Areas PMLS and 21 a of Cat Visual Cortex: Two Functionally Distinct Areas

We have compared the receptive field properties of neurons recordedfrom visuotopically corresponding regions of area 21a and theposteromedial lateral suprasylvian area (PMLS) of cat visualcortex. In both areas, the great majority of neurons were orientation-selectiveand binocular, and their responses to moving contours were modulatedby simultaneous in-phase or anti-phase motion of large texturedbackground stimuli (‘visual noise’). However, despitethe great hodological similarity between the two areas, PMLSneurons had on average significantly higher peak discharge rates,exhibited substantially greater direction selectivity indices,and preferred substantially higher stimulus velocities thanarea 21a neurons. Furthermore, the majority of binocular neuronsin the PMLS area and in area 21a were dominated respectivelyby the contralateral and the ipsilateral eyes. Finally, while46% of PMLS neurons were excited by movement of visual noiseper Se. only 25% of area 21 a neurons could be excited by suchstimuli. We argue that the PMLS area, like its presumed primatehomologue the middle-temporal (MT) area, is mainly involvedin motion analysis. By contrast, area 21a appears to be involvedin pattern analysis rather than motion analysis. It is likelythat phylogenetically area 21a derives from the PMLS area.     

Cortical area MSTd combines visual cues to represent 3-D self-movement

As arboreal primates move through the jungle, they are immersed in visual motion that they must distinguish from the movement of predators and prey. We recorded dorsal medial superior temporal (MSTd) cortical neuronal responses to visual motion stimuli simulating self-movement and object motion. MSTd neurons encode the heading of simulated self-movement in three-dimensional (3-D) space. 3-D heading responses can be evoked either by the large patterns of visual motion in optic flow or by the visual object motion seen when an observer passes an earth-fixed landmark. Responses to naturalistically combined optic flow and object motion depend on their relative directions: an object moving as part of the optic flow field has little effect on neuronal responses. In contrast, an object moving separately from the optic flow field has large effects, decreasing the amplitude of the population response and shifting the population's heading estimate to match the direction of object motion as the object moves toward central vision. These effects parallel those seen in human heading perception with minimal effects of objects moving with the optic flow and substantial effects of objects violating the optic flow. We conclude that MSTd can contribute to navigation by supporting 3-D heading estimation, potentially switching from optic flow to object cues when a moving object passes in front of the observer.     

Natural vision reveals regional specialization to local motion and to contrast-invariant, global flow in the human brain

Visual changes in feature movies, like in real-live, can be partitioned into global flow due to self/camera motion, local/differential flow due to object motion, and residuals, for example, due to illumination changes. We correlated these measures with brain responses of human volunteers viewing movies in an fMRI scanner. Early visual areas responded only to residual changes, thus lacking responses to equally large motion-induced changes, consistent with predictive coding. Motion activated V5+ (MT+), V3A, medial posterior parietal cortex (mPPC) and, weakly, lateral occipital cortex (LOC). V5+ responded to local/differential motion and depended on visual contrast, whereas mPPC responded to global flow spanning the whole visual field and was contrast independent. mPPC thus codes for flow compatible with unbiased heading estimation in natural scenes and for the comparison of visual flow with nonretinal, multimodal motion cues in it or downstream. mPPC was functionally connected to anterior portions of V5+, whereas laterally neighboring putative homologue of lateral intraparietal area (LIP) connected with frontal eye fields. Our results demonstrate a progression of selectivity from local and contrast-dependent motion processing in V5+ toward global and contrast-independent motion processing in mPPC. The function, connectivity, and anatomical neighborhood of mPPC imply several parallels to monkey ventral intraparietal area (VIP).     

Neuronal responses to optic flow in the monkey parietal area PEc

Area PEc, a high order association area, is located in the dorsocaudal portion of the superior parietal cortex. PEc neurons encode visual motion signals, especially the direction of stimulus motion. The present study tested if PEc neurons also process visual correlates of self-motion. The extracellular activity of single neurons in response to optic flow stimuli was recorded in two monkeys (Macaca fascicularis) trained in a fixation task. The stimuli were produced by random dots simulating planar motion, radial expansion and radial contraction. A substantial number of PEc neurons were specifically activated by radial optic flow and were selective for the position of the focus of expansion with respect to the fovea. Eccentric positions of the focus of expansion were preferred. Almost all neurons showed opponent excitatory-inhibitory activity to expanding-contracting visual fields. Planar motion elicited very weak responses. Optic flow responsiveness is not entirely explained by classical bar sensitivity in PEc neurons, suggesting that optic flow and classical bar responses could serve different mechanisms in the integration of visuo-motor signals to prepare body movements.     

