Postoperative speech disorder after medial frontal surgery

Background: Patients undergoing surgical resection of medial frontal lesions may present transient postoperative speech disorders that remain largely unpredictable. Objective: To relate the occurrence of this speech deficit to the specific surgical lesion of the supplementary motor area (SMA) involved during language tasks using fMRI. Methods: Twelve patients were studied using a verbal fluency task before resection of a low-grade glioma of the medial frontal lobe and compared with six healthy subjects. Pre- and postoperative MR variables including the hemispheric dominance for language, the extent of SMA removal, and the volume of resection were compared to the clinical outcome. Results: Following surgery, 6 of 12 patients presented speech disorders. The deficit was similar across patients, consisting of a global reduction in spontaneous speech, ranging from a complete mutism to a less severe speech reduction, which recovered within a few weeks or months. The occurrence of the deficit was related to the resection of the activation in the SMA of the dominant hemisphere for language (p < 0.01). Increased activation in the SMA of the healthy hemisphere on the preoperative fMRI was observed in patients with postoperative speech deficit. Conclusions: fMRI is able to identify the area at risk in the SMA, of which resection is related to the occurrence of characteristic transient postoperative speech disorders. Increased SMA activation in the healthy hemisphere suggested that a plastic change of SMA function occurred in these patients.

[1]  J. A. Frost,et al.  Language dominance in neurologically normal and epilepsy subjects , 1999 .

[2]  Ming-Chyi Pai,et al.  Supplementary motor area aphasia: a case report , 1999, Clinical Neurology and Neurosurgery.

[3]  Wolfram Ziegler,et al.  The role of the left mesial frontal cortex in fluent speech: Evidence from a case of left supplementary motor area hemorrhage , 1997, Neuropsychologia.

[4]  G. Rizzolatti,et al.  Activation of precentral and mesial motor areas during the execution of elementary proximal and distal arm movements: a PET study. , 1993, Neuroreport.

[5]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[6]  R. Turner,et al.  Characterizing Evoked Hemodynamics with fMRI , 1995, NeuroImage.

[7]  U. Bannur, V. Rajshekhar,et al.  Post operative supplementary motor area syndrome: clinical features and outcome , 2000, British journal of neurosurgery.

[8]  V. Haughton,et al.  Functional MR of frontal lobe activation: comparison with Wada language results. , 1998, AJNR. American journal of neuroradiology.

[9]  D. Le Bihan,et al.  Noninvasive assessment of language dominance in children and adolescents with functional MRI , 1997, Neurology.

[10]  J. A. Frost,et al.  Determination of language dominance using functional MRI , 1996, Neurology.

[11]  G A Ojemann,et al.  Postoperative deficits and functional recovery following removal of tumors involving the dominant hemisphere supplementary motor area. , 1991, Journal of neurosurgery.

[12]  J Bancaud,et al.  What stimulation of the supplementary motor area in humans tells about its functional organization. , 1996, Advances in neurology.

[13]  W Grodd,et al.  Impaired procedural learning after damage to the left supplementary motor area (SMA). , 1996, Journal of neurology, neurosurgery, and psychiatry.

[14]  J. Pujol,et al.  Cerebral lateralization of language in normal left-handed people studied by functional MRI , 1999, Neurology.

[15]  M Freedman,et al.  Anatomic basis of transcortical motor aphasia , 1984, Neurology.

[16]  D. Stein,et al.  Mild hypothermia: therapeutic window after experimental cerebral ischemia. , 1996, Neurosurgery.

[17]  Karl J. Friston,et al.  Distribution of cortical neural networks involved in word comprehension and word retrieval. , 1991, Brain : a journal of neurology.

[18]  P. Crino,et al.  Cellular and molecular basis of cerebral dysgenesis , 1997, Journal of neuroscience research.

[19]  R T Constable,et al.  Functional MRI of Language Processing: Dependence on Input Modality and Temporal Lobe Epilepsy , 2001, Epilepsia.

[20]  A Yagishita,et al.  Focal cortical dysplasia: appearance on MR images. , 1997, Radiology.

[21]  V. Jay,et al.  Evidence of abnormal differentiation in giant cells of tuberous sclerosis. , 1997, Pediatric neurology.

[22]  E. Nussbaum,et al.  Complete temporal lobectomy for surgical resuscitation of patients with transtentorial herniation secondary to unilateral hemispheric swelling. , 1991, Neurosurgery.

[23]  M. Duchowny,et al.  Epilepsy Surgery in Children with Tuberous Sclerosis Complex: Presurgical Evaluation and Outcome , 2000, Epilepsia.

[24]  S. Shorvon Plasticity in Epilepsy: Dynamic Aspects of Brain Function , 1999 .

[25]  J. Wheless,et al.  On the surgical treatment of refractory epilepsy in tuberous sclerosis complex. , 1997, Pediatric neurosurgery.

[26]  T. L. Davis,et al.  Language dominance determined by whole brain functional MRI in patients with brain lesions , 1999, Neurology.

[27]  R. Zimmerman,et al.  Solitary cortical tubers. , 1995, AJNR. American journal of neuroradiology.

[28]  D. Le Bihan,et al.  Functional MRI during word generation, using conventional equipment , 1995, Neurology.

