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.

Commissural Inputs to Secondary Vestibular Neurons in Alert Cats After Canal Plugs

Gaze is stabilized during head movements primarily by the vestibuloocular reflex (VOR). After a unilateral canal plug, the VOR's response is reduced. Recovery of the VOR may be brought about by changes in the efficacy of brain stem synapses or by other mechanisms. We measured the responses of horizontal secondary vestibular neurons (HSNs) to stimulation of the contralateral labyrinth. HSN responses in normal alert cats were compared with those in cats that had recovered from unilateral horizontal semicircular canal (HSCC) plugs. After recovery, excitatory commissural inputs to HSNs on the plugged side elicited significantly smaller responses than in normal cats with no change in mean discharge rates. However, mean discharge rates tended to be higher after recovery for cells receiving inhibitory commissural inputs. The change in resting rate invalidates any direct comparison of inhibitory inputs. These results are interpreted in terms of possible mechanisms for recovery from unilateral vestibular loss by the VOR neural network. We conclude that after unilateral HSCC plugs, changes in brain stem excitatory synapses and/or excitability of secondary vestibular neurons may participate in the restoration of normal vestibular reflexes.