Journal of Comparative Physiology A

, Volume 176, Issue 5, pp 641–651 | Cite as

Membrane and firing properties of avian medial vestibular nucleus neurons in vitro

  • S. du Lac
  • S. G. Lisberger
Original Paper


The intrinsic membrane and firing properties of medial vestibular nucleus (MVN) neurons were investigated in slices of the chick brainstem using intracellular recording and current injection. Avian MVN neurons fired spontaneous action potentials with very regular interspike intervals. The rapid repolarization of all action potentials was followed by an after-hyperpolarization. Intracellular injection of steps of hyperpolarizing current revealed both an inward rectification of the membrane potential during the step and a rebound depolarization following the offset of the step. In some neurons, the rebound depolarization resulted in bursts of action potentials. Steps of depolarizing current applied to spontaneously active neurons evoked increases in firing rate that were higher at the onset of the step than during the steady-state response. The relationship between current and firing rate was linear. The membrane and firing properties of avian MVN neurons were distributed continuously across the population of recorded neurons. These properties appear identical to those of rodent MVN neurons, suggesting that the composition and distribution of ion channels in the MVN neuronal membrane has been highly conserved across vertebrate species.

Key words

Chick Brainstem Slice Intracellular recording Action potential 



medial vestibular nucleus


vestibulo-ocular reflex




Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Anastasio TJ, Correia MJ (1988) A frequency and time domain study of the horizontal and vertical vestibuloocular reflex in the pigeon. J Neurophysiol 59: 1143–1161Google Scholar
  2. Anastasio TJ, Correia MJ, Perachio AA (1985) Spontaneous and driven responses of semicircular canal primary afferents in the unanesthetized pigeon. J Neurophysiol 54: 335–347Google Scholar
  3. Bronte-Stewart H, Lisberger SG (1994) Physiological properties of vestibular primary afferents that mediate motor learning and normal performance of the vestibulo-ocular reflex in monkeys. J Neurosci 14: 1290–1308Google Scholar
  4. Buettner UW, Büttner U, Henn V (1978) Transfer characteristics of neurons in the vestibular nuclei of alert monkey. J Neurophysiol 41: 1614–1628Google Scholar
  5. Chubb MC, Fuchs AF, Scudder CA (1984) Neuronal activity in monkey vestibular nuclei during vertical vestibular stimulation and eye movements. J Neurophysiol 52: 724–742Google Scholar
  6. Collewijn H, Grootendorst AF (1978) Adaptation of the rabbit's vestibulo-ocular reflex to modified visual input: importance of stimulus conditions. Arch Ital Biol 116: 273–280Google Scholar
  7. Cox R, Peusner K (1990a) Horseradish peroxidase labelling of the central pathways in the medulla of the ampullary nerves in the chicken, Callus gallus. J Comp Neurol 297: 564–585Google Scholar
  8. Cox R, Peusner K (1990b) Horseradish peroxidase labelling of the efferent and afferent pathways of the avian tangential vestibular nucleus. J Comp Neurol 296: 324–341Google Scholar
  9. Cullen KE, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. I. Secondary vestibular neurons. J Neurophysiol 70: 828–843Google Scholar
  10. Cullen KE, Chen-Huang C, McCrea RA (1993) Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibulo-ocular reflex. II. Eye movement related neurons. J Neurophysiol 70: 844–856Google Scholar
  11. du Lac S, Lisberger SG (1992) Eye movements and brainstem neuronal responses evoked by cerebellar and vestibular stimulation in chicks. J Comp Physiol A 171: 629–638Google Scholar
