Interaction of brain areas of visual and vestibular simultaneous activity with fMRI

Experimental Brain Research

Volumn 233, Issue 1, 2015, Pages 237-252

  Della Justina, Hellen M ^a   Gamba, Humberto R ^a   Lukasova, Katerina ^b   Nucci da Silva, Mariana P ^b   Winkler, Anderson M ^c,d   Amaro, Edson ^b  

^a UNIVERSIDADE TECNOLÓGICA FEDERAL DO PARANÁ   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

fMRI; Simultaneous stimulation; Vestibular system; Visual system; Visual vestibular interaction

Indexed keywords

ADULT; ARTICLE; ASSOCIATION; ASSOCIATION CORTEX; BOLD SIGNAL; BRAIN FUNCTION; BRAIN INTERACTION; CALCARINE SULCUS; CONTROLLED STUDY; CUNEUS; ELECTROENCEPHALOGRAM; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; GALVANIC CURRENT; HEMISPHERE; HUMAN; HUMAN EXPERIMENT; IMAGING SOFTWARE; INFERIOR FRONTAL GYRUS; INFERIOR PARIETAL LOBULE; LINGUAL GYRUS; MALE; MIDDLE FRONTAL GYRUS; NORMAL HUMAN; NUCLEAR MAGNETIC RESONANCE SCANNER; OCCIPITAL CORTEX; PARIETAL CORTEX; PARIETO INSULAR VESTIBULAR CORTEX; PRECUNEUS; PRIMARY MOTOR CORTEX; PRIORITY JOURNAL; RIGHT HANDEDNESS; SOMATOSENSORY CORTEX; STRIATE CORTEX; SUPERIOR TEMPORAL GYRUS; TEMPORAL CORTEX; VESTIBULAR NERVOUS SYSTEM; VESTIBULAR STIMULATION; VISUAL NERVOUS SYSTEM; VISUAL STIMULATION; BRAIN; MOVEMENT PERCEPTION; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOSTIMULATION; PHYSIOLOGY; VISION; YOUNG ADULT;

ADULT; BRAIN; FEMALE; FUNCTIONAL NEUROIMAGING; HUMANS; MAGNETIC RESONANCE IMAGING; MALE; MOTION PERCEPTION; PHOTIC STIMULATION; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84922080202     PISSN: 00144819     EISSN: 14321106     Source Type: Journal    
DOI: 10.1007/s00221-014-4107-6     Document Type: Article

References (87)

