Abstract
Functional neuroimaging studies on the recall or imagination of a distinctive task in the motor network or of sensations in sensory systems (visual, acoustic, nociceptive, gustatory, and olfactory) demonstrated that the respective primary cortex is often involved in the mental imagery process. Our aim was to examine this phenomenon in the vestibular system using fMRI. Sixteen healthy subjects were asked to remember the feeling of a rotatory chair procedure in contrast to an identical situation at rest. Shortly afterwards they were asked to recall the vestibular experience in a 1.5-T scanner. The resulting activations were then compared with the responses of a galvanic vestibular control experiment and a rest condition. The vestibular recall showed significant bihemispheric activations in the inferior frontal gyri, the anterior operculum, the middle cingulate, the putamen, the globus pallidus, the premotor motor cortex, and the anterior insula. We found activations in regions known to play a role in spatial referencing, motor programs, and attention in the recall of vestibular sensations. But important known relay stations for the cortical processing of vestibular information showed neither relevant activations nor deactivations.
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Aleman A, Schutter DJ, Ramsey NF, van Honk J, Kessels RP, Hoogduin JM, Postma A, Kahn RS, de Haan EH (2002) Functional anatomy of top-down visuospatial processing in the human brain: evidence from rTMS. Brain Res Cogn Brain Res 14(2):300–302
Amedi A, Malach R, Pascual-Leone A (2005) Negative BOLD differentiates visual imagery and perception. Neuron 48(5):859–872
Assmus A, Marshall JC, Ritzl A, Noth J, Zilles K, Fink GR (2003) Left inferior parietal cortex integrates time and space during collision judgments. Neuroimage 20(Suppl 1):S82–S88
Bartolomeo P (2002) The relationship between visual perception and visual mental imagery: a reappraisal of the neuropsychological evidence. Cortex 38(3):357–378 (a journal devoted to the study of the nervous system and behavior)
Beckmann CF, DeLuca M, Devlin JT, Smith SM (2005) Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci 360(1457):1001–1013
Bensafi M, Sobel N, Khan RM (2007) Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. J Neurophysiol 98(6):3254–3262
Bense S, Stephan T, Yousry TA, Brandt T, Dieterich M (2001) Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 85(2):886–899
Best C, Tschan R, Eckhardt-Henn A, Dieterich M (2009) Who is at risk for ongoing dizziness and psychological strain after a vestibular disorder? Neuroscience 164(4):1579–1587
Brandt T, Glasauer S, Stephan T, Bense S, Yousry TA, Deutschländer A, Dieterich M (2002) Visual-vestibular and visuovisual cortical interaction: new insights from fMRI and pet. Ann N Y Acad Sci 956:230–241
Bunzeck N, Wuestenberg T, Lutz K, Heinze HJ, Jancke L (2005) Scanning silence: mental imagery of complex sounds. Neuroimage 26(4):1119–1127
Chapman LJ, Chapman JP (1987) The measurement of handedness. Brain Cogn 6(2):175–183
Chen A, DeAngelis GC, Angelaki DE (2010) Macaque parieto-insular vestibular cortex: responses to self-motion and optic flow. J Neurosci 30(8):3022–3042
Creem SH, Downs TH, Wraga M, Harrington GS, Proffitt DR, Downs JH 3rd (2001) An fMRI study of imagined self-rotation. Cogn Affect Behav Neurosci 1(3):239–249
Darlington CL, Dutia MB, Smith PF (2002) The contribution of the intrinsic excitability of vestibular nucleus neurons to recovery from vestibular damage. Eur J Neurosci 15(11):1719–1727
Diedrichsen J (2006) A spatially unbiased atlas template of the human cerebellum. Neuroimage 33(1):127–138
Dieterich M (2007) Functional brain imaging: a window into the visuo-vestibular systems. Curr Opin Neurol 20(1):12–18
Dieterich M, Bense S, Lutz S, Drzezga A, Stephan T, Bartenstein P, Brandt T (2003) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13(9):994–1007
Dieterich M, Bartenstein P, Spiegel S, Bense S, Schwaiger M, Brandt T (2005) Thalamic infarctions cause side-specific suppression of vestibular cortex activations. Brain 128(Pt 9):2052–2067
Diquattro NE, Geng JJ (2011) Contextual knowledge configures attentional control networks. J Neurosci 31(49):18026–18035
Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25(4):1325–1335
