Switching from automatic to controlled behavior: cortico-basal ganglia mechanisms

Abstract

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.

Figure for Box. 1. Retroactive switching by ACC neurons

Activity of a representative ACC neuron recorded while the monkey selected one of two movements (pushing or turning a handle) based on reduced reward. Top: The neuron was not very active after ordinary reward and the monkey continued to select the same movement. Middle: The same neuron increased discharges after the receipt of reduced reward and before the initiation of the alternate movement. Bottom: The neuron remained inactive when the monkey did not switch to the alternate movement despite a reduction of reward.

Figure for Box. 2. Proactive switching by pre-SMA neurons

(a) Oculomotor switching task . Each trial began with the onset of a white fixation point followed by the presentation of two stimuli on each side of the fixation point in two different colors. The positions of the pink and yellow stimuli were randomized out of two possible locations. After a short delay, the fixation point became either pink or yellow as a cue, instructing the monkey to make a saccade to the stimulus whose color was the same as the central cue. The central cue color remained unchanged in a block of 1–10 consecutive trials and then was switched in the next block. For simplicity, display panels demonstrating the onset of fixation point (Fixation) and two peripheral stimuli (Target) are illustrated only for the first three trials. White dotted circles, which were not shown to the monkeys during the actual experiments, indicate the correct saccade target. Red arrows indicate switch trials. (b) The population activity of switch-selective pre-SMA neurons for successful switch trials (red), erroneous switch trials (gray) and successful non-switch trials (blue).

Figure 1. Retroactive and proactive switching

Retroactive switching (left) is triggered by a failure (decreased reward value or an error). In this case the context cue is either absent or unknown to the animal (indicated by gray rectangles). Proactive switching (right) is triggered by a cue signaling a context change so that the subject will not experience the failure. This is possible, however, only after the subject has learned the meaning of the cue (indicated by purple and green rectangles). Highlighted in yellow are triggers of behavioral switching and switched procedures.

Figure 2. Neural mechanism of proactive switching in oculomotor behavior

A neural mechanism of behavioral switching must be able to (1) detect a change in the context, (2) suppress the prepotent, automatic process, and (3) facilitate the alternative, controlled process (conceptual scheme). The suppression must occur quickly because the automatic process emits a motor signal quickly; the facilitation can occur thereafter because the controlled process is slow. Recent studies have suggested that the pre-SMA, together with other frontal cortical areas, acts as a switch mechanism and the basal ganglia may mediate the switch-related signal from the cortical areas. In our study using saccadic eye movement, many neurons in the pre-SMA became active selectively and proactively on switch trials (Box 2). It was also shown, using a go-nogo task, that some pre-SMA neurons suppress the prepotent saccade, others facilitate the alternative saccade, and the rest have both functions. The suppressive pre-SMA neurons tended to be active earlier than the facilitatory pre-SMA neurons, consistent with the conceptual scheme. In the basal ganglia, the STN may serve to suppress the automatic saccade by enhancing the inhibitory output of the basal ganglia (SNr) on the SC or the thalamo-cortical network. The caudate nucleus might serve to facilitate the controlled saccade by disinhibiting the target of the basal ganglia. We speculate that the signals for the automatic and controlled saccades are carried mainly by the frontal eye field (FEF) and the supplementary eye field (SEF) respectively. In the possible neural network, excitatory and inhibitory connections are indicated by (+) and (−) respectively.