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Abstract

Vestibular adaptation can be induced optically or by chemical or physical injury to the vestibular apparatus or the brain stem. In searching for the sites or mechanisms of vestibular adaptation, neurophysiologists often rely on comparing central resting (background) activities and central modulations (sensitivity) during vestibular stimulation, before and after motor learning or vestibular compensation. It is assumed that adapted central sites must exhibit modulation changes that parallel vestibulo-ocular reflex changes. Using model simulations and analysis, we will show that such presumptions may be misleading. First, using a simple schematic of interconnected cells or nuclei, one can show that modulation depth and background “tone” can be modified (or fixed) independently, using weightings on direct or indirect afferent projections. That is, if synaptic weights along all stimulus pathways are altered, one may fix or strongly modify central premotor characteristics in a manner apparently unrelated to global reflex changes. In the vestibulo-ocular reflex, the dominant premotor pathways contain position-vestibular-pause cells and eye-head-velocity cells (which are behaviorally similar to floccular-target neurons). Several experiments have reported negligible changes in the velocity sensitivity of position-vestibular-pause cells, despite large gain changes in the vestibulo-ocular reflex induced by training with visual-vestibular conflict. On the other hand, the modulation changes on floccular-target neurons (position-vestibular-pause) can be much larger than the changes in reflex gain. Using a bilateral vestibulo-ocular reflex model, we show that overall increases or decreases in reflex gain can be expressed (even overexpressed) in one particular subgroup of premotor neurons. Nevertheless, such observations are theoretically compatible with synaptic changes on all primary projections in a widely interconnected central network. Hence, stable neural responses during reflex adaptation are not sufficient to exclude a potential site of sensory-motor adaptation. Similarly, modified neural responses (as in cerebellum) need not necessarily imply a direct role in supporting the adapted state. Model predictions should help to design additional experimental protocols, to test hypotheses, and to refine diagnostic measures of recovery after vestibular lesions.

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References

Scudder

Fuchs

. Physiological and behavioral identification of vestibular nucleus neurons mediating the horizontal vestibuloocular reflex in trained rhesus monkeys. J Neurophysiol 1992;68:244–64.

Lisberger

Pavelko

Broussard

. Responses during eye movements of brain stem neurons that receive monosynaptic inhibition from the flocculus and ventral paraflocculus in monkeys. J Neurophysiol 1994;72:909–27.

Cullen

Chen-Huang

McCrea

. Firing behavior of brain stem neurons during voluntary cancellation of the horizontal vestibuloocular reflex. II. Eye movement related neurons. J Neurophysiol 1993;70:844–56.

Lisberger

Pavelko

Broussard

. Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in responses of brain stem neurons. J Neurophysiol 1994;72:928–53.

Chen-Huang

McCrea

. Vergence related changes in the firing behavior of ascending tract of Deiters neurons during combined angular and linear head rotation [abstract]. Soc Neurosci Abstr 1996;22:1834.

McConville

KMV

Tomlinson

. Behavior of eye-movement related cells in the vestibular nuclei during combined rotational and translational stimuli. J Neurophysiol 1996;76:3136–48.

Lisberger

Miles

. Role of primate medial vestibular nucleus in long-term adaptive plasticity of the vestibuloocular reflex. J Neurophysiol 1980;43:1725–45.

Lac S

Raymond

Sejnowski

et al. Learning and memory in the vestibulo-ocular reflex. Annu Rev Neurosci 1995;18:409–41.

Peterson

Kinney

Quinn

et al. Potential mechanisms of plastic adaptive changes in the vestibulo-ocular reflex. Ann NY Acad Sci 1996;781:499–512.

10.

Lisberger

Pavelko

Bronte-Stewart

et al. Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus. J Neurophysiol 1994;72:954–73.

11.

Partsalis

Zhang

Highstein

. Dorsal Y group in squirrel monkey. I. Neuronal responses during instantaneous and long-term modifications of the vertical VOR. J Neurophysiol 1995;73:615–31.

12.

Partsalis

Zhang

Highstein

. Dorsal Y-group in the squirrel monkey. II. Contribution of the cerebellar flocculus to neuronal responses in normal and adapted animals. J Neurophysiol 1995;73:632–50.

13.

Miles

Lisberger

. Plasticity in the vestibuloocular reflex: A new hypothesis. Annu Rev Neurosci 1981;4:273–99.

14.

Lisberger

. Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning. J Neurophysiol 1994;72:974–98.

15.

Galiana

. A bilateral model for central neural pathways in the vestibuloocular reflex. J Neurophysiol 1984;51:210–41.

16.

Galiana

. A new approach to understanding visual-vestibular interactions in the CNS. J Neurophysiol 1986;55:349–74.

17.

Galiana

. Commissural vestibular nuclear coupling: A powerful putative site for producing adaptive change. In: Berthoz

Jones

Melvill G

, editors. Adaptive mechanisms in gaze control. Vol 1. Series on reviews in oculomotor research. Amsterdam: Elsevier; 1985. p. 327–39.

18.

Green

Galiana

. Modelling on-line adaptation of the VOR gain with target distance and eccentricity. Proceedings of the 17th IEEE EMBS, Montreal; 1995. p. 1459–60.

19.

Green

Galiana

. Exploring sites for short-term VOR modulation using a bilateral model. Ann NY Acad Sci 1996;781:625–8.

20.

Duensing

Schaefer

. Die Aktivitat Einzelner Neurone im Bereich der Vestibulariskerne be Horizontalbeshleunigungen unter Besonderer Berucksichtigung des Vestibularen Nystagmus. Arch Psychiatr Nervenkr 1958;198:225–52.

21.

Nakao

Sasaki

Schor

et al. Functional organization of premotor neurons in the cat medial vestibular nucleus related to slow and fast phases of nystagmus. Exp Brain Res 1982;45:371–85.

22.

Dieringer

Straka

. Steps toward recovery of function after hemilabyrinthectomy in frogs. Otolaryngol Head Neck Surg 1998;119:27–33.

23.

McCrea

Strassman

May

et al. Anatomical and physiological characteristics of vestibular neurons mediating the horizontal vestibulo-ocular reflex of the squirrel monkey. J Comp Neurol 1987;264:547–70.

24.

Broussard

DeCharms

Lisberger

. Inputs from the ipsilateral and contralateral vestibular apparatus to behaviorally characterized abducens neurons in rhesus monkeys. J Neurophysiol 1995;74:2445–59.

25.

Broussard

Lisberger

. Vestibular inputs to brain stem neurons that participate in motor learning in the primate vestibuloocular reflex. J Neurophysiol 1992;68:1906–9.

26.

Ito

. Cerebellar control of the vestibulo-ocular reflex—around the flocculus hypothesis. Annu Rev Neurosci 1982;5:275–96.

27.

Collewijn

Martins

Steinman

. Compensatory eye movements during active and passive head movements: Fast adaptation to changes in visual magnification. J Physiol 1983;340:259–86.

28.

Paige

Tomko

. Eye movement responses to linear head motion in the squirrel monkey. II. Visual-vestibular interactions and kinematic considerations. J Neurophysiol 1991;65:1183–96.

29.

Snyder

Lawrence

King

. Changes in vestibulo-ocular reflex (VOR) anticipate changes in vergence angle in monkey. Vision Res 1992;32:569–75.

30.

Viire

Tweed

Milner

et al. A reexamination of the gain of the vestibuloocular reflex. J Neurophysiol 1986;56:439–50.

Vestibular Adaptation: How Models Can Affect Data Interpretations

Abstract

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References