The Effect of Temperature on the normal and adapted vestibulo-ocular reflex
in the Goldfish.
McElligott, James G., Michael Weiser, and Robert Baker.
Department of Pharmacology, Temple University School of Medicine,
Philadelphia, PA 19140, Department of Physiology and Neuroscience, New York
University School of Medicine, New York, NY 10016.
APStracts 2:0182N, 1995.
SUMMARY AND CONCLUSIONS
1) The vestibulo-ocular reflex, a sensori-motor process, operates in a similar
manner for homeothermic (mammals) and poikilothermic (fish) animals. However,
individual physiological, biochemical, and/or pharmacological thermolabile
processes that underlie the operation of this reflex could alter the operation
of this reflex in a poikilotherm. The object of this study was to determine
what aspects of the vestibulo-ocular reflex are affected by temperature
changes naturally experienced by a poikilothermic animal, the goldfish. 2)
Experiments were conducted on the visuo-vestibulo- (Vis-VOR) and vestibulo-
ocular reflex (VOR) during normal operation and during the acquisition
(learning) and retention (memory) phases of adaptive gain change. These
studies were carried out at temperatures to which goldfish had been acclimated
over several weeks and after rapid (< 5 min) shifts from this acclimation
temperature. 3) Normal sinusoidal Vis-VOR and VOR gains prior to adaptation
were found to be independent of the acclimation temperature over a wide range.
Acute temperature changes of up to 10 C either above or below a 20 C
acclimation temperature (Ac C = 20 C) did not significantly modify normal
visual and/or vestibular oculomotor reflex gains. 4) Surprisingly, slight
reductions in temperature, as small as 2.5 C, noticeably reduced Vis-VOR and
VOR gain adaptations. Both short (3 hours) and intermediate term (up to 48
hours) reflex modifications were affected. Loss of adaptation was observed 10
C below the acclimation temperature (Ac-10 C); however, return to the original
temperature immediately restored most (60-100%) of the previously acquired
Vis-VOR and VOR gain changes. In contrast, elevation of temperature up to 10 C
above the acclimation temperature (Ac+10 C) did not alter either increases or
decreases in the adapted Vis-VOR or VOR gain. 5) A decrease in temperature
reduced the magnitude of an adapted VOR gain increase and elevated the
magnitude of an adapted gain decrease thus returning the VOR gain back towards
its normal control gain prior to adaptation. Since both increases and
decreases in VOR gain were affected by the same temperature reduction, the
cold effect was not a generalized reflex suppression, but inactivation of a
process responsible for maintaining VOR adaptation. 6) During the acquisition
phase, the time course and magnitude of adaptive VOR gain increases at
temperatures acutely set 8-10 C below the acclimation temperature were similar
to those obtained at the acclimation temperature. Since the same temperature
decrease inactivated retention of adapted VOR gain changes, the neuronal
processes underlying the acquisition and the retention phases of Vis-VOR or
VOR adaptation are suggested to differ qualitatively. 7) Using velocity step
stimuli, both the adapted dynamic (<100 ms) and sustained (>100 ms) components
of VOR adaptation were reduced by cooling. This effect on the dynamic
component demonstrates an alteration in the shortest latency pathway through
the vestibular nucleus and indicates that one thermo-sensitive site resides in
the brainstem. 8) These results also show that over a wide range of
temperatures (20 C +/- 10 C), the neuronal processing that is responsible for
the normal operation of the visuo- and/or vestibulo-ocular reflex and for the
retention of reflex adaptation, functions by separate physiological processes
within the same brainstem and cerebellar circuitry. 9) We conclude that
temperature exhibits a unique, and unexpected, state dependent effect on
sensori-motor regulation and adaptation for periods up to 48 hours.
Temperature does not alter normal VOR or the acquisition phase of an adapted
gain change. However, since it inactivates retention of adaptive VOR gain
changes reversibly, we propose that thermo-lability of an adapted VOR gain
change reflects the alteration of a separate ligand and/or current related
membrane event. As a result, visual-vestibular oculomotor learning is masked,
but only temporarily as the complete memory trace or engram is actually never
lost.
Received 16 February 1995; accepted in final form 8 June 1995.
APS Manuscript Number J114-5.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1995 The American Physiological Society.
Published in APStracts on 6 July 1995.