Primary Visual Cortex Encodes Complementary Information about Naturalistic Movies at Different Temporal Scales

Natural stimuli modulate the activity of visual cortex on a variety of temporal scales, yet it is still unclear whether visual cortical neurons employ more than one response time scale to encode such stimuli. We investigated this issue by analyzing the activity of neurons recorded in primary visual cortex (V1) of anesthetized macaques during binocular presentation of naturalistic color movies, and we used information theory to quantify the amount of information carried by neural codes operating at different temporal scales. We divided the recording time into stimulus windows of 40–80 ms, and we computed the information carried by the neural response in each window about which stimulus window was being shown. First we measured the information carried by the spike count, simply quantified by the total number of spikes in the stimulus window. Then we measured the information carried by the temporal pattern of spikes, the latter being computed by subdividing each stimulus window into smaller time bins of size Δt and converting the spike train into a sequence of 0s and 1s denoting the absence/presence of spikes inside each bin [1]. When considering temporal patterns of spikes with a temporal resolution Δt of 8 or 16 ms, the information about which part of the movie was being shown conveyed by temporal spike patterns was up to 15 more than that conveyed by the spike count. This information gain did not increase further when considering resolutions finer than 8 ms, indicating that spike patterns carry information with a resolution of 8–16 ms or coarser. A previous study [2] showed that V1 neurons encode information also with respect to the phase of low frequency (1–4 Hz range) Local Field Potential (LFP) fluctuations. We investigated whether spike patterns carried information complementary to that carried by the phase of firing by quantifying if the joint knowledge of the precise spike pattern and the LFP phase of firing carried more information than either code considered alone. We found that this was the case: The information about the scene of the movie being shown gained by the simultaneous knowledge of the phase of low frequency LFPs and of the spike patterns occurred [3] was 50 higher than the information carried by spike patterns alone and 15 higher than the information carried by the phase of firing alone. This suggests that the information carried by slow LFP fluctuations complements that carried by spike patterns. In summary, we found evidence for multiple and complementary response time scales for the encoding of naturalistic stimuli in visual cortex. Informative codes range from spike timing precision at 10ms resolution to the much coarser phase of firing with respect to low frequency (few Hz) fluctuations. These findings suggest that, as hypothesized e.g. in [3,4], sensory cortices may enhance their information capacity by multiplexing complementary information at different time scales