Advertisement

Experimental Brain Research

, Volume 92, Issue 1, pp 123–138 | Cite as

Nystagmus induced by electrical stimulation of the vestibular and prepositus hypoglossi nuclei in the monkey: evidence for site of induction of velocity storage

  • Jun-Ichi Yokota
  • Harvey Reisine
  • Bernard Cohen
Article

Summary

Electrical stimulation of the vestibular nuclei (VN) and prepositus hypoglossi nuclei (PPH) of alert cynomolgus monkeys evoked nystagmus and eye deviation while they were in darkness. At some sites in VN, nystagmus and after-nystagmus were induced with characteristics suggesting that velocity storage had been excited. We analyzed these responses and compared them to the slow component of optokinetic nystagmus (OKN) and to optokinetic after-nystagmus (OKAN). We then recorded unit activity in VN and determined which types of nystagmus would be evoked from the sites of recording. Nystagmus and eye deviations were also elicited by electrical stimulation of PPH, and we characterized the responses where unit activity was recorded in PPH. Horizontal slow phase velocity of the VN “storage” responses was contralateral to the side of stimulation. The rising time constants and peak steady-state velocities were similar to those of OKN, and the falling time constants of the after-nystagmus and of OKAN were approximately equal. Both the induced after-nystagmus and OKAN were habituated by stimulation of the VN. When horizontal after-nystagmus was evoked with animals on their sides, it developed yaw and pitch components that tended to shift the vector of the slow phase velocity toward the spatial vertical. Similar “cross-coupling” occurs for horizontal OKAN or for vestibular post-rotatory nystagmus elicited in tilted positions. Thus, the storage component of nystagmus induced by VN stimulation had the same characteristics as the slow component of OKN and the VOR. Positive stimulus sites for inducing nystagmus with typical storage components were located in rostral portions of VN. They lay in caudal ventral superior vestibular nucleus (SVN), dorsal portions of central medial vestibular nucleus (MVN) caudal to the abducens nuclei and in adjacent lateral vestibular nucleus (LVN). More complex stimulus responses, but with contralateral after-nystagmus, were induced from surrounding regions of ventral MVN and LVN, rostral descending vestibular nucleus and the marginal zone between MVN and PPH. Vestibular-only (VO), vestibular plus saccade (VPS) and tonic vestibular pause (TVP) units were identified by extracellular recording. Stimulation near type I lateral and vertical canalrelated VO units elicited typical “storage” responses with after-nystagmus in 23 of 29 tracks (79%). Stimulus responses were more complex from the region of neurons with oculomotor-related signals, i.e., TVP or VPS cells, although after-nystagmus was also elicited from these sites. Effects of vestibular nerve and nucleus stimulation were compared. Nerve stimulation evoked nystagmus with both a rapid and slow component and after-nystagmus. There was a more prominent rapid rise in slow phase velocity, higher peak velocities, shorter latencies and a shorter falling time constant from nerve than from nucleus stimulation. This indicates more prominent activation of rapid pathways from nerve stimulation. From a comparison of nerve- and nucleus-induced nystagmus, we infer that there was predominant activation of the network responsible for velocity storage by electrical stimulation at many sites in the VN. Microstimulation at sites in PPH elicited nystagmus with ipsilateral slow phases or ipsilateral eye deviations. Slow phase eye velocity changed rapidly at the onset of nystagmus, and peak eye velocities were about 10–15°/s lower than from VN stimulation. The nystagmus had no slow component, and it was not followed by after-nystagmus. Only burst or burst-tonic neurons were recorded in PPH. Stimulation at sites of recording of these units induced either nystagmus with a rapid component or ipsilateral eye deviation. We conclude that the slow component of optokinetic and vestibular nystagmus, attributable to velocity storage is produced in the VN, not in the PPH. We postulate that VO neurons lying in caudal ventral portions of SVN, dorsal portions of MVN and adjacent LVN are part of the network that generates velocity storage.