Feedforward construction of the receptive field and orientation selectivity of visual neurons in the pigeon

How the receptive field (RF) of visual cells is formed and how to explain the orientation selectivity have been intensely studied and debated. Here we provided direct electrophysiological evidence by single-unit recording and electrophysiological mapping that the elongated excitatory RF of a visual cell in the pigeon nucleus isthmi is constructed from aligned circular excitatory RFs of tectal cells, whereas its inhibitory RF originates from intranuclear inhibitory circuits. The orientation selectivity of an isthmic cell is mainly determined by its excitatory RF and sharply tuned by its inhibitory RF. Retrograde tracing showed that the tectal cells converging onto an isthmic cell are arranged in a narrow dorsoventral column in the tectum. According to the retinotopic map on the tectum, the excitatory RFs of these tectal cells are aligned in a line orthogonal to the horizontal meridian of the visual field in agreement with the result obtained by electrophysiological mapping.     

A neural model of motion processing and visual navigation by cortical area MST

Cells in the dorsal medial superior temporal cortex (MSTd) process optic flow generated by self-motion during visually guided navigation. A neural model shows how interactions between well-known neural mechanisms (log polar cortical magnification, Gaussian motion-sensitive receptive fields, spatial pooling of motion-sensitive signals and subtractive extraretinal eye movement signals) lead to emergent properties that quantitatively simulate neurophysiological data about MSTd cell properties and psychophysical data about human navigation. Model cells match MSTd neuron responses to optic flow stimuli placed in different parts of the visual field, including position invariance, tuning curves, preferred spiral directions, direction reversals, average response curves and preferred locations for stimulus motion centers. The model shows how the preferred motion direction of the most active MSTd cells can explain human judgments of self-motion direction (heading), without using complex heading templates. The model explains when extraretinal eye movement signals are needed for accurate heading perception, and when retinal input is sufficient, and how heading judgments depend on scene layouts and rotation rates.     

Cortical neuronal responses to optic flow are shaped by visual strategies for steering

We hypothesized that neuronal responses to virtual self-movement would be enhanced during steering tasks. We recorded the activity of medial superior temporal (MSTd) neurons in monkeys trained to steer a straight-ahead course, using optic flow. We found smaller optic flow responses during active steering than during the passive viewing of the same stimuli. Behavioral analysis showed that the monkeys had learned to steer using local motion cues. Retraining the monkeys to use the global pattern of optic flow reversed the effects of the active-steering task: active steering then evoked larger responses than passive viewing. We then compared the responses of neurons during active steering by local motion and by global patterns: Local motion trials promoted the use of local dot movement near the center of the stimulus by occluding the peripheral visual field midway through the trial. Global pattern trials promoted the use of radial pattern movement by occluding the central visual field midway through the trial. In this study, identical full-field optic-flow stimuli evoked larger responses in global-pattern trials than in local motion trials. We conclude that the selection of specific visual cues reflects strategies for active steering and alters MSTd neuronal responses to optic flow.     

Direction selectivity in the middle lateral and lateral (ML and L) visual areas in the California ground squirrel

Extracellular recordings obtained from the extrastriate cortex of the California ground squirrel, a diurnal sciurid, show that large receptive fields and a strong direction selectivity are present in the middle lateral area (ML) and the lateral area (L), located laterally to V2 and V3. Direction selectivity was tested by presenting stimuli of varying dimensions, shapes and speeds at different locations in the visual field. Most cells in ML and L (84%) were direction selective, with a preference for fast speeds, indicating that these areas share a role in motion processing. Areas ML and L may be homologous to area MT or may represent a case of homoplasia. A directional anisotropy for motion towards the vertical meridian was found in ML and L cells, suggesting that these areas may be involved in detecting predators and other moving objects coming from the periphery, rather than in processing flow fields caused by forward locomotion, for which a centrifugal bias might be expected.      

Anatomical evidence for classical and extra-classical receptive field completion across the discontinuous horizontal meridian representation of primate area V2

In primates, a split of the horizontal meridian (HM) representation at the V2 rostral border divides this area into dorsal (V2d) and ventral (V2v) halves (representing lower and upper visual quadrants, respectively), causing retinotopically neighboring loci across the HM to be distant within V2. How is perceptual continuity maintained across this discontinuous HM representation? Injections of neuroanatomical tracers in marmoset V2d demonstrated that cells near the V2d rostral border can maintain retinotopic continuity within their classical and extra-classical receptive field (RF), by making both local and long-range intra- and interareal connections with ventral cortex representing the upper visual quadrant. V2d neurons located <0.9-1.3 mm from the V2d rostral border, whose RFs presumably do not cross the HM, make nonretinotopic horizontal connections with V2v neurons in the supra- and infragranular layers. V2d neurons located <0.6-0.9 mm from the border, whose RFs presumably cross the HM, in addition make retinotopic local connections with V2v neurons in layer 4. V2d neurons also make interareal connections with upper visual field regions of extrastriate cortex, but not of MT or MTc outside the foveal representation. Labeled connections in ventral cortex appear to represent the "missing" portion of the connectional fields in V2d across the HM. We conclude that connections between dorsal and ventral cortex can create visual field continuity within a second-order discontinuous visual topography.     

