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Functional neuroanatomy of the vestibular cortex and vestibular stimulation methods for neuroimaging studies

  • Seung-Keun Lee (Department of Neurology, Soonchunhyang University Bucheon Hospital) ;
  • Eek-Sung Lee (Department of Neurology, Soonchunhyang University Bucheon Hospital)
  • Received : 2023.09.26
  • Accepted : 2023.11.08
  • Published : 2024.04.30

Abstract

The vestibular cortex is a distributed network of multisensory areas that plays a crucial role in balance, posture, and spatial orientation. The core region of the vestibular cortex is the parietoinsular vestibular cortex (PIVC), which is located at the junction between the posterior insula, parietal operculum, and retroinsular region. The PIVC is connected to other vestibular areas, the primary and secondary somatosensory cortices, and the premotor and posterior parietal cortices. It also sends projections to the vestibular nuclei in the brainstem. The PIVC is a multisensory region that integrates vestibular, visual, and somatosensory information to create a representation of head-in-space motion, which is used to control eye movements, posture, and balance. Other regions of the vestibular cortex include the primary somatosensory, posterior parietal, and frontal cortices. The primary somatosensory cortex is involved in processing information about touch and body position. The posterior parietal cortex is involved in integrating vestibular, visual, and somatosensory information to create a representation of spatial orientation. The frontal cortex is involved in controlling posture, and eye movements. The various methods used to stimulate the vestibular receptors in neuroimaging studies include caloric vestibular stimulation (CVS), galvanic vestibular stimulation (GVS), and auditory vestibular stimulation (AVS). CVS uses warm or cold water or air to stimulate the semicircular canals, GVS uses a weak electrical current to stimulate the vestibular nerve, and AVS uses high-intensity clicks or short tone bursts to stimulate the otolithic receptors.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korea government (MSIT) (Nos. 2019R1F1A1062752) and was supported by the Soonchunhyang University Research Fund.