  12. Fernandez C, Goldberg J (1971) Physiology of peripheral neurons innervating semicircular canals of the squirrel monkey. II. Response to sinusoidal stimulation and dynamics of peripheral vestibular system. J Neurophysiol 34: 661–675PubMedGoogle Scholar
  13. Fuchs AF, 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
  14. Gallagher JP, Phelan KD, Shinnick-Gallagher P (1992) Modulation of excitatory transmission at the rat medial vestibular nucleus synapse. Ann New York Acad Sci 656: 630–644Google Scholar
  15. Godaux E, Halleus 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: 28–34Google Scholar
  16. Gonshor A, Melvill-Jones G (1976) Extreme vestibulo-ocular adaptation induced by prolonged optical reversal of vision. J Physiol (Lond) 256: 381–414Google Scholar
  17. Graf W, Baker R (1990) Neuronal adaptation accompanying metamorphosis in the flatfish. J Neurobiology 21: 1136–1152Google Scholar
  18. Highstein SM (1973) Synaptic linkage in the vestibulo-ocular and cerebello-vestibular pathways to the VIth nucleus in the rabbit. Exp Brain Res 17: 301–314Google Scholar
  19. Hyson RL, Rubel EW (1989) Transneuronal regulation of protein synthesis in the brainstem auditory system of the chick requires synaptic activation. J Neurosci 2835–2845Google Scholar
  20. Ito M, Shiida T, Yagi N, Yamamoto M (1974) The cerebellar modification of rabbit's horizontal vestibulo-ocular reflex induced by sustained head rotation combined with visual stimulation. Proc Jpn Acad 50: 85–89Google Scholar
  21. Jahnsen H (1986) Electrophysiological characteristics of neurones in the guinea-pig deep cerebellar nuclei in vitro. J Physiol (Lond) 372: 129–147Google Scholar
  22. Labandeira-Garcia JL, Guerra-Seijas MJ, Labandeira-Garcia JA, Suarez-Nunez JM (1989) Afferent connections of the oculomotor nucleus in the chick. J Comp Neurol 282: 523–534Google Scholar
  23. Lewis MR, Gallagher JP, Shinnick-Gallagher P (1987) An in vitro brain slice preparation to study the pharmacology of central vestibular neurons. J Pharm Meth 18: 267–273Google Scholar
  24. Lisberger SG, Miles FA (1980) Role of the primate medial vestibular nucleus in long-term adaptive plasticity of the vestibulo-ocular reflex. J Neurophysiol 43: 1725–1745Google Scholar
  25. Lisberger SG, Pavelko TA (1988) Brainstem neurons in modified pathways for motor learning in the primate vestibulo-ocular reflex. Science 242: 771–773Google Scholar
  26. Lisberger SG, Miles FA, Optican LM (1983) Frequency-selective adaptation: evidence for channels in the vestibulo-ocular reflex? J Neurosci 3: 1234–1244Google Scholar
  27. Lisberger SG, Pavelko TA, Broussard DM (1994a) Responses during eye movements of brainstem neurons that receive mono-synaptic inhibition from the flocculus and ventral paraflocculus in monkeys. J Neurophysiol 72: 909–927Google Scholar
  28. Lisberger SG, Pavelko TA, Broussard DM (1994b) Neural basis for motor learning in the vestibulo-ocular reflex of primates: I. Changes in the responses of brainstem neurons. J Neurophysiol 72: 928–953Google Scholar
  29. Llinas R, Muhlethaler M (1988) Electrophysiology of guinea-pig cerebellar nuclear cells in the in vitro brainstem-cerebellar preparation. J Physiol (Lond) 404: 241–258Google Scholar
  30. Llinas R, Yarom Y (1981) Properties and distribution of ionic conductances generating electroresponsiveness of mammalian inferior olivary neurons in vitro, J Physiol (Lond) 315: 569–584Google Scholar
  31. McCrea RA, Strassman A, May E, Highstein SM (1987a) Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 264: 547–570Google Scholar