1. Akbarian S, Grüsser OJ, Guldin WO (1993) Corticofugal projections to the vestibular nuclei in squirrel monkeys: further evidence of multiple cortical vestibular fields. J Comp Neurol 332:89–104
2. Akbarian S, Grüsser OJ, Guldin WO (1994) Corticofugal connections between the cerebral cortex and brainstem vestibular nuclei in the macaque monkey. J Comp Neurol 339:421–437
3. Amorim P (2002) Mini international neuropsychiatric interview (MINI): validation of a short structured diagnostic psychiatric interview. Rev Bras Psiquiatr 22:106–115
4. Anderson TJ, Jenkins IH, Brooks DJ et al (1994) Cortical control of saccades and fixation in man. A PET study. Brain 117:1073–1084
5. Aw ST, Todd MJ, Halmagyi GM (2006) Latency and initiation of the human vestibuloocular reflex to pulsed galvanic stimulation. J Neurophysiol 96:925–930
6. Baier B, Conrad J, Zu Eulenburg P et al (2013) Insular strokes cause no vestibular deficits. Stroke 44:2604–2606
7. Barton JJ, Simpson T, Kiriakopoulos E et al (1996) Functional MRI of lateral occipitotemporal cortex during pursuit and motion perception. Ann Neurol 40:387–398
8. Bennett CM, Wolford GL, Miller MB (2009) The principled control of false positives in neuroimaging. Soc Cogn Affect Neurosci 4:417–422
9. Bense S, Stephan T, Yousry TA et al (2001) Multisensory cortical signal increases and decreases during vestibular galvanic stimulation (fMRI). J Neurophysiol 85(2):886–899
10. Bianciardi M, Fukunaga M, van Gelderen P et al (2011) Negative BOLD–fMRI signals in large cerebral veins. J Cereb Blood Flow Metab 31:401–412
11. Boisgueheneuc F, Levy R, Volle E et al (2006) Functions of the left superior frontal gyrus in humans: a lesion study. Brain 129:3315–3328
12. Bottini G, Sterzi R, Paulesu E et al (1994) Identification of the central vestibular projections in man: a positron emission tomography activation study. Exp Brain Res 99:164–169
13. Bottini G, Paulesu E, Gandola M et al (2005) Left caloric vestibular stimulation ameliorates right hemianesthesia. Neurology 65:1278–1283
14. Bottini G, Gandola M, Sedda A, Ferrè ER (2013) Caloric vestibular stimulation: interaction between somatosensory system and vestibular apparatus. Front Integr Neurosci 7:1–3
15. Braddick OJ, O’Brien JMD, Wattam-Bell J et al (2001) Brain areas sensitive to coherent visual motion. Percept 30:61–72
16. Brandt T, Dieterich M (1999) The vestibular cortex. Its locations, functions, and disorders. Ann N Y Acad Sci 871:293–312
17. 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
18. Bremmer F (2001) Space coding in primate posterior parietal cortex. Neuroimage 14:S46–S51
19. Bressler D, Spotswood N, Whitney D (2007) Negative BOLD fMRI response in the visual cortex carries precise stimulus-specific information. PLoS ONE 2:e410
20. Brett M, Anton J, Valabregue R, Poline J (2002) Region of interest analysis using an SPM toolbox [abstract]. Paper presented at the 8th International Conference on Functional Mapping of the Human Brain, Sendai, Japan
21. Cambraia S (2003) The concentrated attention test. Vetor, São Paulo
22. Cardin V, Smith AT (2010) Sensitivity of human visual and vestibular cortical regions to egomotion-compatible visual stimulation. Cereb Cortex 20:1964–1973
23. D’Esposito M, Aguirre GK, Zarahn E et al (1998) Functional MRI studies of spatial and nonspatial working memory. Cogn Brain Res 7:1–13
24. Delis D, Kaplan E, Kramer J (2001) Delis-Kaplan executive function system: examiner’s manual. The Psychological Corporation, São António
25. Della-Justina HM, Postorello BF, Santos-Pontelli TEG et al (2008) Human variability of fMRI brain activation in response to oculomotor stimuli. Brain Topogr 20:113–121
26. Della-Justina HM, Manczak T, Winkler AM et al (2014) Galvanic vestibular stimulator for fMRI studies. Braz J Biomed Eng 30:70–82
27. Deutschländer A, Bense S, Stephan T et al (2002) Sensory system interactions during simultaneous vestibular and visual stimulation in PET. Hum Brain Mapp 16:92–103
28. Dieterich M, Bucher SF, Seelos KC, Brandt T (1998) Horizontal or vertical optokinetic stimulation activates visual motion-sensitive, ocular motor and vestibular cortex areas with right hemispheric dominance. An fMRI study. Brain 121:1479–1495
29. Dieterich M, Bense S, Lutz S et al (2003a) Dominance for vestibular cortical function in the non-dominant hemisphere. Cereb Cortex 13:994–1007
30. Dieterich M, Bense S, Stephan T et al (2003b) fMRI signal increases and decreases in cortical areas during small-field optokinetic stimulation and central fixation. Exp Brain Res 148:117–127
