Bottom-up and top-down inputs drive the variability of cortical neurons
Neurons in the cerebral cortex respond inconsistently to a repeated sensory stimulus, so how can they provide the basis for stable sensory experiences? Although the exact causes of neuronal response variability are unknown, the consistency with which it has been observed across a variety of cortical regions has encouraged the general view that each cell produces random spike patterns that noisily represent its response rate. In contrast to this view, we discovered that reversibly inactivating sources of either bottom-up (V2-to- MT) or top-down (V2-to-V1) input to cortical visual areas in the alert primate reduced both the spike train irregularity and the trial-to- trial variability of single neurons. A simple network model of integrate-and- fire neurons in which a fraction of the pre-synaptic inputs are silenced can reproduce this reduction in variability, provided that there exist temporal correlations primarily within, but not between, excitatory and inhibitory input pools. A large component of the variability of cortical neurons can therefore be ascribed to synchronous input produced by signals arriving from multiple sources. Taken together, our results impose strong constraints on theories of neuronal variability by causally linking the presence of bottom-up and top-down input to the spiking statistics of cortical neurons.