Review
Perceptual learning, motor learning and automaticity
Switching from automatic to controlled behavior: cortico-basal ganglia mechanisms

https://doi.org/10.1016/j.tics.2010.01.006Get rights and content

Most daily tasks are performed almost automatically, but occasionally it is necessary to alter a routine if something changes in the environment and the routine behavior becomes inappropriate. Such behavioral switching can occur either retroactively based on error feedback or proactively by detecting a contextual cue. Recent imaging and electrophysiological data in humans and monkeys support the view that the frontal cortical areas play executive roles in behavioral switching. The anterior cingulate cortex acts retroactively and the pre-supplementary motor area acts proactively to enable behavioral switching. The lateral prefrontal cortex reconfigures cognitive processes constituting the switched behavior. The subthalamic nucleus and the striatum in the basal ganglia mediate these cortical signals to achieve behavioral switching. We discuss how breaking a routine to allow more adaptive behavior requires a fine-tuned recruitment of the frontal cortical-basal ganglia neural network.

Section snippets

Breaking a routine: difficult but crucial

Driving to one's workplace is an easy task: a task that most of us do on a daily basis for several years. On our journey to work we see the same houses, the same trees and the same traffic lights. We might not be aware of our car accelerating or slowing down, despite being the driver. If there is unexpected congestion in the main road ahead then we can quickly decide to avoid the traffic jam by changing our route. But if the decision is late, even by only a second, the chance to turn and avoid

Two modes of behavioral switching

To understand the neural mechanisms of behavioral switching, it is important to determine what triggers such switching. Let us consider a situation in which procedure A is the appropriate behavior in order to obtain a reward in context α, whereas procedure B is the appropriate behavior in context β (Fig. 1), and a motivated subject has already learned these associations. Suppose the context changes from α to β. If the subject is unaware that the context has changed, s/he will perform procedure

The ACC and retroactive switching

The brain region that enables retroactive switching needs to be sensitive to negative feedback (e.g. reduced reward or punishment). It also needs to have access to the brain regions that implement alternative learned procedures. The ACC seems to fulfill both of these requirements.

First, many neurons in the monkey ACC are excited by negative feedback. In experiments using monkeys, the monkeys are trained to perform a task in order to obtain a certain amount of reward. If the reward is absent

The pre-SMA and proactive switching

A conflict in information processing characteristically occurs in proactive switching. The subject's performance on switch trials is much worse (high error rate and longer reaction time) than when the same context is repeated (non-switch trial), a phenomenon called ‘switch cost’ [1]. This is thought to occur because multiple cognitive operations are executed in response to the switch cue, which might include suppression of the old procedure and facilitation of the new procedure. The switch cost

The LPFC and rule implementation

Another cortical area that is thought to be essential for behavioral switching is the LPFC [47]. Subjects with prefrontal lesions show impairments in switching behaviors 48, 49, 50 or in inhibiting prepotent responses 51, 52. Similar to the pre-SMA, the LPFC is activated when response inhibition is required 36, 53. Other studies support the view that the LPFC is predominantly active when relevant rules are retrieved, maintained and implemented 13, 54. Strong activation of the LPFC occurs when

Cortico-basal ganglia mechanisms and behavioral switching

The outcome of behavioral switching is a change in motor behavior. A crucial aspect of behavioral switching, as we have suggested above, is the suppression of prepotent body movements. This is particularly clear for proactive switching, but is also true for retroactive switching in which performance often becomes slower after an erroneous trial 62, 63.

One possibility is that the switch-related cortical signals are mediated by an area that has a powerful capacity to inhibit motor areas. A

Concluding remarks

When the circumstances necessitate it, we make the important decision to change our behavior by breaking a routine. Recent studies with human and non-human primate subjects have begun to elucidate the neural mechanisms underlying such behavioral switching. These studies support the view that different areas in the medial and lateral frontal cortices play executive roles in behavioral switching and do so using different algorithms.

What triggers behavioral switching represents one aspect of the

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