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Eye–head coordination in the guinea pig I. Responses to passive whole-body rotations

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Abstract

Vestibular reflexes act to stabilize the head and eyes in space during locomotion. Head stability is essential for postural control, whereas retinal image stability enhances visual acuity and may be essential for an animal to distinguish self-motion from that of an object in the environment. Guinea pig eye and head movements were measured during passive whole-body rotation in order to assess the efficacy of vestibular reflexes. The vestibulo-ocular reflex (VOR) produced compensatory eye movements with a latency of ~7 ms that compensated for 46% of head movement in the dark and only slightly more in the light (54%). Head movements, in response to abrupt body rotations, also contributed to retinal stability (21% in the dark; 25% in the light) but exhibited significant variability. Although compensatory eye velocity produced by the VOR was well correlated with head-in-space velocity, compensatory head-on-body speed and direction were variable and poorly correlated with body speed. The compensatory head movements appeared to be determined by passive biomechanical (e.g., inertial effects, initial tonus) and active mechanisms (the vestibulo-collic reflex or VCR). Chemically induced, bilateral lesions of the peripheral vestibular system abolished both compensatory head and eye movement responses.

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References

  • Andrews J, Li J, Koyama S, Hoffman L (1997) Vestibular and optokinetic function in the normal guinea pig. Ann Otol Rhinol Laryngol 106(10 Pt 1):838–847

    PubMed  CAS  Google Scholar 

  • Baker J (2005) Dynamics and directionality of the vestibulo-collic reflex (VCR) in mice. Exp Brain Res 167(1):108–113

    Article  PubMed  Google Scholar 

  • Bamonte F, Monopoli A, Ongini E, Sabetta F, Ferraresi A, Pettorossi V (1986) Comparative actions of four aminoglycoside antibiotics on the vestibular function in guinea-pigs. Arch Int Pharmacodyn Thér 282(1):161–176

    PubMed  CAS  Google Scholar 

  • Beraneck M, Hachemaoui M, Idoux E, Ris L, Uno A, Godaux E et al (2003) Long-term plasticity of ipsilesional medial vestibular nucleus neurons after unilateral labyrinthectomy. J Neurophysiol 90(1):184–203

    Article  PubMed  Google Scholar 

  • Bizzi E, Kalil R, Tagliasco V (1971) Eye-head coordination in monkeys: evidence for centrally patterned organization. Science 173(3995):452–454

    Article  PubMed  CAS  Google Scholar 

  • Bui B, Vingrys A (1999) Development of receptoral responses in pigmented and albino guinea-pigs (Cavia porcellus). Doc Ophthalmol 99(2):151–170

    Article  PubMed  CAS  Google Scholar 

  • Collewijn H (1977) Optokinetic and vestibulo-ocular reflexes in dark-reared rabbits. Exp Brain Res 27:287–300

    Article  PubMed  CAS  Google Scholar 

  • Crane B, Demer J (1998) Human horizontal vestibulo-ocular reflex initiation: effects of acceleration, target distance, and unilateral deafferentation. J Neurophysiol 80(3):1151–1166

    PubMed  CAS  Google Scholar 

  • Cullen K, Roy J (2004) Signal processing in the vestibular system during active versus passive head movements. J Neurophysiol 91(5):1919–1933

    Article  PubMed  Google Scholar 

  • Cullen K, Rey C, Guitton D, Galiana H (1996) The use of system identification techniques in the analysis of oculomotor burst neuron spike train dynamics. J Comp Neurosci 3(4):347–368

    Article  CAS  Google Scholar 

  • Curthoys I, Topple A, Halmagyi G (1995) Unilateral vestibular deafferentation (UVD) causes permanent asymmetry in the gain of the yaw VOR to high acceleration head impulses in guinea pigs. Acta Otolaryngol Suppl 520(Pt 1):59–61

    Article  PubMed  Google Scholar 

  • Dichgans J, Bizzi E, Morasso P, Tagliasco V (1974) The role of vestibular and neck afferents during eye-head coordination in the monkey. Brain Res 71(2–3):225–232

