Vestibular–Somatosensory Interactions: A Mechanism in Search of a Function?
In: Multisensory ResearchSearch for other papers by Elisa Raffaella Ferrè in
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No unimodal vestibular cortex has been identified in the human brain. Rather, vestibular inputs are strongly integrated with signals from other sensory modalities, such as vision, touch and proprioception. This convergence could reflect an important mechanism for maintaining a perception of the body, including individual body parts, relative to the rest of the environment. Neuroimaging, electrophysiological and psychophysical studies showed evidence for multisensory interactions between vestibular and somatosensory signals. However, no convincing overall theoretical framework has been proposed for vestibular–somatosensory interactions, and it remains unclear whether such percepts are by-products of neural convergence, or a functional multimodal integration. Here we review the current literature on vestibular–multisensory interactions in order to develop a framework for understanding the functions of such multimodal interaction. We propose that the target of vestibular–somatosensory interactions is a form of self-representation.
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-
Akbarian S., Grüsser O. J., Guldin W. O. (1994). Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey, J. Comp. Neurol. 339, 421–437.
-
Angelaki D. E., Cullen K. E. (2008). Vestibular system: the many facets of a multimodal sense, Annu. Rev. Neurosci. 31, 125–150.
-
Bense S., Stephan T., Yousry T. A., Brandt T., Dieterich M. (2001). Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI), J. Neurophysiol. 85, 886–899.
-
Bisiach E., Vallar G. (2000). Unilateral neglect in humans, in: Handbook of Neuropsychology, Boller F., Grafman J., Rizzolatti G. (Eds), pp. 459–502. Elsevier Science Publishers B.V., Amsterdam, The Netherlands.
-
Bisiach E., Rusconi M. L., Vallar G. (1991). Remission of somatoparaphrenic delusion through vestibular stimulation, Neuropsychologia 29, 1029–1031.
-
Blanke O., Mohr C. (2005). Out-of-body experience, heautoscopy, and autoscopic hallucination of neurological origin: implications for neurocognitive mechanisms of corporeal awareness and self-consciousness, Brain Res. Rev. 50, 184–199.
-
Bottini G., Sterzi R., Paulesu E., Vallar G., Cappa S. F., Erminio F., Passingham R. E., Frith C. D., Frackowiak R. S. (1994). Identification of the central vestibular projections in man: a positron emission tomography activation study, Exp. Brain Res. 99, 164–169.
-
Bottini G., Paulesu E., Sterzi R., Warburton E., Wise R. J., Vallar G., Frackowiak R. S., Frith C. D. (1995). Modulation of conscious experience by peripheral sensory stimuli, Nature 376(6543), 778–781.
-
Bottini G., Karnath H. O., Vallar G., Sterzi R., Frith C. D., Frackowiak R. S., Paulesu E. (2001). Cerebral representations for egocentric space: functional-anatomical evidence from caloric vestibular stimulation and neck vibration, Brain 124, 1182–1196.
-
Bottini G., Paulesu E., Gandola M., Loffredo S., Scarpa P., Sterzi R., Santilli I., Defanti C. A., Scialfa G., Fazio F., Vallar G. (2005). Left caloric vestibular stimulation ameliorates right hemianesthesia, Neurology 65, 1278–1283.
-
Brandt T., Bartenstein P., Janek A., Dieterich M. (1998). Reciprocal inhibitory visual–vestibular interaction. Visual motion stimulation deactivates the parieto-insular vestibular cortex, Brain 121, 1749–1758.
-
Bremmer F., Klam F., Duhamel J. R., Ben Hamed S., Graf W. (2002). Visual–vestibular interactive responses in the macaque ventral intraparietal area (VIP), Eur. J. Neurosci. 16, 1569–1586.
-
Büttner U., Buettner U. W. (1978). Parietal cortex (2v) neuronal activity in the alert monkey during natural vestibular and optokinetic stimulation, Brain Res. 153, 392–397.
-
Cappa S., Sterzi R., Vallar G., Bisiach E. (1987). Remission of hemineglect and anosognosia during vestibular stimulation, Neuropsychologia 25, 775–782.
-
Deutschländer A., Bense S., Stephan T., Schwaiger M., Brandt T., Dieterich M. (2002). Sensory system interactions during simultaneous vestibular and visual stimulation in PET, Hum. Brain Mapp. 16, 92–103.
-
Eickhoff S. B., Amunts K., Mohlberg H., Zilles K. (2006a). The human parietal operculum. II. Stereotaxic maps and correlation with functional imaging results, Cereb. Cortex 16, 268–279.