Key words

Velocity storage integrator Vestibular nuclei Prepositus hypoglossi nuclei Optokinetic nystagmus Monkey 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alexander GE, DeLong MR (1985) Microstimulation of the primate neostriatum. I. Physiological properties of striatal microexcitable zones. J Neurophysiol 53: 1401–1416Google Scholar
  2. Benson AJ (1974) Modification of the response to angular accelerations by linear accelerations. In: Kornhuber HH (ed) Handbook of sensory physiology, vol 6. Springer, Berlin Heidelberg New York, pp 281–320Google Scholar
  3. Blanks RHI, Curthoys IS, Bennett ML, Markham CH (1985) Planar relationships of the semicircular canals in rhesus and squirrel monkeys. Brain Res 340: 315–324Google Scholar
  4. Boyle R, Büttner U, Markert G (1985) Vestibular nuclei activity and eye movements in the alert monkey during sinusoidal optokinetic stimulation. Exp Brain Res 57: 362–369Google Scholar
  5. Brodal A (1983) The perihypoglossal nuclei in the macaque monkey and the chimpanzee. J Comp Neurol 218: 257–269Google Scholar
  6. Brodal A (1984) The vestibular nuclei in the macaque monkey. J Comp Neurol 227: 252–266Google Scholar
  7. Büttner-Ennever JA (1992) Patterns of connectivity in the vestibular nuclei. Ann NY Acad Sci 656: 363–378Google Scholar
  8. Büttner U, Waespe W (1981) Vestibular nerve activity in the alert monkey during vestibular and optokinetic nystagmus. Exp Brain Res 41: 310–315Google Scholar
  9. Buettner U, Büttner U, Henn V (1978) Transfer characteristics of neurons in vestibular nuclei of the alert monkey. J Neurophysiol 41: 1614–1628Google Scholar
  10. Cheron G, Gillis P, Godaux E (1986) Lesions in the cat prepositus complex: effects on the optokinetic system. J Physiol (Lond) 372: 95–111Google Scholar
  11. Cohen B, Suzuki J (1963) Eye movements induced by ampullary nerve stimulation. Am J Physiol 204: 347–351Google Scholar
  12. Cohen B, Matsuo V, Raphan T (1977) Quantitative analysis of the velocity characteristics of optokinetic nystagmus and optokinetic after-nystagmus. J Physiol (Lond) 270: 321–344Google Scholar
  13. Cohen B, Suzuki J, Raphan T (1983) Role of the otolith organs in generation of horizontal nystagmus; effects of selective labyrinthine lesions. Brain Res 276: 159–164Google Scholar
  14. Cohen B, Helwig D, Raphan T (1987) Baclofen and velocity storage: a model of the effects of drug on the vestibulo-ocular reflex in the rhesus monkey. J Physiol (Lond) 393: 703–725Google Scholar
  15. Cohen H, Cohen B, Raphan T, Waespe W (1992) Habituation and adaptation of the vestibuloocular reflex; a model of differential control by the vestibulocerebellum. Exp Brain Res 90: 526–538Google Scholar
  16. Dai M, Raphan T, Cohen B (1991) Characterization of the three dimensional structure of velocity storage in the monkey. J Neurophysiol 66: 1421–1439Google Scholar
  17. Epema AH, Gerrits NM, Voogd J (1988) Commissural and intrinsic connections of the vestibular nuclei in the rabbit: a retrograde labeling study. Exp Brain Res 71: 129–146Google Scholar
  18. Fuchs A, Kimm J (1975) Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38: 1140–1161Google Scholar
  19. Galiana HL, Outerbridge JS (1984) A bilateral model for central neural pathways in vetibuloocular reflex. J Neurophysiol 51: 210–241Google Scholar
  20. Gallagher JF, Phelan KD, Shinnick-Gallagher P (1992) Modulation of excitatory transmission at the rat medial vestibular nucleus synapse. Ann NY Acad Sci 656: 630–644Google Scholar
