Saccular stimulation of the human cortex: A functional magnetic resonance imaging study

Recent imaging studies have reported the projection of semicircular canal signals onto wide regions of the cerebral cortex but little is known about otolith projections onto the cerebral cortex. We used functional magnetic resonance imaging (fMRI) to investigate the activation of the cortex by loud clicks that selectively stimulate the sacculus. Twelve normal volunteers were presented with auditory stimuli via an earphone containing a piezo electric element. High-intensity [maximum volume of 120 dB (SPL)] or low-intensity [maximum volume of 110 dB (SPL)] clicks were delivered at a frequency of 1 Hz and lasted 1 ms. We first checked that the high-intensity, but not low-intensity, clicks stimulated the sacculus by determining the vestibular evoked myogenic potentials. We then analyzed two task conditions (high- and low-intensity clicks) in a boxcar paradigm. We obtained gradient echo echo-planar images by using a 1.5 T MRI system. We analyzed the fMRI time series data with SPM2. High-intensity clicks activated wide areas of the cortex, namely, the frontal lobe (prefrontal cortex, premotor cortex, and frontal eye fields), parietal lobe (the region around the intraparietal sulcus, temporo-parietal junction, and paracentral lobule), and cingulate cortex. These areas are similar to those reported in previous imaging studies that analyzed the cortical responses to the activation of the semicircular canals. Thus, semicircular canal and otolith/saccular signals may be processed in similar regions of the human cortex.

[1]  K. Amunts,et al.  Identifying human parieto‐insular vestibular cortex using fMRI and cytoarchitectonic mapping , 2006, Human brain mapping.

[2]  W. Penfield,et al.  The Cerebral Cortex of Man: A Clinical Study of Localization of Function , 1968 .

[3]  Oswald Bumke,et al.  Handbuch der Neurologie , 1936 .

[4]  P. Baudonniere,et al.  Vestibular Projections in the Human Cortex , 1999, Annals of the New York Academy of Sciences.

[5]  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.

[6]  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.

[7]  P. Vidal,et al.  Saccular dysfunction in Meniere's disease. , 1999, The American journal of otology.

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

[9]  Frank Bremmer,et al.  Interaction of linear vestibular and visual stimulation in the macaque ventral intraparietal area (VIP) , 2002, The European journal of neuroscience.

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

[11]  P. Thier,et al.  Responses of Visual‐Tracking Neurons from Cortical Area MST‐I to Visual, Eye and Head Motion , 1992, The European journal of neuroscience.

[12]  Site of Cortical Utricular Representation with Special Reference to the Somatosensory Barrel Field in the Gerbil , 1998, The Annals of otology, rhinology, and laryngology.

[13]  Kikuro Fukushima,et al.  Pursuit-related neurons in the supplementary eye fields: discharge during pursuit and passive whole body rotation. , 2004, Journal of neurophysiology.

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

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

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

[17]  O. Blanke,et al.  Neuropsychology: Stimulating illusory own-body perceptions , 2002, Nature.

[18]  Y. Uchino,et al.  Saccular and utricular inputs to sternocleidomastoid motoneurons of decerebrate cats , 1999, Experimental Brain Research.

[19]  P. Baudonniere,et al.  Vestibular projections in the human cortex , 2001, Experimental Brain Research.

[20]  C. Duffy MST neurons respond to optic flow and translational movement. , 1998, Journal of neurophysiology.

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

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

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

[24]  F. Lacquaniti,et al.  Representation of Visual Gravitational Motion in the Human Vestibular Cortex , 2005, Science.

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

[26]  Kikuro Fukushima,et al.  Role of Vestibular Signals in the Caudal Part of the Frontal Eye Fields in Pursuit Eye Movements in Three‐Dimensional Space , 2005, Annals of the New York Academy of Sciences.

[27]  T. Sato,et al.  Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation. , 2000, Journal of neurophysiology.

[28]  I. Curthoys,et al.  Responses of guinea pig primary vestibular neurons to clicks , 2004, Experimental Brain Research.

[29]  S. Zeki,et al.  The neurology of saccades and covert shifts in spatial attention: an event-related fMRI study. , 2000, Brain : a journal of neurology.