Third tier ventral extrastriate cortex in the New World monkey, Cebus apella

The ventral extrastriate cortex adjacent to the second visual area was studied in the New World monkey Cebus apella, using anaesthetised preparations. The visuotopic organisation and myeloarchitecture of this region demonstrate the existence of a distinct strip of cortex, 3-4 mm wide, with an ordered representation of the contralateral upper visual quadrant, up to 60 degrees eccentricity. This upper-quadrant representation is probably homologous to the ventral subdivision of the third visual complex (V3v) of Old World monkeys, also known as the ventral posterior area. The representation of the horizontal meridian in V3v forms its posterior and medial border with V2, while the upper vertical meridian is represented anterior and laterally, forming a congruent border with the fourth visual area (V4). Central visual fields are represented in posterior and lateral portions of V3v, in the inferior occipital sulcus, while the periphery of the visual field is represented anteriorly, on the tentorial surface. Cortex anterior to V3v, at the ventral occipitotemporal transition, had neurones that had poor visual responses. No representation of the lower quadrant was found adjacent to V3v in ventral cortex. However, we observed cells with perifoveal receptive fields centred in the lower quadrant immediately dorsal to V3v, around the junction of the inferior occipital and lunate sulci. These observations argue against the idea that V3v is an area restricted to the ventral cortex in New World monkeys and support the conclusions of previous anatomical studies in Cebus that showed a continuity of myeloarchitecture and connectional patterns between ventral and lateral extrastriate cortices. Together, these data suggest that V3v may be part of a larger area that extends into dorsolateral extrastriate cortex, overlapping to some extent with the caudal subdivision of the dorsolateral area described in other New World monkeys.     

Remapping in human visual cortex

With each eye movement, stationary objects in the world change position on the retina, yet we perceive the world as stable. Spatial updating, or remapping, is one neural mechanism by which the brain compensates for shifts in the retinal image caused by voluntary eye movements. Remapping of a visual representation is believed to arise from a widespread neural circuit including parietal and frontal cortex. The current experiment tests the hypothesis that extrastriate visual areas in human cortex have access to remapped spatial information. We tested this hypothesis using functional magnetic resonance imaging (fMRI). We first identified the borders of several occipital lobe visual areas using standard retinotopic techniques. We then tested subjects while they performed a single-step saccade task analogous to the task used in neurophysiological studies in monkeys, and two conditions that control for visual and motor effects. We analyzed the fMRI time series data with a nonlinear, fully Bayesian hierarchical statistical model. We identified remapping as activity in the single-step task that could not be attributed to purely visual or oculomotor effects. The strength of remapping was roughly monotonic with position in the visual hierarchy: remapped responses were largest in areas V3A and hV4 and smallest in V1 and V2. These results demonstrate that updated visual representations are present in cortical areas that are directly linked to visual perception.     

Projection patterns of surviving neurons in the dorsal lateral geniculate nucleus following discrete lesions of striate cortex: implications for residual vision

Summary In four monkeys with long-standing partial ablation of the striate cortex pellets of horseradish peroxidase were placed in either the striate cortex immediately adjacent to the ablation, or in the extrastriate cortex of the ventral prelunate gyrus, i.e. in visual area V4. We examined the dorsal lateral geniculate nucleus to see whether surviving neurons, within the region that shows retrograde degeneration as a result of the cortical lesion, project to remaining striate cortex and/or to extrastriate cortex. Neurons labelled from extrastriate cortex were found throughout the degenerated region, whereas neurons labelled from striate cortex were confined to the border between the normal and degenerated region of the nucleus. This shows that isolated neurons found within the degenerated region survive striate cortex damage because they project to an extrastriate visual area, and not because their terminals depart from the otherwise strict topographic representation of the lateral geniculate nucleus on to striate cortex.     

Microsaccades differentially modulate neural activity in the striate and extrastriate visual cortex

 Saccadic eye movements in primates continually shift the location at which a given stimulus strikes the retina. Even during periods of steady fixation, microsaccades frequently jerk the center of gaze by small but resolvable distances, yet perception remains stable and continuous, uninterrupted by sudden jumps or shifts. The effect of such fixational eye movements on the activity of single neurons was examined in several regions of the visual cortex in macaque monkeys. We found that the firing of many neurons in striate and extrastriate cortex is profoundly influenced by saccades much smaller than the neurons’ receptive fields. In striate cortex (V1) many cells showed a transient decrease in their firing shortly following a saccade. In sharp contrast, cells in the extrastriate areas V2 and V4 showed strong excitatory responses that closely coincided in time with the striate depression. No appreciable activity change was observed in the inferotemporal cortex (IT) following saccades. This activity pattern is consistent with the notion that topographic extrastriate areas receive extraretinal input associated with saccadic events. Such signals may be necessary for the stable perception of objects and scenes during eye movements, mediating the mapping between central object representations and the constantly changing retinotopic input. Received: 25 May 1998 / Accepted: 3 August 1998     

