Neural correlates of hemispheric dominance and ipsilaterality within the vestibularsystem

Earlier functional imaging studies on the processing of vestibular information mainly focused on cortical activations due to stimulation of the horizontal semicircular canals in right-handers. Two factors were found to determine its processing in the temporo-parietal cortex: a dominance of the non-dominant hemisphere and an ipsilaterality of the neural pathways. In an investigation of the role of these factors in the vestibular otoliths, we used vestibular evoked myogenic potentials (VEMPs) in a fMRI study of monaural saccular-otolith stimulation. Our aim was to (1) analyze the hemispheric dominance for saccular-otolith information in healthy left-handers, (2) determine if there is a predominance of the ipsilateral saccular-otolith projection, and (3) evaluate the impact of both factors on the temporo-parieto-insular activation pattern. A block design with three stimulation and rest conditions was applied: (1) 102 dB-VEMP stimulation; (2) 65 dB-control-acoustic stimulation, (3) 102 dB-white-noise-control stimulation. After subtraction of acoustic side effects, bilateral activations were found in the posterior insula, the superior/middle/transverse temporal gyri, and the inferior parietal lobule. The distribution of the saccular-otolith activations was influenced by the two factors but with topographic disparity: whereas the inferior parts of the temporo-parietal cortex were mainly influenced by the ipsilaterality of the pathways, the upper parts reflected the dominance of the non-dominant hemisphere. This is in contrast to the processing of acoustic stimulation, which showed a predominance of the contralateral pathways. Our study proves the importance of the hemispheric preponderance also in left-handers, which is of relevance in the superior parts of the insula gyrus V, the inferior parietal lobule, and the superior temporal gyri.

[1]  I. Johnsrude,et al.  Spectral and temporal processing in human auditory cortex. , 2002, Cerebral cortex.

[2]  J. Hornak,et al.  Ocular exploration in the dark by patients with visual neglect , 1992, Neuropsychologia.

[3]  Alan C. Evans,et al.  Dissociation of human mid-dorsolateral from posterior dorsolateral frontal cortex in memory processing. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[5]  M. Corbetta,et al.  Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  Guldin Wo,et al.  Is there a vestibular cortex , 1998 .

[7]  T Maehara,et al.  Functional magnetic resonance imaging of auditory cortex: with special reference to the side of aural stimulation. , 1999, Radiation medicine.

[8]  Marianne Dieterich,et al.  Spatial neglect--a vestibular disorder? , 2006, Brain : a journal of neurology.

[9]  Gereon R Fink,et al.  The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. , 2007, Cerebral cortex.

[10]  T. Brandt,et al.  Thalamic infarctions cause side-specific suppression of vestibular cortex activations. , 2005, Brain : a journal of neurology.

[11]  Rüdiger Wenzel,et al.  Human Vestibular Cortex as Identified with Caloric Stimulation in Functional Magnetic Resonance Imaging , 2002, NeuroImage.

[12]  J. Mäkelä,et al.  Human auditory cortical mechanisms of sound lateralisation: III. Monaural and binaural shift responses , 1994, Hearing Research.

[13]  T. Proffitt,et al.  The influence of voluntary tonic EMG level on the vestibular-evoked myogenic potential. , 2004, Journal of rehabilitation research and development.

[14]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited—Again , 1995, NeuroImage.

[15]  P. Schlindwein,et al.  Cortical representation of saccular vestibular stimulation: VEMPs in fMRI , 2008, NeuroImage.

[16]  Tiit Mathiesen,et al.  Preservation of tap vestibular evoked myogenic potentials despite resection of the inferior vestibular nerve. , 2004, Journal of vestibular research : equilibrium & orientation.

[17]  Karl J. Friston,et al.  Spatial registration and normalization of images , 1995 .

[18]  U. W. Buettner,et al.  Parietal cortex (2v) neuronal activity in the alert monkey during natural vestibular and optokinetic stimulation , 1978, Brain Research.

