Abstract
Successful interaction with the external environment requires a balance between novel or exploratory and routine or exploitative behaviours. This distinction is often expressed in terms of location or orientation of the body relative to surrounding space: functions in which the vestibular system plays an important role. However, the distinction can also be applied to novel versus repetitive production of any behaviour or symbol. Here, we investigated whether vestibular inputs contribute to the balance between novel and routine behaviours, independently of their effects on spatial orienting, by assessing effects of galvanic vestibular stimulation (GVS) on a random number generation task. Right-anodal/left-cathodal GVS, which preferentially activates the left cerebral hemisphere decreased the randomness of the sequence, while left-anodal/right-cathodal GVS, which preferentially activates the right hemisphere increased it. GVS did not induce any spatial biases in locations chosen from the number line. Our results suggest that vestibular stimulation of each hemisphere has a specific effect on the balance between novel and routine actions. We found no evidence for effects of non-specific arousal due to GVS on random number generation, and no evidence for effects on number generation consistent with modulation of spatial attention due to GVS.
Similar content being viewed by others
Abbreviations
- GVS:
-
Galvanic vestibular stimulation
- R score:
-
Redundancy score
- RNG-I:
-
Random number generation index
- FODs:
-
First-order differences
References
Bains W (2008) Random number generation and creativity. Med Hypotheses 70(1):186–190
Barnett-Cowan M, Harris LR (2009) Perceived timing of vestibular stimulation relative e to touch, light and sound. Exp Brain Res 198(2–3):221–231
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
Berthoz A (1996) How does the cerebral cortex process and utilize vestibular signals. In: Halmagyi GM, Baloh RW (eds) Disorders of the vestibular system. Oxford University Press, Oxford, pp 113–125
Bucher SF, Dieterich M, Wiesmann M, Weiss A, Zink R, Yousry TA et al (1998) Cerebral functional magnetic resonance imaging of vestibular, auditory, and nociceptive areas during galvanic stimulation. Ann Neurol 44(1):120–125
Cohen JD, McClure SM, Yu AJ (2007) Should I stay or should I go? How the human brain manages the trade-off between exploitation and exploration. Philos Trans R Soc Lond B Biol Sci 362(1481):933–942
Daniels C, Witt K, Wolff S, Jansen O, Deuschl G (2003) Rate dependency of the human cortical network subserving executive functions during generation of random number series: a functional magnetic resonance imaging study. Neurosci Lett 345(1):25–28
Daw ND, O’Doherty JP, Seymour B, Dayan P, Dolan RJ (2006) Cortical substrates for exploratory decisions in humans. Nature 441:876–879
Day BL, Fitzpatrick RC (2005) Virtual head rotation reveals a process of route reconstruction from human vestibular signals. J Physiol 567(Pt 2):591–597
Day BL, Séverac Cauquil A, Bartolomei L, Pastor MA, Lyon IN (1997) Human body-segment tilts induced by galvanic stimulation: a vestibularly driven balance protection mechanism. J Physiol 500(Pt 3):661–672
de Hevia MD, Vallar G, Girelli L (2008) Visualizing numbers in the mind’s eye: the role of visuo-spatial processes in numerical abilities. Neurosci Biobehav Rev 32(8):1361–1372
Dehaene S (1992) Varieties of numerical abilities. Cognition 44(1–2):1–42
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
Dilda V, MacDougall HG, Curthoys IS, Moore ST (2012) Effects of galvanic vestibular stimulation on cognitive function. Exp Brain Res 216(2):275–285
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(10):1638–1651
Fink GR, Marshall JC, Weiss PH, Stephan T, Grefkes C, Shah NJ et al (2003) Performing allocentric visuospatial judgments with induced distortion of the egocentric reference frame: an fMRI study with clinical implications. Neuroimage 20(3):1505–1517
Fitzpatrick RC, Day BL (2004) Probing the human vestibular system with galvanic stimulation. J Appl Physiol 96(6):2301–2316
Galfano G, Rusconi E, Umilta C (2006) Number magnitude orients attention, but not against one’s will. Psychon Bull Rev 13(5):869–874
Goldberg JM, Smith CE, 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(6):1236–1256
Goldberg E, Podell K, Lovell M (1994) Lateralization of frontal lobe functions and cognitive novelty. J Neuropsychiatry Clin Neurosci 6(4):371–378
Hartmann M, Grabherr L, Mast FW (2011) Moving along the mental number line: Interactions between whole-body motion and numerical cognition. J Exp Psychol Hum Percept Perform. doi:10.1037/a0026706
Jahanshahi M, Profice P, Brown RG, Ridding MC, Dirnberger G, Rothwell JC (1998) The effects of transcranial magnetic stimulation over the dorsolateral prefrontal cortex on suppression of habitual counting during random number generation. Brain 121(Pt 8):1533–1544
