Dissociating the contributions of sensorimotor striatum to automatic and visually-guided motor sequences

Abstract

The ability to sequence discrete movements in new ways enables rich and adaptive behavior. Such flexibility can be computationally costly and result in halting performances. Practicing the same motor sequence repeatedly, however, can render its execution precise, fast, and effortless, i.e., ‘automatic’. The basal ganglia are thought to underlie both flexible and automatic motor sequences, yet how their contributions differ across these modes is unclear. We parse this in rats trained to perform the same motor sequence in both modes, focusing on the sensorimotor striatum. Neural recordings revealed a kinematic code independent of execution mode. While lesions affected the detailed kinematics across modes, they disrupted high-level sequential structure for automatic but not visually-guided flexible behaviors. These results suggest that while the basal ganglia contribute to learned movement kinematics and are essential for ‘automatic’ motor skills, they can be dispensable for the flexible sequencing of discrete motor elements.

Differential kinematic coding in sensorimotor striatum across species-typical and learned behaviors reflects a difference in control

“…While we did not find evidence for the DLS controlling species-typical behaviors, our analysis of motor skills suggested, in concert with earlier studies 36,38,39,41 , that it is essential for shaping learned movement kinematics. Densely innervated by dopaminergic neurons signaling reward prediction error 100 , sensorimotor striatum could learn to map state input from cortex and thalamus to activity patterns that help shape future actions in adaptive and task-specific ways 2,101 .…”

“…Our study considers a fundamental distinction in how the BG contribute to movement, specifically asking whether this region is essential for general control or specialized for acquiring and controlling learned motor skills (Fig 1). Using high-resolution 3D kinematic tracking in freely behaving rats, we showed that lesions of the sensorimotor striatum did not affect the expression ( 36,41 ). To probe the neurophysiological correlates of this difference, we recorded from the same cells in sensorimotor striatum during both learned and species-typical behaviors.…”

“…Our results thus far indicate that DLS lesions do not affect the kinematics or frequency of species-typical behaviors. As this is in stark contrast to our prior work on highly stereotyped learned movement patterns 36,38,51 , we developed an analysis pipeline to directly, in an 'apples-to-apples' manner, compare the effects of DLS lesions on stereotyped species-typical behaviors and similarly precise movement patterns observed after lengthy training on a specific motor task. We utilized a previously collected dataset from rats in which their movements were carefully tracked as they performed a well-practiced learned movement pattern acquired in our timed lever-pressing task 5736 .…”

“…And likewise, studies in rodents likewise point to an essential role for the sensorimotor striatum (termed dorsolateral striatum, or DLS) in the acquisition and faithful execution of learned skills [38][39][40] . For example, in a lever-pressing task in which rats acquire stereotyped and idiosyncratic task-specific movement patterns, DLS lesions in expert animals caused a reversion to species-typical movements expressed early in learning 36,41 . Additionally, DLS activity during the task was closely linked to the animals' movements and could account for trial-to-trial kinematic variability 36,41 , consistent with DLS specifying the details of the learned movement patterns.…”

Motor cortex is required for flexible but not automatic motor sequences

“…This allows us to probe motor cortex's contributions to higherlevel functions without the ambiguity of it being necessary for basic movement control. Second, rats can master fairly complex discrete sequence production tasks 29 akin to those frequently used in human and non-human primate studies of motor sequence learning and execution 30,31 . The rich structure of such tasks allows us to probe motor cortex's contributions to the flexible sequencing of motor elements.…”