    Article  PubMed  CAS  Google Scholar 

  • Escudero M, Waele C, Vibert N, Berthoz A, Vidal P (1993) Saccadic eye movements and the horizontal vestibulo-ocular and vestibulo-collic reflexes in the intact guinea-pig. Exp Brain Res 97(2):254–262

    Article  PubMed  CAS  Google Scholar 

  • Forge A, Li L (2000) Apoptotic death of hair cells in mammalian vestibular sensory epithelia. Hear Res 139(1–2):97–115

    Article  PubMed  CAS  Google Scholar 

  • Forge A, Li L, Corwin J, Nevill G (1993) Ultrastructural evidence for hair cell regeneration in the mammalian inner ear. Science 259(5101):1616–1619

    Article  PubMed  CAS  Google Scholar 

  • Forge A, Li L, Nevill G (1998) Hair cell recovery in the vestibular sensory epithelia of mature guinea pigs. J Comp Neurol 397(1):69–88

    Article  PubMed  CAS  Google Scholar 

  • Freedman E (2008) Coupling between horizontal and vertical components of saccadic eye movements during constant amplitude and direction gaze shifts in the rhesus monkey. J Neurophysiol 100(6):3375–3393

    Article  PubMed  Google Scholar 

  • Fuchs A, Robinson D (1966) A method for measuring horizontal and vertical eye movement chronically in the monkey. J Appl Physiol 21(3):1068–1070

    PubMed  CAS  Google Scholar 

  • Fuller J (1981) Eye and head movements during vestibular stimulation in the alert rabbit. Brain Res 205(2):363–381

    Article  PubMed  CAS  Google Scholar 

  • Gdowski G, McCrea R (1999) Integration of vestibular and head movement signals in the vestibular nuclei during whole-body rotation. J Neurophysiol 82(1):436–449

    PubMed  CAS  Google Scholar 

  • Gilchrist D, Curthoys I, Cartwright A, Burgess A, Topple A, Halmagyi M (1998) High acceleration impulsive rotations reveal severe long-term deficits of the horizontal vestibulo-ocular reflex in the guinea pig. Exp Brain Res 123(3):242–254

    Article  PubMed  CAS  Google Scholar 

  • Goldberg J, Peterson B (1986) Reflex and mechanical contributions to head stabilization in alert cats. J Neurophysiol 56(3):857–875

    PubMed  CAS  Google Scholar 

  • Graf W, de Waele C, Vidal P (1995) Functional anatomy of the head-neck movement system of quadrupedal and bipedal mammals. J Anat 186(Pt. 1):55–74

    PubMed  Google Scholar 

  • Gresty M (1975) Eye, head and body movements of the guinea pig in response to optokinetic stimulation and sinusoidal oscillation in yaw. Pflügers Arch Eur J Physiol 353(3):201–214

    Article  CAS  Google Scholar 

  • Horak F (2010) Postural compensation for vestibular loss and implications for rehabilitation. Restor Neurol Neurosci 28(1):57–68

    PubMed  Google Scholar 

  • Hoshowsky B, Tomlinson D, Nedzelski J (1994) The horizontal vestibulo-ocular reflex gain during active and passive high-frequency head movements. Laryngoscope 104(2):140–145

    PubMed  CAS  Google Scholar 

  • Huterer M, Cullen K (2002) Vestibuloocular reflex dynamics during high-frequency and high-acceleration rotations of the head on body in rhesus monkey. J Neurophysiol 88(1):13–28

    PubMed  Google Scholar 

  • Jones G, Balaban C, Jackson R (2003) Effect of trans-bullar gentamicin treatment on guinea pig angular and linear vestibulo-ocular reflexes. Exp Brain Res 152(3):293–306

    Article  PubMed  CAS  Google Scholar 

  • Judge S, Richmond B, Chu F (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vis Res 20(6):535–538