[29]  D Le Bihan,et al.  Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: comparison with intraoperative stimulation in patients with brain tumors. , 2000, Journal of neurosurgery.

[30]  D Le Bihan,et al.  Functional MR evaluation of temporal and frontal language dominance compared with the Wada test , 2000, Neurology.

[31]  A J Barkovich,et al.  Focal transmantle dysplasia: A specific malformation of cortical development , 1997, Neurology.

[32]  S. Chou,et al.  Tuberous sclerosis in the premature infant: a report of a case with immunohistochemistry on the CNS. , 1989, Clinical Neuropathology.

[33]  J. Trojanowski,et al.  Embryonic neuronal markers in tuberous sclerosis: single-cell molecular pathology. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Sato,et al.  Language dominance in partial epilepsy patients identified with an fMRI reading task , 2002, Neurology.

[35]  H. Funkenstein,et al.  Aphasia following infarction of the left supplementary motor area , 1978, Neurology.

[36]  D. Le Bihan,et al.  Role of the supplementary motor area in motor deficit following medial frontal lobe surgery , 2001, Neurology.

[37]  J. Schramm,et al.  Functional results after resective procedures involving the supplementary motor area. , 1996, Journal of neurosurgery.

[38]  P. T. Fox,et al.  Positron emission tomographic studies of the cortical anatomy of single-word processing , 1988, Nature.

[39]  Alan C. Evans,et al.  BrainWeb: Online Interface to a 3D MRI Simulated Brain Database , 1997 .

[40]  M. Shakudo,et al.  CT and MR imaging of cerebral tuberous sclerosis , 1998, Brain and Development.

[41]  R. Wollmann,et al.  Distribution of the neuronal specific protein, 14-3-2, in central nervous system lesions of tuberous sclerosis , 2004, Acta Neuropathologica.

[42]  M. Wiesendanger,et al.  Transcallosal connections of the distal forelimb representations of the primary and supplementary motor cortical areas in macaque monkeys , 2004, Experimental Brain Research.

[43]  R W Cox,et al.  Language processing is strongly left lateralized in both sexes. Evidence from functional MRI. , 1999, Brain : a journal of neurology.

[44]  B. Brody,et al.  MR imaging of tuberous sclerosis: pathogenesis of this phakomatosis, use of gadopentetate dimeglumine, and literature review. , 1992, Radiology.

[45]  M. Alexander,et al.  The aphasia syndrome of stroke in the left anterior cerebral artery territory. , 1980, Archives of neurology.

[46]  B. Schlaggar,et al.  Is it time to replace the Wada test? , 2002, Neurology.

[47]  P. Goldman-Rakic,et al.  Synaptic development of the cerebral cortex: implications for learning, memory, and mental illness. , 1994, Progress in brain research.

[48]  K Kuppusamy,et al.  Localization of language cortices by functional MR imaging compared with intracarotid amobarbital hemispheric sedation. , 1997, AJR. American journal of roentgenology.

[49]  P. Chauvel,et al.  Postoperative motor deficits and recovery after cortical resections. , 1999, Advances in neurology.

[50]  N. Altman,et al.  Tuberous sclerosis: characteristics at CT and MR imaging. , 1988, Radiology.

[51]  G. McCarthy,et al.  Functional organization of human supplementary motor cortex studied by electrical stimulation , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[52]  H. Lüders,et al.  Surgical ablations of the mesial frontal lobe in humans. , 1996, Advances in neurology.

[53]  K Herholz,et al.  Plasticity of language networks in patients with brain tumors: A positron emission tomography activation study , 2001, Annals of neurology.

[54]  G Rizzolatti,et al.  The classic supplementary motor area is formed by two independent areas. , 1996, Advances in neurology.

[55]  E. Auerbach,et al.  Relative Shift in Activity from Medial to Lateral Frontal Cortex During Internally Versus Externally Guided Word Generation , 2001, Journal of Cognitive Neuroscience.

[56]  A J Barkovich,et al.  MR imaging of tuberous sclerosis in neonates and young infants. , 1999, AJNR. American journal of neuroradiology.

[57]  H. Karbe,et al.  Brain Plasticity in Poststroke Aphasia: What Is the Contribution of the Right Hemisphere? , 1998, Brain and Language.

[58]  N. Arai,et al.  Cortical tubers without other stigmata of tuberous sclerosis: imaging and pathological findings , 1999, Neuroradiology.

[59]  S Grootoonk,et al.  Regional cerebral blood flow during volitional expiration in man: a comparison with volitional inspiration. , 1993, The Journal of physiology.

[60]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[61]  Wilhelm Eisner,et al.  Surgical Resection of Grade II Astrocytomas in the Superior Frontal Gyrus , 2002, Neurosurgery.

[62]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[63]  R. Kuzniecky,et al.  Cortical dysplasia in temporal lobe epilepsy: Magnetic resonance imaging correlations , 1991, Annals of neurology.

[64]  R G Robinson,et al.  Transcortical aphasia. Importance of the nonspeech dominant hemisphere in language repetition. , 1991, Brain : a journal of neurology.

[65]  J. Talairach,et al.  Clinical consequences of corticectomies involving the supplementary motor area in man , 1977, Journal of the Neurological Sciences.

[66]  J. Duncan,et al.  Is it time to replace the Wada test? , 2003, Neurology.