Cortical and basal ganglia contributions to habit learning and automaticity

doi:10.1016/j.tics.2010.02.001

Trends in Cognitive Sciences

Volume 14, Issue 5, May 2010, Pages 208-215

https://doi.org/10.1016/j.tics.2010.02.001 Get rights and content

In the 20th century it was thought that novel behaviors are mediated primarily in cortex and that the development of automaticity is a process of transferring control to subcortical structures. However, evidence supports the view that subcortical structures, such as the striatum, make significant contributions to initial learning. More recently, there has been increasing evidence that neurons in the associative striatum are selectively activated during early learning, whereas those in the sensorimotor striatum are more active after automaticity has developed. At the same time, other recent reports indicate that automatic behaviors are striatum- and dopamine-independent, and might be mediated entirely within cortex. Resolving this apparent conflict should be a major goal of future research.

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.

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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

The role of the associative striatum in habit learning and automaticity

The role of the sensorimotor striatum in habit learning and automaticity

Dopamine and cortico-striatal plasticity

Dopamine and habit expression

The role of cortex in habit expression and automaticity

Concluding remarks

Acknowledgements

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The automaticity of social life

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Review
Perceptual learning, motor learning and automaticity
Cortical and basal ganglia contributions to habit learning and automaticity