Elsevier

NeuroImage

Volume 37, Issue 1, 1 August 2007, Pages 26-39
NeuroImage

Cortical lateralization of bilateral symmetric chin movements and clinical relevance in tumor patients—A high field BOLD–FMRI study

https://doi.org/10.1016/j.neuroimage.2007.02.059Get rights and content

Abstract

Although unilateral lesion studies concerning the opercular part of primary motor cortex report clinically severe motor deficits (e.g. anarthria, masticatory paralysis), functional lateralization of this area has not yet been addressed in neuroimaging studies.

Using BOLD–FMRI, this study provides the first quantitative evaluation of a possible cortical lateralization of symmetric chin movements (rhythmic contraction of masticatory muscles) in right-handed healthy subjects and presurgical patients suffering tumorous lesions in the opercular primary motor cortex. Data were analyzed according to “activation volume” and “activation intensity”.

At group level, results showed a strong left-hemispheric dominance for chin movements in the group of healthy subjects. In contrast, patients indicated dominance of the healthy hemisphere. Here, a clinically relevant dissociation was found between “activation volume” and “activation intensity”: Although “activation volume” may be clearly lateralized to the healthy hemisphere, “activation intensity” may indicate residual functionally important tissue close to the pathological tissue. In these cases, consideration of BOLD–FMRI maps with the exclusive focus on “activation volume” may lead to erroneous presurgical conclusions.

We conclude that comprehensive analyses of presurgical fMRI data may help to avoid sustained postoperative motor deficits and dysarthria in patients with lesions in the opercular part of primary motor cortex.

Introduction

BOLD–FMRI and electrophysiological data indicate a predominant role of the left primary sensorimotor cortex during right hand movements (e.g. Beisteiner et al., 1995, Jancke et al., 2000). In the context of neurosurgical treatment of lesions close to these brain regions, presurgical fMRI maps significantly improve the protection from postoperative motor deficits (Detre, 2006, Roessler et al., 2005, Sunaert, 2006). As the primary sensorimotor cortex undoubtedly plays an essential role within the motor circuitry, avoiding damage to this region is the clue to safe neurosurgical treatment.

When it comes to movements with similar representation in both primary sensorimotor cortices (e.g. opening and closing of mouth), each hemisphere is regarded to be equally important for the task. Both postoperative (Peraud et al., 2004) and post-ischemic (Cruccu et al., 1988, Cruccu et al., 1989) lesion studies on unilateral lesions in the opercular part of M1 (most inferior and lateral part of primary motor cortex) report on motor deficits basically confined to contralesional muscles. In line with these reports, electrophysiological studies underline the direct control of the trigeminal motor nucleus by a majority of crossing (excitatory and inhibitory) corticofugal fibres, but the existence of different kinds of ipsilateral projections is reported on as well (Cruccu et al., 1989, Nordstrom et al., 1999, Pearce et al., 2003). These findings emphasize the importance of primary regions for this kind of task, although masticatory function is a complex motor behavior being subserved by subcortical structures as well (e.g. Sessle et al., 2005, Takada and Miyamoto, 2004, Yamada et al., 2005).

Remarkably, clinical deficits and electrophysiological changes (concerning MEPs) of ipsilateral muscles due to unilateral (right or left) lesions in opercular M1 have been described as well (Cosnett et al., 1988, Cruccu et al., 1989, Kutluay et al., 1996, Starkstein et al., 1988, Weller, 1993). Clinical deficits described in these investigations are anarthria and bilateral central facio-linguovelo-pharyngeo-masticatory paralysis (Foix–Chavany–Marie Syndrome).

In order to anticipate such postoperative motor deficits, several patients suffering unilateral neoplastic lesions close to the most inferior and lateral part of primary motor cortex were transferred to our study group. For three reasons, chin movements (repetitive opening and closing of the mouth against no resistance) were chosen as the appropriate activation task: (1) they are simple to perform, (2) they activate functional tissue close to the lesion in question and (3) they hereby activate primary cortical regions the unilateral damage of which may cause dysarthria (Peraud et al., 2004). In these clinical studies fMRI results showed obvious lateralization of activated primary cortex despite the bilateral and symmetric motor task, providing evidence that habitually symmetric movements may have a lateralized cortical representation. This unexpected finding initiated the current study, since lateralized activation patterns are usually associated with asymmetric use of homologue muscle groups (e.g. with respect to handedness).

Although motor studies examining chin movements, actual chewing or sham chewing (imitation of chewing movements without chewing gum) have been reported for different methods in the field of functional brain topography (Fang et al., 2005, Huckabee et al., 2003, Martin et al., 2004, Momose et al., 1997, Onozuka et al., 2002, Shibukawa et al., 2004, Takada and Miyamoto, 2004, Tamura et al., 2003), none of them reported significant lateralization of sensorimotor cortex.

The current study was set up to test a possible cortical lateralization of symmetric orofacial movements in right-handed healthy subjects and presurgical patients presenting with tumorous lesions. It provides the first effort to evaluate this kind of lateralization in a quantitative sense and to test its clinical relevance in a presurgical context. The motor paradigm of symmetric opening and closing of the mouth allows the performance of non-lateralized (symmetric) muscular activities.

To avoid any bias due to lateralized peripheral activity with movements closely related to our task (e.g. chewing), we determined a possible preferred chewing side through a modified version of the Kazazoglu et al. (1994) test. In addition, special efforts were taken to minimize fMRI artifacts and improve signal to noise ratio. Since head motion artifacts are a critical issue with chin movements, a tight but comfortable precision plaster cast helmet encompassing most of the head and face was applied (Edward et al., 2000). FMRI data were analyzed with respect to (1) general dominance of a specific hemisphere (right or left), (2) hemispheric localization (right or left) of the pathological tissue (patients) and (3) preference of a particular chewing side.

