Summary
The spontaneous activity and dynamic responses to sinusoidal horizontal head angular acceleration of type II horizontal semicircular canal related neurons in the medial vestibular nucleus (MVN) were recorded bilaterally in decerebrate Mongolian gerbils (Meriones unguiculatus) under three experimental conditions: normal labyrinths intact, acutely following unilateral labyrinthine lesion, and four to seven weeks following labyrinthine lesion. The number of type II neurons detected contralateral to the lesion was greatly reduced both in the acutely hemilabyrinthectomized animals and following compensation. The gain of the responses was depressed bilaterally acutely following the lesion. A greater reduction in response gain was noted in cells contralateral to the lesion. The gain of the contralateral type II responses increased with time such that in the compensated animal bilaterally symmetric gains were recorded. While the significant changes which occur in the gain of type II neurons with recovery from peripheral vestibular lesions can largely be attributed to type I neurons on the other side of the midline, changes in type I neurons were not entirely reflected in the type II population. The spontaneous activity of type II neurons did not undergo any significant changes following the labyrinthine lesion. We present a model utilizing the dynamic responses to estimate the functional recovery of commissural connections in compensated animals. The overall gain of the contralateral type I to ipsilateral type I commissural polysynaptic pathway appears to improve, while the efficacy in the reverse direction remains depressed, suggesting that modifications in commissural connections, particularly involving the type II to type I connections within the MVN on the injured side, mediate aspects of behavioral recovery.
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References
Azzena GB, Mameli O, Tolu E (1976) Vestibular nuclei of hemilabyrinthectomized guinea pigs during decompensation. Arch Ital Biol 114:389–398
Baker R, Highstein SM (1975) Physiological identification of interneurons and motoneurons in the abducens nucleus. Brain Res 91:292–298
Baker R, Mano N, Shimazu H (1969) Postsynaptic potentials in abducens motoneurons induced by vestibular stimulation. Brain Res 15:577–580
Bienhold H, Flohr H (1978) Role of commissural connexions between vestibular nuclei in compensation following unilateral labyrinthectomy. J Physiol 284:178P
Blair SM, Gavin M (1981) Brainstem commissures and control of time constant of vestibular nystagmus. Acta Otolaryngol (Stockh) 91:1–8
Bush GA, Perachio AA (1988) Response of medial vestibular nuclei (MVN) neurons during harmonic linear acceleration in decerebrate rats. Neuroscience Abstr 14:330
Curthoys IS, Harris RA, Smith PF (1987) Effect of unilateral labyrinthectomy on neural activity in the guinea pig vestibular nuclei. In. Graham M, Kemink J (eds) The vestibular system: neurophysiologic and clinical research. Raven Press, New York, pp 633–642
Curthoys IS, Markham CH (1971) Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. I. Natural stimulation. Brain Res 35:469–490
Dieringer N, Precht W (1979a) Mechanisms of compensation for vestibular deficits. I. Modification of the excitatory commissural system. Exp Brain Res 36:311–328
Dieringer N, Precht W (1979b) Mechanisms of compensation for vestibular deficits in the frog. II. Modification of the inhibitory pathways. Exp Brain Res 36:329–341
Duensing F, Schaefer KP (1959) Über die Convergenz verschiedener labyrintharer Afferenzen auf einzelne Neurone des Vestibulariskerngebietes. Arch Psychiat Nervenkr 199:345–371
Fetter MTC, Zee DS (1988) Recovery from unilateral labyrinthectomy in rhesus monkey. J Neurophysiol 59:370–393
