Retention of VOR gain following short-term VOR adaptation

Abstract

Motor learning in the vestibular system can be differentially obtained depending upon the context for which the vestibulo-ocular reflex (VOR) has been exposed. Manipulating head orientation relative to gravity is an example of a contextual cue that can elicit independent VOR gains. We were interested in examining retention of short-term VOR adaptation when the adapting stimulus was paired with a novel contextual cue. Two sets of non-human primate VOR adaptation experiments were designed to assess the influence of head position relative to gravity on retention of the pitch VOR. First, the pitch VOR of three squirrel monkeys was adapted for 3 h using minimizing (×0.45) spectacles and a sum-of-sines stimulus (20°/s at 0.5, 1.1, 2.3, and 3.7 Hz) while the animals were positioned left ear down (LED adaptation). Pitch VOR gains were measured in the adapted position (LED) and two non-adapted positions (upright, UP) or right ear down (RED). In the second set of experiments, the pitch VOR was adapted in an upright head position (same adapting stimulus as used in LED) and tested in UP, LED or RED. No head immobility or darkness restrictions were imposed on the animals after the initial adaptation exposure. The pitch VOR gains were measured during the acceleration (G _A) and constant velocity (G _V) portions of 1,000°/s²–150°/s step responses and during 0.5, 2.0, and 4.0 Hz sinusoids with velocities varying from 20 to 100°/s. All measures of VOR gain for UP, LED, and RED were done immediately after the adaptation and for three subsequent days and at post-adaptation day 7 (PAD 7). When tested in the adapting position, all experiments showed immediate reduction in G _A and G _V compared with pre-adaptation levels. For LED adaptation experiments, the pitch G _A and G _V gains were significantly reduced for as long as 7 days. Some retention of the LED-adapted VOR gain also occurred when testing in the RED position. No retention of pitch VOR G _A or G _V existed for the UP position after adaptation in LED. After the UP-adapt experiments, no retention of the G _A or G _V was found when tested in the adapting position. Interestingly, however, some retention of G _A and G _V did exist when the UP-adapted animals were tested in LED or RED. Data from sinusoidal rotations followed a similar adaptation pattern as the step responses. Our findings show that after only 3 h of adaptation exposure, adaptation of the pitch VOR gain is retained for several days. This long-term retention of VOR adaptation after short-term exposure appears to be the result of inducing adaptation with an atypical combination of movement and position for the monkey (LED-adapt). Our results indicate that head orientation relative to gravity is an effective context for retaining learned VOR gains in addition to restricting mobility or keeping animals in the dark. We also show that the adapting head position determines the magnitude of VOR adaptation.