Balanced bidirectional optogenetics reveals the causal impact of cortical temporal dynamics in sensory perception

Abstract

Whether the fast temporal dynamics of neural activity in brain circuits causally drive perception and cognition remains one of most longstanding unresolved questions in neuroscience1-6. While some theories posit a timing code in which dynamics on the millisecond timescale is central to brain function, others instead argue that mean firing rates over more extended periods (a rate code) carry most of the relevant information. Existing tools, such as optogenetics, can be used to alter temporal structure of neural dynamics7, but they invariably change mean firing rates, leaving the interpretation of such experiments ambiguous. Here we developed and validated a new approach based on balanced, bidirectional optogenetics that can alter temporal structure of neural dynamics while mitigating effects on mean activity. Using this new approach, we found that selectively altering cortical temporal dynamics substantially reduced performance in a sensory perceptual task. These results demonstrate that endogenous temporal dynamics in the cortex are causally required for perception and behavior. More generally, this new bidirectional optogenetic approach should be broadly useful for disentangling the causal impact of different timescales of neural dynamics on behavior.