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Vestibular-related eye movements in the rat following selective electrical stimulation of the vestibular sensors

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Abstract

Rats are the most commonly used species in the neurosciences; however, little is known about the effects of selective electrical stimulation of individual vestibular sensors, on their eye movements. This limits their use to study the effects of vestibular stimulation on the brain, and their use in further exploring novel technologies such as artificial vestibular implants. We describe the effects of electrical stimulation of each vestibular sensor on vestibular-related eye movement in rats and compared the results to other species. We demonstrated that each sensor is responsible for specific bilateral eye movements. We found that the eye movements in rats differed from other species. Although the results were similar when stimulating the horizontal canal ampulla, differences appeared when stimulating the vertical canal sensors. During utricular stimulation, the ipsilateral eye moved dorsally in most cases, while the contralateral eye usually moved either caudally, or in extorsion. Saccular stimulation usually moved the ipsilateral eye dorsally or ventrally, while the contralateral eye usually moved ventrally or caudally. This study provides the first data on the application of selective electrical vestibular stimulation in the rat to the study of vestibular-related eye movements.

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Abbreviations

AA:

Anterior canal ampulla

eVOR:

Electrically evoked vestibulo-ocular reflex

HA:

Horizontal canal ampulla

PA:

Posterior canal ampulla

SCCs:

Semi-circular canals

SO:

Superior oblique

VOR:

Vestibulo-ocular reflex

References

  • Brandt T, Schautzer F, Hamilton DA, Brüning R, Markowitsch HJ, Kalla R, Darlington C, Smith PF, Strupp M (2005) Vestibular loss causes hippocampal atrophy and impaired spatial memory in humans. Brain 128(Pt 11):2732–2741

    Article  PubMed  Google Scholar 

  • Cartmill M (1974) Rethinking primate origins. Science 184(4135):436–443

    Article  CAS  PubMed  Google Scholar 

  • Cohen BJ, Suzuki JI (1963) Eye movements induced by ampullary nerve stimulation. Am J Physiol 204(2):347–351

    CAS  PubMed  Google Scholar 

  • Cohen BJ, Suzuki JI, Bender MB (1964) Eye movements from semi-circular canal nerve stimulation in the cat. Ann Otol Rhinol Laryngol 73:153–169

    Article  CAS  PubMed  Google Scholar 

  • Cox PG, Jeffery N (2008) Geometry of the semicircular canals and extraocular muscles in rodents, lagomorphs, felids and modern humans. J Anat 213(5):583–596

    PubMed  PubMed Central  Google Scholar 

  • Curthoys IS (1987) Eye movements produced by utricular and saccular stimulation. Aviat Space Environ Med 58(9 Pt 2):A192–A197

    CAS  PubMed  Google Scholar 

  • Cuthbert PC, Gilchrist DP, Hicks SL, MacDougall HG, Curthoys IS (2000) Electrophysiological evidence for vestibular activation of the guinea pig hippocampus. Neuroreport 11(7):1443–1447

    Article  CAS  PubMed  Google Scholar 

  • Dai C, Fridman GY, Chiang B (2011) Cross-axis adaptation improves 3D vestibulo-ocular reflex alignment during chronic stimulation via a head-mounted multichannel vestibular prosthesis. Exp Brain Res 210(3–4):595–606

    Article  PubMed  PubMed Central  Google Scholar 

  • Desai SS, Zeh C, Lysakowski A (2005) Comparative morphology of rodent vestibular periphery. I. Saccular and utricular maculae. J Neurophysiol 93(1):251–266

    Article  PubMed  Google Scholar 

  • Fluur E (1959) Influences of semicircular ducts on extraocular muscles. Acta Oto-Laryngol Suppl 149:1

    CAS  Google Scholar 

  • Fluur E, Mellström A (1970a) Saccular stimulation and oculomotor reactions. Laryngoscope 80(11):1713–1721

    Article  CAS  PubMed  Google Scholar 

  • Fluur E, Mellström A (1970b) Utricular stimulation and oculomotor reactions. Laryngoscope 80(11):1701–1712

    Article  CAS  PubMed  Google Scholar 

  • Fuller PM, Fuller CA (2006) Genetic evidence for a neurovestibular influence on the mammalian circadian pacemaker. J Biol Rhythm 21(3):177–184

    Article  Google Scholar 

  • Goldberg JM (2000) Afferent diversity and the organization of central vestibular pathways. Exp Brain Res 130(3):277–297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goto F, Meng H, Bai R, Sato H, Imagawa M, Sasaki M, Uchino Y (2003) Eye movements evoked by the selective stimulation of the utricular nerve in cats. Auris Nasus Larynx 30(4):341–348