Feedback of visual object information to foveal retinotopic cortex

The mammalian visual system contains an extensive web of feedback connections projecting from higher cortical areas to lower areas, including primary visual cortex. Although multiple theories have been proposed, the role of these connections in perceptual processing is not understood. We found that the pattern of functional magnetic resonance imaging response in human foveal retinotopic cortex contained information about objects presented in the periphery, far away from the fovea, which has not been predicted by prior theories of feedback. This information was position invariant, correlated with perceptual discrimination accuracy and was found only in foveal, but not peripheral, retinotopic cortex. Our data cannot be explained by differential eye movements, activation from the fixation cross, or spillover activation from peripheral retinotopic cortex or from lateral occipital complex. Instead, our findings indicate that position-invariant object information from higher cortical areas is fed back to foveal retinotopic cortex, enhancing task performance.     

Perceptual continuity and the emergence of perceptual persistence in the ventral visual pathway

Perceptual continuity is an important aspect of our experience of the visual world. In this study, we focus on an example of perceptual continuity involving the maintenance of figure-ground segregation despite the removal of binding cues that initiated the segregation. Fragmented line drawings of objects were superimposed on a background of randomly oriented lines. Global forms could be discriminated from the background based on differences in motion or differences in color/brightness. Furthermore, perception of a global form persisted after the binding cue had been removed. A comparison between the persistence of forms constructed from motion or color demonstrated that both forms produced persistence after the object defining cues were removed. Functional imaging showed a gradual increase in the persistence of brain activity in the lower visual areas (V1, V2, VP), which reached significance in V4v and peaked in the lateral occipital area. There was no difference in the location of persistence for color- or motion-defined forms. These results suggest that the retention of a global percept is an emerging property of the ventral visual processing stream and the maintenance of grouped visual elements is independent of cue type. We postulated that perceptual persistence depends on a system of perceptual memory reflecting the state of perceptual organization.     

Functional degradation of extrastriate visual cortex in senescent rhesus monkeys

The receptive field properties of striate cortical (V1) cells degrade in senescent macaque monkeys. We have now carried out extracellular single unit studies of the receptive field properties of cells in extrastriate visual cortex (area V2) in very old rhesus (Macaca mulatta) monkeys. This study provides evidence that both the orientation and direction selectivities of V2 cells in old monkeys degrade significantly. Decreased selectivity is accompanied by increased visually driven and spontaneous responses. As a result, V2 cells in old animals exhibit markedly decreased signal-to-noise ratios. A significant degradation of neural function in extrastriate cortex may underlie the declines in higher order visual function that accompany normal aging.     

Rapid and precise retinotopic mapping of the visual cortex obtained by voltage-sensitive dye imaging in the behaving monkey

Retinotopy is a fundamental organizing principle of the visual cortex. Over the years, a variety of techniques have been used to examine it. None of these techniques, however, provides a way to rapidly characterize retinotopy, at the submillimeter range, in alert, behaving subjects. Voltage-sensitive dye imaging (VSDI) can be used to monitor neuronal population activity at high spatial and temporal resolutions. Here we present a VSDI protocol for rapid and precise retinotopic mapping in the behaving monkey. Two monkeys performed a fixation task while thin visual stimuli swept periodically at a high speed in one of two possible directions through a small region of visual space. Because visual space is represented systematically across the cortical surface, each moving stimulus produced a traveling wave of activity in the cortex that could be precisely measured with VSDI. The time at which the peak of the traveling wave reached each location in the cortex linked this location with its retinotopic representation. We obtained detailed retinotopic maps from a region of about 1 cm(2) over the dorsal portion of areas V1 and V2. Retinotopy obtained during <4 min of imaging had a spatial precision of 0.11-0.19 mm, was consistent across experiments, and reliably predicted the locations of the response to small localized stimuli. The ability to rapidly obtain precise retinotopic maps in behaving monkeys opens the door for detailed analysis of the relationship between spatiotemporal dynamics of population responses in the visual cortex and perceptually guided behavior.     