Fasold O, von Brevern M, Kuhberg M, Ploner CJ, Villringer A, Lempert T, Wenzel R (2002) Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage 17(3):1384–1393
Friston KJ (1995) Statistical Parametric Mapping: Ontology and Current Issues. J Cereb Blood Flow Metab 15:361–370
Friston KJ, Ashburner J, Frith C, Poline JB, Heather JD, Frackowiak RSJ (1995a) Spatial registration and normalization of images. Hum Brain Mapp 2:165–189
Friston KJ, Frith C, Turner R, Frackowiak RSJ (1995b) Characterizing evoked hemodynamics with fMRI. Neuroimage 2:157–165
Galati G, Pelle G, Berthoz A, Committeri G (2010) Multiple reference frames used by the human brain for spatial perception and memory. Exp Brain Res 206(2):109–120
Gardini S, De Beni R, Cornoldi C, Bromiley A, Venneri A (2005) Different neuronal pathways support the generation of general and specific mental images. Neuroimage 27(3):544–552
Genovese CR, Lazar NA, Nichols T (2002) Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 15(4):870–878
Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130(3):277–297
Grabherr L, Nicoucar K, Mast FW, Merfeld DM (2008) Vestibular thresholds for yaw rotation about an earth-vertical axis as a function of frequency. Exp Brain Res 186(4):677–681
Grabherr L, Cuffel C, Guyot JP, Mast FW (2011) Mental transformation abilities in patients with unilateral and bilateral vestibular loss. Exp Brain Res 209(2):205–214
Guldin WO, Grüsser OJ (1998) Is there a vestibular cortex? Trends Neurosci 21(6):254–259
Ionta S, Ferretti A, Merla A, Tartaro A, Romani GL (2010) Step-by-step: the effects of physical practice on the neural correlates of locomotion imagery revealed by fMRI. Hum Brain Mapp 31(5):694–702
Ionta S, Heydrich L, Lenggenhager B, Mouthon M, Fornari E, Chapuis D, Gassert R, Blanke O (2011) Multisensory mechanisms in temporo-parietal cortex support self-location and first-person perspective. Neuron 70(2):363–374
Ishai A, Ungerleider LG, Haxby JV (2000) Distributed neural systems for the generation of visual images. Neuron 28(3):979–990
Jahn K, Deutschlander A, Stephan T, Strupp M, Wiesmann M, Brandt T (2004) Brain activation patterns during imagined stance and locomotion in functional magnetic resonance imaging. Neuroimage 22(4):1722–1731
Janzen J, Schlindwein P, Bense S, Bauermann T, Vucurevic G, Stoeter P, Dieterich M (2008) Neural correlates of hemispheric dominance and ipsilaterality within the vestibular system. Neuroimage 42(4):1508–1518
Kihlstrom JF, Glisky ML, Peterson MA, Harvey EM, Rose PM (1991) Vividness and control of mental imagery: a psychometric analysis. J Ment Imag 15(3&4):133–142
King AJ (2006) Auditory neuroscience: activating the cortex without sound. Curr Biol 16(11):R410–R411
Klein I, Paradis AL, Poline JB, Kosslyn SM, Le Bihan D (2000) Transient activity in the human calcarine cortex during visual-mental imagery: an event-related fMRI study. J Cogn Neurosci 12(Suppl 2):15–23
Kobayashi M, Takeda M, Hattori N, Fukunaga M, Sasabe T, Inoue N, Nagai Y, Sawada T, Sadato N, Watanabe Y (2004) Functional imaging of gustatory perception and imagery: “top-down” processing of gustatory signals. Neuroimage 23(4):1271–1282
Kosslyn SM, Ganis G, Thompson WL (2001) Neural foundations of imagery. Nat Rev Neurosci 2(9):635–642
Le Bihan D, Turner R, Zeffiro TA, Cuenod CA, Jezzard P, Bonnerot V (1993) Activation of human primary visual cortex during visual recall: a magnetic resonance imaging study. Proc Natl Acad Sci USA 90(24):11802–11805
Logie RH, Pernet CR, Buonocore A, Sala SD (2011) Low and high imagers activate networks differentially in mental rotation. Neuropsychologia 49(11):3071–3077
Lopez C, Blanke O (2011) The thalamocortical vestibular system in animals and humans. Brain Res Rev 67(1–2):119–146
Manni E, Petrosini L (2004) A century of cerebellar somatotopy: a debated representation. Nat Rev Neurosci 5(3):241–249
Mechelli A, Price CJ, Friston KJ, Ishai A (2004) Where bottom-up meets top-down: neuronal interactions during perception and imagery. Cereb Cortex 14(11):1256–1265
Moulton ST, Kosslyn SM (2009) Imagining predictions: mental imagery as mental emulation. Philos Trans R Soc Lond B Biol Sci 364(1521):1273–1280
Nichols T, Hayasaka S (2003) Controlling the familywise error rate in functional neuroimaging: a comparative review. Stat Methods Med Res 12(5):419–446