Contribution of GABAergic inhibition to receptive field structures of monkey inferior temporal neurons.

Receptive field (RF) structures of neurons in area TE of the monkey inferior temporal cortex were investigated under blockade of inhibition mediated by gamma-aminobutyric acid (GABA). Bicuculline methiodide, a GABA(A) receptor antagonist, was microiontophoretically administered to TE neurons. Blockade of inhibition enhanced responses to a particular range of visual stimuli not only at the RF center, but also at the periphery of or outside RFs where the stimuli originally evoked little or no response, enlarging the RFs. The strongest responses under normal and uninhibited conditions occurred at the RF center in most neurons. The largest increase in responses, reflecting the strongest inhibitory input, usually occurred at the RF center, but in some neurons it occurred in the periphery. A neuron had a silent region within its RF where some stimuli effective at adjacent locations could not elicit responses even under blockade of inhibition. We suggest that (i) afferent information to individual TE neurons originates from a wide retinotopic region beyond their normal RF; (ii) the afferent convergence is not necessarily complete throughout a RF; and (iii) GABAergic inhibition contributes to the generation of RF structures of TE neurons.     

Impaired filtering of distracter stimuli by TE neurons following V4 and TEO lesions in macaques

Directing attention to a behaviorally relevant visual stimulus can overcome the distracting effects of other nearby stimuli. Correspondingly, physiological studies indicate that attention serves to filter distracting stimuli from receptive fields (RFs) in several extrastriate areas. Moreover, a recent study demonstrated that lesions of extrastriate areas V4 and TEO produce impairments in attentional filtering. A critical remaining question concerns why lesions of ventral stream areas cause attentional filtering impairments. To address this question, we tested the effects of restricted area V4 and TEO lesions on both behavioral performance and the responses of downstream neurons in area TE. The lesions impaired behavioral discrimination thresholds and altered neuronal selectivity for target stimuli in the presence of distracters. With attention to the target, but in the absence of V4 and/or TEO inputs, TE neurons responded as though attentional inputs could no longer be used to filter distracters from their RFs. This presumably occurred because top-down attentional signals were no longer able to filter distracters from the RFs of the cells that provide TE with major input. Consistent with this interpretation, increasing the spatial separation between targets and distracters, such that they no longer fell within a typical V4 RF dimension, restored both behavioral performance and neuronal selectivity in the portion of TE RFs affected by the V4 lesion.     

Behavioral influences on cortical neuronal responses to optic flow

Optic flow selectively activates neurons in medial superior temporal (MST) cortex. We find that many MST neurons yield larger and more selective responses when the optic flow guides a subsequent eye movement. Smaller, less selective responses are seen when optic flow is preceded by a flashed precue that guides eye movements. Selectivity can decrease by a third (32%) after a flashed precue is presented at a peripheral location as a small spot specifying the target location of the eye movement. Smaller decreases in selectivity (18%) occur when the precue is presented centrally with its shape specifying the target location. Shape precues presented centrally, but not linked to specific target locations, do not appear to alter optic flow selectivity. The effects of spatial precueing can be reversed so that the precue leads to larger and more selective optic flow responses: A flashed precue presented as a distracter before behaviorally relevant optic flow is associated with larger optic flow responses and a 45% increase in selectivity. Together, these findings show that spatial precues can decrease or increase the size and selectivity of optic flow responses depending on the associated behavioral contingencies.     

