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Eye Movements Evoked by Pulsed Infrared Radiation of the Rat Vestibular System

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Abstract

Light at infrared wavelengths has been demonstrated to modulate the pattern of neural signals transmitted from the angular motion sensing semicircular canals of the vestibular system to the brain. In the present study, we have characterized physiological eye movements evoked by focused, pulsed infrared radiation (IR) stimuli directed at an individual semicircular canal in a mammalian model. Pulsed IR (1863 nm) trains were directed at the posterior semicircular canal in a rat using 200–400 µm optical fibers. Evoked bilateral eye movements were measured using a custom-modified video-oculography system. The activation of vestibulo–ocular motor pathways by frequency modulated pulsed IR directed at single posterior semicircular canals evoked significant, characteristic bilateral eye movements. In this case, the resulting eye movements were disconjugate with ipsilateral eye moving upwards with a rotation towards the stimulated ear and the contralateral eye moving downwards. The eye movements were stable through several hours of repeated stimulation and could be maintained with 30 + minutes of continuous, frequency-modulated IR stimulation. Following the measurements, the distance of the fiber from target structures and orientation of the beam relative to vestibular structures were determined using micro-computed tomography. Results highlight the spatial selectivity of optical stimulation. Our results demonstrate a novel strategy for direct optical stimulation of the vestibular pathway in rodents and lays the groundwork for future applications of optical neural stimulation in inner ear research and therapeutic applications.

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References

  1. Barrett, J. N., et al. Pulsed infrared releases Ca2+ from the endoplasmic reticulum of cultured spiral ganglion neurons. J. Neurophysiol. 2018. https://doi.org/10.1152/jn.00740.2017.

    Article  PubMed  PubMed Central  Google Scholar 

  2. Bec, J. M., et al. Characteristics of laser stimulation by near infrared pulses of retinal and vestibular primary neurons. Lasers Surg. Med. 44(9):736–745, 2012.

    Article  PubMed  Google Scholar 

  3. Bernstein, J. G., P. A. Garrity, and E. S. Boyden. Optogenetics and thermogenetics: technologies for controlling the activity of targeted cells within intact neural circuits. Curr. Opin. Neurobiol. 22(1):61–71, 2012.

    Article  CAS  PubMed  Google Scholar 

  4. Boyden, E. S., et al. Millisecond-timescale, genetically targeted optical control of neural activity. Nat. Neurosci. 8(9):1263–1268, 2005.

    Article  CAS  PubMed  Google Scholar 

  5. Cayce, J. M., et al. Calcium imaging of infrared-stimulated activity in rodent brain. Cell Calcium 55(4):183–190, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Cohen, B., and J. I. Suzuki. Eye movements induced by ampullary nerve stimulation. Am. J. Physiol. 204:347–351, 1963.

    Article  CAS  Google Scholar 

  7. Cohen, B., J. I. Suzuki, and M. B. Bender. Eye movements from semicircular canal nerve stimulation in the cat. Ann. Otol. Rhinol. Laryngol. 73:153–169, 1964.

    Article  CAS  PubMed  Google Scholar 

  8. Cohen, B., et al. Spatial orientation of the angular vestibulo–ocular reflex. J. Vestib. Res. 9(3):163–172, 1999.

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  10. Dai, C., et al. Restoration of 3D vestibular sensation in rhesus monkeys using a multichannel vestibular prosthesis. Hear. Res. 281(1–2):74–83, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  11. Deisseroth, K., and M. J. Schnitzer. Engineering approaches to illuminating brain structure and dynamics. Neuron 80(3):568–577, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Dellepiane, M., R. Mora, and A. Salami. Vestibular and optokinetic nystagmus in ketamine-anesthetized rabbits. Int. Tinnitus J. 13(1):15, 2007.

    CAS  PubMed  Google Scholar 

  13. Dittami, G. M., et al. Intracellular calcium transients evoked by pulsed infrared radiation in neonatal cardiomyocytes. J. Physiol. 589(6):1295–1306, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Fenno, L., O. Yizhar, and K. Deisseroth. The development and application of optogenetics. Annu. Rev. Neurosci. 34:389–412, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Fluur, E. Influences of semicircular ducts on extraocular muscles. Acta Otolaryngol. Suppl. 149:1–46, 1959.

    CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  17. Fridman, G. Y., et al. Vestibulo–ocular reflex responses to a multichannel vestibular prosthesis incorporating a 3D coordinate transformation for correction of misalignment. J. Assoc. Res. Otolaryngol. 11(3):367–381, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Fried, N. M., et al. Noncontact stimulation of the cavernous nerves in the rat prostate using a tunable-wavelength thulium fiber laser. J. Endourol. 22(3):409–414, 2008.

    Article  PubMed  Google Scholar 

  19. Hale, G. M., and M. R. Querry. Optical constants of water in the 200 nm to 200 µm region. Appl. Opt. 12:555–563, 1973.

    Article  CAS  PubMed  Google Scholar 

  20. Harris, D.M., et al. Optical nerve stimulation for a vestibular prosthesis. In: Proceedings of SPIE 7180, 2009.

  21. Hernandez, V. H., et al. Optogenetic stimulation of the auditory pathway. J. Clin. Invest. 124(3):1114–1129, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Izzo, A. D., et al. Laser stimulation of the auditory nerve. Lasers Surg. Med. 38(8):745–753, 2006.

    Article  PubMed  Google Scholar 

  23. Jenkins, M. W., et al. Optical pacing of the embryonic heart. Nat. Photon. 4(9):623–626, 2010.

    Article  CAS  Google Scholar 

  24. Katz, E. J., et al. Excitation of primary afferent neurons by near-infrared light in vitro. Neuroreport 21(9):662–666, 2010.

    Article  PubMed  Google Scholar 

  25. Kawashima, Y., et al. Mechanotransduction in mouse inner ear hair cells requires transmembrane channel-like genes. J. Clin. Invest. 121(12):4796–4809, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Lewis, R. F., et al. Spatial and temporal properties of eye movements produced by electrical stimulation of semicircular canal afferents. J. Neurophysiol. 108(5):1511–1520, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Merfeld, D. M., F. O. Black, and S. Wade. Clinical use of three-dimensional video measurements of eye movements. Otolaryngol. Head Neck Surg. 118(3 Pt 2):S35–S38, 1998.

    Article  CAS  PubMed  Google Scholar 

  28. Mettens, P., E. Godaux, and G. Chéron. Effects of ketamine on ocular movements of the cat. J. Vestib. Res. 1:325–338, 1991.

    CAS  Google Scholar 

  29. Minor, L. B. Gentamicin-induced bilateral vestibular hypofunction. JAMA 279(7):541–544, 1998.

    Article  CAS  PubMed  Google Scholar 

  30. Moreau, D., et al. Infrared neural stimulation induces intracellular Ca2+ release mediated by phospholipase C. J. Biophoton. 11:e201700020, 2017.

    Article  CAS  Google Scholar 

  31. Moreno, L. E., et al. Infrared neural stimulation: beam path in the guinea pig cochlea. Hear. Res. 282(1–2):289–302, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Nair, G., et al. Effects of common anesthetics on eye movement and electroretinogram. Doc. Ophthalmol. 122(3):163–176, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  33. Pan, B., et al. TMC1 and TMC2 are components of the mechanotransduction channel in hair cells of the mammalian inner ear. Neuron 79(3):504–515, 2013.

    Article  CAS  PubMed  Google Scholar 

  34. Poon, C. C., and M. G. Irwin. Anaesthesia for deep brain stimulation and in patients with implanted neurostimulator devices. Br. J. Anaesth. 103(2):152–165, 2009.

    Article  CAS  PubMed  Google Scholar 

  35. Rabbitt, R. D., et al. Heat pulse excitability of vestibular hair cells and afferent neurons. J. Neurophysiol. 116(2):825–843, 2016.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Rahman, M. A., et al. Restoring the 3D vestibulo–ocular reflex via electrical stimulation: the Johns Hopkins multichannel vestibular prosthesis project. Conf. Proc. IEEE Eng. Med. Biol. Soc. 2011:3142–3145, 2011.

