An internal model for canceling self-generated sensory input in freely behaving electric fish

Abstract

Internal models that predict the sensory consequences of motor actions are vital for sensory, motor, and cognitive functions. However, the relationship between motor action and sensory input is complex, often varying from one moment to another depending on the state of the animal and the environment. The neural mechanisms for generating predictions under such challenging, real-world conditions remain largely unknown. Using novel methods for underwater neural recording, a quantitative analysis of unconstrained behavior, and computational modeling, we provide evidence for an unexpectedly sophisticated internal model at the first stage of active electrosensory processing in mormyrid fish. Closed-loop manipulations reveal that electrosensory lobe neurons are capable of simultaneously learning and storing multiple predictions of the sensory consequences of motor commands specific to different sensory states. These results provide mechanistic insights into how internal motor signals and information about the sensory environment are combined within a cerebellum-like circuitry to predict the sensory consequences of natural behavior.

Keywords: cerebellum; corollary discharge; electric fish; internal model; neuroethology; sensory processing.