Action sets and decisions in the medial frontal cortex

doi:10.1016/j.tics.2004.07.009

Trends in Cognitive Sciences

Volume 8, Issue 9, September 2004, Pages 410-417

https://doi.org/10.1016/j.tics.2004.07.009 Get rights and content

Activations in human dorsomedial frontal and cingulate cortices are often present in neuroimaging studies of decision making and action selection. Interpretations have emphasized executive control, movement sequencing, error detection and conflict monitoring. Recently, however, experimental approaches, using lesions, inactivation, and cell recording, have suggested that these are just components of the areas’ functions. Here we review these results and integrate them with those from neuroimaging. A medial superior frontal gyrus (SFG) region centred on the pre-supplementary motor area (pre-SMA) is involved in the selection of action sets whereas the anterior cingulate cortex (ACC) has a fundamental role in relating actions to their consequences, both positive reinforcement outcomes and errors, and in guiding decisions about which actions are worth making.

Section snippets

The ACC and lateral PFC: working memory and task switching

It has been argued on the basis of meta-analyses of human imaging results that the ACC, like the lateral PFC, has a role in executive control 7, 8. Although it is true that humans activate both regions during working memory tasks [9] lesions of their homologues in the macaque brain have different effects. Whereas dorsolateral PFC lesions cause a profound working memory impairment [10] ACC lesions have little effect 11, 12, 13. Procyk and Joseph [14] have also questioned the degree to which

Errors and conflict in the ACC and SFG

Niki and Watanabe [27] first recorded changes in the activity of single ACC neurons when a monkey made errors. An error-correlated change is also present in the aggregate activity of many ACC neurons and can be recorded as a surface negative field potential when electrodes are placed beneath the dura of the macaque ACC [28]. An event related potential (ERP), called the error related negativity (ERN), can be recorded with electrodes on the human scalp, with a similar time course, peaking between

The ACC and the coding of action outcomes

Despite preoccupation with the errors vs conflict-monitoring debate it is now clear that the ACC has a broad role in encoding the relationship between an action and the reinforcement value of its outcome even when the outcome is a positive reward and not an error. It is true that macaque ACC sulcal neurons respond when actions lead to errors or when reinforcement is not delivered but similar or higher proportions of ACC sulcal neurons also respond to the delivery of positive reinforcers [40].

The ACC and decisions about the values of actions

The ACC might not just encode which outcome is expected from an action and whether the action is expected to lead to an error. It might also be a crucial part of a system for encoding whether or not an action is worth performing given the value of the expected outcome and the cost of performing the action. Evidence that the ACC encodes the value of outcomes comes from scalp recordings of ERPs with ACC dipole sources [53]. Human subjects picked one of two numbered panels and received either a

The SFG and task control

The SFG role in task control and the selection of action sets can be contrasted with that of the dorsal premotor cortex which selects single actions even in the absence of response conflict [57]. The SFG, on the other hand, may not be needed when a single action is selected but it is necessary when the set of action selection rules themselves are changed or when they are first selected. Activation centred on the pre-SMA region of human SFG can be recorded when subjects are instructed to switch

The SFG and movement sequences

Several divisions of primate SFG have a role in movement sequencing 64, 65. The initiation or changing of what might be called an ‘action set’, a set of rules for selecting responses, may be a common denominator to the SFG's role in both movement sequencing and task switching. In most task switching paradigms the action set is a set of stimulus–response selection rules whereas in sequence paradigms the action set is a set or order of response–response selection rules.

Shima et al. trained

Conclusions

The ACC does not exert supervisory executive control over behaviour in the same manner as lateral PFC but it does detect when actions have led to errors. In addition, any account of medial frontal function is incomplete without reference to the monitoring of response conflict before error commission but the crucial region might be in the SFG. It is clear, however, that error detection is just one aspect of a more general ACC role in associating actions with their reinforcement consequences even

Acknowledgements

Funded by the MRC and by the Royal Society (M.F.S.R.) and Wellcome Trust (M.E.W. and D.M.B.).

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Trends in Cognitive Sciences

Action sets and decisions in the medial frontal cortex

Section snippets

The ACC and lateral PFC: working memory and task switching

Errors and conflict in the ACC and SFG

The ACC and the coding of action outcomes

The ACC and decisions about the values of actions

The SFG and task control

The SFG and movement sequences

Conclusions

Acknowledgements

Trends Neurosci.

Trends Neurosci.

Neuropsychologia

Neuroimage

Brain Res.

Neurosci. Lett.

Electroencephalogr. Clin. Neurophysiol.

Neuroimage

Neuroimage

Neuropsychologia

Neuropsychologia

Neuropharmacology

Behav. Brain Res.

Primate anterior cingulate cortex: where motor control, drive and cognition interface

Nat. Rev. Neurosci.

Activity in the paracingulate and cingulate sulci during word generation: an fMRI study of functional anatomy

Cereb. Cortex

Co-planar Stereotaxic Atlas of the Human Brain

In vivo mormometry of the intrasulcal gray matter in the human cingulate, paracingulate, and superior-rostral sulci: hemispheric asymetries, gender differences and probability maps

J. Comp. Neurol.

Human cingulate cortex: surface features, flat maps, and cytoarchitecture

J. Comp. Neurol.

Sustained activity in the medial wall during working memory delays

J. Neurosci.

Analysis of the delayed-alternation deficit produced by dorsolateral prefrontal lesions in the rhesus monkeys

J. Comp. Physiol. Psychol.

The effect of cingulate cortex lesions on task switching and working memory

J. Cogn. Neurosci.

Effects of fornix transection and cingulate cortical ablation on spatial memory in rhesus monkeys

Exp. Brain Res.

Characterization of serial order encoding in the monkey anterior cingulate sulcus

Eur. J. Neurosci.

Response selection in the human anterior cingulate cortex

Nat. Neurosci.

Anterior cingulate conflict monitoring and adjustments in control

Science

Conflict monitoring and cognitive control

Psychol. Rev.

Fractionating the neural substrate of cognitive control processes

Proc. Natl. Acad. Sci. U. S. A.

Dissociating the role of the dorsolateral prefrontal and anterior cingulate cingulate cortex in cognitive control

Science

Role of the human medial frontal cortex in task switching: a combined fMRI and TMS study

J. Neurophysiol.

Dissociation in prefrontal cortex of affective and attentional shifts

Nature

Dissociation between conflict detection and error monitoring in the human anterior cingulate cortex

Proc. Natl. Acad. Sci. U. S. A.

Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions

J. Neurosci.

Effects of selective excitotoxic prefrontal lesions on acquisition of non-matching- and matching-to-place in the T-maze in the rat: differential involvement of the prelimbic-infralimbic and anterior cingulate cortices in providing behavioural flexibility

Eur. J. Neurosci.

Self-control during response conflict by human supplementary eye field

Nat. Neurosci.