Characterization of the human visual V6 complex by functional magnetic resonance imaging

Magnetoencephalography of a visual area along the human parieto-occipital sulcus suggested that this region represents the human homologue of the monkey visual area V6 complex (visual area V6/visuomotor area V6A) involved in the integration of visual and somatomotor information. We used functional magnetic resonance imaging at 2.0 T and 2 x 2 x 3 mm3 resolution (16 sections) to characterize visual areas along the parieto-occipital sulcus in five healthy human subjects. Paradigms comprised a full-field checkerboard stimulation, a full-field luminance flicker as well as a foveal and peripheral luminance flicker using both a direct and differential design for comparing functional states. Along the parieto-occipital sulcus, and in contrast to primary visual areas, luminance stimulation evoked much larger activation volumes than checkerboard stimulation. Moreover, based on anatomic landmarks, luminance stimulation identified two functionally distinct regions of parieto-occipital sulcus activations: an inferior part (supposedly visual area V6) and a superior portion (supposedly visuomotor area V6A). With these assignments, foveal vs. peripheral luminance stimulation revealed a weaker foveal overrepresentation in visual area V6/visuomotor area V6A than in early visual areas, and only a mild tendency for a retinotopic organization in visual area V6. Further analyses of the functional coding of the human visual area V6 complex require functional magnetic resonance imaging at even higher spatial resolution.     

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.     

Retinotopic mapping of the peripheral visual field to human visual cortex by functional magnetic resonance imaging

Retinotopic mapping is a key property of organization in the human occipital cortex. The retinotopic organization of the central visual field of visual areas V1, V2, and V3 has been well established. We used fMRI to measure the retinotopic map of the peripheral visual field (eccentricity up to 60°). We estimated the sizes of the visual areas between 0° and 60° and obtained results consistent with anatomical studies. We also estimated the cortical distances and magnification factors for reconstruction of the retinotopic map using the peripheral wedge dipole model. By comparing the retinotopic map with the flattened surface, we analyzed the datasets used to reconstruct the map. We found that: (1) the percentage of the striate cortex devoted to peripheral vision in humans is significantly larger than that in the macaque, (2) the estimate of the scaling factor in linear magnification is larger than that found in previous studies focusing on central vision, and (3) the estimate of the peripheral factor in the dipolar model is too large to make the curve direction of the dipolar map in the periphery equivalent to that in the center. On the basis of our results, we revised the dipolar map to fit our conditions. The revised map in humans has a similar elliptical shape to that of macaques, and the central parts of the two species are the same. The different parts of the map are the peripheral regions, for which the peripheral wedge dipole model in humans is reversed compared to that of macaques.     

Identification and viuotopic organization of areas PO and POd in Cebus monkey

Two visual areas of the anterior bank of the parietooccipital sulcus, areas PO and POd, were identified and their visual field representations were studied in six anesthetized and paralyzed Cebus monkeys. The definition of these areas was based on electrophysiological mapping and myeloarchitecture. PO is located in the ventral aspect of the anterior bank of the parietooccipital sulcus and ventral precuneate gyrus. It borders area V2 posteriorly and ventrally in the depth of the parietooccipital sulcus, area V3d laterally, and another undescribed visual area medially. POd was located dorsal to area PO and ventral to architectonic area PE. The representations of the visual field in areas PO and POd are complex. In each hemisphere, these areas have a virtually complete representation of the contralateral visual hemifield. Different from the previously described visual areas, in PO and POd there is a precise organization of isopolar lines and a complex organization of the isoeccentric ones. In PO, as well as in POd, the representation of the horizontal meridian runs dorsoventrally along the parietooccipital sulcus. The upper visual quadrant is represented medially and the lower visual quadrant laterally. A large and complex representation of the periphery, from 20° to 60° eccentricity is present at the lateral and medial portions of these areas. By contrast, the representation of the central 20° is very small in both PO and POd. The central visual field is represented ventrally in PO and dorsally in area POd. Area POd shows a more stratified myeloarchitectonic pattern than PO and both areas can be distinguished from other surrounding areas by their heavier myelinated pattern. © Wiley-Liss, Inc.     

The fidelity of the cortical retinotopic map in human amblyopia

To delineate the fidelity of the functional cortical organization in humans with amblyopia, we undertook an investigation into how spatial information is mapped across the visual cortex in amblyopic observers. We assessed whether the boundaries of the visual areas controlled by the amblyopic and fellow fixing eye are in the same position, the fidelity of the retinotopic map within different cortical areas and the average receptive field size in different visual areas. The functional organization of the visual cortex was reconstructed using a fMRI phase-encoded retinotopic mapping analysis. This method sequentially stimulates each point in the visual field along the axes of a polar-coordinate system, thereby reconstructing the representation of the visual field on the cortex. We found that the cortical areas were very similar in normals and amblyopes, with only small differences in boundary positions of different visual areas between fixing and fellow amblyopic eye activation. Within these corresponding visual areas, we did find anomalies in retinotopy in some but not all amblyopes that were not simply a consequence of the poorer functional responses and affected central and peripheral field regions. Only a small increase in the average (or collective) receptive field size was found for full-field representation in amblyopes and none at all for central field representation. The former may simply be a consequence of the poorer functional responses.     

