Timing Precision in Population Coding of Natural Scenes in the Early Visual System

The timing of spiking activity across neurons is a fundamental aspect of the neural population code. Individual neurons in the retina, thalamus, and cortex can have very precise and repeatable responses but exhibit degraded temporal precision in response to suboptimal stimuli. To investigate the functional implications for neural populations in natural conditions, we recorded in vivo the simultaneous responses, to movies of natural scenes, of multiple thalamic neurons likely converging to a common neuronal target in primary visual cortex. We show that the response of individual neurons is less precise at lower contrast, but that spike timing precision across neurons is relatively insensitive to global changes in visual contrast. Overall, spike timing precision within and across cells is on the order of 10 ms. Since closely timed spikes are more efficient in inducing a spike in downstream cortical neurons, and since fine temporal precision is necessary to represent the more slowly varying natural environment, we argue that preserving relative spike timing at a ∼10-ms resolution is a crucial property of the neural code entering cortex.