Dynamics of directional selectivity in area 18 and PMLS of the cat

Visual latencies and temporal dynamics of area 18 and PMLS direction-selective complex cells were defined with a reverse correlation method. The method allowed us to analyze the time course of responses to motion steps, without confounding temporal integration effects. Several measures of response latency and direction tuning dynamics were quantified: optimal latency (OL), latency of first and last significant responses (FSR, LSR), the increase and decrease of direction sensitivity in time, and the change of direction tuning in time. FSR, OL and LSR values for PMLS and area 18 largely overlapped. The small differences in mean latencies (3-4 ms for FSR and OL and 11.9 ms for the LSR) were not statistically significant. All cells in area 18 and the vast majority of cells in PMLS showed no systematic changes in preferred direction (monophasic neurons). In PMLS 5 out of 41 cells showed a reversal of preferred direction after approximately 56 ms relative to their OL (biphasic neurons). Monophasic cells showed no systematic changes in direction tuning width during the interval from FSR to LSR. In both areas, development of direction sensitivity was significantly faster than return to the non-direction sensitive state, but no significant difference was found between the two areas. We conclude that, for the monophasic type of direction-selective complex cells, the dynamics of primary motion processing are highly comparable for area 18 and PMLS. This suggests that motion information is predominantly processed in parallel, presumably based on input from the fast conducting thalamocortical Y-pathway.     

Simultaneous representation of saccade targets and visual onsets in monkey lateral intraparietal area

The monkey's lateral intraparietal area (LIP) has been associated with attention and saccades. LIP neurons have visual on-responses to objects abruptly appearing in their receptive fields (RFs) and sustained activity preceding saccades to the RF. We studied the relationship between the on-responses and delay activity in LIP using a 'stable-array' task. Monkeys viewed eight distinct, continuously illuminated objects, arranged in a circle with at least one object in the RF. A cue flashed instructing the monkey to make a saccade, after a delay, to the stable object physically matching the cue. The location of the cue was fixed in trial blocks, either in or out of the RF. If the cue was outside the RF, neurons developed delay-period activity tuned for the direction of the saccade target at approximately 190 ms after cue onset. If the cue appeared in the RF, neurons initially responded to cue onset and developed tuning for saccade direction only toward the end of the delay period, 390 ms after cue onset. The cue- and saccade-target responses coexisted throughout a significant portion of the delay period. The results show that visual-on responses and delay-period activity in LIP are functionally separable, and that, although highly selective, the salience representation in LIP can contain more than one object at a time.     

Receptive fields in human visual cortex mapped with surface electrodes

Most of our understanding of the functional organization of human visual cortex comes from lesion and functional imaging studies and by extrapolation from results obtained by neuroanatomical and neurophysiological studies in nonhuman primates. Although some single-unit and field potential recordings have been made in human visual cortex, none has provided quantitative characterization of spatial receptive fields (RFs) of individual sites. Here we use subdural electrodes implanted for clinical purposes to quantitatively measure response properties in different regions of human visual cortex. We find significant differences in RF size, response latency, and response magnitude for sites in early visual areas, versus sites in later stages of both the dorsal and ventral streams. In addition, we use this technique to estimate the cortical magnification factor in early human visual cortex. The spatial and temporal resolution of cortical surface recordings suggest that this technique is well suited to examine further issues in visual processing in humans.     

Physiological responses of New World monkey V1 neurons to stimuli defined by coherent motion

We studied the responses of neurons in area V1 of marmosets to visual stimuli that moved against dynamic textured backgrounds. The stimuli were defined either by a first-order cue ('solid' bars, which were either darker or lighter than the background) or by a second-order cue ('camouflaged' bars, defined only by coherent motion). Forty-two per cent of the neurons demonstrated a similar selectivity for the direction of motion of the solid and camouflaged bars, thereby characterizing a population of cue-invariant (CI) cells. The other cells either showed different selectivity to the movement of solid and camouflaged bars (non-cue-invariant, or NCI cells), or responded equally well to movement in all directions. CI neurons, which were rare in layer 4, tended to have larger receptive fields and to be more strongly direction selective than NCI cells. Although V1 neurons tended to show maximal responses to camouflaged bars that were longer than the 'optimal' solid bars, many CI neurons preferred first- and second-order stimuli of similar lengths. Finally, the activity evoked by the camouflaged bars was delayed in relation to that evoked by solid bars. These results demonstrate that motion CI responses are relatively common in primate V1, especially among a population of strongly direction-selective neurons. They also indicate that this response property may depend on feedback from extrastriate areas, or on complex intrinsic interactions within V1.     

Modulation of responses to optic flow in area 7a by retinotopic and oculomotor cues in monkey

Perception of two- and three-dimensional optic flow critically depends upon extrastriate cortices that are part of the 'dorsal stream' for visual processing. Neurons in area 7a, a sub-region of the posterior parietal cortex, have a dual sensitivity to visual input and to eye position. The sensitivity and selectivity of area 7a neurons to three sensory cues - optic flow, retinotopic stimulus position and eye position - were studied. The visual response to optic flow was modulated by the retinotopic stimulus position and by the eye position in the orbit. The position dependence of the retinal and eye position modulation (i.e. gain field) were quantified by a quadratic regression model that allowed for linear or peaked receptive fields. A local maximum (or minimum) in both the retinotopic fields and the gain fields was observed, suggesting that these sensory qualities are not necessarily linearly represented in area 7a. Neurons were also found that simply encoded the eye position in the absence of optic flow. The spatial tuning for the eye position signals upon stationary stimuli and optic flow was not the same, suggesting multiple anatomical sources of the signals. These neurons can provide a substrate for spatial representation while primates move in the environment.      