Retinotopic effects during spatial audio-visual integration

The successful integration of visual and auditory stimuli requires information about whether visual and auditory signals originate from corresponding places in the external world. Here we report crossmodal effects of spatially congruent and incongruent audio-visual (AV) stimulation. Visual and auditory stimuli were presented from one of four horizontal locations in external space. Seven healthy human subjects had to assess the spatial fit of a visual stimulus (i.e. a gray-scaled picture of a cartoon dog) and a simultaneously presented auditory stimulus (i.e. a barking sound). Functional magnetic resonance imaging (fMRI) revealed two distinct networks of cortical regions that processed preferentially either spatially congruent or spatially incongruent AV stimuli. Whereas earlier visual areas responded preferentially to incongruent AV stimulation, higher visual areas of the temporal and parietal cortex (left inferior temporal gyrus [ITG], right posterior superior temporal gyrus/sulcus [pSTG/STS], left intra-parietal sulcus [IPS]) and frontal regions (left pre-central gyrus [PreCG], left dorsolateral pre-frontal cortex [DLPFC]) responded preferentially to congruent AV stimulation. A position-resolved analysis revealed three robust cortical representations for each of the four visual stimulus locations in retinotopic visual regions corresponding to the representation of the horizontal meridian in area V1 and at the dorsal and ventral borders between areas V2 and V3. While these regions of interest (ROIs) did not show any significant effect of spatial congruency, we found subregions within ROIs in the right hemisphere that showed an incongruency effect (i.e. an increased fMRI signal during spatially incongruent compared to congruent AV stimulation). We interpret this finding as a correlate of spatially distributed recurrent feedback during mismatch processing: whenever a spatial mismatch is detected in multisensory regions (such as the IPS), processing resources are re-directed to low-level visual areas.     

Functional organization of human visual cortex in occipital polymicrogyria

Polymicrogyrias (PMG) are cortical malformations resulting from developmental abnormalities. In animal models PMG has been associated with abnormal anatomy, function, and organization. The purpose of this study was to describe the function and organization of human polymicrogyric cortex using functional magnetic resonance imaging. Three patients with epilepsy and bilateral parasagittal occipital polymicrogyri were studied. They all had normal vision as tested by Humphrey visual field perimetry. The functional organization of the visual cortex was reconstructed using phase-encoded retinotopic mapping analysis. This method sequentially stimulates each point in the visual field along the axes of a polar-coordinate system, thereby reconstructing the representation of the visual field on the cortex. We found normal cortical responses and organization of early visual areas (V1, V2, and V3/VP). The locations of these visual areas overlapped substantially with the PMG. In five out of six hemispheres the reconstructed primary visual cortex completely fell within polymicrogyric areas. Our results suggest that human polymicrogyric cortex is not only organized in a normal fashion, but is also actively involved in processing of visual information and contributes to normal visual perception.     

Projection of rods and cones within human visual cortex

There are two basic types of photoreceptors in the retina: rods and cones. Using a single stimulus viewed at two different light levels, we tested whether input from rods and input from cones are topographically segregated at subsequent levels of human visual cortex. Here we show that rod-mediated visual input produces robust activation in area MT+, and in the peripheral representations of multiple retinotopic areas. However, such activation was selectively absent in: (1) a cortical area selectively activated by colored stimuli (V8) and (2) the foveal representations of lower tier retinotopic areas. These cortical differences reflect corresponding differences in perception between scotopic and photopic conditions.     

The role of the parietal lobe in visual extinction studied with transcranial magnetic stimulation

Interhemispheric competition between homologous areas in the human brain is believed to be involved in a wide variety of human behaviors from motor activity to visual perception and particularly attention. For example, patients with lesions in the posterior parietal cortex are unable to selectively track objects in the contralesional side of visual space when targets are simultaneously present in the ipsilesional visual field, a form of visual extinction. Visual extinction may arise due to an imbalance in the normal interhemispheric competition. To directly assess the issue of reciprocal inhibition, we used fMRI to localize those brain regions active during attention-based visual tracking and then applied low-frequency repetitive transcranial magnetic stimulation over identified areas in the left and right intraparietal sulcus to asses the behavioral effects on visual tracking. We induced a severe impairment in visual tracking that was selective for conditions of simultaneous tracking in both visual fields. Our data show that the parietal lobe is essential for visual tracking and that the two hemispheres compete for attentional resources during tracking. Our results provide a neuronal basis for visual extinction in patients with parietal lobe damage.     

