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Primate striate and prestriate cortical neurons during discrimination. I. simultaneous temporal encoding of information about color and pattern.

1. We recorded the responses of neurons in cortical areas V1, V2, and V4 to a set of 36 colored patterns while monkeys discriminated among the stimuli on the basis of their color or their pattern. In the discrimination task a colored square or a black and white pattern was presented foveally as a cue stimulus. The monkey was required to choose, by making a saccade, which of three peripheral targets had the same property as the cue. One of the peripheral targets was centered on the receptive field of the neuron, and the other two were positioned at equally distant points around the circumference of an imaginary circle centered on the cue and passing through the receptive field. 2. An examination of the responses to the stimuli showed that there was a complex interaction between the effects of color and of pattern on the neuronal responses. Because of these interactions, we tested sensitivity to color and pattern by sorting the responses to all stimuli according to the color or pattern of the stimulus. We found that the number of spikes in the responses was affected by only one or the other of the stimulus parameters, but that the temporal distribution of spikes was affected by both stimulus parameters. We quantified the relative sensitivities of each neuron to color and pattern by dividing the amount of information the neuron transmitted about color by the amount of information the neuron transmitted about pattern. The distributions of information ratios assuming a spike count code were broad, indicating that many neurons were sensitive to only one stimulus parameter or the other. In contrast, the distributions of information ratios assuming a wave-form code were narrow and centered near 1.0, indicating nearly equal sensitivities to both stimulus parameters. 3. In our initial experiments, it appeared that the color or pattern used as the cue for the discrimination task affected the responses of many neurons to stimuli on the receptive field. To determine whether the cue effect was due to simple visual interactions or to the cognitive requirements of the discrimination task, we performed a control experiment in which the cue was turned on 80 ms after the peripheral stimuli. For many of the neurons in the control experiment, an effect related to the cue appeared in the response before the cue had been turned on. Thus the effect we observed must have been due to visual interactions with the distractor targets, even though these were outside the neuron's classically defined receptive field. 4. We compared the rate at which color and pattern information developed in the response over time assuming either a spike count or a waveform code. The spike count code gained more of its information in the first 20ms of the response than did the waveform code, but thereafter the information carried by the spike count code developed more slowly and reached a lower asymptote than did the information carried by the waveform code. 5. The waveform codes carried nearly equal amounts of information about color and pattern, but the messages about these two parameters did not develop at the same rate in all areas. The messages about color and pattern developed at the same rate in area V1, but messages about color developed more slowly than did the messages about pattern in areas V2 and V4. 6. These results offer a neurophysiological basis for both the psychological separateness of color and pattern, and the binding of color and pattern into a unified percept. We propose that the separateness of color and form arises not by virtue of their being encoded by different populations of neurons, but by virtue of their being encoded by separable waveform codes in the responses of single neurons. We propose that the binding of color and form occurs by virtue of their codes being multiplexed on the same neurons.