    Article  PubMed  Google Scholar 

  • Goto F, Meng H, Bai R, Sato H, Imagawa M, Sasaki M, Uchino Y (2004) Eye movements evoked by selective saccular nerve stimulation in cats. Auris Nasus Larynx 31(3):220–225

    Article  PubMed  Google Scholar 

  • Graf W, McCrea RA, Baker R (1983) Morphology of posterior canal related secondary vestibular neurons in rabbit and cat. Exp Brain Res 52(1):125–138

    Article  CAS  PubMed  Google Scholar 

  • Guyot J-P, Sigrist A, Pelizzone M, Feigl GC, Kos MI (2011) Eye movements in response to electrical stimulation of the lateral and superior ampullary nerves. Ann Otol Rhinol Laryngol 120(2):81–87

    Article  PubMed  Google Scholar 

  • Haslwanter T (2002) Mechanics of eye movements: Implications of the ‘orbital revolution’. Ann NY Acad Sci 956(1):33–41

    Article  PubMed  Google Scholar 

  • Heesy CP (2004) On the relationship between orbit orientation and binocular visual field overlap in mammals. Anat Rec 281(1):1104–1110

    Article  Google Scholar 

  • Heesy CP (2008) Ecomorphology of orbit orientation and the adaptive significance of binocular vision in primates and other mammals. Brain Behav Evol 71(1):54–67

    Article  PubMed  Google Scholar 

  • Hess BJM, Dieringer N (1990) Spatial organization of the maculo–ocular reflex of the rat: responses during off-vertical axis rotation. Eur J Neurosci 2(11):909–919

    Article  PubMed  Google Scholar 

  • Hicks SL (2005) Vestibular and optokinetic input to the hippocampus. Ph-D Thesis University of Sydney

  • Hitier M, Besnard S, Vignaux G, Denise P, Moreau S (2010) The ventrolateral surgical approach to labyrinthectomy in rats: anatomical description and clinical consequences. Surg Radiol Anat 32(9):835–842

    Article  CAS  PubMed  Google Scholar 

  • Hitier M, Besnard S, Smith PF (2014) Vestibular pathways involved in cognition. Front Integr Neurosci 8:59

    Article  PubMed  PubMed Central  Google Scholar 

  • Hitier M, Sato G, Zhang Y-F, Zheng Y, Besnard S, Smith PF, Curthoys IS (2016) Anatomy and surgical approach of rat’s vestibular sensors and nerves. J Neurosci Methods 270:1–8

    Article  PubMed  Google Scholar 

  • Hitier, M, Sato G, Zhang Y-F, Besnard S, Smith PF (2018) The effects of electrical stimulation of the rat vestibular labyrinth on c-Fos expression in the hippocampus. Neurosci Lett 677: 60–64

    Article  CAS  PubMed  Google Scholar 

  • Horii A, Takeda N, Mochizuki T, Okakura-Mochizuki K, Yamamoto Y, Yamatodani A (1994) Effects of vestibular stimulation on acetylcholine release from rat hippocampus: an in vivo microdialysis study. J Neurophysiol 72(2):605–611

    Article  CAS  PubMed  Google Scholar 

  • Isu N, Graf W, Sato H, Kushiro K, Zakir M, Imagawa M, Uchino Y (2000) Sacculo–ocular reflex connectivity in cats. Exp Brain Res 131(3):262–268

    Article  CAS  PubMed  Google Scholar 

  • Jamon M (2014) The development of the vestibular system and related functions in mammals: Impact of gravity. Front Integr Neurosci 8:11

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeffery N, Cox PG (2010) Do agility and skull architecture influence the geometry of the mammalian vestibulo-ocular reflex? J Anat 216(4):496–509

    Article  PubMed  PubMed Central  Google Scholar 

  • Khanna S, Porter JD (2001) Evidence for rectus extraocular muscle pulleys in rodents. Investig Ophthalmol Vis Sci 42(9):1986–1992

    CAS  Google Scholar 

  • Kitajima N, Sugita-Kitajima A, Bai R, Sasaki M, Sato H, Imagawa M, Kawamoto E, Suzuki M, Uchino Y (2006) Axonal pathways and projection levels of anterior semicircular canal nerve-activated vestibulospinal neurons in cats. Neurosci Lett 406(1–2):1–5

    Article  CAS  PubMed  Google Scholar 

  • Kremmyda O, Hüfner K, Flanagin VL, Hamilton DA, Linn J, Strupp M, Jahn K, Brandt T (2016) Beyond dizziness: virtual navigation, spatial anxiety and hippocampal volume in bilateral vestibulopathy. Front Hum Neurosci 10:139