  32. McCrea RA, Strassman A, May E, Highstein SM (1987b) Anatomical and physiological characteristics of vestibular neurons mediating the vertical vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 264: 571–594Google Scholar
  33. McFarland JL, Fuchs AF (1992) Discharge patterns of the nucleus hypoglossi prepositus and adjacent medial vestibular nucleus during horizontal eye movements in behaving monkeys. J Neurophysiol 68: 319–332Google Scholar
  34. Melvill-Jones G (1977) Plasticity in the adult vestibulo-ocular reflex arc. Phil Trans R Soc Lond B 278: 319–334Google Scholar
  35. Mile FA, Eighmy BB (1980) Long-term adaptive changes in primate vestibulo-ocular reflex. I. Behavioral observations. J Neurophysiol 43: 1406–1425Google Scholar
  36. Ohgaki T, Curthoys IS, Markham CH (1988) Morphology of physiologically identified second-order vestibular neurons in cat, with intracellularly injected HRP. J Comp Neurol 276: 387–411Google Scholar
  37. Paige GD, Sargent EW (1991) Visually-induced plasticity in the human vestibulo-ocular reflex. Exp Brain Res 84: 25–34Google Scholar
  38. Pastor AM, De La Cruz RR, Baker R (1992) Characterization and adaptive modification of the goldfish vestibuloocular reflex by sinusoidal and velocity step vestibular stimulation. J Neurophysiol 68: 2003–2015Google Scholar
  39. Petersdottir G (1990) Vestibulo-ocular projections in the 11-day chick embryo: pathway specificity. J Comp Neurol 297: 283–297Google Scholar
  40. Robinson DA (1976) Adaptive gain control of the vestibulo-ocular reflex by the cerebellum. J Neurophysiol 39: 954–969Google Scholar
  41. Sato Y, Kanda K-I, Kawasaki, T (1988) Target neurons of floccular middle zone inhibition in medial vestibular nucleus. Brain Res 446: 225–235Google Scholar
  42. Schairer JO, Bennett MVL (1986) Changes in the gain of the vestibulo-ocular reflex by combined visual and vestibular stimulation in goldfish. Brain Res 373: 164–176Google Scholar
  43. Scudder CA, Fuchs AF (1992) Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J Neurophysiol 68: 244–264Google Scholar
  44. Serafin M, Waele C, Khateb A, Vidal PP, Muhlethaler M (1991) Medial vestibular nucleus in the guinea-pig. I. Intrinsic membrane properties in brainstem slices. Exp Brain Res 84: 417–425Google Scholar
  45. Shimazu H, Precht W (1965) Tonic and kinetic responses of cat's vestibular neurons to horizontal angular accelerations. J Neurophysiol 28: 991–1013Google Scholar
  46. Snyder LH, King WM (1992) Effect of viewing distance and location on the axis of head rotation on the monkey's vestibuloocular reflex. I. Eye movement responses. J Neurophysiol 67: 861–874PubMedGoogle Scholar
  47. Snyder LH, Lawrence DM, King WM (1992) Changes in vestibuloocular reflex (VOR) anticipate changes in vergence angle in monkey. Vision Res 32(3): 569–575Google Scholar
  48. Tomlinson RD, Robinson DA (1984) Signals in the vestibular nucleus mediating vertical eye movements in the monkey. J Neurophysiol 51: 1121–1136Google Scholar
  49. Wallman J, Velez J, Weinstein B, Green A (1982) Avian vestibuloocular reflex: adaptive plasticity and developmental changes. J Neurophysiol 48: 952–967Google Scholar
  50. Wilson VJ, Felpel LP (1972) Specificity of semicircular canal input to neurons in the pigeon vestibular nuclei. J Neurophysiol 35: 253–264Google Scholar
  51. Wold JE (1978) The vestibular nuclei in the domestic hen (Gallus domesticus): III. Ascending projections to the mesencephalic motor nuclei. J Comp Neurol 179: 393–406Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • S. du Lac
    • 1
  • S. G. Lisberger
    • 1
  1. 1.Department of Physiology, W.M. Keck Foundation Center for Integrative Neuroscience, and Neuroscience Graduate ProgramUniversity of CaliforniaFranciscoUSA

Personalised recommendations