-
Eickhoff S. B., Schleicher A., Zilles K., Amunts K. (2006b). The human parietal operculum. I. Cytoarchitectonic mapping of subdivisions, Cereb. Cortex 16, 254–267.
-
Eickhoff S. B., Jbabdi S., Caspers S., Laird A. R., Fox P. T., Zilles K., Behrens T. E. (2010). Anatomical and functional connectivity of cytoarchitectonic areas within the human parietal operculum, J. Neurosci. 30, 6409–6421.
-
Emri M., Kisely M., Lengyel Z., Balkay L., Márián T., Mikó L., Berényi E., Sziklai I., Trón L., Tóth Á. (2003). Cortical projection of peripheral vestibular signaling, J. Neurophysiol. 89, 2639–2646.
-
Fasold O., von Brevern M., Kuhberg M., Ploner C. J., Villringer A., Lempert T., Wenzel R. (2002). Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging, Neuroimage 17, 1384–1393.
-
Faugier-Grimaud S., Ventre J. (1989). Anatomic connections of inferior parietal cortex (area 7) with subcortical structures related to vestibulo-ocular function in a monkey (Macaca fascicularis), J. Comp. Neurol. 280, 1–14.
-
Ferrè E. R., Sedda A., Gandola M., Bottini G. (2011a). How the vestibular system modulates tactile perception in normal subjects: a behavioural and physiological study, Exp. Brain Res. 208, 29–38.
-
Ferrè E. R., Bottini G., Haggard P. (2011b). Vestibular modulation of somatosensory perception, Eur. J. Neurosci. 34, 1337–1344.
-
Ferrè E. R., Bottini G., Haggard P. (2012). Vestibular inputs modulate somatosensory cortical processing, Brain Struct. Funct. 217, 859–864.
-
Ferrè E. R., Longo M. R., Fiori F., Haggard P. (2013a). Vestibular modulation of spatial perception, Front. Hum. Neurosci. 7, 660. DOI:10.3389/fnhum.2013.00660.
-
Ferrè E. R., Bottini G., Iannetti G. D., Haggard P. (2013b). The balance of feelings: vestibular modulation of bodily sensations, Cortex 49, 748–758.
-
Ferrè E. R., Day B. L., Bottini G., Haggard P. (2013c). How the vestibular system interacts with somatosensory perception: a sham-controlled study with galvanic vestibular stimulation, Neurosci. Lett. 550, 35–40.
-
Ferrè E. R., Kaliuzhna M., Herbelin B., Haggard P., Blanke O. (2014). Vestibular–somatosensory interactions: effects of passive whole-body rotation on somatosensory detection, PloS One 9, e86379. DOI:10.1371/journal.pone.008637.
-
Fetsch C. R., Turner A. H., DeAngelis G. C., Angelaki D. E. (2009). Dynamic reweighting of visual and vestibular cues during self-motion perception, J. Neurosci. 29, 15601–15612.
-
Fetsch C. R., Pouget A., DeAngelis G. C., Angelaki D. E. (2012). Neural correlates of reliability-based cue weighting during multisensory integration, Nat. Neurosci. 15, 146–154.
-
Figliozzi F., Guariglia P., Silvetti M., Siegler I., Doricchi F. (2005). Effects of vestibular rotatory accelerations on covert attentional orienting in vision and touch, J. Cogn. Neurosci. 17, 1638–1651.
-
Fitzpatrick R. C., Day B. L. (2004). Probing the human vestibular system with galvanic stimulation, J. Appl. Physiol. 96, 2301–2316.
-
Fredrickson J. M., Rubin A. M. (1986). Vestibular cortex, in: Sensory-Motor Areas and Aspects of Cortical Connectivity, Jones E. G., Peters A. (Eds), Cerebral Cortex, Vol. 5, pp. 99–111. Plenum Press, New York, NY, USA.
-
Fredrickson J. M., Figge U., Scheid P., Kornhuber H. H. (1966). Vestibular nerve projection to the cerebral cortex of the rhesus monkey, Exp. Brain Res. 2, 318–327.
-
Gallace A., Spence C. (2011). To what extent do Gestalt grouping principles influence tactile perception? Psychol. Bull. 137, 538–561.
-
Goldberg J. M., Smith C. E., Fernandez C. (1984). Relation between discharge regularity and responses to externally applied galvanic currents in vestibular nerve afferents of the squirrel monkey, J. Neurophysiol. 51, 1236–1256.