Section snippets

Patients/subjects

12 healthy right-handed subjects (mean age 23.4) and 16 right-handed patients (mean age 33.4) suffering from enlarged (diameter > 25 mm) lesions close to the presumed “chin representation area” (most lateral and inferior part of primary motor cortex) participated in the study. According to the routine clinical examination, all participants showed normal masticatory function, and none of the participants reported on any masticatory deficit. Patients were transferred to our laboratory for

Results

All participants were able to adequately perform the required task. Participants did not report on unexpected (positive or negative) emotional experiences or stressful events, neither did the examiner note any expressions of (positive or negative) emotional responses during the experiments.

Discussion

Although the asymmetrical cortical representation of bimanually and symmetrically performed motor tasks has been evaluated (e.g. Stephan et al., 1999), neuroimaging studies have not addressed the issue of lateralized representation of a priori symmetric and bilateral movements such as simple opening/closing of the mouth. We approached this question by executing a chin motor task that a priori avoids asymmetric motion components. During everyday life, the current task (in contrast to hand motor

Acknowledgments

This study was supported by the Austrian Science Foundation (FWF P15102). The first author would like also to acknowledge support by the Austrian Academy of Sciences for receipt of the PhD-fellowship “DOC” [DOKTORANDENPROGRAMM DER ÖSTERREICHISCHEN AKADEMIE DER WISSENSCHAFTEN].

References (79)

  • L. Jancke et al.

    fMRI study of bimanual coordination

    Neuropsychologia

    (2000)
  • A. Jansen et al.

    The assessment of hemispheric lateralization in functional MRI – robustness and reproducibility

    NeuroImage

    (2006)
  • I.S. Kim et al.

    Influence of mastication and salivation on swallowing in stroke patients

    Arch. Phys. Med. Rehabil.

    (2005)
  • S.S. Lee et al.

    Metaphorical vs. literal word meanings: fMRI evidence against a selective role of the right hemisphere

    NeuroImage

    (2006)
  • I. Loubinoux et al.

    Correlation between cerebral reorganization and motor recovery after subcortical infarcts

    NeuroImage

    (2003)
  • M. Naccarato et al.

    Does healthy aging affect the hemispheric activation balance during paced index-to-thumb opposition task? An fMRI study

    NeuroImage

    (2006)
  • M.A. Nordstrom et al.

    Motor cortical control of human masticatory muscles

    Progr. Brain Res.

    (1999)
  • R.C. Oldfield

    The assessment and analysis of handedness: the Edinburgh inventory

    Neuropsychologia

    (1971)
  • E. Ozdemir et al.

    Shared and distinct neural correlates of singing and speaking

    NeuroImage

    (2006)
  • M. Peters et al.

    Cluster analysis reveals at least three, and possibly five distinct handedness groups

    Neuropsychologia

    (1992)
  • M. Peters et al.

    Do “right-armed” lefthanders have different lateralization of motor control for the proximal and distal musculature?

    Cortex

    (1992)
  • E. Plante et al.

    Sex differences in the activation of language cortex during childhood

    Neuropsychologia

    (2006)
  • C.K. Richardson et al.

    Digitizing the moving face during dynamic displays of emotion

    Neuropsychologia

    (2000)
  • D. Salmaso et al.

    Problems in the assessment of hand preference

    Cortex

    (1985)
  • K.L. Schmidt et al.

    Signal characteristics of spontaneous facial expressions: automatic movement in solitary and social smiles

    Biol. Psychol.

    (2003)
  • D.A. Soltysik et al.

    Strategies for block-design fMRI experiments during task-related motion of structures of the oral cavity

    NeuroImage

    (2006)
  • S.E. Starkstein et al.

    Bilateral opercular syndrome and crossed aphemia due to a right insular lesion: a clinicopathological study

    Brain Lang.

    (1988)
  • T. Takada et al.

    A fronto-parietal network for chewing of gum: a study on human subjects with functional magnetic resonance imaging

    Neurosci. Lett.

    (2004)
  • E.M. Weiss et al.

    Language lateralization in unmedicated patients during an acute episode of schizophrenia: a functional MRI study

    Psychiatry Res.

    (2006)
  • Y. Yamada et al.

    Coordination of cranial motoneurons during mastication

    Respir. Physiol. Neurobiol.

    (2005)
  • D.P. Anderson et al.

    FMRI lateralization of expressive language in children with cerebral lesions

    Epilepsia

    (2006)
  • R. Beisteiner

    Funktionelle Magnetresonanztomographie

  • R. Beisteiner et al.

    Probleme und Lösungsmöglichkeiten bei Patientenuntersuchungen mit funktioneller Magnetresonanztomographie (fMRT)

  • S. Bense et al.

    Direction-dependent visual cortex activation during horizontal optokinetic stimulation (fMRI study)

    Hum. Brain Mapp.

    (2006)
  • J.R. Binder et al.

    Determination of language dominance using functional MRI: a comparison with the Wada test

    Neurology

    (1996)
  • V. Bosch

    Statistical analysis of multi-subject fMRI data: assessment of focal activations

    J. Magn. Reson. Imaging

    (2000)
  • M.J. Brammer

    Head motion and its correction

  • R.S. Briellmann et al.

    Language lateralization in temporal lobe epilepsy patients related to the nature of the epileptogenic lesion?

    Epilepsia

    (2006)
  • S.L. Butler et al.

    Task-dependent control of human masseter muscles from ipsilateral and contralateral motor cortex

    Exp. Brain. Res.

    (2001)
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