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Abstract

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.