[19]  K. Zilles,et al.  Polymodal Motion Processing in Posterior Parietal and Premotor Cortex A Human fMRI Study Strongly Implies Equivalencies between Humans and Monkeys , 2001, Neuron.

[20]  M. Tervaniemi,et al.  Lateralization of auditory-cortex functions , 2003, Brain Research Reviews.

[21]  Klaus Scheffler,et al.  fMRI of the auditory system: understanding the neural basis of auditory gestalt. , 2003, Magnetic resonance imaging.

[22]  Martin Wiesmann,et al.  Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies , 2005, NeuroImage.

[23]  Rodney D. Vanderploeg,et al.  Left-handedness and variant patterns of cerebral organization: A case study , 1986 .

[24]  Hans-Otto Karnath,et al.  Neglect-like behavior in healthy subjects , 2003, Experimental Brain Research.

[25]  H. Scheich,et al.  Phonetic Perception and the Temporal Cortex , 2002, NeuroImage.

[26]  J. M. Fredrickson,et al.  Projection of the vestibular nerve to the area 3a arm field in the squirrel monkey (Saimiri Sciureus) , 2004, Experimental Brain Research.

[27]  L. Diller,et al.  Exploratory eye movements and visual hemi-neglect. , 1986, Journal of clinical and experimental neuropsychology.

[28]  Alan C. Evans,et al.  MRI Atlas of the Human Cerebellum , 2000 .

[29]  Karl J. Friston,et al.  Movement‐Related effects in fMRI time‐series , 1996, Magnetic resonance in medicine.

[30]  S. Faugier-Grimaud,et al.  Anatomic connections of inferior parietal cortex (area 7) with subcortical structures related to vestibulo‐ocular function in a monkey (macaca fascicularis) , 1989, The Journal of comparative neurology.

[31]  T. Proffitt,et al.  The effects of click and tone-burst stimulus parameters on the vestibular evoked myogenic potential (VEMP). , 2003, Journal of the American Academy of Audiology.

[32]  Kikuro Fukushima,et al.  Saccular stimulation of the human cortex: A functional magnetic resonance imaging study , 2007, Neuroscience Letters.

[33]  François Klam,et al.  ã Federation of European Neuroscience Societies Visual±vestibular interactive responses in the macaque ventral intraparietal area (VIP) , 2022 .

[34]  T. Murofushi,et al.  The effect of click repetition rate on vestibular evoked myogenic potential. , 1999, Acta oto-laryngologica.

[35]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[37]  Y Shinoda,et al.  Vestibular projection to the periarcuate cortex in the monkey , 2004, Neuroscience Research.

[38]  M Corbetta,et al.  Attentional modulation of neural processing of shape, color, and velocity in humans. , 1990, Science.

[39]  M. Wiesmann,et al.  Cerebral functional magnetic resonance imaging of vestibular, auditory, and nociceptive areas during galvanic stimulation , 1998, Annals of neurology.

[40]  Robert T. Knight,et al.  Right-sided neglect in a left-hander: Evidence for reversed hemispheric specialization of attention capacity , 1989, Neuropsychologia.

[41]  M. Mintun,et al.  Positron emission tomography study of voluntary saccadic eye movements and spatial working memory. , 1996, Journal of neurophysiology.

[42]  A. Longoni,et al.  Problems in the Assessment of Hand Preference , 1985, Cortex.

[43]  T. Brandt,et al.  Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). , 2001, Journal of neurophysiology.

[44]  O. Grüsser,et al.  Is there a vestibular cortex? , 1998, Trends in Neurosciences.

[45]  R. Ito,et al.  Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. , 2001, Brain research. Cognitive brain research.

[46]  Po-Wen Cheng, Toshihisa Murofushi The Effect of Rise/Fall Time on Vestibular-evoked Myogenic Potential Triggered by Short Tone Bursts , 2001, Acta oto-laryngologica.

