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scientific correspondence
the absence of movement? When examined from the view- subjects should be taken into account in neuroscience stud-
point of the ascending cerebello-cerebral projection, the pre- ies7. Here we demonstrate gender differences in the response
dictive nature of the Purkinje cell discharge may act as a to a visuovestibular information conflict created by a deceptive
feedforward motor correction, fine tuning ongoing process- virtual environment.
ing in higher motor centers. Discrepancies between cerebel- The visual system interacts strongly with the vestibular sys-
lar predictions and sensory feedback could arise during tem, as both sensory modalities are directly related to spatial
movement because the cerebellar output is inappropriate for processing. When visual and vestibular signals conflict, the
the current motor state of the animal or because of external dominance of vision in perceiving spatial orientation might
disturbances. Of course, external perturbations may not be cause recalibration of the vestibular system. Alternatively, the
predictable, but this should not stop the cerebellum from try- brain might ignore vestibular inputs altogether. Differences
ing to predict them. Exactly the same causes of discrepancy in the response to conflicting visuovestibular information
are present even without active movement. Thus there may be could characterize inherent gender-related spatial abilities and
one neural mechanism, LTD of parallel fiber synapses driven be related to the increased susceptibility of females to motion
by complex spikes, which seeks to maintain accuracy of the sickness8.
cerebellar output during active movement, during external The experiment used a virtual reality display to induce a
perturbation, and during steady posture. With this finely twofold visuovestibular discrepancy for angular whole-body
honed output, the cerebellum can then contribute to the nor- displacement. Twenty-six right-handed undergraduate stu-
mal smooth and coordinated control of stable posture and of dents (13 males and 13 females) rotated themselves by 90 in
active movement. a virtual visual room (Fig.1a) by controlling a rotating chair
with a joystick. The speed of these rotations was controlled by
the experimenter, and the subjects used the joystick as a start-
stop button. A gain of 0.5 was introduced between the move-
Acknowledgements ments of the chair and the visual feedback given. To achieve
This work was supported by a Wellcome Trust Senior Fellowship to RCM and a 90 rotation in the virtual room, subjects had to rotate the
by a NIH grant to WTT. chair by 180. Subjects performed 180-200 rotations, alter-
nating to the left and right, during 45 min of this visuovestibu-
lar stimulation (VVS). The magnitude and the mean speed of
1. Ito, M. Ann. Review Neurosci. 12, 85102 (1989). rotations were the same for all subjects. Before and after expo-
2. Marr, D. J. Physiol. (Lond. ) 202, 437470 (1969). sure to VVS, passive whole-body angular displacements (45,
3. Albus, J.S. Math. Biosci. 10, 2561 (1971).
4. Keating, J. G. & Thach, W. T. J. Neurophysiol. 73, 13291340 (1995). 90, 135, 180 to the left and to the right, triangular velocity
5. Crepel, F. & Jaillard, D. J. Physiol. (Lond. ) 432, 123141 (1991). profile, 11/s2) were administered in random order to blind-
6. Mauk, M.D. & Donegan, N.H. Learning & Memory 4, 130158 (1997).
7. Kenyon, G.T., Medina, J.F. & Mauk, M.D. J. Computational Neurosci. 5,
folded subjects to assess their turning perception in darkness.
1733 (1998). (See ref. 9 for details on the method.) Subjects gave their writ-
8. Nelson B., Mugnaini, E. in: Strata P. (ed) The olivo-cerebellar system in ten informed consent to the study after the procedure had
motor control. (Experimental Brain Research series 17) Springer, Berlin,
pp. 86107 (1989). been explained and were paid for their time.
9. Miall, R. C., Weir, D. J., Wolpert, D. M. & Stein, J. F. J. Motor Behav. 25, Vestibular stimulation in darkness elicited a sensation of
203216 (1993). whole-body rotation with a magnitude proportional to the
10. Miall RC Weir DJ Stein JF. J Motor Behav 25 5363 (1993).
11. Keele SW and Posner MI. J exp Psychol 77 155158 (1968). angular stimuli. Estimates of imposed rotations were not sig-
12. Carlton LG. J Exp Psychol Human Percept Perform 7 10191030 (1981). nificantly different in males and females prior to VVS. After
13. Thach, W.T., Goodkin H.P. & Keating J.G. Annu Review Neurosci 15, exposure to conflicting VVS, decreases in turning estimates
403442 (1992).
14. Thach, W.T., Kane SA, Mink JW and Goodkin HP. In: Llinas R and Sotelo were significantly greater for males than for females (F(1,24)
C, eds. The cerebellum revisited. New York: Springer-Verlag, pp. 427460 = 7.96, p<0.01) (Fig.1b), although some females did adapt
(1992). more than some males. Interestingly, recalibration of vestibu-
15. Sugihara, I., Lang, E. J. & Llinas, R. J. Physiol. (Lond) 470, 243271 (1993).
16. Welsh, J. P., Lang, E. J., Sugihara, I. & Llinas, R. Nature 374, 453457 lar inputs at the perceptual level occurred without awareness
(1995). of the visual-vestibular information conflict.
scientific correspondence
a b
Decrease in vestibular
perception (%)
Females Males
(n=13) (n=13)
Fig. 1. Virtual room and gender differences in adaptation to sensorial conflict. (a) Subjects seated on a rotating chair were given the experience of
being placed in the center of a virtual square room (non-stereoscopic) by means of a head-mounted display. (b) Decrease in turning estimates in
darkness for males and for females after exposure to conflicting VVS relative to those before VVS.
1998 Nature America Inc. http://neurosci.nature.com
Our results provide evidence for the necessity of taking sex dif- Acknowledgements
ferences into account in psychophysical studies involving dynam- Supported by GIS-Science de la Cognition, SmithKline Beecham, HFSP, FRM.
ic spatial processing. It has been proposed that females are more 1. Halpern, D.F. Sex differences in cognitive abilities (Lawrence Erlbaum,
influenced by visual cues, using tasks that involve spatial memo- Hillsdale, NJ, 1986).
2. Stumpf, H. Mem. Cognit., 21, 828836 (1993).
ry4 or the perception of verticality10. Here we found differences in 3. McBurney, D.H., Gaulin, S.J.C., Devineni, T. & Adams, C. Evolution
adaptation to sensorial conflict during immersion in a virtual envi- Human Behav. 18, 165174 (1997).
ronment. Female subjects were less susceptible to the plastic 4. Eals, M. & Silverman, I. Ethnology Sociobiol.15, 95105 (1995).
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changes induced by exposure to conflicting visuovestibular stimuli. 6. Wittelson, S.F., Glezer, I.I. & Kigar, D.L. J. Neurosci. 15, 34183428 (1995).
The role of visual dependence and other factors influencing rota- 7. Berkley, K.J. Trends Neurosci. 15, 331332 (1992).
tion estimates has to be further assessed. Studies of dynamic mul- 8. Lawther, A. & Griffin, M.J. Aviat. Space Environ. Med. 59, 399406 (1988).
9. Ivanenko, Y.P., Viaud-Delmon, I., Siegler, I., Isral, I. & Berthoz, A.
tisensory integration may contribute to a better understanding of Neurosci. Lett. 241, 167170 (1998).
gender-related differences in spatial processing. 10. Scholan, K. & Smith, M. Percep. Mot. Skills 71, 763768 (1990).