Processing of kinetically defined boundaries in areas V1 and V2 of the macaque monkey.

We recorded responses in 107 cells in the primary visual area V1 and 113 cells in the extrastriate visual area V2 while presenting a kinetically defined edge or a luminance contrast edge. Cells meeting statistical criteria for responsiveness and orientation selectivity were classified as selective for the orientation of the kinetic edge if the preferred orientation for a kinetic boundary stimulus remained essentially the same even when the directions of the two motion components defining that boundary were changed by 90 degrees. In area V2, 13 of the 113 cells met all three requirements, whereas in V1, only 4 cells met the criteria of 107 that were tested, and even these demonstrated relatively weak selectivity. Correlation analysis showed that V1 and V2 populations differed greatly (P < 1.0 x 10(-6), Student's t-test) in their selectively for specific orientations of kinetic edge stimuli. Neurons in V2 that were selective for the orientation of a kinetic boundary were further distinguished from their counterparts in V1 in displaying a strong, sharply tuned response to a luminance edge of the same orientation. We concluded that selectivity for the orientation of kinetically defined boundaries first emerges in area V2 rather than in primary visual cortex. An analysis of response onset latencies in V2 revealed that cells selective for the orientation of the motion-defined boundary responded about 40 ms more slowly, on average, to the kinetic edge stimulus than to a luminance edge. In nonselective cells, that is, those presumably responding only to the local motion in the stimulus, this difference was only about 20 ms. Response latencies for the luminance edge were indistinguishable in KE-selective and -nonselective neurons. We infer that while responses to luminance edges or local motion are indigenous to V2, KE-selective responses may involve feedback entering the ventral stream at a point downstream with respect to V2.

Response latency of macaque area MT/V5 neurons and its relationship to stimulus parameters.

A total of 310 MT/V5 single cells were tested in anesthetized, paralyzed macaque monkeys with moving random-dot stimuli. At optimum stimulus parameters, latencies ranged from 35 to 325 ms with a mean of 87+/-45 (SD) ms. By examining the relationship between latency and response levels, stimulus parameters, and stimulus selectivities, we attempted to isolate the contributions of these factors to latency and to identify delays representing intervening synapses (circuitry) and signal processing (flow of information through that circuitry). First, the relationship between stimulus parameters and latency was investigated by varying stimulus speed and direction for individual cells. Resulting changes in latencies were explainable in terms of response levels corresponding to how closely the actual stimulus matched the preferred stimulus of the cell. Second, the relationship between stimulus selectivity and latency across the population of cells was examined using the optimum speed and direction of each neuron. A weak tendency for cells tuned for slow speeds to have longer latencies was explainable by lower response rates among slower-tuned neurons. In contrast, sharper direction tuning was significantly associated with short latencies even after taking response rate into account, (P = 0.002, ANCOVA). Accordingly, even the first 10 ms of the population response fully demonstrates direction tuning. A third study, which examined the relationship between antagonistic surrounds and latency, revealed a significant association between the strength of the surround and the latency that was independent of response levels (P < 0.002, ANCOVA). Neurons having strong surrounds exhibited latencies averaging 20 ms longer than those with little or no surround influence, suggesting that neurons with surrounds represent a later stage in processing with one or more intervening synapses. The laminar distribution of latencies closely followed the average surround antagonism in each layer, increasing with distance from input layer IV but precisely mirroring response levels, which were highest near the input layer and gradually decreased with distance from input layer IV. Layer II proved the exception with unexpectedly shorter latencies (P< 0.02, ANOVA) yet showing only modest response levels. The short latency and lack of strong direction tuning in layer II is consistent with input from the superior colliculus. Finally, experiments with static stimuli showed that latency does not vary with response rate for such stimuli, suggesting a fundamentally different mode of processing than that for a moving stimulus.

Influence of stimulus speed upon the antagonistic surrounds of area MT/V5 neurons.

We investigated the effect of stimulus speed upon surround antagonism in macaque MT/V5 neurons, using probe stimuli placed at different positions in the surround. Their speed was varied, while the stimulation of the excitatory receptive field (RF) was held at optimal speed. Most Surrounds proved asymmetric, arising from a single region on one side of RF, although bilaterally and circularly symmetric surrounds were occasionally observed. Surround organization was generally retained at faster or slower surround speeds. Speed-dependent changes usually entailed diminished position dependence of surround influence, consequent to reduced surround effect at the position producing maximum inhibition. The effect of a stimulus covering the entire surround was much less dependent upon motion speed. Results show that surround non-uniformity is a robust finding in MT/V5 and endows neurons with multiple mechanisms for extracting surface orientation in depth.

