EFFECT OF TEMPERATURE ON THE NORMAL AND ADAPTED VESTIBULO-OCULAR REFLEX IN THE GOLDFISH

1. The vestibule-ocular reflex, a sensorimotor process, operates in a similar manner for homeothermic (mammals) and poikilothermic (fish) an imals. However, individual physiological, biochemical, and/or pharmaco logical thermolabile processes that underlie the operation of this ref lex could alter the operation of this reflex in a poikilotherm. The ob ject of this study was to determine what aspects of the vestibule-ocul ar reflex are affected by temperature changes naturally experienced by a poikilothermic animal, the goldfish. 2. Experiments were conducted on the visuovestibulo-(Vis-VOR) and vestibule-ocular reflex (VOR) duri ng normal operation as well as during the acquisition (learning) and r etention (memory) phases of adaptive gain change. These studies were c arried out at temperatures to which goldfish had been acclimated over several weeks and after rapid (<5 min) shifts from this acclimation te mperature.3. Normal sinusoidal Vis-VOR and VOR gains before adaptation were found to be independent of the acclimation temperature over a wi de range. Acute temperature changes of up to 10 degrees C either above or below a 20 degrees C acclimation temperature (Ac degrees C = 20 de grees C) did not significantly modify normal visual and/or vestibular oculomotor reflex gains. 4. Surprisingly, slight reductions in tempera ture, as small as 2.5 degrees C, noticeably reduced Vis-VOR and VOR ga in adaptations. Both short (3 h) and intermediate (up to 48 h) term re flex modifications were affected. Loss of adaptation was observed 10 d egrees 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 te mperature (Ac+10 degrees C) did not alter either increases or decrease s in the adapted Vis-VOR or VOR gain. 5. A decrease in temperature red uced the magnitude of an adapted VOR gain increase and elevated the ma gnitude of an adapted gain decrease, thus returning the VOR gain back toward its normal control gain before adaptation. Because both increas es and decreases in VOR gain were affected by the same temperature red uction, 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 adap tive VOR gain increases at temperatures acutely set 8-10 degrees C bel ow the acclimation temperature were similar to those obtained at the a cclimation temperature. Because the same temperature decrease inactiva ted retention of adapted VOR gain changes, the neuronal processes unde rlying the acquisition and the retention phases of Vis-VOR or VOR adap tation are suggested to differ qualitatively. 7. With the use of veloc ity step stimuli, both the adapted dynamic (<100 ms) and sustained (>1 00 ms) components of VOR adaptation were reduced by cooling. This effe ct 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), t he neuronal processing that is responsible for the normal operation of the visuovestibulo- and/or vestibule-ocular reflex and for the retent ion of reflex adaptation functions by separate physiological processes within the same brain stem and cerebellar circuitry. 9. We conclude t hat temperature exhibits a unique, and unexpected, state-dependent eff ect on sensorimotor regulation and adaptation for periods up to 48 h. Temperature does not alter normal VOR or the acquisition phase of an a dapted gain change. However, because it inactivates retention of adapt ive VOR gain changes reversibly, we propose that thermolability of an adapted VOR gain change reflects the alteration of a separate ligand a nd/or current related membrane event. As a result, visual-vestibular o culomotor learning is masked, but only temporarily as the complete mem ory trace or engram is actually never lost.