Discharge of inferior olive cells during reaching errors and perturbations

Abstract

It is widely believed that inferior olive (IO) neurons signal the occurrence of movement errors. The IO compares descending motor commands with information about movement and detects mismatches. Presumably, this error signal is used by the cerebellum to improve motor performance. To test this theory, we trained cats to reach out, grasp and retrieve a handle on cue. After training, the handle was displaced on selected trials so the cats would reach but miss the handle. Fifty-five IO cells with receptive fields on the forelimb were tested with the displaced handle condition. No cell fired at or near the time of “expected” contact, but some cells fired when the cats struck objects while attempting to grasp. A mismatch between a motor command and expected result is not sufficient to activate IO neurons; appropriate stimulation must occur. To define conditions for appropriate stimulation, the limb was stimulated at various times during the task. Sixty-six cells (including the 55 tested under the displaced handle condition) were tested with mechanical stimulation during quiet stance, and 98% responded to stimulation. A smaller percentage (68%) fired when stimulation was introduced during the reaching task, and the probability of these responses varied with the subdivision of the olive as well as the phase of the task. We conclude that it is unlikely that IO discharge provides information about movement or movement error. Olivary cells respond reliably to appropriate somatosensory stimulation but not to active movement or movement error.