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Visual motion drives smooth pursuit eye movements through a sensory-motor decoder that uses multiple parallel neural pathways to transform the population response in extrastriate area MT into movement. We evaluated the decoder by challenging pursuit in monkeys with reduced motion reliability created by reducing coherence of motion in patches of dots. Our strategy was to determine how reduced dot coherence changes the population response in MT. We then predicted the properties of a decoder that transforms the MT population response into dot coherence-induced deficits in the initiation of pursuit and steady-state tracking. During pursuit initiation, decreased dot coherence reduces MT population response amplitude without changing the preferred speed at its peak. The successful decoder reproduces the measured eye movements by multiplication of 1 ) the estimate of target speed from the peak of the population response with 2 ) visual-motor gain based on the amplitude of the population response. During steady-state tracking, the decoder that worked for pursuit initiation failed to reproduce the paradox that steady-state eye speeds do not accelerate to the target speed despite persistent image motion. It predicted eye acceleration to target speed even when monkeys' eye speeds were steady at well below the target speed. To account for the effect of dot coherence on steady-state eye speed, we postulate that the decoder uses sensory-motor gain to modulate the eye velocity positive feedback that normally sustains perfect steady-state tracking. Then, poor steady-state tracking persists because of balance between eye deceleration caused by low positive feedback gain and acceleration driven by MT. NEW & NOTEWORTHY By challenging a sensory-motor system with degraded sensory stimuli, we reveal how the sensory-motor decoder transforms the population response in extrastriate area MT into commands for the initiation and steady-state behavior of smooth pursuit eye movements. Conclusions are based on measuring population responses in MT for multiple target speeds and different levels of motion reliability and evaluating a decoder with a biologically motivated architecture to determine the decoder properties that create the measured eye movements.

The perception of visual motion can be profoundly influenced by visual context. To gain insight into how the visual system represents motion speed, we investigated how a background stimulus that did not move in a net direction influenced the perceived speed of a center stimulus. Visual stimuli were two overlapping random-dot patterns. The center stimulus moved coherently in a fixed direction, whereas the background stimulus moved randomly. We found that human subjects perceived the speed of the center stimulus to be significantly faster than its veridical speed when the background contained motion noise. Interestingly, the perceived speed was tuned to the noise level of the background. When the speed of the center stimulus was low, the highest perceived speed was reached when the background had a low level of motion noise. As the center speed increased, the peak perceived speed was reached at a progressively higher background noise level. The effect of speed overestimation required the center stimulus to overlap with the background. Increasing the background size within a certain range enhanced the effect, suggesting spatial integration. The speed overestimation was significantly reduced or abolished when the center stimulus and the background stimulus had different colors, or when they were placed at different depths. When the center- and background-stimuli were perceptually separable, speed overestimation was correlated with perceptual similarity between the center- and backgroundstimuli. These results suggest that integration of motion energy from random motion noise has a significant impact on speed perception. Our findings put new constraints on models regarding the neural basis of speed perception. [ABSTRACT FROM AUTHOR]

Neurons in area MT/V5 of the macaque visual cortex encode visual motion. Some cells are selective for the motion of oriented features (component direction-selective, CDS); others respond to the true direction of complex patterns (pattern-direction selective, PDS). There is a continuum of selectivity in MT, with CDS cells at one extreme and PDS cells at the other; we compute a pattern index that captures this variation. It is unknown how a neuron's pattern index is related to its other tuning characteristics. We therefore analyzed the responses of 792 MT cells recorded in the course of other experiments from opiate-anesthetized macaque monkeys, as a function of the direction, spatial frequency, drift rate, size, and contrast of sinusoidal gratings and of the direction and speed of random-dot textures. We also compared MT responses to those of 718 V1 cells. As expected, MT cells with higher pattern index tended to have stronger direction selectivity and broader direction tuning to gratings, and they responded better to plaids than to gratings. Strongly PDS cells also tended to have smaller receptive fields and stronger surround suppression. Interestingly, they also responded preferentially to higher drift rates and higher speeds of moving dots. The spatial frequency preferences of PDS cells depended strongly on their preferred temporal frequencies, whereas these preferences were independent in component-selective cells. Pattern direction selectivity is statistically associated with many response properties of MT cells but not strongly associated with any particular property. Pattern-selective signals are thus available in association with most other signals exported by MT. [ABSTRACT FROM AUTHOR]

Many neurons in visual cortical area MT signal the direction of motion of complex visual patterns, such as plaids composed of two superimposed drifting gratings. To compute the direction of pattern motion, MT neurons combine component motion signals over time and space. To determine the spatial and temporal limits of signal integration, we measured the responses of single MT neurons to a novel set of "pseudoplaid" stimuli in which the component gratings were alternated in time or space. As the temporal or spatial separation of the component gratings increased, neuronal selectivity for the direction of pattern motion decreased. Using descriptive models of signal integration, we inferred the temporal and spatial structure of the mechanisms that compute pattern direction selectivity. The median time constant for integration was roughly 10 ms, a timescale characteristic of integration by single cortical pyramidal neurons. The median spatial integration field was roughly one-third of the MT receptive field diameter, suggesting that the spatial limits are set by stages of processing in earlier areas of visual cortex where receptive fields are smaller than in MT. Interestingly, pattern direction-selective neurons had shorter temporal integration times than component direction-selective neurons but similar spatial integration windows. We conclude that pattern motion can only be signaled by MT neurons when the component motion signals co-occur within relatively narrow spatial and temporal limits. We interpret these results in the framework of recent hierarchical models of MT. [ABSTRACT FROM AUTHOR]

We recorded simultaneously from pairs of motion-sensitive neurons in the middle temporal cortex (MT) of macaque monkeys and used cross-correlations in the timing of spikes between neurons to gain insights into cortical circuitry. We characterized the time course and stimulus dependency of the cross-correlogram (CCG) for each pair of neurons and of the auto-correlogram (ACG) of the individual neurons. For some neuron pairs, the CCG showed negative flanks that emerged next to the central peak during stimulus-driven responses. Similar negative flanks appeared in the ACG of many neurons. Negative flanks were most prevalent and deepest when the neurons were driven to high rates by visual stimuli that moved in the neurons' preferred directions. The temporal development of the negative flanks in the CCG coincided with a parallel, modest reduction of the noise correlation between the spike counts of the neurons. Computational analysis of a model cortical circuit suggested that negative flanks in the CCG arise from the excitation-triggered mutual cross-inhibition between pairs of excitatory neurons. Intracortical recurrent inhibition and afterhyperpolarization caused by intrinsic outward currents, such as the calcium-activated potassium current of small conductance, can both contribute to the negative flanks in the ACG. In the model circuit, stronger intracortical inhibition helped to maintain the temporal precision between the spike trains of pairs of neurons and led to weaker noise correlations. Our results suggest a neural circuit architecture that can leverage activity-dependent intracortical inhibition to adaptively modulate both the synchrony of spike timing and the correlations in response variability. [ABSTRACT FROM AUTHOR]