Large-scale remapping of visual cortex is absent in adult humans with macular degeneration

The occipital lobe contains retinotopic representations of the visual field. The representation of the central retina in early visual areas (V1-3) is found at the occipital pole. When the central retina is lesioned in both eyes by macular degeneration, this region of visual cortex at the occipital pole is accordingly deprived of input. However, even when such lesions occur in adulthood, some visually driven activity in and around the occipital pole can be observed. It has been suggested that this activity is a result of remapping of this area so that it now responds to inputs from intact, peripheral retina. We evaluated whether or not remapping of visual cortex underlies this activity. Our functional magnetic resonance imaging results provide no evidence of remapping, questioning the contemporary view that early visual areas of the adult human brain have the capacity to reorganize extensively.     

Combined activation and deactivation of visual cortex during tactile sensory processing

The involvement of occipital cortex in sensory processing is not restricted solely to the visual modality. Tactile processing has been shown to modulate higher-order visual and multisensory integration areas in sighted as well as visually deprived subjects; however, the extent of involvement of early visual cortical areas remains unclear. To investigate this issue, we employed functional magnetic resonance imaging in normally sighted, briefly blindfolded subjects with well-defined visuotopic borders as they tactually explored and rated raised-dot patterns. Tactile task performance resulted in significant activation in primary visual cortex (V1) and deactivation of extrastriate cortical regions V2, V3, V3A, and hV4 with greater deactivation in dorsal subregions and higher visual areas. These results suggest that tactile processing affects occipital cortex via two distinct pathways: a suppressive top-down pathway descending through the visual cortical hierarchy and an excitatory pathway arising from outside the visual cortical hierarchy that drives area V1 directly.     

Retinotopy and color sensitivity in human visual cortical area V8

Prior studies suggest the presence of a color-selective area in the inferior occipital-temporal region of human visual cortex. It has been proposed that this human area is homologous to macaque area V4, which is arguably color selective, but this has never been tested directly. To test this model, we compared the location of the human color-selective region to the retinotopic area boundaries in the same subjects, using functional magnetic resonance imaging (fMRI), cortical flattening and retinotopic mapping techniques. The human color-selective region did not match the location of area V4 (neither its dorsal nor ventral subdivisions), as extrapolated from macaque maps. Instead this region coincides with a new retinotopic area that we call 'V8', which includes a distinct representation of the fovea and both upper and lower visual fields. We also tested the response to stimuli that produce color afterimages and found that these stimuli, like real colors, caused preferential activation of V8 but not V4.     

Cytoarchitectonical analysis and probabilistic mapping of two extrastriate areas of the human posterior fusiform gyrus

The human extrastriate visual cortex comprises numerous functionally defined areas, which are not identified in the widely used cytoarchitectonical map of Brodmann. The ventral part of the extrastriate cortex is particularly devoted to the identification of visual objects, faces and word forms. We analyzed the region immediately antero-lateral to hOc4v in serially sectioned (20 μm) and cell body-stained human brains using a quantitative observer-independent cytoarchitectonical approach to further identify the anatomical organization of the extrastriate cortex. Two novel cytoarchitectonical areas, FG1 and FG2, were identified on the posterior fusiform gyrus. The results of ten postmortem brains were then registered to their MRI volumes (acquired before histological processing), 3D reconstructed, and spatially normalized to the Montreal Neurological Institute reference brain. Finally, probabilistic maps were generated for each cytoarchitectonical area by superimposing the areas of the individual brains in the reference space. Comparison with recent functional imaging studies yielded that both areas are located within the object-related visual cortex. FG1 fills the gap between the retinotopically mapped area VO-1 and a posterior fusiform face patch. FG2 is probably the correlate of this face patch.     

The importance of seeing it coming: a functional magnetic resonance imaging study of motion-in-depth towards the human observer

Despite their crucial biological relevance, the neural structures differentially activated by the detection of optic flow towards the observer remain to be elucidated. Here, we deploy functional magnetic resonance imaging with normal volunteers to locate the areas differentially activated when motion towards the observer is detected. Motion towards the observer, compared with motion away, showed significant activations (P<0.05, corrected for multiple comparisons), as assessed using statistical parametric mapping, in the lateral inferior occipital cortex bilaterally and in right lateral superior occipital cortex. The areas implicated do not extend into area V5 or subdivisions thereof.Our data suggest that the representations of motion towards the observer implicate perceptual and attentional mechanisms acting at early stages of visual processing in extrastriate cortex. From the standpoint of efficient biological engineering, it makes sense that such crucially important functions as object motion towards the observer would be computed in early visual processing areas. Further studies will be required to determine the extent to which the effects we observed in lateral occipital cortex reflect differential attention to different types of motion, as contrasted with the derivation of explicit representations of motion towards the observer.     