The spatial distribution of the antagonistic surround of MT/V5 neurons.

The majority (217/325, 66%) of the neurons in the middle temporal (MT) area/V5 show strong antagonistic surrounds, defined here by a decrease of at least 50% in the summation curve. We mapped the antagonistic surround in 145 such cells, using eight circularly distributed surround stimulus patches (Surround Asymmetry Test, SAT) and also mapped the surround in 51 of these 145 cells using a grid consisting of 25 square patches (Surround Mapping Test, SMT). Both tests showed that the angular surround distribution was non-uniform in the majority of these neurons. In half the neurons, the antagonistic surround was asymmetric, and arose from a single region on one side of the excitatory receptive field (ERF). In another quarter of the sample the surround was bilaterally symmetric, and arose from a pair of regions on opposite sides of the ERF. Only the remaining 20% showed a circularly symmetric surround distribution. These three groups differed in their laminar distribution. The SMT showed that, radially, the surround antagonism reached a maximum, on average, at 1.5 times the ERF radius. Detailed comparisons of the spatial relationships of excitatory and inhibitory regions of the RF components shows that non-homogeneity of the surround influence appears to be an intrinsic property of the surround. Such a property may underly the extraction of the surface orientation and curvature from speed patterns.

Size and shape of receptive fields in the medial superior temporal area (MST) of the macaque.

Ninety-one single units were recorded in area MSTd of anesthetized and paralyzed macaques. Receptive fields (RFs) were mapped quantitatively using small patches of moving random dots in 25 different positions (the two-dimensional position test, or P2D). The dimensions of the receptive fields (RFs) were estimated by fitting P2D data with a generalized Gaussian function. The half-height areas of the RFs in MSTd were found to average 1085 deg2 and were not dependent upon eccentricity, in contrast to those in MT/V5 (n = 295) which averaged 31 deg2 at the fovea but at the periphery approached the RFs of MSTd in size. The RFs of some MSTd neurons extended 30-40 degrees into the ipsilateral hemifield. In comparison, the overlap was only 10-15 degrees in area MT/V5.

Selectivity of macaque MT/V5 neurons for surface orientation in depth specified by motion.

Area MTN5 in the macaque brain is one of the major cortical regions involved in the analysis of retinal image motion. The majority of the neurons in this cortical area have non-uniform antagonistic surrounds as components of their receptive field complexes. Theoretical studies indicate that such asymmetrical surrounds should enable neurons to extract orientation in depth from motion. Here we show that nearly half of the MTN5 neurons encode the tilt component of the orientation in depth of a plane specified by motion. Furthermore, we show that such selectivity for depth from motion depends on the presence of an asymmetrical surround and on the speed tuning of those asymmetrical surround influences.

Spatial heterogeneity of inhibitory surrounds in the middle temporal visual area.

A recurrent theme in the organization of vertebrate visual cortex is that of receptive fields with an associated "silent" opponency component. In the middle temporal area (area MT), a cortical visual area involved in the analysis of retinal motion in primates, this opponency appears in the form of a region outside the classical receptive field (CRF) that in itself gives no response but suppresses responses to motion evoked within the CRF. This antagonistic motion surround has been described as very large and symmetrically arrayed around the CRF. On the basis of this view, the primary function of the surround has long been thought to consist of simple figure-ground segregation based on movement. We have made use of small stimulus patches to map the form and extent of the surround and find evidence that the surround inhibition of many MT cells is in fact confined to restricted regions on one side or on opposite sides of the CRF. Such regions endow MT cells with the ability to make local-to-local motion comparisons, capable of extracting more complex features from the visual environment, and as such, may be better viewed as intrinsic parts of the receptive field, rather than as separate entities responsible for local-to-global comparisons.

Shape and spatial distribution of receptive fields and antagonistic motion surrounds in the middle temporal area (V5) of the macaque.