  21. Goldberg JM, Fernandez C (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. I Resting discharge and response to constant angular accelerations. J Neurophysiol 34: 635–660Google Scholar
  22. Guedry FE (1965) Visual control of habituation to complex vestibular stimulation in man. Acta Otolaryngol 58: 377–384Google Scholar
  23. Hepp K, Henn V, Vilis T, Cohen B (1989) Brainstem regions related to saccade generation. In: Wurtz R, Goldberg ME (eds) The neurobiology of saccadic eye movements. Elsevier, Amsterdam, pp 105–212Google Scholar
  24. Highstein SM, McCrea RA (1988) The anatomy of the vestibular nuclei. In: Büttner-Ennever J (ed) Neuroanatomy of the oculomotor system. Elsevier, Amsterdam, pp 177–202Google Scholar
  25. Isu N, Yokota J (1983) Morphophysiological study on the divergent projection of axon collaterals of medial vestibular nucleus neurons in the cat. Exp Brain Res 53: 151–162PubMedGoogle Scholar
  26. Judge SJ, Richmond BJ, Chu FC (1980) Implantation of magnetic search coils for measurement of eye position: an improved method. Vision Res 20: 535–538Google Scholar
  27. Katz E, Cohen B, deJong JMBV, Büttner-Ennever J (1991) Commissural contributions to velocity storage and the vestibuloocular reflex. Exp Brain Res 87: 505–520Google Scholar
  28. Ladpli R, Brodal A (1968) Experimental studies of commissural and reticular formation projections from the vestibular nuclei in the cat. Brain Res 8: 65–96Google Scholar
  29. Langer T, Fuchs AF, Chubb MC, Scudder CA, Lisberger SG (1985) Floccular efferents in the rhesus macaque as revealed by autoradiography and horseradish peroxidase. J Comp Neurol 235: 26–37Google Scholar
  30. Lopez-Barneo J, Darlot C, Berthoz A, Baker R (1982) Neuronal activity in prepositus nucleus correlated with eye movement in the alert cat. J Neurophysiol 47: 329–352Google Scholar
  31. Matsuo V, Cohen B (1984) Vertical optokinetic nystagmus in the monkey: up-down asymmetry effects of gravity. Exp Brain Res 53: 197–216Google Scholar
  32. McCrea R (1988) The nucleus prepositus. In: Büttner-Ennever J (ed) Neuroanatomy of the oculomotor system. Elsevier, Amsterdam, pp 203–223Google Scholar
  33. McCrea R, Strassman A, May E, Highstein SM (1987) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 264: 547–570Google Scholar
  34. McFarland J, Fuchs AF (1992) Discharge patterns in nucleus prepositus hypoglossi and adjacent medial vestibular nucleus during horizontal eye movement in behaving macaques. J Neurophysiol 68: 319–332Google Scholar
  35. Raphan T, Cohen B (1981) The role of integration in oculomotor control. In: Zuber B (ed) Stored models of oculomotor behavior and control. CRC Press, West Palm Beach, pp 91–109Google Scholar
  36. Raphan T, Cohen B (1985) Velocity storage and the ocular response to multidimensional vestibular stimuli. In: Berthoz A, Melvill Jones G (eds) Adaptive mechanisms in gaze control. Reviews in oculomotor research, vol 1. Elsevier, Amsterdam, pp 123–143Google Scholar
  37. Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35: 229–248PubMedGoogle Scholar
  38. Raphan T, Dai M, Cohen B (1992) Spatial orientation of the vestibular system. Ann NY Acad Sci 656: 140–157Google Scholar
  39. Reisine H, Raphan T (1992) Neural basis for eye velocity generation in the vestibular nuclei of alert monkeys during off-vertical axis rotation (OVAR). Exp Brain Res (in press)Google Scholar
