocellular-dominated processing stream and a role in routing magnocellular-dominated information along pathways leading to both parietal and temporal lobes. The convergence and divergence of pathways involving V3 and VP underscores the distributed nature of hierarchical processing in the visual system. J. Comp. Neurol. 379:21-47, 1997. © 1997 Wiley-Liss, Inc.     

Interindividual and interspecies variations of the extrastriate visual cortex

Functional homology between human and macaque visual cortices has provided an important cue to functional subdivisions of the human visual cortex, but it is unclear beyond V1. We estimated the sizes and the visual field eccentricity functions of the extrastriate visual areas of human brains using MRI and fMRI measurements to analyze the interindividual and interspecies variations. We found distinctive features of the area fraction values relative to V1 and the visual field eccentricity functions beyond V2 between the human and the macaque visual cortices. This suggests that selection on color-form and stereoscopic vision, associated with processing and manipulating socio-visual stimuli, may generate variations of the architecture of the extrastriate visual cortex beyond V2.     

Corticostriatal connections of extrastriate visual areas in rhesus monkeys

The striatal connections of extrastriate visual areas were examined by the autoradiographic technique in rhesus monkeys. The medial as well as the dorsolateral extrastriate regions project preferentially to dorsal and lateral portions of the head and of the body of the caudate nucleus, as well as to the caudodorsal sector of the putamen. The rostral portion of the annectant gyrus has connections to the caudal sector of the body and to the genu, whereas projections from the caudal portion of the lower bank of the superior temporal sulcus are directed to dorsal and central sectors of the head and the body, to the genu and the tail, as well as to the caudal putamen. The ventrolateral extrastriate region is related mainly to the ventral sector of the body, to the genu and the tail, and to the caudal putamen. In contrast, the striatal projections of the ventromedial extrastriate cortex resemble those of the medial and dorsolateral regions. The caudal inferotemporal cortex is related strongly to the tail of the caudate nucleus and to the ventral putamen. The differential corticostriatal connectivity of the various extrastriate regions may contribute to the specific functional roles of these cortices. Thus, the connections from the dorsomedial, dorsolateral, and ventromedial areas to dorsal portions of the caudate nucleus and of the putamen may serve a visuospatial function. In contrast, the connections from the ventrolateral extrastriate and inferotemporal regions to the tail of the caudate nucleus and to the ventral putamen may have a role in visual object-related processes. © 1995 Wiley-Liss, Inc.     

Corticothalamic connections of extrastriate visual areas in rhesus monkeys

Corticothalamic connections of extrastriate visual areas were studied by using the autoradiographic anterograde tracing technique. The results show that the medial extrastriate region above the calcarine sulcus projects mainly to the lateral pulvinar (PL), medial pulvinar (PM), and lateral posterior (LP) nuclei. In addition, the dorsal portion of the medial region has connections to the lateral dorsal (LD) as well as to intralaminar nuclei. The dorsolateral extrastriate region projects strongly to the PL and LP nuclei, to the PM and inferior pulvinar (PI) nuclei, and to the LD and intralaminar nuclei. The lateral extrastriate region above the inferior occipital sulcus (IOS) has strong connections to both the PL and PI nuclei and has minor projections to the PM and oral pulvinar nuclei. The ventrolateral extrastriate region below the IOS projects mainly to the PI nucleus and to the caudal portion of the PL nucleus and has some projections to the PM nucleus. The ventromedial extrastriate region medial to the occipitotemporal sulcus has strong connections with the ventral and medial sectors of the PI nucleus. This region also projects to the caudal portion of the PL nucleus and has minor connections to the LP nucleus. Finally, the annectant gyrus projects to the PL nucleus and to the rostral portion of the PI nucleus and has minor connections to the PM nucleus. Thus, the medial and dorsolateral extrastriate regions are related mainly to the PL and LP nuclei as well as to intralaminar nuclei. In contrast, the ventrolateral and ventromedial regions are connected strongly with the PI nucleus. This connectional organization appears to reflect functional differentiation at the cortical level. J. Comp. Neurol. 378:562–585, 1997. © 1997 Wiley-Liss, Inc.     

Heterogeneity of extrastriate visual areas and multiple parietal areas in the macaque monkey

The definition of visual areas remains a key problem in the effort to elucidate cortical functions. Visual areas vary along a number of dimensions and are increasingly difficult to define according to traditional criteria at higher levels of the hierarchy. Three recently discovered areas in monkey parietal association cortex illustrate a new approach to this problem. Their definition depends on assessment of neuronal response properties in the alert, behaving animal combined with precise reconstruction of recording sites. This approach permits recognition of functionally distinct areas in the absence of retinotopic maps.     

