gms | German Medical Science

100 Jahre Phoniatrie in Deutschland
22. Wissenschaftliche Jahrestagung der Deutschen Gesellschaft für Phoniatrie und Pädaudiologie
24. Kongress der Union Europäischer Phoniater

Deutsche Gesellschaft für Phoniatrie und Pädaudiologie e. V.

16. bis 18.09.2005, Berlin

Functional MRI reveals two distinct cerebral networks subserving speech motor control

Zerebrale Korrelate der Sprechmotorik-Kontrolle: Funktionell-kernspintomographische Untersuchungen

Vortrag

  • corresponding author presenting/speaker Hermann Ackermann - University of Tübingen, Department of General Neurology, Tübingen, Germany
  • author Klaus Mathiak - University of Aachen, Dept. Psychiatry and Psychotherapy, Aachen, Germany
  • author Ingo Hertrich - University of Tübingen, Department of General Neurology, Tübingen, Germany
  • author Wolfgang Grodd - University of Tuebingen, Department of Neuroradiology, Tübingen, Germany
  • author Axel Riecker - University of Ulm, Dept. of Psychiatry III, Ulm, Germany

100 Jahre Phoniatrie in Deutschland. 22. Jahrestagung der Deutschen Gesellschaft für Phoniatrie und Pädaudiologie, 24. Kongress der Union der Europäischen Phoniater. Berlin, 16.-18.09.2005. Düsseldorf, Köln: German Medical Science; 2005. Doc05dgppV05

Die elektronische Version dieses Artikels ist vollständig und ist verfügbar unter: http://www.egms.de/de/meetings/dgpp2005/05dgpp051.shtml

Veröffentlicht: 15. September 2005

© 2005 Ackermann et al.
Dieser Artikel ist ein Open Access-Artikel und steht unter den Creative Commons Lizenzbedingungen (http://creativecommons.org/licenses/by-nc-nd/3.0/deed.de). Er darf vervielf&aauml;ltigt, verbreitet und &oauml;ffentlich zug&aauml;nglich gemacht werden, vorausgesetzt dass Autor und Quelle genannt werden.


Abstract

To further delineate the neural basis of speech motor control, functional magnetic resonance imaging (fMRI) was performed during syllable repetitions synchronized to click trains (8 subjects, 2 - 6 Hz; vs. passive listening task). (a) Bilateral hemodynamic responses emerged within mesiofrontal and sensorimotor cortex, putamen / pallidum, thalamus and cerebellum (two activation spots at either side). In contrast, dorsolateral premotor cortex and anterior insula showed left-sided activation. (b) Calculation of rate / response functions revealed a negative linear relationship between repetition frequency and hemodynamic activation within the striatum whereas both cerebellar hemispheres exhibited a step-like response increase at about 3 Hz. (c) Analysis of the temporal dynamics of hemodynamic activation revealed these cortical and subcortical brain regions to be organized into two separate networks (medial and dorsolateral premotor cortex, anterior insula, superior cerebellum vs. sensorimotor cortex, basal ganglia, inferior cerebellum). These data provide evidence for two levels of speech motor control bound, most presumably, to motor preparation and execution processes. Furthermore, these findings help to explain clinical observations such as an unimpaired or even accelerated speaking rate in Parkinson's disease and slowed speech tempo which does not fall below a rate of about 3 Hz in cerebellar disorders.


Text

Introduction

Compared to other domains of motor control, such as locomotion or upper limb movements, few data are available on the cerebral organization of motor aspects of speech production. Moreover, the pathophysiologic mechanisms of dysarthria or dysarthrophonia subsequent to dysfunctions of the CNS are incompletely understood. So far, our knowledge of the neural basis of speech motor control is predominantly based on clinical studies. Lesions / dysfunctions of the motor cortex, corticobulbar tracts, cranial nerve nuclei, basal ganglia, or cerebellar structures may disrupt execution of vocal tract muscles during speech production and, thus, give rise to more or less specific constellations of dysarthric deficits each [1]. Another syndrome of articularory performance reflecting, most presumably, disordered higher-order aspects of speech motor control (programming / planning of speech gestures) has been observed in association wih damage to dorsolateral prefrontal and / or anterior insular cortex of the left hemisphere (apraxia of speech). Some further insights into the cerebral organization of speech motor control come from electrophysiologic investigations during brain surgery or preoperative diagnositc evaluation of patients with epilepsy. For example, electrical stimulation of the supplementary motor area (SMA) in awake patients elicits speech arrest or involuntary vocalizations. Functional brain imaging such as positron emission tomography (PET) or functional magnetic resonance imaging (fMRI) now provide a further approach to the study of the cerebral organization of speech motor control. The cerebral network subserving articulatory / phonatory functions as delineated by these techniques during production of single nouns or series of words is in line with the available clinical and electrophysiological data (see [2] for a review). To further elucidate the motor control mechanisms bound to the various cortical and subcortical brain structures engaged in speech production, fMRI was conducted during syllable repetitions at various iteration rates.

