Cortical dynamics during naturalistic sensory stimulations: experiments and models

We report the results of our experimental and theoretical investigations of the neural response dynamics in primary visual cortex (V1) during naturalistic visual stimulation. We recorded Local Field Potentials (LFPs) and spiking activity from V1 of anaesthetized macaques during binocular presentation of Hollywood color movies. We analyzed these recordings with information theoretic methods, and found that visual information was encoded mainly by two bands of LFP responses: the network fluctuations measured by the phase and power of low-frequency (less than 12 Hz) LFPs; and fast gamma-range (50-100 Hz) oscillations. Both the power and phase of low frequency LFPs carried information largely complementary to that carried by spikes, whereas gamma range oscillations carried information largely redundant to that of spikes. To interpret these results within a quantitative theoretical framework, we then simulated a sparsely connected recurrent network of excitatory and inhibitory neurons receiving slowly varying naturalistic inputs, and we determined how the LFPs generated by the network encoded information about the inputs. We found that this simulated recurrent network reproduced well the experimentally observed dependency of LFP information upon frequency. This network encoded the overall strength of the input into the power of gamma-range oscillations generated by inhibitory-excitatory neural interactions, and encoded slow variations in the input by entraining the network LFP at the corresponding frequency. This dynamical behavior accounted quantitatively for the independent information carried by high and low frequency LFPs, and for the experimentally observed cross-frequency coupling between phase of slow LFPs and the power of gamma LFPs. We also present new results showing that the model's dynamics also accounted for the extra visual information that the low-frequency LFP phase of spike firing carries beyond that carried by spike rates. Overall, our results suggest biological mechanisms by which cortex can multiplex information about naturalistic sensory environments.