Some properties of extrastriate visual units in the cortex of the rabbit

Receptive fields and trigger properties of 306 units in the visual cortex of the rabbit have been examined in detail. Reconstruction of the electrode tracks revealed that 276 of these recordings were made from cells located in the striate cortex, whilst the remaining 30 were found to lie in cortex lateral to the striate field. These latter units have been termed ‘extrastriate’. Five penetrations involved both striate and extrastriate units enabling a direct comparison of their properties to be made.The most outstanding feature of the extrastriate units was their huge receptive field sizes (up to80° × 130°) and high rates of spontaneous activity (usually between 10 and 20 imp./sec). None of these cells responded well to stationary stimuli and most preferred moving targets. Responses could be elicited regardless of the nature of stimulus-to-background contrast and were constant over a wide range of stimulus sizes. No cells were found which were orientation selective.Approximately half the extrastriate units were direction selective, the majority preferring anterior movement in the visual field. Movement in the counter-preferred direction generally resulted in suppression of the spontaneous discharge.In contrast to this the receptive fields of cells in the striate cortex were small, and were often sensitive to features such as stimulus size, orientation, and contrast, in addition to movement and direction of movement.The similarity between one class of extrastriate unit, and units recently observed in the pretectum of the rabbit is pointed out.     

Retinotopic organization of striate and extrastriate visual cortex in the hooded rat

The visuotopic organization of the primary visual cortex (area 17) and the extrastriate visual regions surrounding it (areas 18a and 18) has been studied in gray rats using standard microelectrode mapping techniques. The results confirm and extend previous observations in the rat. Apart from the representation of the contralateral visual field (VF) in area 17, in which the upper VF is represented caudally and the nasal VF laterally, there are additional representations of the VF in the extrastriate cortex. In lateral extrastriate cortex (area 18a) there are at least 4 such representations, namely lateromedial (LM), anterolateral (AL), laterointermediate (LI) and laterolateral (LL). In LM (second visual area) the upper VF is represented caudally and the nasal VF medially, being thus a mirror image of V1. In AL (third visual area) the upper VF is represented rostrally and the nasal VF, medially, being thus a mirror image of LM. In LI, the upper VF is medial and the nasal VF, lateral, being thus a mirror image of LM, or a reduced copy of V1. In medial extrastriate cortex (area 18) there are two representations of the temporal VF, labeled anteromedial (AM) and posteromedial (PM). In AM, the upper temporal VF is medial and the lower temporal VF, lateral, the extreme temporal field being rostral. The 30° azimuth provides the boundary between AM and PM. Thus, AM is organized as a counter-clockwise rotation by 90° of the V1 representation. In PM, the upper lower VF topography is like in AM, but the extreme temporal VF is caudal, being thus a mirror image of AM.     

Cortical connections of striate and extrastriate visual areas in tree shrews

The ipsilateral and contralateral cortical connections of visual cortex of tree shrews (Tupaia belangeri)were investigated by placing restricted injections of fluorochrome tracers, wheat germ agglutinin-horseradish peroxidase, or biotinylated dextran amine into area 17 (V1), area 18 (V2), or the adjoining temporal dorsal area (TD). As previously reported, V1 was characterized by a widespread, patchy pattern of intrinsic connections; ipsilateral connections with V2, TD, and to a lesser extent, other areas of the temporal cortex; and contralateral connections with V1, V2, and TD. A surface-view of the myelin pattern in V1 revealed a patchwork of light and dark module-like regions. The ipsilateral connections with V2 and TD were roughly topographic, whereas heterotopic locations in V1 were callosally connected. Injections in V2 labeled as much as one third of V2 in a patchy pattern, and portions of ipsilateral V1 and TD in roughly topographic patterns. In addition, connections with several other visual areas in the temporal lobe were revealed. Contralaterally, most of the label was in V2, with some in V1 and TD. Injections in TD demonstrated connections within the region, and with adjoining portions of the temporal cortex, V2, and V1. There were sparse connections with an oval of densely myelinated cortex, which we have termed the temporal inferior area (TI). Callosal connections were concentrated in TD, but also included V2. The results provide further evidence for modular organizations within V1 and V2, and reveal for the first time the complete patterns of cortical connections of V2 and TD. The results are consistent with the proposal that at least three visual areas, the temporal anterior area, TA, the temporal dorsal area, TD, and the temporal posterior area, TP, exist along the rostrolateral border of V2 in tree shrews; suggest visual involvement of at least three other areas, the temporal inferior area, TI, the temporal anterior lateral area, and the temporal posterior inferior area located more ventrally in the temporal cortex; and fortify the conclusion that TD is the likely homologue of the middle temporal visual area of primates. Because tree shrews are considered close relatives of primates, the evidence for several visual areas along the border of V2 is more compatible with theories that propose a series of visual areas along V2 in primates, rather than a single visual area, V3. J. Comp. Neurol. 401:109–128, 1998. © 1998 Wiley-Liss, Inc.     

Direct intracranial recording of body-selective responses in human extrastriate visual cortex

We recorded intracranial local field potentials (iLFPs) in right extrastriate visual cortex of a patient prior to surgery for epilepsy. Visual evoked potentials revealed a highly selective response to images of bodies, relative to faces, mammals, and tools, which was restricted to a focal region in the lateral occipitotemporal cortex that corresponds to the location of the extrastriate body area (EBA). Body-selective activity started around 190 ms and peaked 260 ms post-stimulus onset. These findings provide the first direct electrophysiological evidence for an early visual processing stage in human lateral occipitotemporal cortex that is specialized for processing human body shapes.     