Jahanshahi M, Dirnberger G, Fuller R, Frith CD (2000) The role of the dorsolateral prefrontal cortex in random number generation: a study with positron emission tomography. Neuroimage 12(6):713–725
Kerkhoff G, Hildebrandt H, Reinhart S, Kardinal M, Dimova V, Utz KS (2011) A long-lasting improvement of tactile extinction after galvanic vestibular stimulation: two Sham-stimulation controlled case studies. Neuropsychologia 49(2):186–195
Lobel E, Kleine JF, Bihan DL, Leroy-Willig A, Berthoz A (1998) Functional MRI of galvanic vestibular stimulation. J Neurophysiol 80(5):2699–2709
Loetscher T, Brugger P (2007) Exploring number space by random digit generation. Exp Brain Res 180(4):655–665
Loetscher T, Brugger P (2009) Random number generation in neglect patients reveals enhanced response stereotypy, but no neglect in number space. Neuropsychologia 47(1):276–279
Loetscher T, Schwarz U, Schubiger M, Brugger P (2008) Head turns bias the brain’s internal random generator. Curr Biol 22(18(2)):R60–R62
Lopez C, Lenggenhager B, Blanke O (2010) How vestibular stimulation interacts with illusory hand ownership. Conscious Cogn 19(1):33–47
Lopez C, Blanke O, Mast FW (2012) The human vestibular cortex revealed by coordinate-based activation likelihood estimation meta-analysis. Neuroscience 212:159–179
Lumer ED, Friston KJ, Rees G (1998) Neural correlates of perceptual rivalry in the human brain. Science 280(5371):1930–1934
Miller SM, Liu GB, Ngo TT, Hooper G, Riek S, Carson RG et al (2000) Interhemispheric switching mediates perceptual rivalry. Curr Biol 10(7):383–392
Norman W, Shallice T (1986) Attention to action. In: Davidson RJ, Schwartz GE, Shapiro D (eds) Consciousness and self regulation: advances in research and theory, vol 4. Plenum, New York, pp 1–18
Peters M, Giesbrecht T, Jelicic M, Merckelbach H (2007) The random number generation task: psychometric properties and normative data of an executive function task in a mixed sample. J Int Neuropsychol Soc 13(4):626–634
Rorden C, Karnath HO, Driver J (2001) Do neck-proprioceptive and caloric-vestibular stimulation influence covert visual attention in normals, as they influence visual neglect? Neuropsychologia 39(4):364–375
Rubens AB (1985) Caloric stimulation and unilateral visual neglect. Neurology 35(7):1019–1024
Sandson J, Albert ML (1987) Perseveration in behavioral neurology. Neurology 37(11):1736–1741
Spatt J, Goldenberg G (1993) Components of random generation by normal subjects and patients with dysexecutive syndrome. Brain Cogn 23(2):231–242
Stephan T, Deutschlander A, Nolte A, Schneider E, Wiesmann M, Brandt T et al (2005) Functional MRI of galvanic vestibular stimulation with alternating currents at different frequencies. Neuroimage 26(3):721–732
Strenge H, Bohm J (2004) Random number generation in native and foreign languages. Percept Mot Skills 98(3 Pt 2):1153–1161
Strenge H, Rogge C (2010) Strategic use of number representation is independent of test instruction in random number generation. Percept Mot Skills 110(2):453–462
Sugrue LP, Corrado G, Newsome WT (2004) Matching behavior and the representation of value in the parietal cortex. Science 304:1782–1787
Towse JN (1998) On random generation and the central executive of working memory. Br J Psychol 89(Pt 1):77–101
Towse J, Neil D (1998) Analyzing human random generation behavior: a review of methods used and a computer program for describing performance. Behav Res Methods Instrum Comput 30(4):583–591
Trainor LJ, Gao X, Lei JJ, Lehtovaara K, Harris LR (2009) The primal role of the vestibular system in determining musical rhythm. Cortex 45(1):35–43
Utz KS, Dimova V, Oppenlander K, Kerkhoff G (2010a) 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(10):2789–2810
Utz KS, Korluss K, Schmidt L, Rosenthal A, Oppenlander K, Keller I et al (2010b) Minor adverse effects of galvanic vestibular stimulation in persons with stroke and healthy individuals. Brain Inj 25(11):1058–1069
Utz KS, 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(5):1219–1225
Vallar G, Sterzi R, Bottini G, Cappa S, Rusconi ML (1990) Temporary remission of left hemianesthesia after vestibular stimulation. A sensory neglect phenomenon. Cortex 26(1):123–131
Acknowledgments
This work was supported by a BIAL Foundation Bursary (215/10) awarded to PH. PH was further supported by EU FP7 project VERE and by a Leverhulme Trust Major Research Fellowship.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ferrè, E.R., Vagnoni, E. & Haggard, P. Galvanic vestibular stimulation influences randomness of number generation. Exp Brain Res 224, 233–241 (2013). https://doi.org/10.1007/s00221-012-3302-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00221-012-3302-6