Temporal relation of population activity in visual areas MT/MST and in primary motor cortex during visually guided tracking movements

There is growing evidence that in primate cerebral cortex the areas along the 'dorsal pathway' are involved in the transformation of visual motion information towards a motor command. To pursue this cortical flow of information from visual motion areas to the motor cortex, single-cell activity was recorded from visual areas MT/MST (middle temporal area/medial superior temporal area) and from primary motor cortex (M1) while monkeys tracked moving targets with their right hand. Spike activity of 353 directionally tuned motor cortex cells was combined to a time-varying population vector, and similarly a time-resolved visual population vector was calculated from 252 MT/MST cells. Both population vectors code faithfully for the direction of the collinear motion of target and hand. For a given direction, the length of the population vectors varied over time during the performance of the task. The temporal evolution of both population responses reflects the different relationship between the early visual responses to the moving target and the directional motor command controlling the hand movement. The results indicate that during the visual tracking task visual and motor populations which code for similar directions of movement are co-activated with considerable temporal overlap. Despite this co-activation in both modalities, we failed to observe any significant synchronization between areas MT/MST and M1.     

Representation of surface luminance and contrast in primary visual cortex

In visual perception, object identification requires both the ability to define regions of uniform luminance and zones of luminance contrast. Neural processes underlying contrast detection have been well studied, while those defining luminance remain poorly understood and controversial. Partially because stimuli comprised of uniform luminance are relatively ineffective in driving responses of cortical neurons, little effort has been made to systematically compare responses of individual neurons to both uniform luminance and contrast. Using large static uniform luminance and contrast stimuli, modulated temporally in luminance or contrast, we found a continuum of responses ranging from a few cells modulated only by luminance (luminance-only), to many cells modulated by both luminance and contrast (luminance-contrast), and to many others modulated only by contrast (contrast-only) in primary visual cortex. Moreover, luminance-contrast cells had broader orientation tuning, larger receptive field (RF) and lower spatial frequency Preference, on average, than contrast-only cells. Contrast-only cells had contrast responses more linearly correlated to the spatial structure of their RFs than luminance-contrast cells. Taken together these results suggest that luminance and contrast are represented, to some degree, by independent mechanisms that may be shaped by different classes of subcortical and/or cortical inputs.     

Eye-hand coordination during reaching. II. An analysis of the relationships between visuomanual signals in parietal cortex and parieto-frontal association projections

The relationships between the distribution of visuomanual signals in parietal cortex and that of parieto-frontal projections are the subject of the present study. Single cell recording was performed in areas PEc and V6A, where different anatomical tracers were also injected. The monkeys performed a variety of behavioral tasks, aimed at studying the visual and motor properties of parietal cells, as well as the potential combination of retinal-, eye- and hand-related signals on cell activity. The activity of most cells was related to the direction of movement and the active position of the hand. Many of these reach-related cells were influenced by eye position information. Fewer cells displayed relationships to saccadic eye movements. The activity of most neurons related to a combination of both hand and eye signals. Many cells were also modulated during preparation for hand movement. Light-dark differences of activity were common and interpreted as related to the sight and monitoring of hand motion and/or position in the visual field. Most cells studied were very sensitive to moving visual stimuli and also responded to optic flow stimulation. Visual receptive fields were generally large and extended to the periphery of the visual field. For most neurons, the orientation of the preferred directions computed across different epochs and tasks conditions clustered within a limited sector of space, the field of global tuning. This can be regarded as an ideal frame to combine spatially congruent eye- and hand-related information for different forms of visuomanual behavior. All these properties were common to both PEc and V6A. Retinal, eye- and hand-related activity types, as well as parieto-frontal association cells, were distributed in a periodic fashion across the tangential domain of areas PEc and V6A. These functional and anatomical distributions were characterized and compared through a spectral and coherency analysis, which revealed the existence of a selective 'match' between activity types and parieto-frontal connections. This match depended on where each individual efferent projection was addressed. The results of the present and of the companion study can be relevant for a re-interpretation of optic ataxia as the consequence of the breakdown of the combination of retinal-, eye- and hand-related directional signals within the global tuning fields of parietal neurons.