Evaluation of inputs to rat primary auditory cortex from the suprageniculate nucleus and extrastriate visual cortex

Evidence indicates that visual stimuli influence cells in the primary auditory cortex. To evaluate potential sources of this visual input and how they enter into the circuitry of the auditory cortex, we examined axonal terminations in the primary auditory cortex from nonprimary extrastriate visual cortex (V2M, V2L) and from the multimodal thalamic suprageniculate nucleus (SG). Gross biocytin/biotinylated dextran amine (BDA) injections into the SG or extrastriate cortex labeled inputs terminating primarily in superficial and deep layers. SG projects primarily to layers I, V, and VI while V2M and V2L project primarily to layers I and VI, with V2L also targeting layers II/III. Layer I inputs differ in that SG terminals are concentrated superficially, V2L are deeper, and V2M are equally distributed throughout. Individual axonal reconstructions document that single axons can 1) innervate multiple layers; 2) run considerable distances in layer I; and 3) run preferentially in the dorsoventral direction similar to isofrequency axes. At the electron microscopic level, SG and V2M terminals 1) are the same size regardless of layer; 2) are non‐γ‐aminobutyric acid (GABA)ergic; 3) are smaller than ventral medial geniculate terminals synapsing in layer IV; 4) make asymmetric synapses onto dendrites/spines that 5) are non‐GABAergic and 6) are slightly larger in layer I. Thus, both areas provide a substantial feedback‐like input with differences that may indicate potentially different roles. J. Comp. Neurol. 518:3679–3700, 2010. © 2010 Wiley‐Liss, Inc.     

Five topographically organized fields in the somatosensory cortex of the flying fox: microelectrode maps, myeloarchitecture, and cortical modules.

Five somatosensory fields were defined in the grey-headed flying fox by using microelectrode mapping procedures. These fields are: the primary somatosensory area, SI or area 3b; a field caudal to area 3b, area 1/2; the second somatosensory area, SII; the parietal ventral area, PV; and the ventral somatosensory area, VS. A large number of closely spaced electrode penetrations recording multiunit activity revealed that each of these fields had a complete somatotopic representation. Microelectrode maps of somatosensory fields were related to architecture in cortex that had been flattened, cut parallel to the cortical surface, and stained for myelin. Receptive field size and some neural properties of individual fields were directly compared. Area 3b was the largest field identified and its topography was similar to that described in many other mammals. Neurons in 3b were highly responsive to cutaneous stimulation of peripheral body parts and had relatively small receptive fields. The myeloarchitecture revealed patches of dense myelination surrounded by thin zones of lightly myelinated cortex. Microelectrode recordings showed that myelin-dense and sparse zones in 3b were related to neurons that responded consistently or habituated to repetitive stimulation respectively. In cortex caudal to 3b, and protruding into 3b, a complete representation of the body surface adjacent to much of the caudal boundary of 3b was defined. Neurons in this area habituated rapidly to repetitive stimulation. We termed this caudal field area 1/2 because it had properties of both area 1 and area 2 of primates. In cortex caudolateral to 3b and lateral to area 1/2 (cortex traditionally defined as SII) we describe three separate representations of the body surface coextensive with distinct myeloarchitectonic appearances. The second somatosensory area, SII, shared a congruent border with 3b at the representation of the nose. In SII, the overall orientation of the body representation was erect. The lips were represented rostrolaterally, the digits were represented laterally, and the toes were caudolateral to the digits. The trunk was represented caudally and the head was represented medially. A second complete representation, PV, had an inverted body representation with respect to SII and bordered SII at the representation of the distal limbs. The proximal body parts were represented rostrolaterally in PV. Finally, caudal to both SII and PV, an additional representation, VS, shared a congruent border with the distal hindlimb representation of both SII and PV. VS had a crude topography, and receptive fields of neurons in VS were relatively large. Many neurons in VS responded to both somatosensory and auditory stimulation.     

Processing of color, form and disparity information in visual areas VP and V2 of ventral extrastriate cortex in the macaque monkey

The responses of single cells to light bars of different orientation, direction of motion, speed, binocular disparity, and wavelength were systematically analyzed in areas V2 and VP of ventral extrastriate visual cortex in the macaque monkey. Selectivity for each of these parameters was assessed quantitatively using computer-controlled procedures. In both VP and V2 (both representing the superior contralateral quadrant), more than half of the cells studied were selective for stimulus color and more than half for stimulus orientation. In contrast, only a small minority of the VP and V2 cells were selective for the direction of stimulus motion. Comparison with reports of single-unit properties in dorsal extrastriate cortex suggests there are no major differences in the incidence of orientation, direction, and color selectivity between ventral and dorsal subdivisions of V2. Between V3 and VP, though, there are marked differences: Color-selective cells are much less common in V3 than VP, whereas direction-selective cells are more common in V3. This dorsoventral difference in the distribution of neuronal response properties suggests a significant asymmetry in the way visual information is processed in upper and lower parts of the visual field. The properties of cells in VP suggest that it plays an important role in both form and color vision, similar to that attributed to area V4.