-
Grüsser O. J., Pause M., Schreiter U. (1990). Localization and responses of neurones in the parieto-insular vestibular cortex of awake monkeys (Macaca fascicularis), J. Physiol. 430, 537–557.
-
Guldin W. O., Grüsser O. J. (1998). Is there a vestibular cortex? Trends Neurosci. 21, 254–259.
-
Guldin W. O., Akbarian S., Grüsser O. J. (1992). Cortico-cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus), J. Comp. Neurol. 326, 375–401.
-
Haggard P., Iannetti G. D., Longo M. R. (2013). Spatial sensory organization and body representation in pain perception, Curr. Biol. 23, R164–R176.
-
Horak F. B., Shupert C. L., Dietz V., Horstmann G. (1994). Vestibular and somatosensory contributions to responses to head and body displacements in stance, Exp. Brain Res. 100, 93–106.
-
Horstmann G. A., Dietz V. (1988). The contribution of vestibular input to the stabilization of human posture: a new experimental approach, Neurosci. Lett. 95, 179–184.
-
Iwamura Y., Iriki A., Tanaka M. (1994). Bilateral hand representation in the postcentral somatosensory cortex, Nature 369(6481), 554–556.
-
Jijiwa H., Kawaguchi T., Watanabe S., Miyata H. (1991). Cortical projections of otolith organs in the cat, Acta Oto-Laryngol. 111(S481), 69–72.
-
Jung P., Baumgärtner U., Stoeter P., Treede R. D. (2009). Structural and functional asymmetry in the human parietal opercular cortex, J. Neurophysiol. 101, 3246–3257.
-
Kerkhoff G., Hildebrandt H., Reinhart S., Kardinal M., Dimova V., Utz K. S. (2011). A long-lasting improvement of tactile extinction after galvanic vestibular stimulation: two sham-stimulation controlled case studies, Neuropsychologia 49, 186–195.
-
Lenggenhager B., Lopez C., Blanke O. (2008). Influence of galvanic vestibular stimulation on egocentric and object-based mental transformations, Exp. Brain Res. 184, 211–221.
-
Lopez C., Blanke O. (2011). The thalamocortical vestibular system in animals and humans, Brain Res. Rev. 67, 119–146.
-
Lopez C., Blanke O., Mast F. W. (2012). The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis, Neuroscience 212, 159–179.
-
Macaluso E., Driver J. (2005). Multisensory spatial interactions: a window onto functional integration in the human brain, Trends Neurosci. 28, 264–271.
-
McGeoch P. D., Ramachandran V. S. (2008a). Vestibular stimulation can relieve central pain of spinal origin, Spinal Cord 46, 756–757.
-
McGeoch P. D., Williams L. E., Lee R. R., Ramachandran V. S. (2008b). Behavioural evidence for vestibular stimulation as a treatment for central post-stroke pain, J. Neurol. Neurosurg. Psychiatry 79, 1298–1301.
-
Melzack R., Wall P. D. (1965). Pain mechanisms: a new theory, Science 150(3699), 971–979.
-
Miller S. M., Ngo T. T. (2007). Studies of caloric vestibular stimulation: implications for the cognitive neurosciences, the clinical neurosciences and neurophilosophy, Acta Neuropsychiatr. 19, 183–203.
-
Ödkvist L. M., Rubin A. M., Schwarz D. W. F., Fredrickson J. M. (1973). Vestibular and auditory cortical projection in the guinea pig (Cavia porcellus), Exp. Brain Res. 18, 279–286.
-
Ödkvist L. M., Schwarz D. W. F., Fredrickson J. M., Hassler R. (1974). Projection of the vestibular nerve to the area 3a arm field in the squirrel monkey (Saimiri sciureus), Exp. Brain Res. 21, 97–105.
-
Ödkvist L. M., Liedgren S. R. C., Larsby B., Jerlvall L. (1975). Vestibular and somatosensory inflow to the vestibular projection area in the post cruciate dimple region of the cat cerebral cortex, Exp. Brain Res. 22, 185–196.
-
Ploner M., Schmitz F., Freund H. J., Schnitzler A. (1999). Parallel activation of primary and secondary somatosensory cortices in human pain processing, J. Neurophysiol. 81, 3100–3104.
-
Ramachandran V. S., McGeoch P. D., Williams L., Arcilla G. (2007). Rapid relief of thalamic pain syndrome induced by vestibular caloric stimulation, Neurocase 13, 185–188.
-
Rode G., Perenin M. T. (1994). Temporary remission of representational hemineglect through vestibular stimulation, Neuroreport 5, 869–872.