References

  1. Cullen KE. The vestibular system: multimodal integration and encoding of self-motion for motor control. Trends Neurosci 2012;35:185-196.
  2. Lopez C, Blanke O, Mast FW. The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 2012;212:159-179.
  3. Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A, Lempert T, et al. Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage 2002;17:1384-1393.
  4. Frank SM, Greenlee MW. An MRI-compatible caloric stimulation device for the investigation of human vestibular cortex. J Neurosci Methods 2014;235:208-218.
  5. Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M. Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 2001;85:886-899.
  6. Lobel E, Kleine JF, Bihan DL, Leroy-Willig A, Berthoz A. Functional MRI of galvanic vestibular stimulation. J Neurophysiol 1998;80:2699-2709.
  7. Stephan T, Deutschlander A, Nolte A, Schneider E, Wiesmann M, Brandt T, et al. Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 2005;26:721-732.
  8. Janzen J, Schlindwein P, Bense S, Bauermann T, Vucurevic G, Stoeter P, et al. Neural correlates of hemispheric dominance and ipsilaterality within the vestibular system. Neuroimage 2008;42:1508-1518.
  9. Miyamoto T, Fukushima K, Takada T, de Waele C, Vidal PP. Saccular stimulation of the human cortex: a functional magnetic resonance imaging study. Neurosci Lett 2007;423:68-72.
  10. Schlindwein P, Mueller M, Bauermann T, Brandt T, Stoeter P, Dieterich M. Cortical representation of saccular vestibular stimulation: VEMPs in fMRI. Neuroimage 2008;39:19-31.
  11. Ward BK, Roberts DC, Otero-Millan J, Zee DS. A decade of magnetic vestibular stimulation: from serendipity to physics to the clinic. J Neurophysiol 2019;121:2013-2019.
  12. Ibitoye RT, Mallas EJ, Bourke NJ, Kaski D, Bronstein AM, Sharp DJ. The human vestibular cortex: functional anatomy of OP2, its connectivity and the effect of vestibular disease. Cereb Cortex 2023;33:567-582.
  13. Geschwind N. Specializations of the human brain. Sci Am 1979;241:180-199.
  14. Woldorff MG, Tempelmann C, Fell J, Tegeler C, Gaschler-Markefski B, Hinrichs H, et al. Lateralized auditory spatial perception and the contralaterality of cortical processing as studied with functional magnetic resonance imaging and magnetoencephalography. Hum Brain Mapp 1999;7:49-66.
  15. Brandt T, Dieterich M. The vestibular cortex. Its locations, functions, and disorders. Ann N Y Acad Sci 1999;871:293-312.
  16. Dieterich M, Bense S, Lutz S, Drzezga A, Stephan T, Bartenstein P, et al. Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 2003;13:994-1007.
  17. Cauzzo S, Singh K, Stauder M, Garcia-Gomar MG, Vanello N, Passino C, et al. Functional connectome of brainstem nuclei involved in autonomic, limbic, pain and sensory processing in living humans from 7 Tesla resting state fMRI. Neuroimage 2022;250:118925.
  18. Grusser OJ, Pause M, Schreiter U. Localization and responses of neurones in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis). J Physiol 1990;430:537-557.
  19. Guldin WO, Mirring S, Grusser OJ. Connections from the neocortex to the vestibular brain stem nuclei in the common marmoset. Neuroreport 1993;5:113-116.
  20. Brandt T, Dieterich M, Danek A. Vestibular cortex lesions affect the perception of verticality. Ann Neurol 1994;35:403-412.
  21. zu Eulenburg P, Caspers S, Roski C, Eickhoff SB. Meta-analytical definition and functional connectivity of the human vestibular cortex. Neuroimage 2012;60:162-169.
  22. Mazzola L, Lopez C, Faillenot I, Chouchou F, Mauguiere F, Isnard J. Vestibular responses to direct stimulation of the human insular cortex. Ann Neurol 2014;76:609-619.
  23. Amunts K, Mohlberg H, Bludau S, Zilles K. Julich-Brain: a 3D probabilistic atlas of the human brain's cytoarchitecture. Science 2020;369:988-992.
  24. Suzuki M, Kitano H, Ito R, Kitanishi T, Yazawa Y, Ogawa T, et al. Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. Brain Res Cogn Brain Res 2001;12:441-449.
  25. Schwarz DW, Fredrickson JM. Rhesus monkey vestibular cortex: a bimodal primary projection field. Science 1971;172:280-281.
  26. Bottini G, Sterzi R, Paulesu E, Vallar G, Cappa SF, Erminio F, et al. Identification of the central vestibular projections in man: a positron emission tomography activation study. Exp Brain Res 1994;99:164-169.
  27. Emri M, Kisely M, Lengyel Z, Balkay L, Marian T, Miko L, et al. Cortical projection of peripheral vestibular signaling. J Neurophysiol 2003;89:2639-2646.
  28. Odkvist LM, Schwarz DW, Fredrickson JM, Hassler R. Projection of the vestibular nerve to the area 3a arm field in the squirrel monkey (saimiri sciureus). Exp Brain Res 1974;21:97-105.
  29. Guldin WO, Grusser OJ. Is there a vestibular cortex? Trends Neurosci 1998;21:254-259.
  30. Ferre ER, Bottini G, Iannetti GD, Haggard P. The balance of feelings: vestibular modulation of bodily sensations. Cortex 2013;49:748-758.
  31. Lopez C. A neuroscientific account of how vestibular disorders impair bodily self-consciousness. Front Integr Neurosci 2013;7:91.
  32. Klam F, Graf W. Discrimination between active and passive head movements by macaque ventral and medial intraparietal cortex neurons. J Physiol 2006;574:367-386.
  33. Bremmer F, Klam F, Duhamel JR, Ben Hamed S, Graf W. Visual-vestibular interactive responses in the macaque ventral intraparietal area (VIP). Eur J Neurosci 2002;16:1569-1586.
  34. Vitte E, Derosier C, Caritu Y, Berthoz A, Hasboun D, Soulie D. Activation of the hippocampal formation by vestibular stimulation: a functional magnetic resonance imaging study. Exp Brain Res 1996;112:523-526.
  35. Smith AT, Wall MB, Thilo KV. Vestibular inputs to human motion-sensitive visual cortex. Cereb Cortex 2012;22:1068-1077.
  36. Paus T. Primate anterior cingulate cortex: where motor control, drive and cognition interface. Nat Rev Neurosci 2001;2:417-424.
  37. Guterstam A, Bjornsdotter M, Gentile G, Ehrsson HH. Posterior cingulate cortex integrates the senses of self-location and body ownership. Curr Biol 2015;25:1416-1425.
  38. O'Mara SM, Rolls ET, Berthoz A, Kesner RP. Neurons responding to whole-body motion in the primate hippocampus. J Neurosci 1994;14:6511-6523.
  39. Smith PF. Vestibular-hippocampal interactions. Hippocampus 1997;7:465-471.
  40. Stackman RW, Clark AS, Taube JS. Hippocampal spatial representations require vestibular input. Hippocampus 2002;12:291-303.
  41. Irving S, Pradhan C, Dieterich M, Brandt T, Zwergal A, Schoberl F. Transient topographical disorientation due to right-sided hippocampal hemorrhage. Brain Behav 2018;8:e01078.
  42. Spiegel DR, Smith J, Wade RR, Cherukuru N, Ursani A, Dobruskina Y, et al. Transient global amnesia: current perspectives. Neuropsychiatr Dis Treat 2017;13:2691-2703.
  43. Lopez C, Blanke O. Nobel Prize centenary: Robert Barany and the vestibular system. Curr Biol 2014;24:R1026-R1028.
  44. Nguyen TT, Kang JJ, Oh SY. Thresholds for vestibular and cutaneous perception and oculomotor response induced by galvanic vestibular stimulation. Front Neurol 2022;13:955088.