The bidirectionality of motor learning in the vestibulo-ocular reflex is a function of cerebellar mGluR1 receptors.

Bidirectional changes in synaptic transmission have the potential to optimize the control of movement. However, it can be difficult to establish a causal relationship between the bidirectionality of synaptic plasticity and bidirectional changes in the speed of actual movements. We asked whether metabotropic glutamate receptor 1 (mGluR1) receptors, which participate in cerebellar long-term depression (LTD), are necessary for bidirectional motor learning in the vestibulo-ocular reflex (VOR). Cerebellar LTD and long-term potentiation (LTP) are thought to cause increases and decreases, respectively, in the gain of the VOR; the direction of learning depends on the behavioral protocol. We injected either the mGluR1 agonist (S)-DHPG or the antagonist YM 298198 bilaterally into the flocculus of alert cats, and then induced motor learning. In the presence of YM 298198, the VOR gain decreased in gain-up, as well as in gain-down protocols. (S)-DHPG augmented gain-up learning. Gain-down learning was not significantly affected by either drug. These results supported the hypothesis that gain-up learning relies on cerebellar LTD, but gain-down learning relies on a different mechanism. In the absence of mGluR1 activity, cerebellar LTD may be replaced with LTP, permitting learning in only one direction.

Consolidation and disruption of motor memory generalize across stimulus conditions in the vestibulo-ocular reflex.

The vestibulo-ocular reflex (VOR) exhibits motor learning that initially depends on synaptic plasticity in the cerebellar cortex. Learned decreases in VOR gain can be disrupted by rotation in darkness immediately following learning, but consolidate rapidly if the disruption stimulus is delayed. Disruption may simply reverse the synaptic changes that have recently occurred, or it may reflect new learning at other sites. The alternative to disruption, rapid consolidation, also may take place by altering the existing memory trace or may require changes at other locations. To test these possibilities, we induced decreases in the gain of the VOR in cats that wore miniaturizing goggles. Using a range of frequencies of rotation, we investigated the patterns of generalization for disruption and for rapid consolidation of the learned changes in gain. Learning was most effective at the particular frequencies that were used during training. However, disruption and rapid consolidation were not more effective at the rotation frequencies that were used during training. Instead, after consolidation, the memory retained the frequency tuning that had been established during the learning process. We conclude that disruption and rapid consolidation may not require new learning.

Rapid consolidation of motor memory in the vestibuloocular reflex.

Motor memory is relatively labile immediately after learning but can become more stable through consolidation. We investigated consolidation of motor memory in the vestibuloocular reflex (VOR). Cats viewed the world through telescopic lenses during 60 min of passive rotation. Learned decreases (gain-down learning) and increases in the VOR gain (gain-up learning) were measured during sinusoidal rotation at 2 Hz. We found that if rotation in darkness immediately followed learning, the gain of the VOR reverted toward its prelearning value, indicating that expression of the memory was disrupted. If after gain-down learning the cat spent another 60 min stationary without form vision, subsequent disruption did not occur, suggesting that memory had consolidated. Consolidation was less robust for gain-up learning. We conclude that memory in the VOR is initially labile but consolidates rapidly and consistently after gain-down learning.

Adaptive rescaling of central sensorimotor signals is preserved after unilateral vestibular damage.

Adaptive rescaling is a widespread phenomenon that dynamically adjusts the input-output relationship of a sensory system in response to changes in the ambient stimulus conditions. Rescaling has been described in the central vestibular neurons of normal cats. After recovery from unilateral vestibular damage, the vestibulo-ocular reflex (VOR) remains nonlinear for rotation toward the damaged side. Therefore, rescaling in the VOR pathway may be especially important after damage. Here, we demonstrate that central vestibular neurons adjust their input-output relationships depending on the input velocity range, suggesting that adaptive rescaling is preserved after vestibular damage and can contribute to the performance of the VOR. We recorded from isolated vestibular neurons in alert cats that had recovered from unilateral vestibular damage. The peak velocity of 1-Hz sinusoidal rotation was varied from 10 to 120 degrees/s and the sensitivities and dynamic ranges of vestibular neurons were measured. Most neuronal responses showed significant nonlinearities even at the lowest peak velocity that we tested. Significant rescaling was seen in the responses of neurons both ipsilateral and contralateral to chronic unilateral damage. On the average, when the peak rotational velocity increased by a factor of 8, the average sensitivity to rotation decreased by roughly a factor of 2. Rescaling did not depend on eye movement signals. Our results suggest that the dynamic ranges of central neurons are extended by rescaling and that, after vestibular damage, adaptive rescaling may act to reduce nonlinearities in the response of the VOR to rotation at high speeds.