Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills

Abstract

A novel study in rodents suggests that corticostriatal plasticity is necessary for abstract skill learning. Corticostriatal circuits are known to be involved in physical skill learning, but it is not clear whether these pathways are also important for abstract skill learning. Here, Jose Carmena and colleagues train mice to manipulate an auditory cue towards a goal using activity in the primary motor cortex, but without overt movements. Striatal neurons changed their activity throughout training, with an increasing number modulating their output on the basis of whether the target was reached or not. This modulation and learning was based on standard plasticity mechanisms, as demonstrated when the disruption of NMDA-receptor action eroded the animal's ability to learn the skill. These findings show that corticostriatal plasticity is central to abstract skill learning, and imply that the nervous system's storage and retrieval mechanisms, developed for skilled behaviour, may be transferrable to the control of neuroprosthetic movements. The ability to learn new skills and perfect them with practice applies not only to physical skills but also to abstract skills1, like motor planning or neuroprosthetic actions. Although plasticity in corticostriatal circuits has been implicated in learning physical skills2,3,4, it remains unclear if similar circuits or processes are required for abstract skill learning. Here we use a novel behavioural task in rodents to investigate the role of corticostriatal plasticity in abstract skill learning. Rodents learned to control the pitch of an auditory cursor to reach one of two targets by modulating activity in primary motor cortex irrespective of physical movement. Degradation of the relation between action and outcome, as well as sensory-specific devaluation and omission tests, demonstrate that these learned neuroprosthetic actions are intentional and goal-directed, rather than habitual. Striatal neurons change their activity with learning, with more neurons modulating their activity in relation to target-reaching as learning progresses. Concomitantly, strong relations between the activity of neurons in motor cortex and the striatum emerge. Specific deletion of striatal NMDA receptors impairs the development of this corticostriatal plasticity, and disrupts the ability to learn neuroprosthetic skills. These results suggest that corticostriatal plasticity is necessary for abstract skill learning, and that neuroprosthetic movements capitalize on the neural circuitry involved in natural motor learning.