Velocity-selective adaptation of the horizontal and cross-axis vestibulo-ocular reflex in the mouse

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• 作者：Patrick P. Hübner ; Serajul I. Khan ; Americo A. Migliaccio
• 关键词：VOR ; Visual–vestibular training ; Vestibular adaptation ; Oculomotor learning ; Plasticity ; Afferent pathways
• 刊名：Experimental Brain Research
• 出版年：2014
• 出版时间：October 2014
• 年：2014
• 卷：232
• 期：10
• 页码：3035-3046
• 全文大小：845 KB
• 参考文献：1. Albus JS (1971) A theory of cerebellar function. Math Biosci 10:25-1 CrossRef
  2. Angelaki DE, Dickman JD (2000) Spatiotemporal processing of linear acceleration: primary afferent and central vestibular neuron responses. J Neurophysiol 84:2113-132
  3. Angelaki DE, Hess BJM (1998) Visually induced adaptation in three-dimensional organization of primate vestibuloocular reflex. J Neurophysiol 79:791-07
  4. Boyden ES, Katoh A, Raymond JL (2004) Cerebellum-dependent learning: the role of multiple plasticity mechanisms. Annu Rev Neurosci 27:581-09. doi:10.1146/annurev.neuro.27.070203.144238 CrossRef
  5. Broussard DM, Titley HK, Antflick J, Hampson DR (2011) Motor learning in the VOR: the cerebellar component. Exp Brain Res 210:451-63. doi:10.1007/s00221-011-2589-z CrossRef
  6. Buettner UW, Büttner U, Henn V (1978) Transfer characteristics of neurons in vestibular nuclei of the alert monkey. J Neurophysiol 41:1614-628
  7. Calabrese DR, Hullar TE (2006) Planar relationships of the semicircular canals in two strains of mice. JARO 7:151-59. doi:10.1007/s10162-006-0031-1 CrossRef
  8. Clendaniel RA, Lasker DM, Minor LB (2001) Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. IV. Responses after spectacle-induced adaptation. J Neurophysiol 86:1594-611
  9. Clendaniel RA, Lasker DM, Minor LB (2002) Differential adaptation of the linear and nonlinear components of the horizontal vestibuloocular reflex in squirrel monkeys. J Neurophysiol 88:3534-540. doi:10.1152/jn.00404.2002 CrossRef
  10. Collewijn H, Grootendorst AF (1979) Adaptation of optokinetic and vestibulo-ocular reflexes to modified visual input in the rabbit. Prog Brain Res 50:771-81. doi:10.1016/S0079-6123(08)60874-2 CrossRef
  11. De Zeeuw CI, Hansel C, Bian F et al (1998) Expression of a protein kinase C inhibitor in Purkinje cells blocks cerebellar LTD and adaptation of the vestibulo-ocular reflex. Neuron 20:495-08 CrossRef
  12. Dean P, Porrill J, Ekerot C-F, J?rntell H (2009) The cerebellar microcircuit as an adaptive filter: experimental and computational evidence. Nat Rev Neurosci 11:30-3. doi:10.1038/nrn2756 CrossRef
  13. Dickman JD, Angelaki DE (2004) Dynamics of vestibular neurons during rotational motion in alert rhesus monkeys. Exp Brain Res 155:91-01. doi:10.1007/s00221-003-1692-1 CrossRef
  14. Fujita M (1982) Simulation of adaptive modification of the vestibulo-ocular reflex with an adaptive filter model of the cerebellum. Biol Cybern 45:207-14 CrossRef
  15. Godaux E, Halleux J, Gobert C (1983) Adaptive change of the vestibulo-ocular reflex in the cat: the effects of a long-term frequency-selective procedure. Exp Brain Res 49:28-4 CrossRef
  16. Holstein GR, Rabbitt RD, Martinelli GP et al (2004) Convergence of excitatory and inhibitory hair cell transmitters shapes vestibular afferent responses. Proc Natl Acad Sci USA 101(44):15766-5771 CrossRef
  17. Hübner PP, Lim R, Brichta AM, Migliaccio AA (2013) Glycine receptor deficiency and its effect on the horizontal vestibulo-ocular reflex: a study on the SPD1J mouse. JARO. doi:10.1007/s10162-012-0368-6
  18. Hullar TE, Santina Della CC, Hirvonen T et al (2005) Responses of irregularly discharging chinchilla semicircular canal vestibular-nerve afferents during high-frequency head rotations. J Neurophysiol 93:2777-786. doi:10.1152/jn.01002.2004 CrossRef
  19. Ito M (1982) Cerebellar control of the vestibulo-ocular reflex—around the flocculus hypothesis. Annu Rev Neurosci 5:275-96. doi:10.1146/annurev.ne.05.030182.001423 CrossRef
  20. Ito M (2002) Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann N Y Acad Sci 978:273-88. doi:10.1111/j.1749-6632.2002.tb07574.x CrossRef
  21. Iwashita M, Kanai R, Funabiki K et al (2001) Dynamic properties, interactions and adaptive modifications of vestibulo-ocular reflex and optokinetic response in mice. Neurosci Res 39:299-11 CrossRef
  22. Jones GM, Milsum JH (1971) Frequency-response analysis of central vestibular unit activity resulting from rotational stimulation of the semicircular canals. J Physiol 219(1):191-15
  23. Khater TT, Quinn KJ, Pena J et al (1993) The latency of the cat vestibulo-ocular reflex before and after short- and long-term adaptation. Exp Brain Res 94:16-2 CrossRef
