A functional MRI study: cerebral laterality for lexical-semantic processing and human voice perception.

BACKGROUND AND PURPOSE Language dominance research using functional neuroimaging has made important contributions to clinical applications. Nevertheless, although recent neuroimaging studies demonstrated right-lateralized activation by human voice perception, the influence of voice perception in terms of language dominance has not been adequately studied. We aimed to accurately clarify language dominance for lexical-semantic processing in the temporal cortices by focusing on human voice perception. METHODS Thirty normal right-handed subjects were scanned by functional MR imaging while listening to sentences (SEN), reverse sentences (rSEN), and identifiable nonvocal sounds (SND). We investigated cerebral activation and the distribution of individual Laterality Index under 3 contrasts: rSEN-SND, SEN-SND, and SEN-rSEN. RESULTS The rSEN-SND contrast, including human voice perception, revealed right-lateralized activation in the anterior temporal cortices. Both SEN-SND and SEN-rSEN contrasts, including lexical-semantic processing, showed left-lateralized activation in the inferior and middle frontal gyrus and middle temporal gyrus. The SEN-rSEN contrast, without the influence of human voice perception, showed no temporal activation in the right hemisphere. Symmetrical or right-lateralized activation was observed in 22 of 27 subjects (81.4%) under the rSEN-SND contrast in the temporal cortices. Although 9 of 27 subjects (33.3%) showed symmetrical or right-lateralized activation under the SEN-SND contrast in the temporal cortices, all subjects showed left-lateralized activation under the SEN-rSEN contrast. CONCLUSION Our results demonstrated that right-lateralized activation by human voice perception could mask left-lateralized activation by lexical-semantic processing. This finding suggests that the influence of human voice perception should be adequately taken into account when language dominance is determined.

[1]  A. Kleinschmidt,et al.  Modulation of neural responses to speech by directing attention to voices or verbal content. , 2003, Brain research. Cognitive brain research.

[2]  H. Rusinek,et al.  Functional magnetic resonance imaging of human brain activity in a verbal fluency task , 1998, Journal of neurology, neurosurgery, and psychiatry.

[3]  Karl J. Friston,et al.  Hearing and saying. The functional neuro-anatomy of auditory word processing. , 1996, Brain : a journal of neurology.

[4]  D. V. von Cramon,et al.  Crossed Nonaphasia in a Dextral With Left Hemispheric Lesions: A Functional Magnetic Resonance Imaging Study of Mirrored Brain Organization , 2001, Stroke.

[5]  K. Saberi,et al.  Cognitive restoration of reversed speech , 1999, Nature.

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

[7]  A. Stevens,et al.  Dissociating the cortical basis of memory for voices, words and tones. , 2004, Brain research. Cognitive brain research.

[8]  T. Rasmussen,et al.  Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance. 1960. , 2007, Journal of neurosurgery.

[9]  Stephen M. Rao,et al.  Human Brain Language Areas Identified by Functional Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[10]  G McCarthy,et al.  Comparative localization of auditory comprehension by using functional magnetic resonance imaging and cortical stimulation. , 1999, Journal of neurosurgery.

[11]  Byron Bernal,et al.  False lateralization of language cortex on functional MRI after a cluster of focal seizures. , 2002, Neurology.

[12]  D. LeBihan,et al.  Functional anatomy of cognitive development , 2000, Neurology.

[13]  G. J. M. Rutten,et al.  fMRI-Determined Language Lateralization in Patients with Unilateral or Mixed Language Dominance According to the Wada Test , 2002, NeuroImage.

[14]  D. V. von Cramon,et al.  Language dominance assessment by means of fMRI: Contributions from task design, performance, and stimulus modality , 2001, Journal of magnetic resonance imaging : JMRI.

[15]  S. Knecht,et al.  Re: Crossed nonaphasia in a dextral with left hemispheric lesions: a functional magnetic resonance imaging study of mirrored brain organization. , 2002, Stroke.

[16]  Sonja A. Kotz,et al.  Modulation of the Lexical–Semantic Network by Auditory Semantic Priming: An Event-Related Functional MRI Study , 2002, NeuroImage.

[17]  J. Talairach,et al.  Co-Planar Stereotaxic Atlas of the Human Brain: 3-Dimensional Proportional System: An Approach to Cerebral Imaging , 1988 .

[18]  Sharlene D. Newman,et al.  Imagery in sentence comprehension: an fMRI study , 2004, NeuroImage.

[19]  Alan C. Evans,et al.  Lateralization of phonetic and pitch discrimination in speech processing. , 1992, Science.

[20]  B. Devaux,et al.  Functional MR Imaging in Assessment of Language Dominance in Epileptic Patients , 2003 .

[21]  R. Elliott,et al.  The neural response to emotional prosody, as revealed by functional magnetic resonance imaging , 2003, Neuropsychologia.

[22]  S. Sato,et al.  fMRI language task panel improves determination of language dominance , 2004, Neurology.

[23]  G. Vingerhoets,et al.  Lessons for neuropsychology from functional MRI in patients with epilepsy , 2004, Epilepsy & Behavior.

