How vestibular neurons solve the tilt/translation ambiguity: Comparison of brainstem, cerebellum, and thalamus

Annals of the New York Academy of Sciences

Volumn 1164, Issue , 2009, Pages 19-28

  Angelaki, Dora E ^a   Yakusheva, Tatyana A ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Cerebellum; Linear acceleration; Purkinje cell; Rotation; Translation; Velocity storage; Vermis; Vestibular

Indexed keywords

BRAIN STEM; CEREBELLUM; CEREBELLUM CORTEX; COMPARATIVE STUDY; CONFERENCE PAPER; FASTIGIAL NUCLEUS; GRAVITY; HEAD MOVEMENT; HEAD POSITION; HEAD TILTING; HUMAN; OTOLITH; PALATE; PURKINJE CELL; SEMICIRCULAR CANAL; SPATIAL ORIENTATION; THALAMUS; VESTIBULAR NUCLEUS;

EID: 66149133201     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2009.03939.x     Document Type: Conference Paper

References (65)

1. Angelaki, D.E. et al. 2004. Neurons compute internal models of the physical laws of motion. Nature 430 : 560 564.
2. Dickman, J.D., D.E. Angelaki and M.J. Correia. 1991. Response properties of gerbil otolith afferents to small angle pitch and roll tilts. Brain Res. 556 : 303 310.
3. Fernandez, C., J.M. Goldberg and W.K. Abend. 1972. Response to static tilts of peripheral neurons innervating otolith organs of the squirrel monkey. J. Neurophysiol. 35 : 978 987.
4. Angelaki, D.E. et al. 1999. Computation of inertial motion: neural strategies to resolve ambiguous otolith information. J. Neurosci. 19 : 316 327.
5. Merfeld, D.M., L. Zupan and R.J. Peterka. 1999. Humans use internal models to estimate gravity and linear acceleration. Nature 398 : 615 618.
6. Zupan, L.H. and D.M. Merfeld. 2003. Neural processing of gravito-inertial cues in humans. IV. Influence of visual rotational cues during roll optokinetic stimuli. J. Neurophysiol. 89 : 390 400.
7. MacNeilage, P.R., et al. 2007. A Bayesian model of the disambiguation of gravitoinertial force by visual cues. Exp. Brain Res. 179 : 263 290.
8. Green, A.M. and D.E. Angelaki. 2003. Resolution of sensory ambiguities for gaze stabilization requires a second neural integrator. J. Neurosci. 23 : 9265 9275.
9. Merfeld, D.M. et al. 2005. Vestibular perception and action employ qualitatively different mechanisms. I. Frequency response of VOR and perceptual responses during Translation and Tilt. J. Neurophysiol. 94 : 186 198.
10. Merfeld, D.M. et al. 2005. Vestibular perception and action employ qualitatively different mechanisms. II. VOR and perceptual responses during combined Tilt and Translation. J. Neurophysiol. 94 : 199 205.
11. Glasauer, S. and D.M. Merfeld. 1997. Modeling three-dimensional responses during complex motion stimulation. In Three-dimensional kinematics of eye, head and limb movements. M. Fetter, et al., Eds 387 398. Harwood Academic. Amsterdam.
12. Merfeld, D.M. 1995. Modeling the vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp. Brain Res. 106 : 123 134.
13. Merfeld, D.M. and L.H. Zupan. 2002. Neural processing of gravitoinertial cues in humans. III. Modeling tilt and translation responses. J. Neurophysiol. 87 : 819 833.
14. Mergner, T. and S. Glasauer. 1999. A simple model of vestibular canal-otolith signal fusion. Ann. N. Y. Acad. Sci. 871 : 430 434.
15. Zupan, L.H., D.M. Merfeld and C. Darlot. 2002. Using sensory weighting to model the influence of canal, otolith and visual cues on spatial orientation and eye movements. Biol. Cybern. 86 : 209 w230.
16. Glasauer, S. 1995. Linear acceleration perception: frequency dependence of the hilltop illusion. Acta Otolaryngol. Suppl. 520 (Pt 1 37 40.
17. Carpenter, M.B., B.M. Stein and P. Peter. 1972. Primary vestibulocerebellar fibers in the monkey: distribution of fibers arising from distinctive cell groups of the vestibular ganglia. Am. J. Anat. 135 : 221 249.
