Corticostriatal plasticity is necessary for learning intentional neuroprosthetic skills

Abstract

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 skills2–4, it remains unclear if similar circuits or processes are required for abstract skill learning. We utilized a novel behavioral paradigm 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, demonstrated that these learned neuroprosthetic actions were intentional and goal-directed, rather than habitual. Striatal neurons changed their activity with learning, with more neurons modulating their activity in relation to target-reaching as learning progressed. Concomitantly, strong relations between the activity of neurons in motor cortex and the striatum emerged. Specific deletion of striatal NMDA receptors impaired the development of this corticostriatal plasticity, and disrupted 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.

Closed-loop brain training: the science of neurofeedback

“…Functional and structural changes in the dorsomedial striatum have been shown to be associated with the early phase, whereas such changes in the dorsolateral striatum have been shown to be associated with the late phase. Recently, similar changes have been observed in neurofeedback learning in animals 45 and humans 85 (FIG. 2), providing support to this theory.…”

“…The specificity of the trained neural substrate was first noted in a study involving non-human primates 44 , which showed that the regulation of single-cell firing in the motor cortex could be learned. The local specificity of learned physiological regulation at the microscopic level was later confirmed by a series of impressive experiments in which rats were rewarded for increasing the firing rate of a cell in the motor cortex and simultaneously decreasing the firing rate of an adjacent cell 45 . Another study in rats showed that neurofeedback could be used to induce selective temporal coherence between neurons in M1 and in the dorsal striatum 46 .…”

“…The study showed that learning SCP control correlates with the activation of striatal and motor networks that are related to the associative binding of behaviour to the reward. These human studies are complemented by animal work 45,46 demonstrating complete abolition of neuro feedback learning with NMDA receptor (NMDAR) blockade in the basal ganglia (see below and BOX 3).…”

“…Recently, there have been proposals to view neurofeedback and braincomputer interfaces (BCI) or brain-machine interfaces (BMI) learning 45,207 within the framework of cognitive skill learning 208,209 . According to this proposal, neurofeedback learning involves an initial phase of rapid change in performance and a late phase of more gradual improvement 209 as the skill is consolidated and performance asymptotes.…”

The self-regulating brain and neurofeedback: Experimental science and clinical promise

“…Moreover, comparing veritable feedback with no feedback , inversely proportional feedback , or feedback from a distinct brain region (Paret et al, 2014), revealed similar neural changes from baseline to the first trial in both experimental and control groups. On the other hand, findings from both human and animal studies suggest that explicit techniques are unnecessary and that contingent feedback alone is responsible for neural regulation (Caria et al, 2010;Koralek, Jin, Long, Costa, & Carmena, 2012). Thus, the degree to which explicit mental strategies relate to learned brain modulation remains unclear.…”