  24. Kimpo RR, Boyden ES, Katoh A et al (2005) Distinct patterns of stimulus generalization of increases and decreases in VOR gain. J Neurophysiol 94:3092-100. doi:10.1152/jn.00048.2005 CrossRef
  25. Koekkoek SK, v Alphen AM, Vd Burg J et al (1997) Gain adaptation and phase dynamics of compensatory eye movements in mice. Genes Funct 1:175-90. doi:10.1046/j.1365-4624.1997.00018.x CrossRef
  26. Lasker DM, Hullar TE, Minor LB (2000) Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. III. Responses after labyrinthectomy. J Neurophysiol 83:2482-496
  27. Lasker DM, Han GC, Park HJ, Minor LB (2008) Rotational responses of vestibular-nerve afferents innervating the semicircular canals in the C57BL/6 mouse. JARO 9:334-48. doi:10.1007/s10162-008-0120-4 CrossRef
  28. Lisberger SG, Miles FA, Optican LM (1983) Frequency-selective adaptation: evidence for channels in the vestibulo-ocular reflex? J Neurosci 3:1234-244
  29. Marr D (1969) A theory of cerebellar cortex. J Physiol 202:437-70
  30. Menzies JRW, Porrill J, Dutia M, Dean P (2010) Synaptic plasticity in medial vestibular nucleus neurons: comparison with computational requirements of VOR adaptation. PLoS One 5:e13182. doi:10.1371/journal.pone.0013182.g012 CrossRef
  31. Migliaccio AA, MacDougall HG, Minor LB, Santina Della CC (2005) Inexpensive system for real-time 3-dimensional video-oculography using a fluorescent marker array. J Neurosci Methods 143:141-50. doi:10.1016/j.jneumeth.2004.09.024 CrossRef
  32. Migliaccio AA, Meierhofer R, Santina Della CC (2011) Characterization of the 3D angular vestibulo-ocular reflex in C57BL6 mice. Exp Brain Res 210:489-01. doi:10.1007/s00221-010-2521-y CrossRef
  33. Minor LB, Lasker DM (2009) Tonic and phasic contributions to the pathways mediating compensation and adaptation of the vestibulo-ocular reflex. J Vestib Res 19:159-70. doi:10.3233/VES-2009-0353
  34. Minor LB, Lasker DM, Backous DD, Hullar TE (1999) Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. I. Normal responses. J Neurophysiol 82:1254-270
  35. Powell KD, Quinn KJ, Rude SA et al (1991) Frequency dependence of cat vestibulo-ocular reflex direction adaptation: single frequency and multifrequency rotations. Brain Res 550:137-41. doi:10.1016/0006-8993(91)90417-T CrossRef
  36. Raymond JL, Lisberger SG (1996) Behavioral analysis of signals that guide learned changes in the amplitude and dynamics of the vestibulo-ocular reflex. J Neurosci 16:7791-802
  37. Sadeghi SG, Minor LB, Cullen KE (2006) Dynamics of the horizontal vestibuloocular reflex after unilateral labyrinthectomy: response to high frequency, high acceleration, and high velocity rotations. Exp Brain Res 175:471-84. doi:10.1007/s00221-006-0567-7 CrossRef
  38. Sadeghi SG, Goldberg JM, Minor LB, Cullen KE (2009) Efferent-mediated responses in vestibular nerve afferents of the alert macaque. J Neurophysiol 101:988-001. doi:10.1152/jn.91112.2008 CrossRef
  39. Schneider LW, Anderson DJ (1976) Transfer characteristics of first and second order lateral canal vestibular neurons in gerbil. Brain Res 112:61-6 CrossRef
  40. Serafin M, Ris L, Bernard P et al (1999) Neuronal correlates of vestibulo-ocular reflex adaptation in the alert guinea-pig. Eur J Neurosci 11:1827-830 CrossRef
  41. Shelhamer M, Robinson DA, Tan HS (1992) Context-specific adaptation of the gain of the vestibulo-ocular reflex in humans. J Vestib Res 2:89-6
  42. Simpson JI, Leonard CS, Soodak RE (1988) The accessory optic system of rabbit. II. Spatial organization of direction selectivity. J Neurophysiol 60:2055-072
  43. Stahl JS, van Alphen AM, De Zeeuw CI (2000) A comparison of video and magnetic search coil recordings of mouse eye movements. J Neurosci Methods 99:101-10 CrossRef
  44. Straka H, Lambert FM, Pfanzelt S, Beraneck M (2009) Vestibulo-ocular signal transformation in frequency-tuned channels. Ann N Y Acad Sci 1164:37-4. doi:10.1111/j.1749-6632.2008.03740.x CrossRef
  45. Titley HK, Heskin-Sweezie R, Broussard DM (2009) Consolidation and disruption of motor memory generalize across stimulus conditions in the vestibulo-ocular reflex. Brain Res 1267:37-3. doi:10.1016/j.brainres.2009.02.041 CrossRef
  46. Watanabe S, Hattori K, Koizuka I (2003) Flexibility of vestibulo-ocular reflex adaptation to modified visual input in human. Auris Nasus Larynx 30(Suppl):S29–S34 CrossRef
  47. Yoshikawa A, Hirata Y (2006) Mechanism of frequency selectivity in VOR motor learning: frequency channel or waveform learning? Conf Proc IEEE Eng Med Biol Soc 1:6217-220. doi:10.1109/IEMBS.2006.260163 CrossRef
  
