Trends in Cognitive Sciences
ReviewPerceptual learning, motor learning and automaticityCortical and basal ganglia contributions to habit learning and automaticity
Section snippets
The classical view of automaticity
Almost all cognitive or motor skills are executed faster and more accurately the more they are practiced. Eventually these improvements become so great that the behavior is executed habitually or automatically (see Box 1 for some behavioral criteria of habits and automatic behaviors). Such dramatic improvements following practice have been documented in motor and cognitive behaviors as diverse as cigar rolling and proving geometry theorems [1].
Interest in the neural basis of automaticity has a
The role of the associative striatum in habit learning and automaticity
One of the first revisions to the classical view occurred with the discovery that there are significant subcortical contributions to initial learning. For example, there is solid evidence that the initial learning of many skills depends critically on the striatum (Box 2; for reviews, see e.g. 11, 12, 13).
More recent evidence indicates that associative and sensorimotor regions of the striatum might play different roles in learning and automaticity (see the following section for a discussion of
The role of the sensorimotor striatum in habit learning and automaticity
Whereas the associative striatum seems more critical to early than late stages of learning, the sensorimotor striatum shows the opposite pattern. For example, Miyachi et al. [14] found that most striatal neurons that responded more strongly after over-learning a motor sequence were in the sensorimotor striatum (Figure 1). Furthermore, temporary inactivation of the sensorimotor striatum does not interfere with the learning of new motor sequences, but it does disrupt the execution of previously
Dopamine and cortico-striatal plasticity
Cortico-striatal synapses can undergo both strengthening (long-term potentiation, or LTP), and weakening (long-term depression, or LTD; 32, 33). Cortical high-frequency stimulation has most frequently been observed to produce LTD at cortico-striatal synapses. However, when dopamine is applied in brief pulses coinciding with the time of presynaptic stimulation and postsynaptic depolarization of the striatal cell, cortico-striatal synapses show potentiation rather than depression [33].
When
Dopamine and habit expression
Dopamine plays a role not only in reinforced learning, but also in the expression of previously learned behaviors 42, 43, 44. Of particular interest, dopamine seems to play a diminishing role in behavioral expression over the course of extended training 38, 42. For example, some human subjects with Parkinson's disease are able to emit an automatic motor response when presented with a familiar visual cue (e.g. kicking a ball), despite difficulties in initiating novel voluntary movements [45]. As
The role of cortex in habit expression and automaticity
Many neuroimaging studies have examined cortical activity during practice on a cognitive or motor task (for a review, see [51]). Depending on the task, some studies have reported a general decrease in cortical activity 52, 53, 54, 55, a few have reported increases 56, 57, 58, 59, and some have reported a more complex redistribution where activity increases in some areas and decreases in others 60, 61, 62. Kelly and Garavan [51] noted that decreases are often observed in prefrontal and parietal
Concluding remarks
Understanding the neural basis of automaticity is tremendously important, not only from a theoretical perspective, but also because many societal problems are due to maladaptive automatic behaviors. For example, a complicating factor in treating drug addiction is that many aspects of drug-seeking behaviors become automatized 79, 80, 81, 82; this is also true of many other harmful habits. Thus, an accurate model of how automaticity develops could lead to new behavioral and pharmacological
Acknowledgements
Preparation of this article was supported in part by National Institute of Health Grant R01 MH3760-2 and by support from the US Army Research Office through the Institute for Collaborative Biotechnologies under grant W911NF-07-1-0072.
References (86)
Contributions of the basal ganglia and functionally related brain structures to motor learning
Behav. Brain. Res.
(2009)- et al.
The role of the basal ganglia in category learning
- et al.
The basal ganglia
Parallel and interactive learning processes within the basal ganglia: Relevance for the understanding of addiction
Behav. Brain Res.
(2009)Birdbrains could teach basal ganglia research a new song
Trends Neurosci.
(2005)Dopamine-mediated regulation of corticostriatal synaptic plasticity
Trends Neurosci.
