Emergent reliability in sensory cortical coding and inter-area communication

Reliable sensory discrimination must arise from high-fidelity neural representations and communication between brain areas. However, how neocortical sensory processing overcomes the substantial variability of neuronal sensory responses remains undetermined(1-6). Here we imaged neuronal activity in eight neocortical areas concurrently and over five days in mice performing a visual discrimination task, yielding longitudinal recordings of more than 21,000 neurons. Analyses revealed a sequence of events across the neocortex starting from a resting state, to early stages of perception, and through the formation of a task response. At rest, the neocortex had one pattern of functional connections, identified through sets of areas that shared activity cofluctuations(7,8). Within about 200 ms after the onset of the sensory stimulus, such connections rearranged, with different areas sharing cofluctuations and task-related information. During this short-lived state (approximately 300 ms duration), both inter-area sensory data transmission and the redundancy of sensory encoding peaked, reflecting a transient increase in correlated fluctuations among task-related neurons. By around 0.5 s after stimulus onset, the visual representation reached a more stable form, the structure of which was robust to the prominent, day-to-day variations in the responses of individual cells. About 1 s into stimulus presentation, a global fluctuation mode conveyed the upcoming response of the mouse to every area examined and was orthogonal to modes carrying sensory data. Overall, the neocortex supports sensory performance through brief elevations in sensory coding redundancy near the start of perception, neural population codes that are robust to cellular variability, and widespread inter-area fluctuation modes that transmit sensory data and task responses in non-interfering channels.

Automated summary

This study investigated the process of neocortical sensory processing during visual discrimination tasks in mice. The results showed that the neocortex had a specific functional connectivity pattern at rest, which rearranged after the onset of sensory stimulus. A short-lived state with increased inter-area sensory data transmission and sensory encoding redundancy was observed, followed by a more stable visual representation that was robust to day-to-day variations in individual cell responses. In addition, a global fluctuation mode conveyed the upcoming response of the mouse to every area examined. These findings suggest that the neocortex supports sensory performance through dynamic changes in connectivity and robust population codes.