Two hierarchically organized neural systems for object information in human visual cortex

The primate visual system is broadly organized into two segregated processing pathways, a ventral stream for object vision and a dorsal stream for space vision. Here, evidence from functional brain imaging in humans demonstrates that object representations are not confined to the ventral pathway, but can also be found in several areas along the dorsal pathway. In both streams, areas at intermediate processing stages in extrastriate cortex (V4, V3A, MT and V7) showed object-selective but viewpoint- and size-specific responses. In contrast, higher-order areas in lateral occipital and posterior parietal cortex (LOC, IPS1 and IPS2) responded selectively to objects independent of image transformations. Contrary to the two-pathways hypothesis, our findings indicate that basic object information related to shape, size and viewpoint may be represented similarly in two parallel and hierarchically organized neural systems in the ventral and dorsal visual pathways.     

Relating retinotopic and object-selective responses in human lateral occipital cortex

What is the relationship between retinotopy and object selectivity in human lateral occipital (LO) cortex? We used functional magnetic resonance imaging (fMRI) to examine sensitivity to retinal position and category in LO, an object-selective region positioned posterior to MT along the lateral cortical surface. Six subjects participated in phase-encoded retinotopic mapping experiments as well as block-design experiments in which objects from six different categories were presented at six distinct positions in the visual field. We found substantial position modulation in LO using standard nonobject retinotopic mapping stimuli; this modulation extended beyond the boundaries of visual field maps LO-1 and LO-2. Further, LO showed a pronounced lower visual field bias: more LO voxels represented the lower contralateral visual field, and the mean LO response was higher to objects presented below fixation than above fixation. However, eccentricity effects produced by retinotopic mapping stimuli and objects differed. Whereas LO voxels preferred a range of eccentricities lying mostly outside the fovea in the retinotopic mapping experiment, LO responses were strongest to foveally presented objects. Finally, we found a stronger effect of position than category on both the mean LO response, as well as the distributed response across voxels. Overall these results demonstrate that retinal position exhibits strong effects on neural response in LO and indicates that these position effects may be explained by retinotopic organization.     

Responses of primate visual cortical neurons to stimuli presented by flash,saccade, blink,and external darkening

Our visual experience constitutes an unending chain of transient events, including those caused by saccadic eye movements, by blinks, and by localized or global changes in the external world. The categorical perception of objects is maintained across different classes of transient events, suggesting that the neural circuitry underlying visual perception responds to different transient events in a similar manner. However, different sorts of transients do have different perceptual impacts: for example, the sudden changes in a scene due to a saccade or a blink do not disturb our perceptual continuity of a visual scene as much as an external change does. We recorded the responses of 103 single visual cortical neurons in two rhesus monkeys (V1: n = 38, V2: n = 19, V3V/VP: n = 30, V4V: n = 16) to the onset and offset of a visual stimulus that was elicited by four different conditions: 1) stimulus flashed on and off while the eyes remain fixed; 2) stimulus turned on and off along with the entire scene (external darkening); 3) stimulus constant, onset and offset induced by rapid saccadic eye movements; and 4) offset induced by an eyeblink. For most neurons the onset and offset of a visual stimulus elicited qualitatively similar responses regardless of condition. We found no systematic effect of different conditions across the neuronal population. Previously we have shown that when the visual scene is occluded by a blink V1 neuronal firing declines in a similar manner as when the external scene is darkened and the eyes left open. Here we show that this is also the case in V2, V3V/VP, and V4V. However, for a substantial minority of neurons, the response varied strongly as a function of the transient event. This overall pattern was the same in all four cortical areas studied here. We hypothesize that most neurons in visual cortex constitute a passive "filter bank", analyzing the scene for specific details regardless of condition. However, there are neurons that respond in a qualitatively different manner depending on how a stimulus is presented, and we hypothesize that these signals may be important for determining the perceptual salience of a visual event.     