[47]  A. Shmuel,et al.  Sustained Negative BOLD, Blood Flow and Oxygen Consumption Response and Its Coupling to the Positive Response in the Human Brain , 2002, Neuron.

[48]  O J Grüsser,et al.  Localization and responses of neurones in the parieto‐insular vestibular cortex of awake monkeys (Macaca fascicularis). , 1990, The Journal of physiology.

[49]  J. Dichgans,et al.  Space exploration in neglect. , 1998, Brain : a journal of neurology.

[51]  M. Schönwiesner,et al.  Hemispheric asymmetry for spectral and temporal processing in the human antero‐lateral auditory belt cortex , 2005, The European journal of neuroscience.

[52]  T Wüstenberg,et al.  Asymmetric hemodynamic responses of the human auditory cortex to monaural and binaural stimulation , 2002, Hearing Research.

[53]  T. Brandt,et al.  Dominance for vestibular cortical function in the non-dominant hemisphere. , 2003, Cerebral cortex.

[54]  K. Fukushima,et al.  Saccular Projections in the Human Cerebral Cortex , 2005, Annals of the New York Academy of Sciences.

[55]  P. Goldman-Rakic,et al.  Activation of human prefrontal cortex during spatial and nonspatial working memory tasks measured by functional MRI. , 1996, Cerebral cortex.

[56]  C. G. Phillips,et al.  Projection from low-threshold muscle afferents of hand and forearm to area 3a of baboon's cortex. , 1971, The Journal of physiology.

[57]  Po-Wen Cheng, Toshihisa Murofushi The Effects of Plateau Time on Vestibular-evoked Myogenic Potentials Triggered by Tone Bursts , 2001, Acta oto-laryngologica.

[58]  A. Berthoz,et al.  Functional MRI of galvanic vestibular stimulation. , 1998, Journal of neurophysiology.

[59]  J. M. Fredrickson,et al.  Cortical projection of group I muscle afferents to areas 2, 3a, and the vestibular field in the rhesus monkey , 1973, Experimental Brain Research.

[60]  Hidenao Fukuyama,et al.  Cortical correlates of vestibulo-ocular reflex modulation: a PET study. , 2003, Brain : a journal of neurology.

[61]  E A Cabanis,et al.  Location of the human posterior eye field with functional magnetic resonance imaging. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[62]  D. Basta,et al.  Vestibular evoked myogenic potentials induced by intraoperative electrical stimulation of the human inferior vestibular nerve , 2005, Hearing Research.

[63]  R. Woods Modeling for Intergroup Comparisons of Imaging Data , 1996, NeuroImage.

[64]  D. Yves von Cramon,et al.  Understanding non-biological dynamics with your own premotor system , 2007, NeuroImage.

[65]  G M Halmagyi,et al.  Myogenic potentials generated by a click-evoked vestibulocollic reflex. , 1994, Journal of neurology, neurosurgery, and psychiatry.

[66]  S. Sterbing-D’Angelo,et al.  Behavioral/systems/cognitive Multisensory Space Representations in the Macaque Ventral Intraparietal Area , 2022 .

[67]  Timothy Edward John Behrens,et al.  Functional Asymmetry for Auditory Processing in Human Primary Auditory Cortex , 2003, The Journal of Neuroscience.

[68]  P. Scheid,et al.  Vestibular nerve projection to the cerebral cortex of the Rhesus monkey , 2004, Experimental Brain Research.

[69]  S. Ferber,et al.  Spatial awareness is a function of the temporal not the posterior parietal lobe , 2001, Nature.

[70]  D. Perani,et al.  The anatomy of unilateral neglect after right-hemisphere stroke lesions. A clinical/CT-scan correlation study in man , 1986, Neuropsychologia.

[71]  Karl J. Friston,et al.  Analysis of fMRI Time-Series Revisited , 1995, NeuroImage.