Operant conditioning of cortical waves through a brain-machine interface

ABSTRACT At the surface of the cerebral cortex, mesoscopic scale brain dynamics are characterized by waves of synchronized neuronal activity. These waves have been shown to impact the processing of sensory information, but can they be actively shaped by the subject in a goal directed manner? To address this question, we designed a fast widefield optical brain-machine interface that enables real-time detection and reinforcement of individual traveling waves that display a specific displacement at the surface of the mouse somatosensory-motor cortex. Mice learned to generate such Conditioned Waves, which became progressively more stereotyped and were preceded by a characteristic suppression of cortical activity. Conditioned Waves were typically related to a limb movement that triggered somatosensory inputs. However, only the movements that occurred in conjunction with the identified suppressive cortical state could drive Conditioned Waves. This work demonstrates that propagating cortical waves can be subject to operant control. It provides evidence for the plasticity and functional relevance of large-scale cortical dynamics, and establishes a new paradigm for manipulating mesoscale brain activity.