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

Abstract

Although we carry out most daily tasks nearly automatically, it is occasionally necessary to change a routine if something changes in our environment and the 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 have suggested 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.

Early error detection is generic, but subsequent adaption to errors is not: Evidence from ERPs

“…Alternatively, because the dorsal ACC is usually considered to be the main generator of the ERN as well as the CRN component (see Roger, Bénar, Vidal, Hasbroucq, & Burle, 2010), while the SMA may be related to proactive behavioural adjustments (Hikosaka & Isoda, 2010;Ullsperger & King, 2010), our new ERP results (110-170 ms post-response onset) suggest that a prolonged CRN/action monitoring effect may be at stake in the non-familiarised condition. By contrast, in the familiarised condition, there is likely a rapid transition following response onset from dorsal ACC (CRN) to more dorsal frontal regions (including the SMA), consistent with the involvement of a differential proactive behavioural control mechanism when monitoring the adequacy of actions performed with pre-familiarised stimulus attributes.…”

“…The dissociation in the locus of maximal activity may have a functional significance. Behavioural adjustments after errors have been described to take two different forms, so-called retroactive adaptation governed by the ACC and proactive adaptation handled by the pre-SMA (Hikosaka & Isoda, 2010;Ullsperger & King, 2010). Proactive adaptation refers to the active enhancement of cognitive control processes and implies an attentional component that reduces interference from irrelevant contextual information.…”

“…However, recently Hikosaka and Isoda (2010) discussed two mechanisms by which individuals are able to rapidly switch their behaviour to adapt to a new context, namely proactive and retroactive behavioural switching. Proactive switching, controlled by the pre-supplementary motor area, refers to the exertion of top-down control to prevent errors.…”

Deep Brain Stimulation of the Subthalamic Nucleus, but not Dopaminergic Medication, Improves Proactive Inhibitory Control of Movement Initiation in Parkinson's Disease

“…1). In other words, along with others [33], the proactive inhibitory control model hypothesizes that healthy participants can switch easily from controlled inhibition of response (anticipated suppression of the neuronal processes underlying movement initiation) to automatic processing of sensorimotor information (unlocked state), depending on their expectations of upcoming events. We assume that an impairment of this mechanism in PD would result in a slowing down of movement initiation.…”

Dopamine Effects on Human Error Processing Depend on Catechol-O-Methyltransferase VAL158MET Genotype

“…While D1 states have been associated with relative network stability and presumably improved working memory, D2 states presumably facilitate modulations of PFC neural activation patterns (Durstewitz and Seamans, 2008). Because (1) error feedback sensitivity of single medial PFC neurons (Shima and Tanji, 1998;Hikosaka and Isoda, 2010) and error-related brain activity in humans (Yasuda et al, 2004;Hester et al, 2008) are linked to increased response and/or neural network variability typically found in D2 states (Durstewitz and Seamans, 2008), and (2) brain and behavioral responses to errors reflect dynamic, presumably DA-sensitive, processes, particularly tied to D2 receptor activation (Zirnheld et al, 2004;Frank and Hutchison, 2009), we hypothesized that error-induced transitions of brain activity and behavior are enhanced at relatively high and low DA levels associated with lowstability D2-dominated regimes.…”