Positron emission tomography visualized stimulation of the vestibular organ is localized in Heschl's gyrus

The existence of a human primary vestibular cortex is still debated. Current knowledge mainly derives from functional magnetic resonance imaging (fMRI) and positron emission tomography (PET) acquisitions during artificial vestibular stimulation. This may be problematic as artificial vestibular stimulation entails coactivation of other sensory receptors. The use of fMRI is challenging as the strong magnetic field and loud noise during MRI may both stimulate the vestibular organ. This study aimed to characterize the cortical activity during natural stimulation of the human vestibular organ. Two fluorodeoxyglucose (FDG)‐PET scans were obtained after natural vestibular stimulation in a self‐propelled chair. Two types of stimuli were applied: (a) rotation (horizontal semicircular canal) and (b) linear sideways movement (utriculus). A comparable baseline FDG‐PET scan was obtained after sitting motion‐less in the chair. In both stimulation paradigms, significantly increased FDG uptake was measured bilaterally in the medial part of Heschl's gyrus, with some overlap into the posterior insula. This is the first neuroimaging study to visualize cortical processing of natural vestibular stimuli. FDG uptake was demonstrated in the medial‐most part of Heschl's gyrus, normally associated with the primary auditory cortex. This anatomical localization seems plausible, considering that the labyrinth contains both the vestibular organ and the cochlea.

[1]  Koen Van Laere,et al.  EANM procedure guidelines for PET brain imaging using [18F]FDG, version 2 , 2009, European Journal of Nuclear Medicine and Molecular Imaging.

[2]  M. Mintun,et al.  Nonoxidative glucose consumption during focal physiologic neural activity. , 1988, Science.

[3]  G. Bruce Pike,et al.  Oxidative metabolism and the detection of neuronal activation via imaging , 2001, Journal of Chemical Neuroanatomy.

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

[5]  Dave R. M. Langers,et al.  Tonotopic mapping of human auditory cortex , 2014, Hearing Research.

[6]  M D Ginsberg,et al.  Increases in both cerebral glucose utilization and blood flow during execution of a somatosensory task , 1988, Annals of neurology.

[7]  L. Sokoloff,et al.  RELATION BETWEEN PHYSIOLOGICAL FUNCTION AND ENERGY METABOLISM IN THE CENTRAL NERVOUS SYSTEM , 1977, Journal of neurochemistry.

[8]  P. Morosan,et al.  Human Primary Auditory Cortex: Cytoarchitectonic Subdivisions and Mapping into a Spatial Reference System , 2001, NeuroImage.

[9]  Karl Herholz,et al.  Metabolic rates in small brain nuclei determined by high-resolution PET. , 2004, Journal of Nuclear Medicine.

[10]  Katrin Amunts,et al.  Cytoarchitecture and probabilistic maps of the human posterior insular cortex. , 2010, Cerebral cortex.

[11]  O. Blanke,et al.  The thalamocortical vestibular system in animals and humans , 2011, Brain Research Reviews.

[12]  Ayse Pinar Saygin,et al.  Smoothing and cluster thresholding for cortical surface-based group analysis of fMRI data , 2006, NeuroImage.

[13]  R. C. Oldfield THE ASSESSMENT AND ANALYSIS OF HANDEDNESS , 1971 .

[14]  I. Curthoys,et al.  The new vestibular stimuli: sound and vibration—anatomical, physiological and clinical evidence , 2017, Experimental Brain Research.

[15]  Thomas Stephan,et al.  Magnetic vestibular stimulation modulates default mode network fluctuations , 2016, NeuroImage.

[16]  O. Blanke,et al.  Oscillatory neural responses evoked by natural vestibular stimuli in humans. , 2016, Journal of neurophysiology.

[17]  Brian L. Day,et al.  On the Vertigo Due to Static Magnetic Fields , 2013, PloS one.

[18]  David S Zee,et al.  Vestibular stimulation by magnetic fields , 2015, Annals of the New York Academy of Sciences.

[19]  O. Grüsser,et al.  Cortico‐cortical connections and cytoarchitectonics of the primate vestibular cortex: A study in squirrel monkeys (Saimiri sciureus) , 1992, The Journal of comparative neurology.

[20]  L. Sokoloff,et al.  Relationships among local functional activity, energy metabolism, and blood flow in the central nervous system. , 1981, Federation proceedings.

[21]  Dale C. Roberts,et al.  MRI Magnetic Field Stimulates Rotational Sensors of the Brain , 2011, Current Biology.

[22]  M. Dieterich,et al.  On the recall of vestibular sensations , 2012, Brain Structure and Function.

[23]  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.

[24]  M. Shinder,et al.  Sensory convergence in the parieto-insular vestibular cortex. , 2014, Journal of neurophysiology.

[25]  T. Brandt,et al.  The parietal lobe and the vestibular system. , 2018, Handbook of clinical neurology.

[26]  Hamish G. MacDougall,et al.  The Video Head Impulse Test , 2017, Front. Neurol..

[27]  I. Curthoys,et al.  Vestibular primary afferent responses to sound and vibration in the guinea pig , 2011, Experimental Brain Research.

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

[29]  O B Paulson,et al.  Focal increase of blood flow in the cerebral cortex of man during vestibular stimulation. , 1985, Brain : a journal of neurology.

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

[31]  O. Grüsser,et al.  Vestibular neurones in the parieto‐insular cortex of monkeys (Macaca fascicularis): visual and neck receptor responses. , 1990, The Journal of physiology.

[32]  M E Raichle,et al.  Correlation Between Regional Cerebral Blood Flow and Oxidative Metabolism: In Vivo Studies in Man , 1976 .

[33]  I S Curthoys,et al.  The video head impulse test , 2009, Neurology.

[34]  Douglas G Altman,et al.  The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: guidelines for reporting observational studies. , 2014, International journal of surgery.

[35]  Randy L. Johnson,et al.  Development of the Mouse Inner Ear and Origin of Its Sensory Organs , 1998, The Journal of Neuroscience.

[36]  Bruce R. Rosen,et al.  Dynamic functional imaging of brain glucose utilization using fPET-FDG , 2014, NeuroImage.

[37]  Dora E Angelaki,et al.  Macaque Parieto-Insular Vestibular Cortex: Responses to Self-Motion and Optic Flow , 2010, Journal of Neuroscience.

[38]  M. Jinzaki,et al.  Comparison of [15O] H2O Positron Emission Tomography and Functional Magnetic Resonance Imaging in Activation Studies , 2016, World journal of nuclear medicine.

[39]  S. Pocock,et al.  The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: guidelines for reporting observational studies. , 2007, Preventive medicine.

[40]  M. Higuchi,et al.  18F-FDG PET mapping of regional brain activity in runners. , 2001, The Journal of sports medicine and physical fitness.

[41]  Anders M. Dale,et al.  An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest , 2006, NeuroImage.

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

[43]  Simon B. Eickhoff,et al.  Meta-analytical definition and functional connectivity of the human vestibular cortex , 2012, NeuroImage.

[44]  Hiroshi Fukuda,et al.  Functional brain mapping of actual car-driving using [18F]FDG-PET , 2006, Annals of nuclear medicine.

[45]  J. Melcher,et al.  Isolating the auditory system from acoustic noise during functional magnetic resonance imaging: examination of noise conduction through the ear canal, head, and body. , 2001, The Journal of the Acoustical Society of America.