Fuchs AF, Kimm J (1975) Unit activity in vestibular nucleus of the alert monkey during horizontal angular acceleration and eye movement. J Neurophysiol 38:1140–1161
Furuya N, Kawano K, Shimazu H (1975) Functional organization of vestibulofastigial projection in the horizontal semicircular canal system in the cat. Exp Brain Res 24:75–87
Furuya N, Kawano K, Shimazu H (1976) Transcerebellar inhibitory interaction between the bilateral vestibular nuclei and its modulation by cerebellocortical activity. Exp Brain Res 25:447–463
Galiana HL, Flohr H, Melvill Jones G (1984) A reevaluation of intervestibular nuclear coupling: its role in vestibular compensation. J Neurophysiol 51:242–259
Hamann K, Lannou J (1988) Dynamic characteristics of vestibular nuclear neurons responses to vestibular and optokinetic stimulation during vestibular compensation in the rat. Acta Otolaryngol (Stockh) Suppl 446:1–19
Harris LR (1984) The effect of tilt on the responses of vestibular nucleus neurons to horizontal angular acceleration in the rat. Acta Otolaryngol (Stockh) 406:149–153
Jensen DW (1979) Vestibular compensation: tonic spinal influence upon spontaneous descending vestibular nuclear activity. Neuroscience 4:1075–1084
Kasahara M, Mano N, Oshima T, Ozawa S, Shimazu H (1968) Contralateral short latency inhibition of central vestibular neurons in the horizontal canal system. Brain Res 8:376–378
Kasahara M, Uchino Y (1974) Bilateral semicircular canal inputs to neurons in cat vestibular nuclei. Exp Brain Res 20:285–296
Katz E, deJong J, Cohen B, Buettner J (1988) The slow component of the VOR (velocity storage) depends on commissural connections caudal to the abducens nucleus. Neuroscience Abstr 14:173
Maciewicz RJ, Eagen K, Kaneko CRS, Highstein SM (1977) Vestibular and medullary brain stem afferents to the abducensnucleus in the cat. Brain Res 123:229–240
Maeda M, Shimazu H, Shinoda Y (1972) Nature of synaptic events in cat abducens motoneurons at slow and quick phase of vestibular nystagmus. J Neurophysiol 35:279–296
Maioli C, Precht W, Ried S (1983) Short- and long-term modifications of vestibuloocular response dynamics following unilateral vestibular nerve lesion in the cat. Exp Brain Res 50:259–274
Mano N, Oshima T, Shimazu H (1968) Inhibitory commissural fibers interconnecting the bilateral vestibular nuclei. Brain Res 8:378–382
Markham CH, Curthoys IS, (1972) Convergence of labyrinthine influences on units in the vestibular nuclei of the cat. II. Electrical stimulation. Brain Res 43:383–396
Markham CH, Curthoys IS, Yagi T (1978) The influence of the contralateral labyrinth on static and dynamic properties of brainstem vestibular neurons in the cat, guinea pig and rat. In: Hood J (eds) Vestibular mechanisms in health and disease. Academic Press, London, pp 86–94
Markham CH, Yagi T, Curthoys IS (1977) The contribution of the contralateral labyrinth to second order vestibular neuronal activity in the cat. Brain Res 138:99–109
Melvill Jones G, Milsum JH (1970) Characteristics of neural transmission from the semicircular canal to the vestibular nuclei of cats. J Physiol 209:295–316
Newlands SD, Perachio AA (1986) Effects of commissurotomy on vestibular compensation. Neuroscience Abstr 12:254
Newlands SD, Perachio AA (1988) Recovery of activity of type II neurons in the medial vestibular nucleus (MVN) following unilateral labyrinthectomy in the decerebrate gerbil. Neuroscience Abstr 14:331
Newlands SD, Perachio AA (1989) Compensation of type I horizontal canal related activity in the medial vestibular nucleus following hemilabyrinthectomy in the decerebrate gerbil. ARO Abstr 12:330
Newlands SD, Perachio AA (1990) Compensation of horizontal canal related activity in the medial vestibular nucleus following unilateral labyrinth ablation in the decerebrate gerbil. I. Type I neurons. Exp Brain Res 82:359–372