18. Gerrits, N.M. et al. 1989. The primary vestibulocerebellar projection in the rabbit: absence of primary afferents in the flocculus. Neurosci. Lett. 105 : 27 33.
19. Barmack, N.H. et al. 1993. Vestibular primary afferent projection to the cerebellum of the rabbit. J. Comp. Neurol. 327 : 521 534.
20. Kevetter, G.A. and A.A. Perachio. 1986. Distribution of vestibular afferents that innervate the sacculus and posterior canal in the gerbil. J. Comp. Neurol. 254 : 410 424.
21. Kevetter, G.A. et al. 2004. Central distribution of vestibular afferents that innervate the anterior or lateral semicircular canal in the mongolian gerbil. J. Vestib. Res. 14 : 1 15.
22. Newlands, S.D. et al. 2003. Central projections of the saccular and utricular nerves in macaques. J. Comp. Neurol. 466 : 31 47.
23. Angelaki, D.E. and B.J. Hess. 1994. The cerebellar nodulus and ventral uvula control the torsional vestibulo-ocular reflex. J. Neurophysiol. 72 : 1443 1447.
24. Angelaki, D.E. and B.J. Hess. 1994. Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. Vestibuloocular reflex. J. Neurophysiol. 71 : 1222 1249.
25. Angelaki, D.E. and B.J. Hess. 1995. Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus. J. Neurophysiol. 73 : 1729 1751.
26. Angelaki, D.E. and B.J. Hess. 1995. Lesion of the nodulus and ventral uvula abolish steady-state off-vertical axis otolith response. J. Neurophysiol. 73 : 1716 1720.
27. Wearne, S., T. Raphan and B. Cohen. 1998. Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J. Neurophysiol. 79 : 2690 2715.
28. Solomon, D. and B. Cohen. 1994. Stimulation of the nodulus and uvula discharges velocity storage in the vestibulo-ocular reflex. Exp. Brain Res. 102 : 57 68.
29. Yakusheva, T.A. et al. 2007. Purkinje cells in posterior cerebellar vermis encode motion in an inertial reference frame. Neuron 54 : 973 985.
30. Yakusheva, T., P.M. Blazquez and D.E. Angelaki. 2008. Frequency-selective coding of translation and tilt in macaque cerebellar nodulus and uvula. J. Neurosci. 28 : 9997 10009.
31. Green, A.M., A.G. Shaikh and D.E. Angelaki. 2005. Sensory vestibular contributions to constructing internal models of self-motion. J. Neural Eng. 2 : S164 S179.
32. Shaikh, A.G. et al. 2005. Properties of cerebellar fastigial neurons during translation, rotation, and eye movements. J. Neurophysiol. 93 : 853 863.
33. Shaikh, A.G. et al. 2005. Sensory convergence solves a motion ambiguity problem. Curr. Biol. 15 : 1657 1662.
34. Meng, H. et al. 2007. Vestibular signals in primate thalamus: properties and origins. J. Neurosci. 27 : 13590 13602.
35. Graybiel, A. and B. Clark. 1952. Duration of oculogyral illusion as a function of the interval between angular acceleration and deceleration; its significance in terms of dynamics of semicircular canals in man. J. Appl. Physiol. 5 : 147 152.
36. Clark, B. and A. Graybiel. 1963. Contributing factors in the perception of the oculogravic illusion. Am. J. Psychol. 76 : 18 27.
37. Clark, B. and A. Graybiel. 1966. Factors contributing to the delay in the perception of the oculogravic illusion. Am. J. Psychol. 79 : 377 388.
38. Fernandez, C. and J.M. Goldberg. 1976. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. I. Response to static tilts and to long-duration centrifugal force. J. Neurophysiol. 39 : 970 984.
39. Fernandez, C. and J.M. Goldberg. 1976. Physiology of peripheral neurons innervating otolith organs of the squirrel monkey. III. Response dynamics. J. Neurophysiol. 39 : 996 1008.
40. Shojaku, H. et al. 1987. Topographical distribution of Purkinje cells in the uvula and the nodulus projecting to the vestibular nuclei in cats. Brain Res. 416 : 100 112.
41. Voogd, J., N.M. Gerrits and T.J. Ruigrok. 1996. Organization of the vestibulocerebellum. Ann. N. Y. Acad. Sci. 781 : 553 579.