    Article  PubMed  CAS  Google Scholar 

  • Keshner E, Peterson B (1995) Mechanisms controlling human head stabilization. I. Head-neck dynamics during random rotations in the horizontal plane. J Neurophysiol 73(6):2293–2301

    PubMed  CAS  Google Scholar 

  • Keshner E, Cromwell R, Peterson B (1995) Mechanisms controlling human head stabilization. II. Head-neck characteristics during random rotations in the vertical plane. J Neurophysiol 73(6):2302–2312

    PubMed  CAS  Google Scholar 

  • Kim A, Beyer L, King W, Raphael Y (2007) Restoration of balance sensory epithelium and function by notch signaling inhibition. Assoc Res Otolaryngol Annu Meet 1218

  • Kopke R, Jackson R, Li G, Rasmussen M (2001) Growth factor treatment enhances vestibular hair cell renewal and results in improved vestibular function. Proc Natl Acad Sci 98(10):5886–5891

    Article  PubMed  CAS  Google Scholar 

  • Lue JH, Day AS, Cheng PW, Young YH (2008) Vestibular evoked myogenic potentials are heavily dependent on type I hair cell activity of the saccular macula in guinea pigs. Audiol Neurootol 14:59–66

    Google Scholar 

  • Marlinsky V, Kröller J (2000) Optokinetic eye movements elicited by an apparently moving visual pattern in guinea pigs. Exp Brain Res 131(3):350–358

    Article  PubMed  CAS  Google Scholar 

  • Minor L, Lasker D, Backous D, Hullar T (1999) Horizontal vestibuloocular reflex evoked by high-acceleration rotations in the squirrel monkey. I. Normal responses. J Neurophysiol 82(3):1254–1270

    PubMed  CAS  Google Scholar 

  • Peng G, Hain T, Peterson B (1996) A dynamical model for reflex activated head movements in the horizontal plane. Biol Cybern 75(4):309–319

    Article  PubMed  CAS  Google Scholar 

  • Pettorossi V, Bamonte F, Errico P, Ongini E, Draicchio F, Sabetta F (1986) Vestibulo-ocular reflex (VOR) in guinea pigs. Impairment induced by aminoglycoside antibiotics. Acta Otolaryngol 101(5–6):378–388

    Article  PubMed  CAS  Google Scholar 

  • Ris L, Godaux E (1998) Neuronal activity in the vestibular nuclei after contralateral or bilateral labyrinthectomy in the alert guinea pig. J Neurophysiol 80(5):2352–2366

    PubMed  CAS  Google Scholar 

  • Ris L, de Waele C, Serafin M, Vidal P, Godaux E (1995) Neuronal activity in the ipsilateral vestibular nucleus following unilateral labyrinthectomy in the alert guinea pig. J Neurophysiol 74(5):2087–2099

    PubMed  CAS  Google Scholar 

  • Ris L, Capron B, de Waele C, Vidal P, Godaux E (1997) Dissociations between behavioural recovery and restoration of vestibular activity in the unilabyrinthectomized guinea-pig. J Physiol 500(Pt 2):509–522

    PubMed  CAS  Google Scholar 

  • Robinson D (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IRE Trans Biomed Electron 10(4):137–145

    Article  CAS  Google Scholar 

  • Roy J, Cullen K (1998) A neural correlate for vestibulo-ocular reflex suppression during voluntary eye-head gaze shifts. Nat Neurosci 1(5):404–410

    Article  PubMed  CAS  Google Scholar 

  • Roy J, Cullen K (2001) Selective processing of vestibular reafference during self-generated head motion. J Neurosci 21(6):2131–2142

    PubMed  CAS  Google Scholar 

  • Roy J, Cullen K (2002) Vestibuloocular reflex signal modulation during voluntary and passive head movements. J Neurophysiol 87(5):2337–2357