  40. Robinson DA (1963) A method of measuring eye movement using a scleral search coil in a magnetic field. IEEE Trans Biomed Eng 10: 137–145PubMedGoogle Scholar
  41. Robinson DA (1975) Oculomotor control signals. In: G Lennerstrand, P Bach-y-Rita (eds) Basic mechanisms of ocular motility and their clinical implications. Pergamon Press, Oxford, 337–374Google Scholar
  42. Schiff D, Cohen B, Raphan T (1988) Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Exp Brain Res 70: 1–14Google Scholar
  43. Schiff D, Cohen B, Büttner-Ennever J, Matsuo V (1990) Effects of lesions of the nucleus of the optic tract on optokinetic nystagmus and after-nystagmus in the monkey. Exp Brain Res 79: 225–239Google Scholar
  44. Shantha TR, Manocha SL, Bourne GH (1968) A stereotaxis atlas of the Java monkey brain (Macaca irus). Williams and Wilkins, BaltimoreGoogle Scholar
  45. Shimazu H (1983) Neuronal organization of the premotor system controlling horizontal conjugate movements and vestibular nystagmus. In: Desmedt JE (ed) Motor control mechanisms in health and disease. Raven Press, New York, pp 565–588Google Scholar
  46. Solomon D, Cohen B (1992) Stabilization of gaze during circular locomotion in darkness. II. Contribution of velocity storage to compensatory eye and head nystagmus in the running monkey. J Neurophysiol 67: 1158–1170Google Scholar
  47. Stoney SD Jr, Thompson WD, Asanuma H (1968) Excitation of pyramidal tract cells by intracortical microstimulation: effective extent of stimulating current. J Neurophysiol 31: 659–669Google Scholar
  48. Szabo J, Cowan WM (1984) A stereotaxic atlas of the brain of the cynomolgus monkey. (Macaca fascicularis). J Comp Neurol 222: 265–300PubMedGoogle Scholar
  49. Tomlinson RD, Bahra PS (1986) Combined eye-head gaze shifts in the primate. II. Metrics. J Neurophysiol 56: 1558–1570Google Scholar
  50. Tomlinson RD, Robinson DA (1984) Signals in vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 36: 725–738Google Scholar
  51. Uemura T, Cohen B (1973) Effects of vestibular nuclei lesion on vestibulo-ocular reflexes and posture in monkeys. Acta Otolaryngol [Suppl] 315: 1–71Google Scholar
  52. Waespe W, Henn V (1977a) Neuronal activity in the vestibular nuclei of the alert monkey during vestibular and optokinetic stimulation. Exp Brain Res 27: 523–538Google Scholar
  53. Waespe W, Henn V (1977b) Vestibular nuclei activity during optokinetic afternystagmus (OKAN) in the alert monkey. Exp Brain Res 30: 323–330Google Scholar
  54. Waespe W, Cohen B, Raphan T (1983) Role of the flocculus and paraflocculus in optokinetic nystagmus and visual-vestibular interactions: effects of lesions. Exp Brain Res 50: 9–33Google Scholar
  55. Waespe W, Cohen B, Raphan T (1985) Dynamic modifications of the vestibulo-ocular reflex by the nodulus and uvula. Science 228: 199–202Google Scholar
  56. Wilson VJ, Melvill-Jones GM (1979) Mammalian vestibular physiology. Plenum, New YorkGoogle Scholar
  57. Young LR, Henn V (1974) Selective habituation of vestibular nystagmus by visual stimulation. Acta Otolaryngol 77: 159–166Google Scholar
  58. Zee DS, Yamazaki A, Butler PH, Gücer G (1981) Effects of ablation of flocculus and paraflocculus on eye movements in primates. J Neurophysiol 46: 878–899Google Scholar

Copyright information

© Springer-Verlag 1992

Authors and Affiliations

  • Jun-Ichi Yokota
    • 1
  • Harvey Reisine
    • 1
  • Bernard Cohen
    • 1
  1. 1.Departments of Neurology and Physiology & BiophysicsMount Sinai School of MedicineNew YorkUSA

Personalised recommendations