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Abstract:
How neurons in sensory cortices represent the environment still remains a matter of investigation. With regard to
individual neurons, it is of particular interest on what time scales their responses carry information, and hence
what are the time scales that define the neural code. Given that the responses of sensory neurons are temporally
modulated by the environment, and given that the sensory environment can change on different time scales,
however, it might well be that there is no unique time scale of neural coding in a particular sensory area.
Analyzing data recorded in primate auditory and visual cortices, we show that this is indeed the case.
Specifically, we recorded the responses of neurons in primary auditory cortex of alert macaque monkeys listening
passively to complex and natural sounds. In addition, we analyzed the activity of neurons recorded in primary
visual cortex of anesthetized macaques during the presentation of naturalistic movies. For each neuron and
stimulus set, we quantified the amount of stimulus information carried by firing rates at different temporal scales
(bins) and systematically compared the information derived from progressively longer time bins. From this we
determined the shortest time scale (i.e. precision of neural code) that still provided all stimulus information.
We found that the critical time scale of neural coding depends on the temporal stimulus dynamics. In auditory
cortex, we compared responses to sequences of random tones (stimulus auto-correlation scale of below 10ms) to
responses to a sequence of natural sounds (auto-correlation of more than 30ms). The temporal precision required
to obtain maximal information was shorter for the tone sequence (median 5ms) than for the natural sounds (median
12ms). In visual cortex, we compared responses to natural movie epochs containing fast temporal modulation to
responses to epochs of slower modulation (the temporal auto-correlation of the latter being about 2-3 times
longer). We found that the time scale of optimal coding was shorter for the faster movie epochs (about 12ms) than
for the slower epochs (about 20ms).These results demonstrate that the time scale of neural coding can only be
specified in the context of a particular sensory environment.