The spatial organization of receptive fields in the middle temporal (MT) area of anaesthetized and paralysed macaque monkeys was studied. In all, 288 neurons were successfully recorded. The size and shape of the receptive field (RF) was mapped with small patches of translating random dots and the resulting data were fitted with a generalized Gaussian. Results show that the RF area increases with eccentricity, and is larger in lamina 5 than in other layers. Most of these RFs are elongated, and the axis of elongation tends to be orthogonal to the preferred direction of motion. The direction selectivity is maintained in all positions in the RF, but layer 5 cells are less direction-selective than cells in other layers. In a second series of experiments, radial dimensions of the classical RF and the antagonistic surround were estimated from area summation tests. These data were fitted with the difference of the integrals of two Gaussians. Surrounds were weakest in layer 4 and strongest in layer 2. Optimal stimulus diameters, also estimated from the area summation curve, were larger in the infragranular layers than in the other layers. The maximum sensitivity of the surround was clearly displaced from the classical RF (CRF) centre, indicating that the surround is not concentric with the CRF. This radial offset and the extent of the surround were largest in layers 2 and 5 and smallest in 3a. The extent of the surround half-height equalled, on average, 3-4 times that of the CRF. These results suggest that antagonistic surrounds are constructed in MT, probably through horizontal connections, and that a strong vertical organization exists in area MT, as has been shown for V1.

Processing of kinetically defined boundaries in the cortical motion area MT of the macaque monkey.

1. Electrophysiological recordings of 68 cells in the middle temporal area MT were made in paralyzed and anesthetized macaque monkeys. 2. Testing with our kinetic boundary stimuli always occurred under optimized conditions. To this end, the preferred direction, speed, stimulus position, and stimulus size of each cell were determined by quantitative tests. 3. The orientation selectivity to stationary luminance contrast edges served as a reference by which a response to kinetic boundaries could be compared. We found cells in area MT to be less selective to the orientation of luminance contrast stimuli than to the direction of motion. We confirmed the presence of neurons with preferred orientation aligned with their preferred direction. 4. The responses to kinetic edges defined by motion vectors moving in opposite directions, kinetic gratings with motion vectors in opposite directions, kinetic edges containing coherent motion and a stationary complementary field or coherent motion and a complementary field containing visual dynamic noise were compared. Kinetic boundaries were generated so that the motion vectors moved either parallel or orthogonal to the orientation of the discontinuity. For a cell to be considered as responding to the orientation of a kinetic boundary, it had to exhibit the same preferred orientation when the local motion vectors changed from parallel to orthogonal to the orientation of the kinetic boundary. 5. All cells in area MT changed their preferred orientation by 90 degrees when the coherent motion vectors changed from moving parallel to moving orthogonal to the boundary. This was the case independent of the types of kinetic boundary tested. We concluded that cells in area MT appear to respond to the motion vector over their classical receptive field (CRF) only and were unable to code the orientation of the kinetic boundary. 6. In those cells exhibiting an antagonistic surround, we examined the ability of the cell to code the position of a kinetic boundary. None of the cells tested signaled the position of a kinetic boundary. The side preference of the stimulus of the cells changed from left to right as the motion vectors in the stimulus reversed. This indicates that the cells were only selective for the motion vectors present over their CRF. 7. We found that the directional sensitivity of cells in area MT remained unaltered by the presence of additional motion vectors within the CRF. This suggests that cells in area MT extract a specific motion vector from a spatial configuration of vectors.(ABSTRACT TRUNCATED AT 400 WORDS)

The speed tuning of medial superior temporal (MST) cell responses to optic-flow components.

The responses of macaque medial superior temporal (MST) cells to translation and to the optic-flow components-rotation, expansion/contraction, and deformation-were examined with particular regard to the speed tuning of MST cells for optic-flow stimuli and the effect of removing speed gradients from those stimuli. The use of position invariance as an indispensable criterion for assessing the authenticity of responses to optic flow is reviewed. By extending the scope of testing to include higher speeds it is found, in contrast to in previous reports, that MST cells generally respond to optic-flow components with a speed-response profile which is tuned for a particular range of speeds. Removal of the speed gradient had little effect on this observation. These and other properties of MST cells lead to the conclusion that one of the major functions of MST is the detection and encoding of self-motion.

Responses of macaque STS neurons to optic flow components: a comparison of areas MT and MST.

