Neural Code of Motor Planning and Execution during Goal-Directed Movements in Crows

Abstract

The planning and execution of head-beak movements are vital components of bird behavior. They require integration of sensory input and internal processes with goal-directed motor output. Despite its relevance, the neurophysiological mechanisms underlying action planning and execution outside of the song system are largely unknown. We recorded single-neuron activity from the associative endbrain area nidopallium caudolaterale (NCL) of two male carrion crows (Corvus corone) trained to plan and execute head-beak movements in a spatial delayed response task. The crows were instructed to plan an impending movement toward one of eight possible targets on the left or right side of a touchscreen. In a fraction of trials, the crows were prompted to plan a movement toward a self-chosen target. NCL neurons signaled the impending motion direction in instructed trials. Tuned neuronal activity during motor planning categorically represented the target side, but also specific target locations. As a marker of intentional movement preparation, neuronal activity reliably predicted both target side and specific target location when the crows were free to select a target. In addition, NCL neurons were tuned to specific target locations during movement execution. A subset of neurons was tuned during both planning and execution period; these neurons experienced a sharpening of spatial tuning with the transition from planning to execution. These results show that the avian NCL not only represents high-level sensory and cognitive task components, but also transforms behaviorally-relevant information into dynamic action plans and motor execution during the volitional perception-action cycle of birds.SIGNIFICANCE STATEMENT Corvid songbirds have become exciting new models for understanding complex cognitive behavior. As a key neural underpinning, the endbrain area nidopallium caudolaterale (NCL) represents sensory and memory-related task components. How such representations are converted into goal-directed motor output remained unknown. In crows, we report that NCL neurons are involved in the planning and execution of goal-directed movements. NCL neurons prospectively signaled motion directions in instructed trials, but also when the crows were free to choose a target. NCL neurons showed a target-specific sharpening of tuning with the transition from the planning to the execution period. Thus, the avian NCL not only represents high-level sensory and cognitive task components, but also transforms relevant information into action plans and motor execution.

Keywords: NCL; bird; crow; motor execution; motor planning; single-neuron recordings.