Inferior olivary neurons in the awake cat: detection of contact and passive body displacement

Abstract

We have recorded from 306 neurons in the inferior olive of six alert cats. Most of the cats were trained to perform a simple task with the forelimb. We observed the neural responses to a wide variety of cutaneous and proprioceptive stimuli, as well as responses during spontaneous and learned active movements. Neurons responsive to somatosensory stimulation were found in all parts of the inferior olive, and they were roughly evenly divided between those responsive to cutaneous stimulation and those responsive to proprioceptive stimulation. In the dorsal accessory olive all neurons were responsive to somatosensory stimulation. In the medial accessory nucleus 88% and in the principal olive 74% of cells were responsive to somatosensory stimulation. Cells responsive to cutaneous stimulation usually had small receptive fields, commonly on the paw. These cells had low-threshold responses to one or more forms of cutaneous stimulation and typically fired one spike at the onset of the stimulus on 80% or more of stimulus applications. Cells responsive to proprioceptive stimulation most commonly responded to passive displacements of a limb. These cells were often very sensitive, responding to linear displacements of less than 1 cm in one specific direction. No cells in our sample responded reliably during active movement by the animal. Only 21% of cells responding to passive proprioceptive stimulation showed any modulation during active movement, and the modulation was weak. Likewise, cells responsive to cutaneous stimulation generally failed to respond when a similar stimulus was produced by an active movement by the animal. Exceptions to this were stimuli produced during exploratory movements or when the receptive field unexpectedly made contact with an object during active movement. Electrical stimulation applied in the inferior olive failed to evoke movements or to modify ongoing movement. Our results are consistent with the hypothesis that inferior olivary neurons function as somatic event detectors responding particularly reliably to unexpected stimuli.

Role of olivocerebellar system in timing without awareness

“…The response of the inferior olive to deviant stimuli shown in the present study is consistent with early electrophysiological studies demonstrating that the olivary neurons are highly sensitive to unexpected external sensory stimuli (22,(34)(35)(36)(37). This finding was interpreted from the perspective of motor control to indicate that the inferior olive signals unexpected events and therefore errors or mismatches between intended and achieved movement (38-41).…”

“…The results were consistent with the enhanced response of the inferior olive and climbing fiber system to unexpected sensory input consistently shown in electrophysiological studies, and further indicated that the inferior olive response to unexpected stimuli is specific to timing (22,23). In the present study, we used a similar eventrelated fMRI paradigm to determine the effect of the subject's awareness on the transient neural responses of the inferior olive and cerebellar cortex to changes in stimulus timing.…”

“…were also shown during passive limb displacement in the absence of active movement, and indeed certain phases of movement were shown to inhibit the inferior olive responsiveness to sensory input (22,36,42). An alternative to the long-held error detection hypothesis is that the inferior olive is sensitive to the timing of sensory input.…”

“…In vitro experiments that used intracellular recording and voltage-sensitive dye imaging of inferior olive slices have shown that an extracellular stimulus "resets" the olivary neuronal oscillations and leads to synchronized firing of a large group of neurons in phase with the external stimulus (43,44). This self-referential phase resetting of subthreshold intrinsic oscillations of the olivary neurons and their synchronized firing in response to external stimuli have been proposed as the underlying mechanism of the enhanced inferior olive and climbing fibers response to unexpected stimuli (11,22,23,38,39,45). A similar mechanism likely explains the inferior olive response to the modulation of stimulus timing with or without awareness shown by fMRI methods.…”

A neural model of cortico-cerebellar interactions during attentive imitation and predictive learning of sequential handwriting movements

“…Since the cerebellum is more active during error corrections, it is likely that climbing fibers are signaling movement error, leading to LTD of Purkinje cell-parallel fiber synapses (Gellman et a!., 1985;Ito, 1991;Ito & Karachot, 1992;Oscarsson, 1969;Simpson eta!., 1996).…”