1. We recorded and tested quantitatively 65 middle temporal (MT) and 82 middle superior temporal (MST) cells in paralyzed and anesthetized monkeys. 2. Responses to the three elementary optic flow components (EFCs)--rotation, deformation, and expansion/contraction--and to translation (in the display) were compared after optimization of stimulus direction, speed, size, and position. As a control responses to flicker were measured. 3. Response windows were adapted in correspondence with our finding that latencies of MT and MST cells decrease with increasing speed for all types of motion. 4. There was a response continuum in MT as well as in MST cells. Compared with translation, MST cells responded significantly more to rotation but less to flicker than MT cells. MST cells were significantly more direction selective for expansion/contraction than MT cells. 5. MST cells generally responded to fewer motion types than MT cells. 6. Position invariance of EFC direction selectivity was tested over a region of the visual field centered on the translation receptive field (RF). Direction selectivity for an EFC was not position invariant in MT cells but it was invariant in 40% of the MST cells tested. These cells were considered EFC selective. 7. Most EFC-selective MST cells were selective for a single EFC, possibly combined with translation. Few of them were selective for deformation. 8. EFC selectivity was also speed invariant and EFC-selective MST cells usually had RFs summating inputs over wide portions of the visual field. 9. EFC-selective MST cells with similar selectivities were clustered.

Effects of visual cortex lesions on orientation discrimination of illusory contours in the cat.

We have trained five cats in orientation discrimination using different contours, and compared the deficits caused by lesions of cortical areas 17 and 18 (tier I) to the deficits induced by removal of those areas receiving afferents originating in areas 17 and 18 (tier II). As contour stimuli we used two types of illusory contours and a luminance bar. The two illusory contours were defined by opposed line-ends. One of them coincided with a luminance gradient whereas the other did not. Tier I lesions destroyed the capacity to discriminate the orientation of both illusory contours, and also caused an important, though less severe, deficit in bar orientation discrimination. The deficits induced by tier I lesions were permanent. Tier II lesions also caused significant deficits in orientation discrimination of illusory contours, but only a negligible deficit in bar orientation discrimination, and this result was not a mere consequence of a difference in difficulty between the tasks involving bars and illusory contours. In addition, tier II lesions differentiated between illusory contour types, the deficit being more pronounced for the illusory contour without luminance gradient than for the one with luminance gradient. In contrast to tier I lesions, tier II lesions allowed significant recovery, leading to small final deficits for all contour types tested.

Speed and direction selectivity of macaque middle temporal neurons.

1. We tested quantitatively the responses of 147 middle temporal (MT) cells to light and dark bars moving at different speeds ranging over a 1,000-fold range (0.5-512 deg/s). 2. We derived the following quantities from the speed-response (SR) curves obtained for opposite directions of motion. Speed selectivity was characterized by the maximum response, optimum speed, upper cutoff speed, response to slow movement, and tuning width. Direction selectivity was characterized by the direction index (DI) averaged over speeds yielding significant responses (MDI) and by the direction index at optimal speed (PDI). 3. There was an excellent correlation between speed characteristics for light and dark bars. These correlations were stronger than the correlations between direction indexes. The strongest correlations were obtained for maximum response and upper cutoff. 4. SR curves were classified into three groups: low pass (25%), tuned (43%), and broadband (28%), leaving 4% unclassified. 5. In the majority (75%) of MT cells, there was an agreement between the typology of speed selectivity for light and dark bars. Cells were classified as tuned (33%), low pass (22%), broadband (19%), and mixed (22%), leaving 4% unclassified. In addition to differences in speed characteristics, these groups also differed in response level, direction selectivity, and distribution of preferred directions. 6. For tuned cells, there was a very tight correlation of most speed characteristics for light and dark bars. 7. Direction selectivity depended on stimulus speed in most neurons, yielding a tuned average speed-DI curve. 8. Speed characteristics, proportions of speed selectivity types, and direction selectivity indexes showed little dependence on laminar position. 9. Speed characteristics and direction selectivity indexes were not dependent on eccentricity. Proportion of speed selectivity types however, changed dramatically with eccentricity: low-pass cells dominated foveally, tuned cells parafoveally, and broadband cells peripherally. 10. There were also small eccentricity effects on the range of optimal speeds shown by tuned cells and on the speed at which direction selectivity decreases in the slow speed range.

First-order analysis of optical flow in monkey brain.