[24]  Nader Pouratian,et al.  Utility of preoperative functional magnetic resonance imaging for identifying language cortices in patients with vascular malformations. , 2002, Journal of neurosurgery.

[25]  A. Vignoli,et al.  Symptomatic epilepsy with facial myoclonus triggered by language. , 2001, Epileptic disorders : international epilepsy journal with videotape.

[26]  Ayse Pinar Saygin,et al.  Action comprehension in aphasia , 2004 .

[27]  M. Haneda,et al.  Braille alexia during visual hallucination in a blind man with selective calcarine atrophy , 2003, Psychiatry and clinical neurosciences.

[28]  R. Zatorre,et al.  Voice-selective areas in human auditory cortex , 2000, Nature.

[29]  G Hickok,et al.  Role of anterior temporal cortex in auditory sentence comprehension: an fMRI study , 2001, Neuroreport.

[30]  E. T. Possing,et al.  Language lateralization in left-handed and ambidextrous people: fMRI data , 2002, Neurology.

[31]  R. Zatorre,et al.  Structure and function of auditory cortex: music and speech , 2002, Trends in Cognitive Sciences.

[32]  S. Golaszewski,et al.  Brain activation patterns during a verbal fluency test—a functional MRI study in healthy volunteers and patients with schizophrenia , 2004, Schizophrenia Research.

[33]  A Schulze-Bonhage,et al.  Unsuspected Atypical Hemispheric Dominance for Language as Determined by fMRI , 2001, Epilepsia.

[34]  P. Fox,et al.  The Neural System Underlying Chinese Logograph Reading , 2001, NeuroImage.

[35]  A D Friederici,et al.  Phonological processing during language production: fMRI evidence for a shared production-comprehension network. , 2003, Brain research. Cognitive brain research.

[36]  Isabel Gauthier,et al.  Auditory and Action Semantic Features Activate Sensory-Specific Perceptual Brain Regions , 2003, Current Biology.

[37]  Erica B. Michael,et al.  fMRI investigation of sentence comprehension by eye and by ear: Modality fingerprints on cognitive processes , 2001, Human brain mapping.

[38]  Kyoung-Min Lee,et al.  Functional MRI comparison between reading ideographic and phonographic scripts of one language , 2004, Brain and Language.

[39]  C. Elger,et al.  Memory reorganization in adult brain: observations in three patients with temporal lobe epilepsy , 2002, Epilepsy Research.

[40]  S. Small,et al.  The Anatomy of Auditory Word Processing: Individual Variability , 2001, Brain and Language.

[41]  J. Kassubek,et al.  Determination of hemisphere dominance for language: comparison of frontal and temporal fMRI activation with intracarotid amytal testing , 2002, Neuroradiology.

[42]  M Deppe,et al.  Behavioural relevance of atypical language lateralization in healthy subjects. , 2001, Brain : a journal of neurology.

[43]  Christine Delmaire,et al.  Productive and perceptive language reorganization in temporal lobe epilepsy , 2005, NeuroImage.

[44]  A. Friederici.  Towards a neural basis of auditory sentence processing , 2002, Trends in Cognitive Sciences.

[45]  Norihiro Sadato,et al.  Age-dependent plasticity in the superior temporal sulcus in deaf humans: a functional MRI study , 2004, BMC Neuroscience.

[46]  R. Zatorre,et al.  Adaptation to speaker's voice in right anterior temporal lobe , 2003, Neuroreport.

[47]  Karl J. Friston,et al.  The cortical localization of the lexicons. Positron emission tomography evidence. , 1992, Brain : a journal of neurology.

[48]  P. Belin,et al.  Thinking the voice: neural correlates of voice perception , 2004, Trends in Cognitive Sciences.

[49]  Stanislas Dehaene,et al.  Distinct unimodal and multimodal regions for word processing in the left temporal cortex , 2004, NeuroImage.

[50]  R. Zatorre,et al.  Human temporal-lobe response to vocal sounds. , 2002, Brain research. Cognitive brain research.

[51]  P A Bandettini,et al.  Effects of stimulus rate on signal response during functional magnetic resonance imaging of auditory cortex. , 1994, Brain research. Cognitive brain research.

[52]  E. Ringelstein,et al.  Language lateralization in healthy right-handers. , 2000, Brain : a journal of neurology.

[53]  Hongkeun Kim,et al.  Lateralization of epileptic foci by neuropsychological testing in mesial temporal lobe epilepsy. , 2004, Neuropsychology.

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

[55]  E. T. Possing,et al.  Human temporal lobe activation by speech and nonspeech sounds. , 2000, Cerebral cortex.

[56]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[57]  Stefan Knecht,et al.  How atypical is atypical language dominance? , 2003, NeuroImage.

[58]  Elizabeth Bates,et al.  Action comprehension in aphasia: linguistic and non-linguistic deficits and their lesion correlates , 2004, Neuropsychologia.

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

[60]  P. Maeder,et al.  Chronic cognitive impairment following laterothalamic infarcts: a study of 9 cases. , 2003, Archives of neurology.

[61]  Kuniyoshi L Sakai,et al.  Sign and speech: amodal commonality in left hemisphere dominance for comprehension of sentences. , 2005, Brain : a journal of neurology.