Elsevier

Brain and Language

Volume 89, Issue 2, May 2004, Pages 320-328
Brain and Language

The contribution of the insula to motor aspects of speech production: A review and a hypothesis

https://doi.org/10.1016/S0093-934X(03)00347-XGet rights and content

Abstract

Based on clinical and functional imaging data, the left anterior insula has been assumed to support prearticulatory functions of speech motor control such as the “programming” of vocal tract gestures. In order to further elucidate this model, a recent functional magnetic resonance imaging (fMRI) study of our group (Riecker, Ackermann, Wildgruber, Dogil, & Grodd, 2000) investigated both overt (aloud) and covert (silent) production of highly overlearned word strings (“automatic speech”), based on the suggestion that “inner speech” might provide a “window” into preparatory motor activities (Jeannerod, 1994). As a control condition, subjects were asked to reproduce a nonlyrical tune. In contrast to hemodynamic responses within motor cortex and cerebellum, activation of the intrasylvian cortex turned out to be bound to overt task performance. Rather than prearticulatory processes, these findings suggest the left insula to contribute to the actual coordination of the up to 100 muscles engaged in articulation and phonation. Conceivably, the association of speech production with intrasylvian cortex might have evolved within the framework of phylogenetically older connections between the insula and limbic structures, on the one hand, and nonspeech functions of the upper midline musculature such as swallowing, on the other. Whereas (overt) speech tasks predominantly elicit activation within left anterior insula, reproduction of a nonlyrical tune yielded an opposite response pattern. Conceivably, the opposite distributional pattern of speaking and singing at the level of intrasylvian cortex reflects operation of the two hemispheres across different time domains (“double filtering by frequency theory”: left hemisphere=segmental information, right hemisphere=intonation contours of verbal utterances and musical melodies; Ivry & Robertson, 1998). In line with this suggestion, a further study of our group (Ackermann et al., 2001) provided first evidence that differential hemispheric filtering might be bound to insular cortex.

Section snippets

Clinico-neuroradiological correlation studies in patients with apraxia of speech: The role of the anterior insula

Speech production poses considerable demands on motor control mechanisms requiring fast and accurate (skilled) execution of orofacial gestures properly adjusted in time to laryngeal and respiratory activities, i.e., the sequenced activation of the up to 100 muscles engaged in verbal communication. Skilled motor tasks depend upon the integrity of the motor cortex and its efferent fiber tracts (Brooks, 1986). Apart from a few exceptions, e.g., innervation of lower facial musculature, the

Hemodynamic activation of insular cortex during speech production: Lateralization effects at the level of the anterior insula

Only a few functional imaging studies explicitly addressed motor aspect of speech production. As a by-product, the seminal positron emission tomography (PET) investigation by Petersen et al., 1988, Petersen et al., 1989 provided the first systematic account of hemodynamic activation patterns associated with speech motor control. Subjects were confronted with a set of tasks of increasing complexity: (a) fixation of a sign appearing on a screen, (b) passive exposure to written or spoken English

Does the anterior insula support prearticulatory processes of speech motor control? An fMRI investigation of auditory verbal imagery

Because of unimpaired upper motor neuron functions at the level of vocal tract musculature, AOS is considered a prearticulatory deficit of speech motor control characterized by disrupted programming or planning of articulatory and phonatory activities. Jeannerod (1994) suggested motor imagery to provide a “window” into the mechanisms of action planning, i.e., preparatory activities preceding actual performance of movement sequences. Thus, functional imaging of internal speech (“auditory verbal

The insula as a nodal point of emotional processes, sensory input and motor control

The phonotactic rules of, e.g., the English language system allow for the generation of more than 12,000 different syllables (Levelt, Roelofs, & Meyer, 1999; Levelt, 2001). However, the 500 highest-ranked items suffice to handle about 80% of verbal utterances (cumulative frequency of use). These syllables, by definition, involve the most exercised motor activities and, thererore, should represent highly overlearned movement patterns. Storage of at least the highest-ranked syllables as

Participation of the anterior insula in motor activities: Control of upper midline musculature

The findings that the left anterior insula supports the coordination of vocal tract innervation raises the question of whether this engagement reflects a more generalized contribution of intrasylvian cortex to movement control. Based on an extensive review of the relevant literature, the insula has been considered a supplementary motor region (Augustine, 1985) or a motor association area, respectively (Augustine, 1996). Indeed, a multitude of experimental studies in subhuman primates revealed

Hemispheric lateralization effects at the level of the insula: Different time domains of vocal tract control

Speaking and singing have been found to be associated with two complementary cerebral networks: Reproduction of a nonlyrical tune predominantly elicited activation within the right motor cortex, the right anterior insula, and the left cerebellum whereas the opposite response pattern emerged during a speech task. The right hemisphere, first, exhibits a higher proficiency for the processing of harmonic sounds (Sidtis, 1984) and, second, appears to house a pitch working memory (Zatorre, Evans,

Conclusions

There is now broad clinical and functional imaging evidence for a participation of the left anterior insula in speech motor control. At variance with widespread suggestions about the pathomechanisms of AOS, the insula seems to support the temporo-spatial pattern of vocal tract muscle innervation during verbal utterances rather than prearticulatory functions of speech motor control such as the programming or planning of vocal tract gestures. This dependency of speech production upon intrasylvian

Acknowledgments

This work was supported by the German Research Foundation (SPP “Sprachproduktion”). We wish to thank Wolfgang Grodd and Dirk Wildgruber for helpful comments on the manuscript.

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