Optical flow is a rich source of information about the three-dimensional motion and structure of the visual environment. Little is known of how the brain derives this information. One possibility is that it analyzes first-order elementary components of optical flow, such as expansion, rotation, and shear. Using a combination of physiological recordings and modeling techniques, we investigated the contribution of the middle superior temporal area (MST), a third-order cortical area in the dorsal visual pathway that receives inputs from the medial temporal area (MT). The results show (i) that MST cells, but not MT cells, are selective for elementary flow components (EFCs) alone or their combination with translation, (ii) that MST cells selective for an EFC do not extract this component from a more complex motion pattern, and (iii) that position invariance as observed in MST is compatible with an input arrangement from MT cells matching the selectivity of MST neurons.

Patterns of glutamate immunoreactivity in the goldfish retina.

Postembedding silver-intensified immunogold procedures reveal high levels of glutamate immunoreactivity in "vertical" elements of the goldfish retina: (1) Red-sensitive and green-sensitive cones display strong glutamate immunoreactivity, especially in their synaptic terminals, but blue-sensitive cones are poorly immunoreactive. (2) All type Mb (on-center) and Ma (off-center) mixed rod-cone bipolar cells and all identifiable cone bipolar cells are highly glutamate immunoreactive. We find no evidence for bipolar cells that lack glutamate immunoreactivity. (3) The majority of the somas in the ganglion cell layer and certain large cells of the amacrine cell layer resembling displaced ganglion cells are strongly glutamate immunoreactive. (4) Despite their high affinity symport of acidic amino acids, the endogenous levels of glutamate in Müller's cells are among the lowest in the retina. (5) GABAergic neurons possess intermediate levels of glutamate immunoreactivity. Quantitative immunocytochemistry coupled with digital image analysis allows estimates of intracellular glutamate levels. Photoreceptors and bipolar and ganglion cells contain from 1 to 10 mM glutamate. The bipolar and ganglion cell populations maintain high intracellular glutamate concentrations, averaging about 5 mM, whereas red-sensitive and green-sensitive cones apparently maintain lower levels. Importantly, photoreceptor glutamate levels are extremely volatile, and in vitro maintenance is required to preserve cone glutamate immunoreactivity in the goldfish. GABAergic horizontal and amacrine cells contain about 0.3-0.7 mM glutamate, which matches the values predicted from the Km of glutamic acid decarboxylase. Müller's cells and non-GABAergic amacrine cells contain less than 0.1 mM glutamate. Though Müller's cells are known to possess potent glutamate symport, they clearly possess equally potent mechanisms for maintaining low intracellular glutamate concentrations.

Laminar analysis of motion information processing in macaque V5.

Although it has been repeatedly shown that properties of striate cells depend on laminar position, no information is available about the vertical organization of primate extrastriate cortex. Laminar analysis in the part of macaque V5 (the middle temporal visual area) devoted to the central 10 degrees in the visual field, reveals that interaction between a moving bar and a moving texture differs systematically between layers. We found that cells for which the direction selectivity does not depend on texture motion occur mainly in layer 4 and in the infragranular layers. Cells with only pseudomodulation of direction selectivity were found throughout the cortical depth. Cells for which direction selectivity was abolished when both patterns moved inphase occur outside layer 4 and therefore represent a higher processing stage. These 3 types differ not only in laminar position but also in velocity selectivity and in strength of texture response. These findings suggest that the 3 classes represent distinct physiological types of neurons dedicated to different stages of motion processing which takes place in V5, and suggest that these cells may play different roles in the guidance of eye movements.

Response latencies of visual cells in macaque areas V1, V2 and V5.

The response to moving light and dark slits was recorded from a total of 94 cells in V1, V2, and V5 (MT) in 9 anesthetized and paralyzed macaque monkeys (M. fascicularis). Using the spatial lag method2, response latencies were calculated for each cell. We obtained median latencies of 85, 96, and 94 ms for cells in areas V1, V2, and V5, respectively. The higher median latencies of V2 and V5 cells compared to V1 are commensurate with later stages of information processing, and are predictable from the anatomy of the interconnections. In addition, a distinct, second population of high-latency cells is present in all 3 regions, but is most abundant in lamina 4 of V5. These may represent either external feedback from other regions or ongoing processing. Extensive overlap of latencies in all 3 regions at both the high and low ends of their respective ranges indicates a considerable degree of parallel interaction between striate and extrastriate cortex.