Corticostriatal dynamics encode the refinement of specific behavioral variability during skill learning

Abstract

Learning to perform a complex motor task requires the optimization of specific behavioral features to cope with task constraints. We show that when mice learn a novel motor paradigm they differentially refine specific behavioral features. Animals trained to perform progressively faster sequences of lever presses to obtain reinforcement reduced variability in sequence frequency, but increased variability in an orthogonal feature (sequence duration). Trial-to-trial variability of the activity of motor cortex and striatal projection neurons was higher early in training and subsequently decreased with learning, without changes in average firing rate. As training progressed, variability in corticostriatal activity became progressively more correlated with behavioral variability, but specifically with variability in frequency. Corticostriatal plasticity was required for the reduction in frequency variability, but not for variability in sequence duration. These data suggest that during motor learning corticostriatal dynamics encode the refinement of specific behavioral features that change the probability of obtaining outcomes.

DOI: http://dx.doi.org/10.7554/eLife.09423.001

eLife digest

Learning a new motor skill typically involves a degree of trial and error. Movements that achieve the desired outcome—from catching a ball to playing scales—are repeated and refined until they can be produced on demand. This process is made more difficult as the activity of individual neurons and muscle fibers can vary at random, and this reduces the ability to reproduce a given movement precisely and reliably.

It has been suggested that the motor system overcomes this problem by identifying those parts of a task that are essential for achieving the end goal, and then focusing resources on reducing the variability in the performance of those parts alone. Santos et al. now provide direct evidence in support of this proposal by recording the activity of neurons in motor regions of the mouse brain as the animals learn a lever pressing task.

By giving mice a food reward each time they pressed the lever four times in a row, Santos et al. trained the animals to press the lever in bouts. The experiment was then slightly modified, so that the mice had to perform the four lever presses more rapidly in order to earn their reward. Consistent with predictions, the average speed of lever pressing initially varied greatly, but this variability decreased as the animals learned the task. By contrast, the total duration of individual bouts of lever pressing—which depends largely on the number of times the mice press the lever—was just as variable after training as before.

A similar pattern emerged for the activity of individual motor neurons in the mouse brain. Whereas their activity initially varied greatly, this variability decreased over training. Moreover, it became increasingly linked to the variability in the speed of lever pressing, but not with the variability in the duration of individual bouts.

The work of Santos et al. has thus shown in real time how the motor system focuses its efforts on reducing variability in those specific parts of a task that are essential for achieving a goal. Without a process called corticostriatal plasticity, by which the motor system adapts, mice could not refine this variability.

DOI: http://dx.doi.org/10.7554/eLife.09423.002