The role of the supplementary motor area for speech and language processing

doi:10.1016/j.neubiorev.2016.06.030

Neuroscience & Biobehavioral Reviews

Volume 68, September 2016, Pages 602-610

https://doi.org/10.1016/j.neubiorev.2016.06.030 Get rights and content

Highlights

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The supplementary motor area (SMA) is a superordinate control region for speech and language processing.
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The posterior/anterior dimension reflects a subdivision into articulatory versus semantic aspects of language.
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The SMA plays an important role for the integration of subcortical functions.
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The SMA contributes to the coordination of left- and right-hemispheric functions.
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The SMA is part of the interface between declarative and procedural language representations.

Abstract

Apart from its function in speech motor control, the supplementary motor area (SMA) has largely been neglected in models of speech and language processing in the brain. The aim of this review paper is to summarize more recent work, suggesting that the SMA has various superordinate control functions during speech communication and language reception, which is particularly relevant in case of increased task demands. The SMA is subdivided into a posterior region serving predominantly motor-related functions (SMA proper) whereas the anterior part (pre-SMA) is involved in higher-order cognitive control mechanisms. In analogy to motor triggering functions of the SMA proper, the pre-SMA seems to manage procedural aspects of cognitive processing. These latter functions, among others, comprise attentional switching, ambiguity resolution, context integration, and coordination between procedural and declarative memory structures. Regarding language processing, this refers, for example, to the use of inner speech mechanisms during language encoding, but also to lexical disambiguation, syntax and prosody integration, and context-tracking.

Introduction

The aim of this review paper is to provide a short overview regarding the various control functions of the supplementary motor area (SMA) for language and speech processing. In this context, the term “speech” will be used for the phonetic and motor-related aspects of speech communicaton, in contrast to “language” being related to higher-order and more abstract representations of linguistic structure in terms of syntax and semantics. Considering modular structures in the brain as, e.g., outlined in Hickok and Poeppel (2007), “speech” mainly refers to the articulatory network and its connections to the parietal and temporal lobe via the dorsal stream whereas “language” is mainly associated with lexical representations in inferior and anterior temporal cortex, linked to anterior and inferior parts Broca’s area in frontal cortex via the ventral stream (Rauschecker and Scott, 2009). However, these two domains are functionally intertwined, for example, in the verbal working memory where speech functions are engaged to maintain higher-order language representations (Baddeley, 2003, Buchsbaum and D’Esposito, 2008, Camos and Barrouillet, 2014).

Traditionally, the SMA does not belong to the major language areas in the brain as outlined in the classical work of Geschwind (Geschwind, 1970) or other models (Hickok and Poeppel, 2007, Hickok, 2009, Hickok, 2012, Hagoort, 2014, Friederici and Gierhan, 2013). Dick et al. (2014) included the SMA in their expanded language network as a region that is linked to inferior frontal language areas via the aslant tract. Furthermore, in response to studies on speech motor control showing significant SMA activity, the so-called DIVA (Directions Into Velocities of Articulators) model of speech production and acquisition was provided with an “initiation map” corrsponding to the superordinate control function of the SMA for speech initiation and triggering (Tourville and Guenther, 2011). The importance of such a control mechanism for the evolution of speech was already emphasized in a review paper by MacNeilage and Davis (2001), citing lesion studies as well as experiments using electrical stimulation of SMA. Indeed, if we are interested in the entire process of speech and language communication, it is necessary to consider a network that includes various superordinate control mechanisms. In this respect, the SMA seems to play a central role, and its major functions seem to be related to initiation and timing control, automatization, monitoring, and task switching. Traditionally, its functions were assigned to the motor control domain, but there is increasing evidence that particularly the anterior part of the SMA (pre-SMA) serves higher-order cognitive functions such as lexical disambiguation, context-tracking, monitoring, or inhibition of erroneous language representations. An important aspect of the SMA is its particular role of representing an interface between cortical areas, on the one hand, and subcortical networks comprising the basal ganglia, the cerebellum, and thalamic structures, on the other.

Section snippets

Anatomy and connectivity

The supplementary motor area (SMA), roughly located in the medial part of Brodmann area (BA) 6, can be subdivided into SMA proper and a more anterior part, i.e., the pre-SMA (Picard and Strick, 2001, Nachev et al., 2008). However, some authors also consider part of the prefrontal BA8 to belong to pre-SMA (Usami et al., 2013). The border between SMA proper and pre-SMA is mostly defined by the vertical line (in MNI space) crossing the anterior commissure (Kim et al., 2010, Picard and Strick, 2001

Clinical aspects

As concerns clinical studies, speech disorders seem to occur after left- rather than right-hemispheric SMA lesions, may affect language aspects of speech (e.g., word finding) as well as motor performance (articulation and phonation), and largely depend on the stage or time course of recovery (Jonas, 1981). For example, hemorrhage in left SMA resulted in dysfluent speech due to impaired initiation of sequential articulations in the absence of higher-order linguistic deficits or impaired motor

Procedural aspects of language and speech processing

A sensitive task for finger and speech motor performance is the assessment of finger tapping and syllable repetition, respectively. In case of both tasks, SMA and pre-SMA activity have been documented, and this activity seems to reflect an aspect of effort by showing a linear increase in hemodynamic activity along with accelerated repetition rates (Brendel et al., 2010, Riecker et al., 2003, Riecker et al., 2005, Riecker et al., 2010). In a syllable production study, pre-SMA activity was

Conclusion, tentative model, and outlook

Taken together, SMA proper seems to be primarily involved in speech motor control as an initiation and timing interface, but may also be engaged in other language functions such as verbal working memory and predictive top-down mechanisms during speech perception as far as these functions include representations of inner- or silently articulated speech. By contrast, pre-SMA can be considered as an area of cognitive control managing complex sequencing, ambiguity resolution and task switching.

Acknowledgments

This work was supported by the German Research Council (DFG Project HE 1573/6-2) and by the Hertie Institute for Clinical Brain Research (Tübingen, Germany).

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Review articleThe role of the supplementary motor area for speech and language processing

Highlights

Abstract

Introduction

Section snippets

Anatomy and connectivity

Clinical aspects

Procedural aspects of language and speech processing

Conclusion, tentative model, and outlook

Acknowledgments

Neuroimage

Brain Lang.

Brain Res.

J. Commun. Disord.

Trends Cogn. Sci.

Brain Lang.

Neuroimage

Brain Lang.

Neuroimage

Neuroimage

Neuroimage

Cortex

Clin. Neurol. Neurosurg.

Neuroimage

Neuroimage

Cortex

Neuroimage

Neuropsychologia

J. Affect. Disord.

Neuroimage

Curr. Opin. Neurobiol.

Neuron

Trends Cogn. Sci.

Curr. Opin. Neurobiol.

Biol. Psychiatry

Brain Lang.

Neuroimage

Phys. Life Rev.

Brain Cogn.

Curr. Opin. Neurobiol.

J. Commun. Disord.

Brain Lang.

Neuroimage

Trends Cogn. Sci.

Cortex

Cognition

J. Phon.

Brain Lang.

Cortex

Curr. Opin. Neurobiol.

Cortex

Clin. Neurol. Neurosurg.

Pediatr. Neurol.

Brain Lang.

Recruitment of contralateral supplementary motor area in functional recovery following medial frontal lobe surgery: an fMRI case study

J. Neurol. Surg. Part A

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Review article
The role of the supplementary motor area for speech and language processing