• 作者单位：Patrick P. Hübner (1) (2)
  Serajul I. Khan (1) (2)
  Americo A. Migliaccio (1) (2) (3)
  
  1. Balance and Vision Laboratory, Neuroscience Research Australia, Cnr Barker Street and Easy Street, Randwick, Sydney, NSW, 2031, Australia
  2. University of New South Wales, Sydney, NSW, 2033, Australia
  3. Department of Otolaryngology—Head and Neck Surgery, Johns Hopkins University, Baltimore, MD, 21205, USA
  
• ISSN：1432-1106

文摘

One commonly observed phenomenon of vestibulo-ocular reflex (VOR) adaptation is a frequency-selective change in gain (eye velocity/head velocity) and phase (relative timing between the vestibular stimulus and response) based on the frequency content of the adaptation training stimulus. The neural mechanism behind this type of adaptation is not clear. Our aim was to determine whether there were other parameter-selective effects on VOR adaptation, specifically velocity-selective and acceleration-selective changes in the horizontal VOR gain and phase. We also wanted to determine whether parameter selectivity was also in place for cross-axis adaptation training (a visual–vestibular training stimulus that elicits a vestibular-evoked torsional eye movement during horizontal head rotations). We measured VOR gain and phase in 17 C57BL/6 mice during baseline (no adaptation training) and after gain-increase, gain-decrease and cross-axis adaptation training using a sinusoidal visual–vestibular (mismatch) stimulus with whole-body rotations (vestibular stimulus) with peak velocity 20 and 50°/s both with a fixed frequency of 0.5?Hz. Our results show pronounced velocity selectivity of VOR adaptation. The difference in horizontal VOR gain after gain-increase versus gain-decrease adaptation was maximal when the sinusoidal testing stimulus matched the adaptation training stimulus peak velocity. We also observed similar velocity selectivity after cross-axis adaptation training. Our data suggest that frequency selectivity could be a manifestation of both velocity and acceleration selectivity because when one of these is absent, e.g. acceleration selectivity in the mouse, frequency selectivity is also reduced.