Methods

Eight healthy native German subjects performed two different tasks in a 1.5 T whole-body MRI scanner: (a) passive listening to click trains via earphones, (b) syllabe repetitions synchronized to these auditory stimuli (see [3], [4] for further details on experimental design and signal analysis). Six different click series (2.0, 2.5, 3.0, 4.0, 5.0, and 6.0 Hz) were administered 15 times each in pseudorandomized order. At first, activation patterns obtained during passive listening and syllable repetitions were modeled and subtracted from each other. Based upon a parametric approach, second, the relationship between syllable frequency and regional hemodynamic activation was calculated (linear and non-linear rate / response functions). As a final step of analysis, the temporal dynamics of the blood oxygen level-dependent (BOLD) signal within the various regions of interest was determined.

Results

(a) Bilateral hemodynamic responses emerged within mesiofrontal and sensorimotor cortex, putamen / pallidum, thalamus and cerebellum (two activation spots at either side; Figure 1 [Fig. 1]). In contrast, dorsolateral premotor cortex and anterior insula showed left-sided activation. (b) Calculation of rate / response functions revealed a positive-linear relationship between repetition frequency and hemodynamic activation at the level of cortical structures (SMA, sensorimotor and premotor cortex, anterior insula) and the thalamus, a negative rate / response function of the basal ganglia, and a step-like increase of the BOLD signal at about 3 Hz within both cerebellar hemispheres. (c) Analysis of the temporal dynamics of hemodynamic activation ("functional connectivity") revealed these cortical and subcortical brain regions to be organized into two separate networks (medial and dorsolateral premotor cortex, anterior insula, superior cerebellum vs. sensorimotor cortex, basal ganglia, inferior cerebellum; Figure 2 [Fig. 2]).

Discussion

There is an ongoing controversy whether / inhowfar damage to the dominant premotor cortex or to the anterior insula causes apraxia of speech, a constellation of speech motor deficits encompassing effortful and groping articulatory movements. Our observations that left prefrontal and intrasylvian cortex pertain to a network subserving motor preparation processes during syllable repetitions suggest both these structures to participate in higher-order aspects of speech motor control. The specific contribution of these two structures to articulatory / phonatory performance remains to be further elucidated. The various cortical and subcortical structures engaged in motor execution processes have a differential impact upon speech production. Whereas bilateral corticobulbar dysfunctions ultimately may result in a paralysis of vocal tract muscles, syllable repetition rate does not fall below a level of about 3 Hz in cerebellar disorders. Furthermore, dysfunctions of the basal ganglia may give rise to "speech hastening", i.e., involuntary acceleration of speaking tempo. The findings of different rate / response functions in association with sensorimotor cortex, striatum, and cerebellum help to explain these clinical observations.


References

1.
Ackermann, H (1999) "Acquired disorders of articulation: Classification and intervention". In F. Fabbro (ed.). Concise Encyclopedia of Language Pathology. Amsterdam, Elsevier. 261-268.
2.
Ackermann, H, Riecker, A, Wildgruber, D (2004): "Functional brain imaging of motor aspects of speech production". In B. Maassen, R.D. Kent, H.F.M. Peters, P.H.H.M. van Lieshout, W. Hulstijn (eds.). Speech Motor Control in Normal and Disordered Speech. Oxford, Oxford University Press. 85-111.
3.
Riecker, A, Mathiak, K, Wildgruber, D, Erb, M, Hertrich, I, Grodd, W, Ackermann, H (2005): "fMRI reveals two distinct cerebral networks subserving speech motor control". Neurology 64: 700-706.
4.
Riecker, A, Kassubek, J, Gröschel, K, Grodd, W, Ackermann, H (2005): "The cerebral control of speech tempo: Opposite relationships between speaking rate and BOLD signal change at striatal and erebellar structures". Neuroimage, in press.