31. Driver J, Noesselt T (2008) Multisensory interplay reveals crossmodal influences on “sensory-specific” brain regions, neural responses, and judgments. Neuron 57:11–23
32. Eickhoff SB, Stephan K, Mohlberg H et al (2005) A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage 25:1325–1335
33. Eickhoff SB, Heim S, Zilles K, Amunts K (2006a) Testing anatomically specified hypotheses in functional imaging using cytoarchitectonic maps. Neuroimage 32:570–582
34. Eickhoff SB, Weiss PH, Amunts K et al (2006b) Identifying human parieto-insular vestibular cortex using fMRI and cytoarchitectonic mapping. Hum Brain Mapp 27:611–621
35. Eickhoff SB, Paus T, Caspers S et al (2007) Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. Neuroimage 36:511–521
36. Fasold O, von Brevern M, Kuhberg M et al (2002) Human vestibular cortex as identified with caloric stimulation in functional magnetic resonance imaging. Neuroimage 17:1384–1393
37. Ferrè ER, Bottini G, Haggard P (2011a) Vestibular modulation of somatosensory perception. Eur J Neurosci 34:1337–1344
38. Ferrè ER, Sedda A, Gandola M, Bottini G (2011b) How the vestibular system modulates tactile perception in normal subjects: a behavioural and physiological study. Exp Brain Res 208:29–38
39. Ferrè ER, Bottini G, Haggard P (2012) Vestibular inputs modulate somatosensory cortical processing. Brain Struct Funct 217:859–864
40. Ferrè ER, Day BL, Bottini G, Haggard P (2013) How the vestibular system interacts with somatosensory perception: a sham-controlled study with galvanic vestibular stimulation. Neurosci Lett 550:35–40
41. Fink G, Marshall JC, Weiss PH et al (2003) Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: an fMRI study with clinical implications. Neuroimage 20:1505–1517
42. Fox PT, Raichle ME (1985) Stimulus rate determines regional brain blood flow in striate cortex. Ann Neurol 17:303–305
43. Friston KJ, Holmes AP, Worsley KJ et al (1995) Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp 2:189–210
44. Glover GH (1999) Deconvolution of impulse response in event-related BOLD fMRI. Neuroimage 9:416–429
45. Guldin W, Grüsser OJ (1996) The anatomy of the vestibular cortices of primates. In: Collard M, Jeannerod M, Christen Y (eds) Le cortex vestibulaire. Irvinn, Paris, pp 17–26
46. Guldin WO, Grüsser OJ (1998) Is there a vestibular cortex? Trends Neurosci 21:254–259
47. Guldin W, Akbarian S, Grüsser OJ (1992) Cortico–cortical connections and cytoarchitectonics of the primate vestibular cortex: a study in squirrel monkeys (Saimiri sciureus). J Comp Neurol 326:375–401
48. Harel N, Lee SP, Nagaoka T et al (2002) Origin of negative blood oxygenation level-dependent fMRI signals. J Cereb Blood Flow Metab 22:908–917
49. Kahane P, Hoffmann D, Minotti L, Berthoz A (2003) Reappraisal of the human vestibular cortex by cortical electrical stimulation study. Ann Neurol 54:615–624
50. Kleinschmidt A, Thilo KV, Büchel C et al (2002) Neural correlates of visual-motion perception as object- or self-motion. Neuroimage 16:873–882
51. Lacquaniti F, Bosco G, Indovina I et al (2013) Visual gravitational motion and the vestibular system in humans. Front Integr Neurosci 7:1–12. doi:10.3389/fnint.2013.00101
52. Lobel E, Kleine JF, Le Bihan D et al (1998) Functional MRI of galvanic vestibular stimulation. J Neurophysiol 80:2699–2709
53. Logothetis NK (2002) The neural basis of the blood-oxygen-level-dependent functional magnetic resonance imaging signal. Philos Trans R Soc Lond B Biol Sci 357:1003–1037
54. Lopez C, Halje P, Blanke O (2008) Body ownership and embodiment: vestibular and multisensory mechanisms. Clin Neurophysiol 38:149–161. doi:10.1016/j.neucli.2007.12.006
55. Lopez C, Blanke O, Mast FW (2012) The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 212:159–179. doi:10.1016/j.neuroscience.2012.03.028
56. Macaluso E, Driver J (2005) Multisensory spatial interactions: a window onto functional integration in the human brain. Trends Neurosci 28:264–271. doi:10.1016/j.tins.2005.03.008
57. MacDougall HG, Moore ST, Curthoys IS, Black FO (2006) Modeling postural instability with galvanic vestibular stimulation. Exp Brain Res 172:208–220
58. Marcelli V, Esposito F, Aragri A et al (2009) Spatio-temporal pattern of vestibular information processing after brief caloric stimulation. Eur J Radiol 70:312–316
