Fluctuating internal states mediate neural-behavioral covariations in V1

Our perception of the world depends on a complex interplay between external sensory inputs and our internal states. How and where in the brain the interactions between internal states and sensory inputs are implemented remain open questions. To study the neural basis of these interactions, we used whole-cell recording to measure membrane potential (Vm) of single V1 neurons in macaque monkeys performing a reaction-time detection task. We find that most V1 neurons gradually depolarize in preparation for target onset. Remarkably, trial-to-trial variations in this preparatory buildup are correlated with the monkey’s reaction times, and these covariations are similar when the animal selects a target in either hemifield. This finding implies that variation in the preparatory buildup are shared between hemispheres and are unrelated to a competitive spatial attention mechanism. Further, we find that while the gradual buildup is largely uncorrelated with the animals’ choices, transient fluctuations in Vm around target-evoked response onset time are correlated with choice. The dependence of these Vm-to-choice covariations on the visual stimulus is consistent with a multiplicative gain, reflecting a variable internal state that interacts with variable sensory signals. Overall, our results reveal surprising covariations between the membrane potential of single V1 neurons and behavior, and that these covariations are mediated by mixture of additive and multiplicative task-related modulations of incoming sensory information.