Coding of Serial Order by Neostriatal Neurons: A “Natural Action” Approach to Movement Sequence

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Abstract
The neostriatum controls behavioral sequencing, or action syntax, as well as simpler aspects of movement. Yet the precise nature of the neostriatums role in sequencing remains unclear. Here we used a “natural action” approach that combined electrophysiological and neuroethological techniques. We identified neostriatal neurons that code the serial order of natural movement sequences of rats. During grooming behavior, rats emit complex but highly predictable species-specific sequences of movements, termed “syntactic chains.” Neuronal activity of 41% of cells in the dorsolateral and ventromedial neostriatum coded the sequential pattern of syntactic chains. Only 14% coded simple motor properties of grooming movements. Neurons fired preferentially during syntactic chains compared with similar grooming movements made in different sequential order or to behavioral resting. Sequential coding differed between the dorsolateral and ventromedial neostriatum. Neurons in the dorsolateral site increased firing by 116% during syntactic chains, compared with only a 30% increase by neurons in the ventromedial site, and dorsolateral neurons showed strongest coding of grooming syntax by several additional criteria. These data demonstrate that neostriatal neurons code abstract properties of serial order for natural movement and support the hypothesis that the dorsolateral neostriatum plays a special role in implementing action syntax.