59. Moore ST, MacDougall HG, Peters BT et al (2006) Modeling locomotor dysfunction following spaceflight with galvanic vestibular stimulation. Exp Brain Res 174:647–659
60. Naito Y, Tateya I, Hirano S et al (2003) Cortical correlates of vestibulo-ocular reflex modulation: a PET study. Brain 126:1562–1578
61. Nigmatullina Y, Hellyer PJ, Nachev P et al (2013) The neuroanatomical correlates of training-related perceptuo-reflex uncoupling in dancers. Cereb Cortex. doi:10.1093/cercor/bht266 [Epub ahead of print]
62. Oldfield R (1971) The assessment and analysis of handedness: the Edinburgh inventory. Neurophysiologia 9:97–113
63. Owen AM (1997) The functional organization of working memory processes within human lateral frontal cortex: the contribution of functional neuroimaging. Eur J Neurosci 9:1329–1339
64. Pasley BN, Inglis BA, Freeman RD (2007) Analysis of oxygen metabolism implies a neural origin for the negative BOLD response in human visual cortex. Neuroimage 36:269–276
65. Petit L, Haxby JV (1999) Functional anatomy of pursuit eye movements in humans as revealed by fMRI. J Neurophysiol 82:463–471
66. Probst T, Wist E (1990) Electrophysiological evidence for visual–vestibular interaction in man. Neurosci Lett 108:255–260
67. Probst T, Straube A, Bles W (1985) Differential effects of ambivalent visual–vestibular-somatosensory stimulation on the perception of self-motion. Behav Brain Res 16:71–79
68. Probst T, Brandt T, Degner D (1986) Object-motion detection affected by concurrent self-motion perception: psychophysics of a new phenomenon. Behav Brain Res 22:1–11
69. Ronchi R, Rode G, Cotton F et al (2013) Remission of anosognosia for right hemiplegia and neglect after caloric vestibular stimulation. Restor Neurol Neurosci 31:19–24
70. Schneider E, Glasauer S, Dieterich M (2000) Central processing of human ocular torsion analyzed by galvanic vestibular stimulation. NeuroReport 11:1559–1563
71. Schubert T, Szameitat AJ (2003) Functional neuroanatomy of interference in overlapping dual tasks: an fMRI study. Cogn Brain Res 17:733–746
72. Seemungal BM, Guzman-Lopez J, Arshad Q et al (2013) Vestibular activation differentially modulates human early visual cortex and V5/MT excitability and response entropy. Cereb Cortex 23:12–19
73. Shaikh AG, Palla A, Marti S et al. (2013) Role of cerebellum in motion perception and vestibulo-ocular reflex-similarities and disparities. Cerebellum 12:97–107. doi:10.1007/s12311-012-0401-7
74. Shmuel A, Yacoub E, Pfeuffer J et al (2002) Sustained negative BOLD, blood flow and oxygen consumption response and its coupling to the positive response in the human brain. Neuron 36:1195–1210
75. 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 9:569–577
76. Singh M, Kim S, Kim T-S (2003) Correlation between BOLD–fMRI and EEG signal changes in response to visual stimulus frequency in humans. Magn Reson Med 49:108–114
77. Smith AT, Wall MB, Thilo KV (2012) Vestibular inputs to human motion-sensitive visual cortex. Cereb Cortex 22:1068–1077
78. Stephan T, Deutschländer A, Nolte A et al (2005) Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 26:721–732
79. Stoodley CJ, Schmahmann JD (2009) Functional topography in the human cerebellum: a meta-analysis of neuroimaging studies. Neuroimage 44:489–501. doi:10.1016/j.neuroimage.2008.08.039
80. Suzuki M, Kitano H, Ito R et al (2001) Cortical and subcortical vestibular response to caloric stimulation detected by functional magnetic resonance imaging. Cogn Brain Res 12:441–449
81. Vallar G (1998) Spatial hemineglect in humans. Trends Cogn Sci 2:87–97
82. Wall MB, Smith AT (2008) The representation of egomotion in the human brain. Curr Biol 18:191–194
83. Wardman DL, Taylor JL, Fitzpatrick RC (2003) Effects of galvanic vestibular stimulation on human posture and perception while standing. J Physiol 551:1033–1042. doi:10.1113/jphysiol.2003.045971
84. Watson SRD, Brizuela AE, Curthoys IS et al (1998) Maintained ocular torsion produced by bilateral and unilateral galvanic (DC) vestibular stimulation in humans. Exp Brain Res 122:453–458
85. Wechsler D (2004) The Wechsler adult intelligence scale. Translation and validation of Brazilian version. Casa do Psicólogo, São Paulo
86. Weeks RA, Aziz-Sultan A, Bushara KO et al (1999) A PET study of human auditory spatial processing. Neurosci Lett 262:155–158
87. Zink R, Bucher SF, Weiss A et al (1998) Effects of galvanic vestibular stimulation on otolithic and semicircular canal eye movements and perceived vertical. Electroencephalogr Clin Neurophysiol 107:200–205