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The Journal of Neuroscience, October 13, 2004, 24(41):9185-9194; doi:10.1523/JNEUROSCI.1884-04.2004

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Behavioral/Systems/Cognitive
The Integration of Multiple Stimulus Features by V1 Neurons

Alexander Grunewald and Evelyn K. Skoumbourdis

Harlow Center for Biological Psychology, Departments of Psychology and Physiology, University of Wisconsin-Madison, Madison, Wisconsin 53706

We investigated how V1 neurons integrate two stimulus features by presenting stimuli from a stimulus set made up of all combinations of eight different directions of motion and nine binocular disparities. We investigated the occurrence and shape of the resulting joint tuning function. Among V1 neurons, 80% were jointly tuned for disparity with orientation or direction. The joint tuning function of all jointly tuned neurons was separable into distinct tuning for disparity on the one hand, and orientation or direction tuning on the other. The degree of separability and the mutual information between the stimulus and the firing rates were strongly correlated. The mutual information of jointly tuned neurons when both features were decoded together was highly correlated with the mutual information when the two features were decoded separately, and the information was then summed. Jointly tuned neurons were just as good at representing information about single features as neurons tuned for only a single feature. The tuning properties of most jointly tuned neurons did not dynamically evolve over time, nor did jointly tuned neurons respond earlier than neurons tuned for only a single feature. The response selectivity of V1 neurons is low and decreases the information that a neuron represents about a stimulus. Together these results suggest that distinct stimulus features are integrated very early in visual processing. Furthermore, V1 generates a distributed representation through low response selectivity that avoids the curse of dimensionality by using separable joint tuning functions.

Key words: striate cortex; orientation; direction; disparity; joint tuning; separability; information; binocular; motion; depth

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Received May 14, 2004; revised August 20, 2004; accepted September 9, 2004.

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