Nir Y, Hasson U, Levy I, Yeshurun Y, Malach R (2006) Widespread functional connectivity and fMRI fluctuations in human visual cortex in the absence of visual stimulation. Neuroimage 30(4):1313–1324
Ogino Y, Nemoto H, Inui K, Saito S, Kakigi R, Goto F (2007) Inner experience of pain: imagination of pain while viewing images showing painful events forms subjective pain representation in human brain. Cereb Cortex 17(5):1139–1146
Olivetti Belardinelli M, Palmiero M, Sestieri C, Nardo D, Di Matteo R, Londei A, D’Ausilio A, Ferretti A, Del Gratta C, Romani GL (2009) An fMRI investigation on image generation in different sensory modalities: the influence of vividness. Acta Psychol (Amst) 132(2):190–200
Orban GA (2008) Higher order visual processing in macaque extrastriate cortex. Physiol Rev 88(1):59–89
Palmiero M, Belardinelli MO, Nardo D, Sestieri C, Di Matteo R, D’Ausilio A, Romani GL (2009) Mental imagery generation in different modalities activates sensory-motor areas. Cogn Process 10(Suppl 2):S268–S271
Poldrack RA (2007) Region of interest analysis for fMRI. Social Cogn Affect Neurosci 2(1):67–70
Poldrack RA, Fletcher PC, Henson RN, Worsley KJ, Brett M, Nichols TE (2008) Guidelines for reporting an fMRI study. Neuroimage 40(2):409–414
Pylyshyn ZW (2002) Mental imagery: in search of a theory. The Behavioral and brain sciences 25(2):157–182 (discussion 182–237)
Ranganath C, D’Esposito M (2005) Directing the mind’s eye: prefrontal, inferior and medial temporal mechanisms for visual working memory. Curr Opin Neurobiol 15(2):175–182
Rizzolatti G, Luppino G (2001) The cortical motor system. Neuron 31(6):889–901
Roland PE, Gulyas B (1994) Visual imagery and visual representation. Trends Neurosci 17(7):281–287 (discussion 294–287)
Sato H, Noda H (1992) Posterior vermal Purkinje cells in macaques responding during saccades, smooth pursuit, chair rotation and/or optokinetic stimulation. Neurosci Res 12(5):583–595
Schlindwein P, Mueller M, Bauermann T, Brandt T, Stoeter P, Dieterich M (2008) Cortical representation of saccular vestibular stimulation: VEMPs in fMRI. Neuroimage 39(1):19–31
Schmahmann JD, Doyon J, Toga AW, Petrides M, Evans AC (2000) MRI Atlas of the human cerebellum. Academic Press, San Diego
Shinmei Y, Yamanobe T, Fukushima J, Fukushima K (2002) Purkinje cells of the cerebellar dorsal vermis: simple-spike activity during pursuit and passive whole-body rotation. J Neurophysiol 87(4):1836–1849
Shmuel A, Augath M, Oeltermann A, Logothetis NK (2006) Negative functional MRI response correlates with decreases in neuronal activity in monkey visual area V1. Nat Neurosci 9(4):569–577
Smith PF, Darlington CL, Zheng Y (2010) Move it or lose it—is stimulation of the vestibular system necessary for normal spatial memory? Hippocampus 20(1):36–43
Smith AT, Wall MB, Thilo KV (2011) Vestibular inputs to human motion-sensitive visual cortex. Cereb Cortex (Epub ahead of print)
Stephan T, Deutschländer A, Nolte A, Schneider E, Wiesmann M, Brandt T, Dieterich M (2005) Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 26(3):721–732
Suzuki M, Kitano H, Ito R, Kitanishi T, Yazawa Y, Ogawa T, Shiino A, Kitajima K (2001) Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. Brain Res Cogn Brain Res 12(3):441–449
Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289
Westlye LT, Grydeland H, Walhovd KB, Fjell AM (2011) Associations between regional cortical thickness and attentional networks as measured by the attention network test. Cereb Cortex 21(2):345–356
Wraga M, Shephard JM, Church JA, Inati S, Kosslyn SM (2005) Imagined rotations of self versus objects: an fMRI study. Neuropsychologia 43(9):1351–1361
Zacks JM (2008) Neuroimaging studies of mental rotation: a meta-analysis and review. J Cogn Neurosci 20(1):1–19
Zaehle T, Jordan K, Wustenberg T, Baudewig J, Dechent P, Mast FW (2007) The neural basis of the egocentric and allocentric spatial frame of reference. Brain Res 1137(1):92–103
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We are grateful to Judy Benson and Sara Duke for copyediting the manuscript.
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zu Eulenburg, P., Müller-Forell, W. & Dieterich, M. On the recall of vestibular sensations. Brain Struct Funct 218, 255–267 (2013). https://doi.org/10.1007/s00429-012-0399-0
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DOI: https://doi.org/10.1007/s00429-012-0399-0