    PubMed  Google Scholar 

  • Serafin M, Ris L, Bernard P, Muhlethaler M, Godaux E, Vidal PP (1999) Neuronal correlates of vestibulo-ocular reflex adaptation in the alert guinea-pig. Eur J Neurosci 11(5):1827–1830

    Article  PubMed  CAS  Google Scholar 

  • Sha S, Schacht J (2000) Antioxidants attenuate gentamicin-induced free radical formation in vitro and ototoxicity in vivo: D-methionine is a potential protectant. Hear Res 142(1–2):34–40

    Article  PubMed  CAS  Google Scholar 

  • Shanidze N, Kim AH, Loewenstein S, Raphael Y, King WM (2010) Eye-head coordination in the guinea pig II. Responses to self-generated (voluntary) head movements. Exp Brain Res. doi: 10.1007/s00221-010-2375-3

  • Snyder L, King W (1992) Effect of viewing distance and location of the axis of head rotation on the monkey’s vestibuloocular reflex. I. Eye movement responses. J Neurophysiol 67(4):861–874

    PubMed  CAS  Google Scholar 

  • Song B, Anderson D, Schacht J (1997) Protection from gentamicin ototoxicity by iron chelators in guinea pig in vivo. J Pharmacol Exp Ther 282(1):369–377

    PubMed  CAS  Google Scholar 

  • Stahl J, van Alphen A, de Zeeuw C (2000) A comparison of video and magnetic search coil recordings of mouse eye movements. J Neurosci Method 99(1–2):101–110

    Article  CAS  Google Scholar 

  • Takemura K, King W (2005) Vestibulo-collic reflex (VCR) in mice. Exp Brain Res 167(1):103–107

    Article  PubMed  Google Scholar 

  • Tweed D, Glenn B, Vilis T (1995) Eye-head coordination during large gaze shifts. J Neurophysiol 73(2):766–779

    PubMed  CAS  Google Scholar 

  • Vibert N, de Waele C, Escudero M, Vidal P (1993) The horizontal vestibulo-ocular reflex in the hemilabyrinthectomized guinea-pig. Exp Brain Res 97(2):263–273

    Article  PubMed  CAS  Google Scholar 

  • Vingrys A, Bui B (2001) Development of postreceptoral function in pigmented and albino guinea pigs. Vis Neurosci 18(4):605–613

    Article  PubMed  CAS  Google Scholar 

  • Walsh R, Hackney C, Furness D (2000) Regeneration of the mammalian vestibular sensory epithelium following gentamicin-induced damage. J Otolaryngol 29(6):351–360

    PubMed  CAS  Google Scholar 

  • Yamane H, Nakagawa T, Iguchi H, Shibata S, Takayama M, Nishimura K et al (1995) In vivo regeneration of vestibular hair cells of guinea pig. Acta Otolaryngol Suppl 520(Pt 1):174–177

    Article  PubMed  Google Scholar 

  • Yang T-H, Young Y-H (2005) Click-evoked myogenic potentials recorded on alert guinea pigs. Hear Res 205(1–2):277–283

    Article  PubMed  Google Scholar 

  • Zhou W, Weldon P, Tang B, King W (2003) Rapid motor learning in the translational vestibulo-ocular reflex. J Neurosci 23(10):4288–4298

    PubMed  CAS  Google Scholar 

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Acknowledgments

We want to acknowledge the contribution of Keiji Takemura, M.D. who helped us develop the methodology for testing guinea pigs; Kevin Lim for his programming expertise; Scott Loewenstein who collected some of the data reported here; Beth Hand and James Liadis for data collection and animal care and handling. Dwayne Valliencourt designed and built the specialized animal restraints and Chris Ellinger kept our electronics running. This research was supported by National Institutes of Health grants: P30 NDC005188-07, R21-DC008607-01, and T32 DC000011–30.

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Shanidze, N., Kim, A.H., Raphael, Y. et al. Eye–head coordination in the guinea pig I. Responses to passive whole-body rotations. Exp Brain Res 205, 395–404 (2010). https://doi.org/10.1007/s00221-010-2374-4

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