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Functional role of the supplementary and pre-supplementary motor areas

Key Points

  • The dorsomedial frontal cortex contains a cluster of areas that are designated the supplementary motor area (SMA), the supplementary eye field (SEF) and the pre-supplementary motor area (pre-SMA). The defining functional feature of the members of this supplementary motor complex (SMC) is a marked sensitivity to various aspects of action.

  • The anatomical features of the SMC are not homogeneous: there is a gradient of morphological and connectional change where affinity with the prefrontal and primary motor cortices changes reciprocally in the rostro–caudal plane. More-rostral regions show greater kinship with the prefrontal cortex than with the primary motor cortex; for more-caudal regions the reverse is true.

  • The SMC is also heterogeneous neurophysiologically. The subregions of the SMC show different patterns of effector predilection and exhibit relative differences in the preponderance of cells that are sensitive to more-complex aspects of action.

  • Compared with primary motor areas, the SMC exhibits greater sensitivity to tasks in which action contingencies are broader in range and not unambiguously specified by the immediate external environment. This contrast is illustrated by differences in SMC activity between 'self-initiated' and 'externally triggered' actions, by movement sequences, by well-learnt and poorly learnt actions, and by switching between action possibilities.

  • Damage to the SMC disrupts behaviour in complex ways, affecting not just the commission but also the omission of actions, and the effects are broadly reflective of the neurophysiological properties of the region.

  • This plurality of functional responses has traditionally been taken as implying a plurality of neural functions, including implementing intentions, learning and performing temporally organized actions, switching between actions, and inhibiting unwanted actions.

  • Traditional accounts of the role of the SMC in voluntary action assume a fundamentally discrete modular architecture, with different functions assigned to macroscopically defined and functionally homogeneous regions. Thus, one function could be assigned to the SMA (for example, performing sequences) and another could be assigned to the pre-SMA (for example, changing between sequences). To explain the full range of behaviours, these discrete units must be able to switch between different functions depending on task demands — a feature we term functional pleomorphism.

  • Functional pleomorphism is conceptually problematic owing to the difficulty of explaining the process of switching between different neural functions. Moreover, a discrete modular architecture implies greater functional and structural homogeneity within functional modules than between them, a premise that is not supported by the empirical data. The differences across the region are better described by smoothly varying continuities than by any kind of discrete pattern, and they therefore need correspondingly smooth models of functional organization.

  • The plurality of functions that has been assigned to the SMC is undercut by a single elemental confound: the conditional complexity of the underlying condition–action association. Framed in the terms of information theory, internal, sequential, new and otherwise-flexible actions require more information than externally triggered, non-sequential and well-learnt actions (which were previously considered to be matched in complexity).

  • We suggest that gaining further insight into the role of the SMC requires a unified account of the region that is based on a faithful picture of the anatomical and neurophysiological features and a conceptually rigorous analysis of the models supposed to explain them.

Abstract

The supplementary motor complex consists of the supplementary motor area, the supplementary eye field and the pre-supplementary motor area. In recent years, these areas have come under increasing scrutiny from cognitive neuroscientists, motor physiologists and clinicians because they seem to be crucial for linking cognition to action. However, theories regarding their function vary widely. This Review brings together the data regarding the supplementary motor regions, highlighting outstanding issues and providing new perspectives for understanding their functions.

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Figure 1: Anatomy of the supplementary motor complex (SMC).
Figure 2: Electrophysiological responses in the supplementary motor complex.
Figure 3: Neuronal activity in the supplementary motor cortex related to movement sequences.
Figure 4: Neuronal activity in the pre-supplementary motor area related to switching responses.
Figure 5: Focal human supplementary eye field (SEF) lesion.
Figure 6: The structure and connectivity of supplementary motor cortex subregions vary in a continuous fashion.

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Acknowledgements

This work was supported by the Wellcome Trust (Programme Grant WT073735AIA), the National Institute for Health Research Clinical Biomedical Research Centre at University College London/University College London Hospital and Imperial College Healthcare National Health Service Trust.

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Correspondence to Masud Husain.

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Supplementary information

Supplementary information S1 (figure)

Proportions of new-preferring (New > Learned) and learned-preferring cells (Learned > New) relative to the total number of task-related cells in the pre-SmA and SmA in two monkeys (bo and GA), described in Nakamura (1998). (PDF 323 kb)

Supplementary information S2 (figure)

Summary of the variety of single-cell neurophysiological responses in the region of the supplementary eye field observed by Schall (1991) in the context of a simple oculomotor task. (PDF 177 kb)

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Glossary

Effector

An organ (a gland or, in the context of this article, a muscle) that becomes active in response to nerve impulses.

Saccade

Quick, simultaneous movements of both eyes in the same direction, allowing one to fixate rapidly on elements of a visual scene.

Stroop task

A behavioural task in which subjects are asked to rapidly respond to visually presented colour words by saying either the word itself or the colour of the ink in which the words are displayed. When the word is not the colour of the typeface, subjects tend to be slower and less accurate than when the two are the same.

Eriksen flanker task

A behavioural task in which subjects have to respond to a central stimulus that is flanked by distractor stimuli that code an alternative response — for example, the opposite of the response that is cued by the central stimulus.

Contralesional

The side of the body that is opposite to the side of a brain lesion.

Muscimol

A GABAA receptor agonist, 3-hydroxy-5-aminomethyl-isoxazole, that can be injected into the brain to temporarily disrupt activity at the site of injection.

Functional pleomorphism

The notion that a given area of the brain has different functions in different circumstances.

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Nachev, P., Kennard, C. & Husain, M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci 9, 856–869 (2008). https://doi.org/10.1038/nrn2478

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