-
Rorsman I., Magnusson M., Johansson B. B. (1999). Reduction of visuo-spatial neglect with vestibular galvanic stimulation, Scand. J. Rehabil. Med. 31, 117–124.
-
Rubens A. B. (1985). Caloric stimulation and unilateral visual neglect, Neurology 35, 1019.
-
Sang F. Y. P., Jauregui-Renaud K., Green D. A., Bronstein A. M., Gresty M. A. (2006). Depersonalisation/derealisation symptoms in vestibular disease, J. Neurol. Neurosurg. Psychiatry 77, 760–766.
-
Schmidt L., Utz K. S., Depper L., Adams M., Schaadt A. K., Reinhart S., Kerkhoff G. (2013). Now you feel both: galvanic vestibular stimulation induces lasting improvements in the rehabilitation of chronic tactile extinction, Front. Hum. Neurosci. 7, 90. DOI:10.3389/fnhum.2013.00090.
-
Schwarz D. W., Fredrickson J. M. (1971). Rhesus monkey vestibular cortex: a bimodal primary projection field, Science 172(3980), 280–281.
-
Schwarz D. W. F., Deecke L., Fredrickson J. M. (1973). Cortical projection of group I muscle afferents to areas 2, 3a and the vestibular field in the rhesus monkey, Exp. Brain Res. 17, 516–526.
-
Silberfenning J. (1941). Contribution to the problem of eye movements. III. Disturbances of ocular movements with pseudohemianopsia in frontal tumors, Confin. Neurol. 4, 1–13.
-
Uttal W. R., Spillmann L., Stürzel F., Sekuler A. B. (2000). Motion and shape in common fate, Vision Res. 40, 301–310.
-
Utz K. S., Dimova V., Oppenländer K., Kerkhoff G. (2010). Electrified minds: transcranial direct current stimulation (tDCS) and galvanic vestibular stimulation (GVS) as methods of non-invasive brain stimulation in neuropsychology — a review of current data and future implications, Neuropsychologia 48, 2789–2810.
-
Utz K. S., Keller I., Kardinal M., Kerkhoff G. (2011). Galvanic vestibular stimulation reduces the pathological rightward line bisection error in neglect — a sham stimulation-controlled study, Neuropsychologia 49, 1219–1225.
-
Vallar G., Sterzi R., Bottini G., Cappa S., Rusconi M. L. (1990). Temporary remission of left hemianesthesia after vestibular stimulation. A sensory neglect phenomenon, Cortex 26, 123–131.
-
Vallar G., Bottini G., Rusconi M. L., Sterzi R. (1993). Exploring somatosensory hemineglect by vestibular stimulation, Brain 116, 71–86.
-
Wenzel R., Bartenstein P., Dieterich M., Danek A., Weindl A., Minoshima S., Ziegler S., Schwaiger M., Brandt T. (1996). Deactivation of human visual cortex during involuntary ocular oscillations. A PET activation study, Brain 119, 101–110.
-
Wilkinson D., Zubko O., DeGutis J., Milberg W., Potter J. (2010). Improvement of a figure copying deficit during subsensory galvanic vestibular stimulation, J. Neuropsychol. 4, 107–118.
-
Zu Eulenburg P., Caspers S., Roski C., Eickhoff S. B. (2012). Meta-analytical definition and functional connectivity of the human vestibular cortex, Neuroimage 60, 162–169.
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Vestibular–Somatosensory Interactions: A Mechanism in Search of a Function?
In: Multisensory ResearchSearch for other papers by Elisa Raffaella Ferrè in
Current site
Google Scholar
PubMed
Search for other papers by Patrick Haggard in
Current site
Google Scholar
PubMed
No unimodal vestibular cortex has been identified in the human brain. Rather, vestibular inputs are strongly integrated with signals from other sensory modalities, such as vision, touch and proprioception. This convergence could reflect an important mechanism for maintaining a perception of the body, including individual body parts, relative to the rest of the environment. Neuroimaging, electrophysiological and psychophysical studies showed evidence for multisensory interactions between vestibular and somatosensory signals. However, no convincing overall theoretical framework has been proposed for vestibular–somatosensory interactions, and it remains unclear whether such percepts are by-products of neural convergence, or a functional multimodal integration. Here we review the current literature on vestibular–multisensory interactions in order to develop a framework for understanding the functions of such multimodal interaction. We propose that the target of vestibular–somatosensory interactions is a form of self-representation.
| All Time | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1111 | 167 | 12 |
| Full Text Views | 252 | 19 | 0 |
| PDF Views & Downloads | 98 | 12 | 0 |