Scene-selective cortical regions in human and nonhuman primates

fMRI studies have revealed three scene-selective regions in human visual cortex [the parahippocampal place area (PPA), transverse occipital sulcus (TOS), and retrosplenial cortex (RSC)], which have been linked to higher-order functions such as navigation, scene perception/recognition, and contextual association. Here, we document corresponding (presumptively homologous) scene-selective regions in the awake macaque monkey, based on direct comparison to human maps, using identical stimuli and largely overlapping fMRI procedures. In humans, our results showed that the three scene-selective regions are centered near-but distinct from-the gyri/sulci for which they were originally named. In addition, all these regions are located within or adjacent to known retinotopic areas. Human RSC and PPA are located adjacent to the peripheral representation of primary and secondary visual cortex, respectively. Human TOS is located immediately anterior/ventral to retinotopic area V3A, within retinotopic regions LO-1, V3B, and/or V7. Mirroring the arrangement of human regions fusiform face area (FFA) and PPA (which are adjacent to each other in cortex), the presumptive monkey homolog of human PPA is located adjacent to the monkey homolog of human FFA, near the posterior superior temporal sulcus. Monkey TOS includes the region predicted from the human maps (macaque V4d), extending into retinotopically defined V3A. A possible monkey homolog of human RSC lies in the medial bank, near peripheral V1. Overall, our findings suggest a homologous neural architecture for scene-selective regions in visual cortex of humans and nonhuman primates, analogous to the face-selective regions demonstrated earlier in these two species.     

Topographic organization of the projections of the retina to the pretectal region in the rat.

The pattern of projection of the retina to the pretectal region and its retinotopic organization were investigated in the rat by autoradiographic and silver impregnation techniques for axonal pathways. The endings of retinal axons form three terminal fields in the pretectum in: 1, olivary pretectal nucleus (PO), bilaterally; 2, posterior pretectal nucleus (PP), bilaterally; and 3, nucleus of the optic tract (NTO), contralaterally. The following retinotopic pattern was observed in rats surviving peripheral retinal lesions and injections of 3H-proline in the same eye, when the positions occupied by terminal degeneration in Fink-Heimer stained sections were matched with the corresponding areas deficient in radiolabel in adjacent autoradiographic sections showing the surviving parts of the terminal fields. The nasal periphery of the retina maps along the adjoining edges of PO and PP, both of which extend obliquely, in a posterolateral direction, through the entire extent of the pretectum. Both nuclei map the line of representation of the anterior midline (in the temporal retina) along their opposite edges (anterolaterally, in PO; posteromedially, in PP). This mirror-image symmetry is completed by the representation of the ventral peripheral retina separately in the rostral poles and the dorsal peripheral retina separately in the caudal poles of both nuclei. The map in NTO is vertically oriented, with the temporal retina, dorsally, the nasal retina, ventrally, the ventral retina, rostrally, and the dorsal retina caudally represented. The binocular area of the terminal field in PO is subdivided by a terminal-free zone into two parts that may process separately events in the central and lateral visual field.     

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.     

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)     

Widespread distribution of visual responsiveness in frontal, prefrontal, and prelimbic cortical areas of the cat: an electrophysiologic investigation

By using multiple-unit recording techniques, we explored the visual responsiveness of regions of cortex in and around the area described by others as the cat's "frontal eye fields" (Schlag J, Schlag-Rey M [1970] Brain Res 22:1-13; Guitton D, Mandl G [1978] Brain Res 149:295-312; Pigarev IN [1984] Neirofiziologiia 16:761-766). Our exploration included most of the cat's motor areas (subdivisions of areas 4 and 6) as well as prefrontal and prelimbic regions. Visual responses were routinely obtained from portions of each of the areas we explored, including prefrontal and prelimbic cortex. The qualitative characteristics of visual responses appeared to vary with cytoarchitectonic area. With few exceptions, receptive fields in these areas were large (most exceeding 2,500 deg2) and included the area centralis. Such large fields and inclusion of central vision at nearly all sites precluded retinotopic organization and prevented delineating distinct visual field representations. The most reliable and robust visual activity was observed on the ventral bank of the cruciate sulcus in area 6aalpha. The regions reported to correspond to the "frontal eye fields" did not exhibit any unique visual properties that distinguished them from surrounding areas. The widespread distribution of visually driven activity we observed is consistent with the known pattern of both cortical and subcortical inputs to this broad region of cortex. The observation of visually responsive activity across broad regions of cortex that is nominally motor is consistent with recent studies involving awake animals.     