Ozawa S, Precht W, Shimazu H (1974) Crossed effects on central vestibular neurons in the horizontal canal system of the frog. Exp Brain Res 19:394–405
Perachio AA, Correia MJ (1983) Responses of semicircular canal and otolith afferents to small angle static head tilts in the gerbil. Brain Res 280:287–298
Pompeiano O, Xerri C, Gianni S, Manzoni D (1984) Central compensation of vestibular deficits. II. Influences of roll tilt on different size lateral vestibular neurons after ipsilateral deafferentation. J Neurophysiol 52:18–38
Precht W, Shimazu H, Markham CH (1966) A mechanism of central compensation of vestibular function following hemilabyrinthectomy. J Neurophysiol 29:996–1009
Raphan T, Matsuo V, Cohen B (1979) Velocity storage in the vestibulo-ocular reflex arc (VOR). Exp Brain Res 35:321–344
Ried S, Maioli C, Precht W (1984) Vestibular nuclear neuron activity in chronically hemilabyrinthectomized cats. Acta Otolaryngol (Stockh) 98:1–13
Shimazu H, Precht W (1965) Tonic and kinetic responses of cat's vestibular neurons to horizontal angular acceleration. J Neurophysiol 28:991–1013
Shimazu H, Precht W (1966) Inhibition of central vestibular neurons from the contralateral labyrinth and its mediating pathway. J Neurophysiol 29:467–492
Smith PF, Curthoys IS (1988a) Neuronal activity in the contralateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy. Brain Res 444:295–307
Smith PF, Curthoys IS (1988b) Neuronal activity in the ipsilateral medial vestibular nucleus of the guinea pig following unilateral labyrinthectomy. Brain Res 444:308–319
Smith PF, Darlington CL, Curthoys IS (1986) The effect of visual deprivation on vestibular compensation in the guinea pig. Brain Res 364:195–198
Tolu E, Mameli O, Azzena MT, Azzena GB (1980) Dynamic responses of vestibular cells during spinal decompensation. Physiol Behav 25:637–640
Wilson VJ, Wylie RM, Marco LA (1968) Synaptic inputs to cells in the medial vestibular nucleus. J Neurophysiol 31:176–185
Wolfe JW, Kos CM (1976) Nystagmic responses of the rhesus monkey to rotational stimulation following unilateral labyrinthectomy: a preliminary report. Trans Am Acad Opthalmol Otolaryngol 82:ORL-60-ORL-69
Wolfe JW, Kos CM (1977) Nystagmic responses of the rhesus monkey to rotational stimulation following unilateral labyrinthectomy: final report. Trans Am Acad Opthalmol Otolaryngol 84:ORL-38-ORL-45
Wolfe JW, Engelken EJ, Olson JW, Kos CM (1978) Vestibular responses to bithermal caloric and harmonic acceleration. Ann Otol Rhinol Laryngol 87:1–7
Xerri C, Gianni S, Manzoni D, Pompeiano O (1983) Central compensation of vestibular deficits. I. Response characteristics of lateral vestibular neurons to roll tilt after ipsilateral labyrinth deafferentation. J Neurophysiol 50:428–448
Xerri C, Gianni S, Manzoni D, Pompeiano O (1985) Central compensation of vestibular deficits. IV. Responses of lateral vestibular neurons to neck rotation after labyrinth deafferentation. J Neurophysiol 54:1006–1025
Yagi T, Markham CH (1984) Neural correlates of compensation after hemilabyrinthectomy. Exp Neurol 84:98–108
Zee DS, Fetter MTC, Proctor L (1988) Recovery from unilateral labyrinthectomy in primates: effects of visual inputs and considerations upon Ewalds second law. In: Hwang JC, Daunton NG, Wilson VJ (eds) Basic and applied aspects of vestibular function. University of Hong Kong Press, Hong Kong, pp 125–132
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Newlands, S.D., Perachio, A.A. Compensation of horizontal canal related activity in the medial vestibular nucleus following unilateral labyrinth ablation in the decerebrate gerbil. Exp Brain Res 82, 373–383 (1990). https://doi.org/10.1007/BF00231256
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DOI: https://doi.org/10.1007/BF00231256