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The Journal of Neuroscience, March 15, 2006, 26(11):2941-2950; doi:10.1523/JNEUROSCI.3936-05.2006

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Behavioral/Systems/Cognitive
Tuning for Spatiotemporal Frequency and Speed in Directionally Selective Neurons of Macaque Striate Cortex

Nicholas J. Priebe,1 Stephen G. Lisberger,1 and J. Anthony Movshon2

1Department of Physiology, Howard Hughes Medical Institute, W. M. Keck Foundation Center for Integrative Neuroscience and the Neuroscience Graduate Program, University of California, San Francisco, San Francisco, California 94143, and 2Center for Neural Science, New York University, New York, New York 10003

Correspondence should be addressed to Nicholas Priebe at his present address: Department of Neurobiology and Physiology, Northwestern University, 2145 North Sheridan Drive, Evanston, IL 60208. Email: nico{at}northwestern.edu

We recorded the responses of direction-selective simple and complex cells in the primary visual cortex (V1) of anesthetized, paralyzed macaque monkeys. When studied with sine-wave gratings, almost all simple cells in V1 had responses that were separable for spatial and temporal frequency: the preferred temporal frequency did not change and preferred speed decreased as a function of the spatial frequency of the grating. As in previous recordings from the middle temporal visual area (MT), approximately one-quarter of V1 complex cells had separable responses to spatial and temporal frequency, and one-quarter were "speed tuned" in the sense that preferred speed did not change as a function of spatial frequency. Half fell between these two extremes. Reducing the contrast of the gratings caused the population of V1 complex cells to become more separable in their tuning for spatial and temporal frequency. Contrast dependence is explained by the contrast gain of the neurons, which was relatively higher for gratings that were either both of high or both of low temporal and spatial frequency. For stimuli that comprised two spatially superimposed sine-wave gratings, the preferred speeds and tuning bandwidths of V1 neurons could be predicted from the sum of the responses to the component gratings presented alone, unlike neurons in MT that showed nonlinear interactions. We conclude that spatiotemporal modulation of contrast gain creates speed tuning from separable inputs in V1 complex cells. Speed tuning in MT could be primarily inherited from V1, but processing that occurs after V1 and possibly within MT computes selective combinations of speed-tuned signals of special relevance for downstream perceptual and motor mechanisms.

Key words: direction tuning; speed tuning; visual motion processing; sine wave gratings; MT; spatial frequency


Received Sept. 18, 2005; revised Jan. 29, 2006; accepted Jan. 30, 2006.

Correspondence should be addressed to Nicholas Priebe at his present address: Department of Neurobiology and Physiology, Northwestern University, 2145 North Sheridan Drive, Evanston, IL 60208. Email: nico{at}northwestern.edu


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