Static Ocular Counterroll Is Implemented Through the 3-D Neural Integrator

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Abstract
Static head roll about the naso-occipital axis is known to produce an opposite ocular counterroll with a gain of approximately 10%, but the purpose and neural mechanism of this response remain obscure. In theory counterroll could be maintained either by direct tonic vestibular inputs to motoneurons, or by a neurally integrated pulse, as observed in the saccade generator and vestibulo-ocular reflex. When simulated together with ocular drift related to torsional integrator failure, the direct tonic input model predicted that the pattern of drift would shift torsionally as in ordinary counterroll, but the integrated pulse model predicted that the equilibrium position of torsional drift would be unaffected by head roll. This was tested experimentally by measuring ocular counterroll in 2 monkeys after injection of muscimol into the mesencephalic interstitial nucleus of Cajal. Whereas 90° head roll produced a mean ocular counterroll of 8.5° (±0.7° SE) in control experiments, the torsional equilibrium position observed during integrator failure failed to counterroll, showing a torsional shift of only 0.3° (±0.6° SE). This result contradicted the direct tonic input model, but was consistent with models that implement counterroll by a neurally integrated pulse.