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

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Abstract
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. Neurons convey information about the world in the form of trains of action potentials (spikes). These trains are highly repeatable when the same stimulus is presented multiple times, and this temporal precision across repetitions can be as fine as a few milliseconds. It is usually assumed that this time scale also corresponds to the timing precision of several neighboring neurons firing in concert. However, the relative timing of spikes emitted by different neurons in a local population is not necessarily as fine as the temporal precision across repetitions within a single neuron. In the visual system of the brain, the level of contrast in the image entering the retina can affect single-neuron temporal precision, but the effects of contrast on the neural population code are unknown. Here we show that the temporal scale of the population code entering visual cortex is on the order of 10 ms and is largely insensitive to changes in visual contrast. Since closely timed spikes are more efficient in inducing a spike in downstream cortical neurons, and since fine temporal precision is necessary in representing the more slowly varying natural environment, preserving relative spike timing at a ∼10-ms resolution may be a crucial property of the neural code entering cortex.