42. Wylie, D.R. et al. 1994. Projections of individual Purkinje cells of identified zones in the ventral nodulus to the vestibular and cerebellar nuclei in the rabbit. J. Comp. Neurol. 349 : 448 463.
43. Merfeld, D.M., L.H. Zupan and C.A. Gifford. 2001. Neural processing of gravito-inertial cues in humans. II. Influence of the semicircular canals during eccentric rotation. J. Neurophysiol. 85 : 1648 1660.
44. Zupan, L.H., R.J. Peterka and D.M. Merfeld. 2000. Neural processing of gravito-inertial cues in humans. I. Influence of the semicircular canals following post-rotatory tilt. J. Neurophysiol. 84 : 2001 2015.
45. Green, A.M. and D.E. Angelaki. 2004. An integrative neural network for detecting inertial motion and head orientation. J. Neurophysiol. 92 : 905 925.
46. Fernandez, C. and J.M. Goldberg. 1971. Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J. Neurophysiol. 34 : 661 675.
47. Angelaki, D.E. and J.D. Dickman. 2000. Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J. Neurophysiol. 84 : 2113 2132.
48. Dickman, J.D. and D.E. Angelaki. 2002. Vestibular convergence patterns in vestibular nuclei neurons of alert primates. J. Neurophysiol. 88 : 3518 3533.
49. Musallam, S. and R.D. Tomlinson. 2002. Asymmetric integration recorded from vestibular-only cells in response to position transients. J. Neurophysiol. 88 : 2104 2113.
50. Zhou, W. et al. 2006. Responses of monkey vestibular-only neurons to translation and angular rotation. J. Neurophysiol. 96 : 2915 2930.
51. Kaptein, R.G. and J.A. Van Gisbergen. 2006. Canal and otolith contributions to visual orientation constancy during sinusoidal roll rotation. J. Neurophysiol. 95 : 1936 1948.
52. Seidman, S.H., L. Telford and G.D. Paige. 1998. Tilt perception during dynamic linear acceleration. Exp. Brain Res. 119 : 307 314.
53. Dichgans, J. et al. 1972. Moving visual scenes influence the apparent direction of gravity. Science 178 : 1217 1219.
54. Howard, I.P. and G. Hu. 2001. Visually induced reorientation illusions. Perception 30 : 583 600.
55. Barmack, N.H. and H. Shojaku. 1995. Vestibular and visual climbing fiber signals evoked in the uvula-nodulus of the rabbit cerebellum by natural stimulation. J. Neurophysiol. 74 : 2573 2589.
56. Fushiki, H. and N.H. Barmack. 1997. Topography and reciprocal activity of cerebellar Purkinje cells in the uvula-nodulus modulated by vestibular stimulation. J. Neurophysiol. 78 : 3083 3094.
57. Barmack, N.H. and V. Yakhnitsa. 2002. Vestibularly evoked climbing-fiber responses modulate simple spikes in rabbit cerebellar Purkinje neurons. Ann. N. Y. Acad. Sci. 978 : 237 254.
58. Barmack, N.H. and V. Yakhnitsa. 2003. Cerebellar climbing fibers modulate simple spikes in Purkinje cells. J. Neurosci. 23 : 7904 7916.
59. Yakhnitsa, V. and N.H. Barmack. 2006. Antiphasic Purkinje cell responses in mouse uvula-nodulus are sensitive to static roll-tilt and topographically organized. Neuroscience 143 : 615 626.
60. Angelaki, D.E., B.J. Hess and J. Suzuki. 1995. Differential processing of semicircular canal signals in the vestibulo-ocular reflex. J. Neurosci. 15 : 7201 7216.
61. Reisine, H. and T. Raphan. 1992. Unit activity in the vestibular nuclei of monkeys during off-vertical axis rotation. Ann. N. Y. Acad. Sci. 656 : 954 956.
62. Merfeld, D.M. et al. 1993. A multidimensional model of the effect of gravity on the spatial orientation of the monkey. J. Vestib. Res. 3 : 141 161.
63. Merfeld, D.M. and L.R. Young. 1995. The vestibulo-ocular reflex of the squirrel monkey during eccentric rotation and roll tilt. Exp. Brain Res. 106 : 111 122.
64. Wearne, S., T. Raphan and B. Cohen. 1999. Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation. J. Neurophysiol. 81 : 2175 2190.
65. Fetter, M. et al. 1992. The influence of head reorientation on the axis of eye rotation and the vestibular time constant during postrotatory nystagmus. Ann. N. Y. Acad. Sci. 656 : 838 840.