    PubMed  PubMed Central  Google Scholar 

  37. Rajguru, S. M., et al. Infrared photostimulation of the Crista Ampullaris. J. Physiol. 589(6):1283–1294, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Rajguru, S. M., et al. Infrared photostimulation of the Crista Ampullaris. J. Physiol. 589(Pt 6):1283–1294, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Raphan, T., V. Matsuo, and B. Cohen. Velocity storage in the vestibulo–ocular reflex arc (VOR). Exp. Brain Res. 35(2):229–248, 1979.

    Article  CAS  PubMed  Google Scholar 

  40. Rein, M. L., and J. M. Deussing. The optogenetic (r)evolution. Mol. Genet. Genom. 287(2):95–109, 2012.

    Article  CAS  Google Scholar 

  41. Richter, C. P., and X. Tan. Photons and neurons. Hear. Res. 311:72–88, 2014.

    Article  PubMed  Google Scholar 

  42. Simpson, J. I., and W. Graf. Eye-muscle geometry and compensatory eye movements in lateral-eyed and frontal-eyed animals. Ann. N. Y. Acad. Sci. 374:20–30, 1981.

    Article  CAS  PubMed  Google Scholar 

  43. Smith, N. I., et al. A femtosecond laser pacemaker for heart muscle cells. Opt. Expr. 16(12):8604–8616, 2008.

    Article  CAS  Google Scholar 

  44. Stahl, J. S., A. M. van Alphen, and C. I. De Zeeuw. A comparison of video and magnetic search coil recordings of mouse eye movements. J. Neurosci. Methods 99(1–2):101–110, 2000.

    Article  CAS  PubMed  Google Scholar 

  45. Suzuki, J. I. Vestibular and spinal control of eye movements. Bibl. Ophthalmol. 82:109–115, 1972.

    CAS  PubMed  Google Scholar 

  46. Suzuki, J. I., and B. Cohen. Head, eye, body and limb movements from semicircular canal nerves. Exp. Neurol. 10:393–405, 1964.

    Article  CAS  PubMed  Google Scholar 

  47. Suzuki, J. I., B. Cohen, and M. B. Bender. Compensatory eye movements induced by vertical semicircular canal stimulation. Exp. Neurol. 9:137–160, 1964.

    Article  CAS  PubMed  Google Scholar 

  48. Suzuki, J. I., K. Tokumasu, and K. Goto. Eye movements from single utricular nerve stimulation in the cat. Acta Otolaryngol. 68(4):350–362, 1969.

    Article  CAS  PubMed  Google Scholar 

  49. Tan, X., et al. Auditory neural activity in congenitally deaf mice induced by infrared neural stimulation. Sci. Rep. 8(1):388, 2018.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Teudt, I. U., et al. Optical stimulation of the facial nerve: a new monitoring technique? Laryngoscope 117(9):1641–1647, 2007.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Tian, L., et al. Short-wavelength infrared laser activates the auditory neurons: comparing the effect of 980 vs. 810 nm wavelength. Lasers Med. Sci. 32(2):357–362, 2017.

    Article  PubMed  Google Scholar 

  52. van de Berg, R., et al. 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, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Walsh, A. J., et al. Action potential block in neurons by infrared light. Neurophotonics 3(4):040501, 2016.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Wells, J., et al. Application of infrared light for in vivo neural stimulation. J. Biomed. Opt. 10(6):064003, 2005.

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors sincerely thank Dr. Gaëtan Delcroix for his technical help and the GRECC Lab at the Miami VA Medical Center for generously giving us access to the MicroCT scanner.

Conflict of interest

The authors declare no competing financial interests.

Funding

This work was supported by R01DC013798 (SMR).

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Correspondence to Suhrud M. Rajguru.

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Associate Editor Leonidas D. Iasemidis oversaw the review of this article.

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Jiang, W., Rajguru, S.M. Eye Movements Evoked by Pulsed Infrared Radiation of the Rat Vestibular System. Ann Biomed Eng 46, 1406–1418 (2018). https://doi.org/10.1007/s10439-018-2059-x

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  • DOI: https://doi.org/10.1007/s10439-018-2059-x

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