Scientific Understanding of Consciousness
Basal Ganglia and Corticostriatal Pasticity in Learning
Nature, 483, Pages: 331–335 (15 March 2012)
Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills
Aaron C. Koralek, Xin Jin, John D. Long II, Rui M. Costa & Jose M. Carmena
Helen Wills Neuroscience Institute, University of California, Berkeley, California 94720, USA
Department of Electrical Engineering and Computer Sciences, University of California, Berkeley, California 94720, USA
Program in Cognitive Science, University of California, Berkeley, California 94720, USA
UC Berkeley and UC San Francisco Joint Graduate Group in Bioengineering, University of California, Berkeley, California 94720, USA
Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health, 5625 Fishers Lane, Bethesda, Maryland 20892-9412, USA
Champalimaud Neuroscience Programme, Champalimaud Center for the Unknown, Avenida de Brasília, 1400-038 Lisbon, Portugal
The ability to learn new skills and perfect them with practice applies not only to physical skills but also to abstract skills, like motor planning or neuroprosthetic actions. Although plasticity in corticostriatal circuits has been implicated in learning physical skills, 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.
The ability to learn new actions and perfect them with practice allows us to master skills like playing the piano or riding a bicycle. Learning these skills usually implies moving faster, more accurately and less variably. However, mastering other types of skills, like playing board games or controlling neuroprosthetic devices, often does not directly involve changes in physical movement. Cortico-basal ganglia circuits have been implicated in the learning, selection and execution of physical skills. In particular, plasticity in the motor cortices and the striatum, the major input region of the basal ganglia, has been shown to accompany the learning of physical skills. The motor cortex and frontal cortices have also been implicated in the learning of abstract skills, and in learning to control neuroprosthetic devices irrespective of physical movement. Some studies suggest that not only cortical areas, but also the striatum, are involved in learning abstract skills. However, it is still unclear if the striatum is required for abstract skill learning, and if corticostriatal circuits undergo plasticity during the learning of such skills as they do during the learning of physical skills. Here, we use a novel behavioural task in conjunction with electrophysiology and genetic manipulation in rodents to investigate the role of corticostriatal circuits and corticostriatal plasticity in the learning of intentional neuroprosthetic actions: that is, actions performed with disembodied actuators based on the modulation of specific neural activity and irrespective of physical movement.
We used a novel operant task in rodents to demonstrate that corticostriatal networks exhibit profound plasticity during the learning of intentional neuroprosthetic skills and, further, that disrupting this plasticity impairs learning. This adds great support to the claims that cortico-basal ganglia circuits play a role in abstract cognitive processes. We observed that dorsal striatum (DS) neurons strongly modulated their activity in relation to M1 activity, even when the latter was dissociated from physical movements, suggesting that the striatum is important for learning and selecting abstract actions that are controlled by cortical output. Hence, these data suggest that cortico-basal ganglia circuits may be involved in learning mental actions and skills that do not require physical movement, indicating that they may have a broader function involved in intention and decision-making than previously acknowledged.
Our results also have important implications for the field of brain–machine interfaces. The abstract actions investigated here form the basis for skilful neuroprosthetic control and, as we have shown here, they recruit elements of the natural motor system outside of M1. Thus, our results suggest that neuroprosthetic movements capitalize on the neural circuitry for motor learning and therefore have great potential to feel naturalistic, generalize well to novel movements and environments, and benefit from our nervous system’s highly developed storage and retrieval mechanisms for skilled behaviour.
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