Brain State Control by Closed-Loop Environmental Feedback

Abstract: Brain state regulates sensory processing and motor control for adaptive behavior. Internal mechanisms of brain state control are well studied, but the role of external modulation from the environment is not well understood. Here, we examined the role of closed-loop environmental (CLE) feedback, in comparison to open-loop sensory input, on brain state and behavior in diverse vertebrate systems. In fictively swimming zebrafish, CLE feedback for optomotor stability controlled brain state by reducing coherent neuronal activity. The role of CLE feedback in brain state was also shown in a model of rodent active whisking, where brief interruptions in this feedback enhanced signal-to-noise ratio for detecting touch. Finally, in monkey visual fixation, artificial CLE feedback suppressed stimulus-specific neuronal activity and improved behavioral performance. Our findings show that the environment mediates continuous closed-loop feedback that controls neuronal gain, regulating brain state, and that brain function is an emergent property of brain-environment interactions.