A comparison of magnification functions in area 19 and the lateral suprasylvian visual area in the cat

A retinotopic map can be described by a magnification function that relates magnification factor to visual field eccentricity. Magnification factor for primary visual cortex (VI) in both the cat and the macaque monkey is directly proportional to retinal ganglion cell density. However, among those extrastriate areas for which a magnification function has been described, this is often not the case. Deviations from the pattern established in V1 are of considerable interest because they may provide insight into an extrastriate area's role in visual processing. The present study explored the magnification function for the lateral suprasylvian area (LS) in the cat. Because of its complex retinotopic organization, magnification was calculated indirectly using the known magnification function for area 19. Small tracer injections were made in area 17, and the extent of anterograde label in LS and in area 19 was measured. Using the ratio of cortical area labeled in LS to that in area 19, and the known magnification factor for area 19 at the corresponding retinotopic location, we were able to calculate magnification factor for LS. We found that the magnification function for LS differed substantially from that for area 19: central visual field was expanded, and peripheral field compressed in LS compared with area 19. Additionally, we found that the lower vertical meridian's representation was compressed relative to that of the horizontal meridian. We also examined receptive field size in areas 17, 19, and LS and found that, for all three areas, receptive field size was inversely proportional to magnification factor.     

Early extrastriate activity without primary visual cortex in humans

Damage to the primary visual cortex (V1) destroys the major source of anatomical input to extrastriate cortical areas (V2, V3, V4 and V5) and produces cortical blindness--an absence of any sensation of light and colour--in the visual field contralateral to the side of the lesion. Neuroimaging studies, nevertheless, have recently demonstrated dorsal and ventral extrastriate activation for stationary stimuli presented to the blind visual field in the absence of V1 activity in human subjects. To clarify the moment in time that visual information reaches extrastriate areas, by means of event-related potentials (ERPs) we tracked the temporal course of responses to complex visual stimuli (faces) presented in the blind field of a hemianopic patient. Stimulation of the normal visual field elicited a positive occipital deflection (P1) at 140 ms. A P1 response was also observed with stimulation of the blind field, although slightly delayed (20 ms) and reduced. Its topography and timing demonstrate that early neural activity for stationary stimuli takes place within extrastriate regions despite V1 denervation.     

The role of human extra-striate visual areas V5/MT and V2/V3 in the perception of the direction of global motion: a transcranial magnetic stimulation study

Several published single case studies reveal a double dissociation between the effects of brain damage in separate extra-striate cortical visual areas on the perception of global visual motion defined by a difference in luminance (first-order motion) versus motion defined by a difference in contrast (second-order motion). In particular, the medial extrastriate cortical region V2/V3 seems to be crucial for the perception of first-order motion, but not for second-order, whereas a lateral and more anterior portion of the cortex close to the temporo–parieto–occipital junction (in the territory of the human motion area hV5/MT⁺) seems to be essential only for the perception of second-order motion. In order to test the hypothesis of a functional specialization of different visual areas for different types of motion, we applied repetitive transcranial magnetic stimulation (rTMS) unilaterally over areas V2/V3, V5/MT, or posterior parietal cortex (PPC) while subjects performed a 2AFC task with first- or second-order global motion displays in the contralateral visual field. Results showed a comparable disruption of the two types of motion, with both rTMS over V2/V3 or over MT/V5, and little or no effect with rTMS over PPC. The results suggest that either the previous psychophysical results with neurological patients are incorrect (highly unlikely) or that the lateral and medial regions are directly connected (as they are in macaque monkeys) such that stimulating one automatically affects the other, in this instance disruptively     

Interhemispheric transfer of visual motion information after a posterior callosal lesion: a neuropsychological and fMRI study

Interhemispheric transfer of visual information was investigated behaviourally and with functional magnetic resonance imaging (fMRI) 6 months after a lesion of the posterior two-thirds of the corpus callosum. On tachistoscopical left hemifield presentation, the patient was severely impaired in reading letters, words and geographical names and moderately impaired in naming pictures and colours. In contrast, interhemispheric transfer of visual motion information, tested by verbal report of the direction of short sequences of coherent dot motion presented within the left hemifield, was preserved. The pattern of cerebral activation elicited by apparent motion stimuli was studied with fMRI and compared to that of normal subjects. In normal subjects, apparent motion stimuli, as compared to darkness, activated strongly striate and extrastriate cortex. When presented to one hemifield only, the contralateral calcarine region was activated while regions on the occipital convexity, including putative area V5, were activated bilaterally. A similar activation pattern was found in the patient with a posterior callosal lesion; unilateral left or right hemifield stimulation was accompanied by activation in the contralateral and ipsilateral occipital convexity. Ipsilateral hemifield representation in the extrastriate visual cortex is believed to depend on callosal input. Our observation suggests that this is not the case for visual motion representation and that other, probably parallel, pathways may mediate visual motion transfer after posterior callosotomy.