    Article  PubMed  PubMed Central  Google Scholar 

  • Kushiro K, Bai R, Kitajima N, Sugita-Kitajima A, Uchino Y (2008) Properties and axonal trajectories of posterior semicircular canal nerve-activated vestibulospinal neurons. Exp Brain Res 191(3):257–264

    Article  PubMed  Google Scholar 

  • Lopez C (2013) A neuroscientific account of how vestibular disorders impair bodily self-consciousness. Front Integr Neurosci 7:91

    Article  PubMed  PubMed Central  Google Scholar 

  • Lopez C (2016) The vestibular system: balancing more than just the body. Curr Opin Neurol 29(1):74–83

    Article  PubMed  Google Scholar 

  • Lopez C, Blanke O (2011) The thalamocortical vestibular system in animals and humans. Brain Res Rev 67(1–2):119–146

    Article  PubMed  Google Scholar 

  • Lopez C, Elzière M (2018) Out-of-body experience in vestibular disorders—a prospective study of 210 patients with dizziness. Cortex 104:193–206

    Article  PubMed  Google Scholar 

  • Martin T, Mauvieux B, Bulla J, Quarck G, Davenne D, Denise P, Philoxène B, Besnard S (2015) Vestibular loss disrupts daily rhythm in rats. J Appl Physiol 118(3):310–318

    Article  CAS  PubMed  Google Scholar 

  • McCrea R, Strassman AA, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflexes of the squirrel monkey. J Comp Neurol 264(4):571–594

    Article  CAS  PubMed  Google Scholar 

  • Misslisch H, Hess BJM (2000) Three-dimensional vestibuloocular reflex of the monkey: optimal retinal image stabilization versus Listing’s Law. J Neurophysiol 83(6):3264–3276

    Article  CAS  PubMed  Google Scholar 

  • Misslisch H, Tweed D (2001) Neural and mechanical factors in eye control. J Neurophysiol 86(4):1877–1883

    Article  CAS  PubMed  Google Scholar 

  • Moser I, Kropff E, Moser MB (2008) Place cells, grid cells, and the brain’s spatial representation system. Ann Rev Neurosci 31:69–89

    Article  CAS  PubMed  Google Scholar 

  • Moser I, Vibert D, Caversaccio MD, Mast F (2017) Impaired math achievement in patients with acute vestibular neuritis. Neuropsychologia 107:1–8

    Article  PubMed  Google Scholar 

  • O’Keefe J (1976) Place units in the hippocampus of the freely moving rat. Exp Neurol 51(1):78–109

    Article  PubMed  Google Scholar 

  • Pellionisz A, Graf W (1987) Tensor network model of the ‘three-neuron vestibulo-ocular reflex-arc’ in cat. J Theor Neurobiol 5:127–151

    Google Scholar 

  • Prince JH, Diesem CD, Eglitis I, Ruskell GL (1960) Anatomy and histology of the eye and orbit in domestic animals. Anatomy and histology of the eye and orbit in domestic animals. https://www.cabdirect.org/cabdirect/abstract/19622201306. Accessed 20 Feb 2018

  • Ruskell GL, Haugen I-BK, Bruenech JR, van der Werf (2005) Double insertions of extraocular rectus muscles in humans and the pulley theory. J Anat 206(3):295–306

    Article  PubMed  PubMed Central  Google Scholar 

  • Schilling R (1919) Ein beitrag zur funktion des vestibular apparates. Eur Arch Oto-Rhino-Laryngol 104(3):120–156

    Article  Google Scholar 

  • Simpson JI, Graf W (1981) Eye muscle geometry and compensatory eye movements in lateral-eyed and frontal-eyed animals. Ann NY Acad Sci 374(1):20–30

    Article  CAS  PubMed  Google Scholar 

  • Smith PF (2012) Dyscalculia and vestibular function. Med Hypothese 79(4):493–496

    Article  CAS  Google Scholar 

  • Smith PF (2017) The vestibular system and cognition. Curr Opin Neurol 30(1):84–89

    Article  PubMed  Google Scholar 

  • Smith PF, Darlington CL (2013) Personality changes in patients with vestibular dysfunction. Front Hum Neurosci 7:678

    PubMed  PubMed Central  Google Scholar 

  • Smith PF, Zheng Y (2013) From ear to uncertainty: vestibular contributions to cognitive function. Front Integr Neurosci 7:84

    Article  PubMed  PubMed Central  Google Scholar 

  • Sprent P, Smeeton NC (2007) Applied nonparametric statistical methods. Chapman and Hall/CRC, Boca Raton

