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.

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.

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)

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.