Location of human face‐selective cortex with respect to retinotopic areas

Functional Magnetic Resonance Imaging (fMRI) was used to identify a small area in the human posterior fusiform gyrus that responds selectively to faces (PF). In the same subjects, phase‐encoded rotating and expanding checkerboards were used with fMRI to identify the retinotopic visual areas V1, V2, V3, V3A, VP and V4v. PF was found to lie anterior to area V4v, with a small gap present between them. Further recordings in some of the same subjects used moving low‐contrast rings to identify the visual motion area MT. PF was found to lie ventral to MT. In addition, preliminary evidence was found using fMRI for a small area that responded to inanimate objects but not to faces in the collateral sulcus medial to PF. The retinotopic visual areas and MT responded equally to faces, control randomized stimuli, and objects. Weakly face‐selective responses were also found in ventrolateral occipitotemporal cortex anterior to V4v, as well as in the middle temporal gyrus anterior to MT. We conclude that the fusiform face area in humans lies in non‐retinotopic visual association cortex of the ventral form‐processing stream, in an area that may be roughly homologous in location to area TF or CITv in monkeys. Hum. Brain Mapping 7:29–37, 1999. © 1999 Wiley‐Liss, Inc.     

Retinotopic mapping in cat visual cortex using high-field functional magnetic resonance imaging

In the field of neuroscience, there has always been a need for imaging techniques that provide high-resolution, large field-of-view measurements of neural activity. Functional MRI has this capability, but the link between the blood oxygenation level dependent (BOLD) functional magnetic resonance imaging (fMRI) signal and neural activity is indirect. High magnetic field strengths (>3 T) improve the strength and specificity of the BOLD signal, but there are additional concerns about imaging artifacts at high field. We have tested the capabilities of ultra high field fMRI in the anesthetized juvenile cat, demonstrating rapid, non-invasive retinotopic mapping of early visual areas. Maps of topographic organization and measured cortical magnification factors are in good agreement with electrophysiological studies. Measurement precision was estimated at 1 mm. This mapping, performed with an MRI scanner at ultra high field (9.4 T), demonstrates the capabilities of high-resolution functional mapping of the visual system at ultra high field.     

The retinotopic organization of the posterior suprasylvian area of the cerebral cortex in the cat

Posterior suprasylvian area (PSA) is one of the extrastriate visual structures of the cat cortex. Representation of the visual field in the PSA has been investigated by the mapping method. Results of experiments revealed that receptive fields (RF) of the PSA neurons were located mostly in the upper contralateral quadrant of the visual field. About 10% of RF were located in the upper ipsilateral quadrant of the visual field. In the upper PSA (21a, 21b) area centralis is mainly represented including the space of the radius of 20-30 degrees of the visual field. In the lower PSA (20a, 20b) more peripheral part of the visual field was represented. The experiments did not confirm essential differences in the retinotopic organization between areas 20a and 20b, 21a and 21b. Proceeding from the presented experiments the suggestion is put forward that PSA consists of two main areas (21 and 20) without dividing into subareas.     

Retinotopic organization of areas 18 and 19 in the cat.

The location and retinotopic organization of areas 18 and 19 in cat cortex were determined using electrophysiological mapping techniques. These two areas each contain a single representation of the visual hemifield and each has a distinctive cytoarchitecture. The visual hemifield representations in these two areas are nearly mirror images of each other. Compared to area 17, areas 18 and 19 have less cortical surface area, have a lower cortical magnification factor, contain less of the visual field and contain second order instead of first order transformations of the visual hemifield. An unusual asymmetry was found between the representations of the upper and lower visual quadrants not seen before in maps of other areas of cat or other species. A considerable amount of variability in the retinotopic organization of these two areas was found among cats.     

The search for the neural mechanisms of the set size effect

The set size effect in visual search refers to the linear increase in response time (RT) or decrease in accuracy as the number of distractors increases. Previous human and monkey studies have reported a correlation between set size and neural activity in the frontal eye field (FEF) and intraparietal sulcus (IPS). In a recent functional magnetic resonance imaging study, we did not observe a set size effect in the superior precentral sulcus (sPCS, thought to be the human homolog of the FEF) and IPS in an oculomotor visual search task (Ikkai et al., 2011). Our task used placeholders in the search array, along with the target and distractors, in order to equate the amount of retinal stimulation for each set size. We here attempted to reconcile these differences with the results from a follow-up experiment in which the same oculomotor visual search task was used, but without placeholders. A strong behavioral set size effect was observed in both studies, with very similar saccadic RTs and slopes between RT and set size. However, a set size effect was now observed in the sPCS and IPS. We comment on this finding and discuss the role of these neural areas in visual search.