The synaptic pathways in the striatum are central to basal ganglia functions including motor control, learning, and organization, action selection, the acquisition of motor skills, cognitive function, and emotion. Here we review the role of the striatum and its connections in motor learning and performance. The development of new techniques to record neuronal activity and animal models of motor disorders using neurotoxin, pharmacological, and genetic manipulations are revealing pathways that underlie motor performance and motor learning, as well as how they are altered by pathophysiological mechanisms. We discuss approaches that can be used to analyze complex motor skills, particularly in rodents, and identify specific questions central to understanding how striatal circuits mediate motor learning. Overview of the phases of motor learningThe goals of motor skills acquisition range from a predator learning to adjust speed to intercept a moving prey, a musician learning precise movements for performance, a person learning to ride a bicycle, or more habitual behaviors, such as habitually reaching for a coffee mug in a particular Accepted ArticleThis article is protected by copyright. All rights reserved cabinet in the kitchen 1 . These forms of learning require a series of steps, including the selection of a particular action by comparing the expected value of possible actions, executing the chosen action, and evaluating the result of the decision. With experience, we learn to associate sensory cues with rewarding or aversive events, and to optimize activity for a preferred outcome.As these steps can entail very complex behaviors, motor learning occurs through the acquisition of a sequence of simple actions or events (defined as 'chunks') necessary to accomplish a specific task and linking the information together into a single executable program 2,3 . Successful motor learning has been suggested to require transitions between four distinct phases 4 . The first phase involves random actions driven by motivation. During this phase, animals perform multiple trials with poor performance related to the outcome. The second phase involves insightful behavior, when a subject links a motor action with a goal, compares appropriate and inappropriate ways to achieve that goal, and begins to repeat the action. In the third phase, motor activity is adjusted to optimize the goal outcome: during this optimization phase, if the reward contingency is altered, the subject will easily learn to change strategies. In the fourth phase, the goal directed action becomes a skill or a habit: if the reward contingencies are altered at this phase, change in strategies becomes more difficult (Figure 1) 1,4-7 . Identification of specific brain regions in motor learning From cortex to basal gangliaThe motor cortex has long been considered the main player in motor activity, starting with the discovery by Wilder Penfield and Edwin Boldrey of motor-sensory representation of the entire human body in the cerebral cortex 8 . Through electrical stimulat...
The ability to identify and avoid environmental stimuli that signal danger is essential to survival. Our understanding of how the brain encodes aversive behaviors has been primarily focused on roles for the amygdala, hippocampus (HIPP), prefrontal cortex, ventral midbrain, and ventral striatum. Relatively little attention has been paid to contributions from the dorsal striatum (DS) to aversive learning, despite its well-established role in stimulus-response learning. Here, we review studies exploring the role of DS in aversive learning, including different roles for the dorsomedial and dorsolateral striatum in Pavlovian fear conditioning as well as innate and inhibitory avoidance (IA) behaviors. We outline how future investigation might determine specific contributions from DS subregions, cell types, and connections that contribute to aversive behavior.
The cerebellar cortex receives a widespread noradrenergic projection from the locus coeruleus, consistent with the evidence that the norepinephrine (NE) system is involved in the modulation of cerebellar function including motor learning (Abbott
The modulation of dopamine release from midbrain projections to the striatum has long been demonstrated in reward-based learning, but the synaptic basis of aversive learning is far less characterized. The cerebellum receives axonal projections from the locus coeruleus, and norepinephrine release is implicated in states of arousal and stress, but whether aversive learning relies on plastic changes in norepinephrine release in the cerebellum is unknown. Here we report that in mice, norepinephrine is released in the cerebellum following an unpredicted noxious event (a foot-shock) and that this norepinephrine release is potentiated powerfully with fear acquisition as animals learn that a previously neutral stimulus (tone) predicts the aversive event. Importantly, both chemogenetic and optogenetic inhibition of the locus coeruleus-cerebellum pathway block fear memory without impairing motor function. Thus, norepinephrine release in the cerebellum is modulated by experience and underlies aversive learning.
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