Effect of temperature on the normal and adapted vestibulo-ocular reflex in the goldfish.

Abstract

1. The vestibulo-ocular reflex, a sensorimotor 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 visuovestibulo-(Vis-VOR) and vestibulo-ocular reflex (VOR) during normal operation as well as 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 before adaptation were found to be independent of the acclimation temperature over a wide range. Acute temperature changes of up to 10 degrees C either above or below a 20 degrees C acclimation temperature (Ac degree C = 20 degrees C) did not significantly modify normal visual and/or vestibular oculomotor reflex gains. 4. Surprisingly, slight reductions in temperature, as small as 2.5 degrees C, noticeably reduced Vis-VOR and VOR gain adaptations. Both short (3 h) and intermediate (up to 48 h) term reflex modifications were affected. Loss of adaptation was observed 10 degrees C below the acclimation temperature (Ac - 10 degrees 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 degrees C above the acclimation temperature (Ac + 10 degrees 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 toward its normal control gain before adaptation. Because 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 degrees C below the acclimation temperature were similar to those obtained at the acclimation temperature. Because 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. With the use of 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 thermosensitive site resides in the brain stem. 8. These results also show that, over a wide range of temperatures (20 +/- 10 degrees C), the neuronal processing that is responsible for the normal operation of the visuovestibulo- and/or vestibulo-ocular reflex and for the retention of reflex adaptation functions by separate physiological processes within the same brain stem and cerebellar circuitry. 9. We conclude that temperature exhibits a unique, and unexpected, state-dependent effect on sensorimotor regulation and adaptation for periods up to 48 h. Temperature does not alter normal VOR or the acquisition phase of an adapted gain change. (ABSTRACT TRUNCATED)