State Dependence of Stimulus-Induced Variability Tuning in Macaque MT

Average response properties of cortical sensory neurons such as firing rate and feature tuning are known to change with behavioral state. Here, we show anesthetic state also modifies the tuning of the variance of spiking responses in a fashion that is neither predicted by a Poisson model of spike count variance nor the neuron’s tuning curve. Neurons recorded in the visual motion-sensitive middle temporal cortex (area MT) in sufentanil-anesthetized non-human primates tend to have lower average spike counts and greater trial-to-trial variability in response to constant direction stimuli compared to the alert state. Anesthesia-induced increases in response variation create supra-Poisson variance-to-mean ratios (Fano factors) on time scales of ∼ 250 ms. We find that alert-state MT neurons have higher mean firing rates, lower spike count variance, and largely sub-Poisson variability that is stimulus-dependent and cannot be explained by firing rate differences alone. The absence of such stimulus-induced variability tuning in the anesthetized state suggests different sources of variability between states. A simple model explains qualitative shifts in the distribution of observed Fano factors in the two states via a suppression in the variance of gain fluctuations in the alert state.