Reversal of motor learning in the vestibulo-ocular reflex in the absence of visual input

Abstract

Motor learning in the vestibulo-ocular reflex (VOR) and eyeblink conditioning use similar neural circuitry, and they may use similar cellular plasticity mechanisms. Classically conditioned eyeblink responses undergo extinction after prolonged exposure to the conditioned stimulus in the absence of the unconditioned stimulus. We investigated the possibility that a process similar to extinction may reverse learned changes in the VOR. We induced a learned alteration of the VOR response in rhesus monkeys using magnifying or miniaturizing goggles, which caused head movements to be accompanied by visual image motion. After learning, head movements in the absence of visual stimulation caused a loss of the learned eye movement response. When the learned gain was low, this reversal of learning occurred only when head movements were delivered, and not when the head was held stationary in the absence of visual input, suggesting that this reversal is mediated by an active, extinction-like process.

Figure 1

Comparison between eyeblink conditioning and motor learning in the VOR. Before training in the eyeblink conditioning paradigm, an air puff to the eye (unconditioned stimulus; US) elicits a reflexive blink (unconditioned response; UR). When a tone (conditioned stimulus; CS) is paired with the air puff during training, the animal learns to blink (conditioned response; CR) in response to the tone alone. During extinction training, the tone is presented repeatedly without the air puff, leading to the eventual extinction of the learned response. Before training in the VOR, image movement across the retina elicits a tracking eye movement response, and head movement elicits the normal VOR eye movement response. During training, head movements (CS) are paired with image movements (US) and these two stimuli together elicit an altered eye movement response which is approximately the sum of the eye movement response to the image movement and the eye movement response to the head movement. Following training, head movement elicits this altered eye movement response in the absence of the visual stimulus (CR). In the second phase of training, the head movement is presented repeatedly in the absence of image movement. We tested whether this would lead to an extinction-like change in the eye movement response to the head movement.

Figure 2

Learned changes in VOR gain following training with goggles. (A) Example traces of eye velocity during head movements in the dark. The top trace shows the sinusoidal head velocity profile used to measure the VOR (± 10°/sec, 0.5 Hz). The bottom three traces show the eye velocity responses to the head movements before training (eye normal gain), following training with magnifying goggles (eye high gain), and following training with miniaturizing goggles (eye low gain). The sharp discontinuities in the traces are saccades, which were removed for analysis. (B) Example time course, showing the VOR gain as a function of days of training with miniaturizing goggles. (C) Average VOR gain at the start of the experiments following training with magnifying goggles (left), miniaturizing goggles (right), or no goggles (middle). Each bar represents the average gain for one monkey. Numbers above the bars are the number of experiments for each monkey in each condition, and error bars represent standard errors.

Figure 3

Reversal of learned changes in VOR gain. (A) Change in VOR gain after 1 h of head movements in the dark (post minus pre). When the initial gain was high (left) or low (right), the VOR gain returned toward normal. (B) Change in VOR gain after 1 h of sitting stationary in the dark.

Figure 4

Confirmation of the lack of visual stimuli during head rotations in the dark. After training with miniaturizing goggles in Monkey B, the change in VOR gain after 1 h of head movements in the dark was similar when the goggles were removed during the experiments (left) and when they remained on during the experiments (right), suggesting that the effects could not be explained by stray visual stimulation.

Figure 5

Time course of the reversal of learned changes in VOR gain. (A) Example time course of changes in VOR gain in Monkey B during head rotations in the dark after the gain had been lowered through training with miniaturizing goggles. Most of the change occurred during the first few minutes of head movements, but changes continued throughout the hour. (B) Change in VOR gain after 10 min of head movements in the dark (left) compared with the change after the full hour of head movements in the dark when the initial gain was high. (C) Same as B, when initial trained gain was low.