(2007)Neural mechanisms of reward-related motor learning
Curr. Opin. Neurobiol.
(2003)Getting formal with dopamine and reward
Neuron
(2002)Stimulus-response and response-outcome learning mechanisms in the striatum
Behav. Brain Res.
(2009)- et al.
Interaction of raclopride and preparatory interval effects on simple reaction time performance
Behav. Brain Res.
(2006)
Dopamine gating of glutamatergic sensorimotor and incentive motivational input signals to the striatum
Behav. Brain Res.
Learning arbitrary visuomotor associations: temporal dynamic of brain activity
Neuroimage
Inactivation of the infralimbic prefrontal cortex reinstates goal-directed responding in overtrained rats
Behav. Brain Res.
Pharmacology and behavioral pharmacology of the mesocortical dopamine system
Prog. Neurobiol.
Rapid sampling of extracellular dopamine in the rat prefrontal cortex during food consumption, handling and exposure to novelty
Brain Res.
It could be habit forming: Drugs of abuse and synaptic plasticity
Trends Neurosci.
Stimulant-induced adaptations in neostriatal matrix and striosome systems: Transiting from instrumental responding to habitual behavior in drug addiction
Neurobiol. Learn. Mem.
Acquisition of intellectual and perceptual-motor skills
Annu. Rev. Psychol.
The integrative action of the nervous system
Skill representation in the primary motor cortex after long-term practice
J. Neurophysiol.
Automaticity: A theoretical and conceptual analysis
Psychol. Bull.
The automaticity of social life
Curr. Dir. Psychol. Sci.
Inside the brain of an elite athlete: The neural processes that support high achievement in sports
Nat. Rev. Neurosci.
Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning
Ann. N. Y. Acad. Sci.
The primate cortico-cerebellar system: anatomy and function
Nat. Rev. Neurosci.
Functional anatomy of motor skill learning
Learning and memory functions of the basal ganglia
Annu. Rev. Neurosci.
Differential activation of monkey striatal neurons in the early and late stages of procedural learning
Exp. Brain Res.
Distinct basal ganglia territories are engaged in early and advanced motor sequence learning
Proc. Natl. Acad. Sci. U. S. A.
The neural correlates of motor skill automaticity
J. Neurosci.
How self-initiated memorized movements become automatic: A functional MRI study
J. Neurophysiol.
Differential roles of monkey striatum in learning of sequential hand movement
Exp. Brain Res.
Reward-guided learning beyond dopamine in the nucleus accumbens: The integrative functions of cortico-basal ganglia networks
Eur. J. Neurosci.
The role of the dorsomedial striatum in instrumental conditioning
Eur. J. Neurosci.
Lesions of dorsolateral striatum preserve outcome expectancy but disrupt habit formation in instrumental learning
Eur. J. Neurosci.
Loss of lever press-related firing of rat striatal forelimb neurons after repeated sessions in a lever pressing task
J. Neurosci.
Activity of striatal neurons reflects dynamic encoding and recoding of procedural memories
Nature
Changes in activity of the striatum during formation of a motor habit
Eur. J. Neurosci.
Macro-architecture of basal ganglia loops with the cerebral cortex: Use of rabies virus to reveal multisynaptic circuits
Prog. Brain Res.
Plastic corticostriatal circuits for action learning: What's dopamine got to do with it?
Ann. N. Y. Acad. Sci.
The role of the basal ganglia in habit formation
Nat. Rev. Neurosci.
Cited by (340)
How do alterations of the basal ganglia affect procedural memory in Tourette syndrome?
2024, Current Opinion in Behavioral SciencesSB-258585 reduces food motivation while blocking 5-HT<inf>6</inf> receptors in the non-human primate striatum
2024, Progress in Neuro-Psychopharmacology and Biological PsychiatryGolf skill learning: An external focus of attention enhances performance and motivation
2024, Psychology of Sport and ExerciseCortico-spinal modularity in the parieto-frontal system: A new perspective on action control
2023, Progress in Neurobiology