    Google Scholar 

  • Suzuki JI, Cohen B (1964) Head, eye, body and limb movements from semi-circular canal nerves. Exp Neurol 10:393–405

    Article  CAS  PubMed  Google Scholar 

  • Suzuki JI, Cohen B, Bender MB (1964) Compensatory eye movements induced by vertical semicircular canal stimulation. Exp Neurol 9(2):137–160

    Article  CAS  PubMed  Google Scholar 

  • Taube JS (2007) The head direction signal: origins and sensory-motor integration. Ann Rev Neurosci 30:181–207

    Article  CAS  PubMed  Google Scholar 

  • Thurtell MJ, Kunin M, Raphan T (2000) Role of muscle pulleys in producing eye position-dependence in the angular vestibuloocular reflex: a model-based study. J Neurophysiol 84(2):639–650

    Article  CAS  PubMed  Google Scholar 

  • Tokumasu K, Goto K, Cohen B (1969) Eye movements from vestibular nuclei stimulation in monkeys. Ann Otol Rhinol Laryngol 78(5):1105–1119

    Article  CAS  PubMed  Google Scholar 

  • Tokumasu K, Suzuki JI, Goto K (1971) A study of the current spread of electric stimulation of the individual utricular and ampullary nerves. Acta Oto-Laryngol 71(1–6):313–318

    Article  CAS  Google Scholar 

  • Uchino Y, Kushiro K (2011) Differences between otolith- and semicircular canal-activated neural circuitry in the vestibular system. Neurosci Res 71(4):315–327

    Article  PubMed  Google Scholar 

  • Uchino Y, Suzuki S, Watanabe S (1980) Vertical semicircular canal inputs to cat extraocular motoneurons. Exp Brain Res 41(1):45–53

    Article  CAS  PubMed  Google Scholar 

  • Van de Berg R, Guinand N, Guyot J-P, Kingma H, Stokroos RJ (2012) The modified ampullar approach for vestibular implant surgery: feasibility and its first application in a human with a long-term vestibular loss. Front Neurol 3:18

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van de Berg R, Guinand N, Nguyen TA, Ranieri M, Cavuscens S, Guyot JP, Stokroos R, Kingma H, Perez-Fornos A (2015) The vestibular implant: frequency-dependency of the electrically evoked vestibulo-ocular reflex in humans. Front Syst Neurosci 8:255

    PubMed  PubMed Central  Google Scholar 

  • Wackym PA, Balaban CD, Mackay HT, Wood SJ, Lundell CJ, Carter DM, Siker DA (2016) Longitudinal cognitive and neurobehavioral functional outcomes before and after repairing otic capsule dehiscence. Otol Neurotol 37(1):70–82

    Article  PubMed  Google Scholar 

  • Waele CDE, Graf W, Josset P, Vidal PP (1989) A radiological analysis of the postural syndromes following hemilabyrinthectomy and selective canal and otolith lesions in the guinea pig. Exp Brain Res 77(1):166–182

    Article  PubMed  Google Scholar 

  • Wall C 3rd, Kos MI, Guyot J-P (2007) Eye Movements in response to electric stimulation of the human posterior ampullary nerve. Ann Otol Rhinol Laryngol 116(5):369–374

    Article  PubMed  Google Scholar 

  • Yamamoto M, Shimoyama I, Highstein SM (1978) Vestibular nucleus neurons relaying excitation from the anterior canal to the oculomotor nucleus. Brain Res 148(1):31–42

    Article  CAS  PubMed  Google Scholar 

  • Yates BJ, Bronstein AM (2005) The effects of vestibular system lesions on autonomic regulation: observations, mechanisms, and clinical implications. J Vestib Res 15(3):119–129

    PubMed  Google Scholar 

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Acknowledgements

This research was funded from the People Programme (Marie Curie Actions) of the European Union’s Seventh Framework Programme FP7/2007-2013/ under REA Grant agreement no. 318980, a grant from Region Basse Normandie, CNES, and the Royal Society of New Zealand Marsden Fund (to PFS and YZ).

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Correspondence to Paul F. Smith.

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All of the research reported in this paper was conducted in accordance with the Regulations of the University of Otago Committee on Ethics in the Care and Use of Laboratory Animals and the procedures were approved by that Committee (55/12).

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Hitier, M., Sato, G., Zhang, YF. et al. Vestibular-related eye movements in the rat following selective electrical stimulation of the vestibular sensors. J Comp Physiol A 204, 835–847 (2018). https://doi.org/10.1007/s00359-018-1286-9

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