Specificity of Inferior Olive Response to Stimulus Timing

Liu, Tao; Xu, Duo; Ashe, James; Bushara, Khalaf

doi:10.1152/jn.00961.2007

Cited by 40 publications

(35 citation statements)

References 39 publications

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“…The present study significantly extends the findings of previous studies on the importance of the olivocerebellar system in the timing of sensory events (21,25). Our data demonstrate that the response of the inferior olive and multiple areas within the cerebellar cortex to changes in stimulus timing occur regardless of whether the subjects were aware of such changes.…”

Section: Discussionsupporting

confidence: 87%

“…By using event-related functional MRI (fMRI) and a perceptual task that dissociates the temporal from nontemporal attributes of sensory input, we have shown inferior olive activation when subjects perceived unexpected changes in the timing but not the spatial orientation or color of visual stimuli (21). 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).…”

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confidence: 99%

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Role of olivocerebellar system in timing without awareness

Ashe²,

Bushara

2011

Proc. Natl. Acad. Sci. U.S.A.

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The timing of events can be implicit or without awareness yet critical for task performance. However, the neural correlates of implicit timing are unknown. One system that has long been implicated in event timing is the olivocerebellar system, which originates exclusively from the inferior olive. By using event-related functional MRI in human subjects and a specially designed behavioral task, we examined the effect of the subjects' awareness of changes in stimulus timing on the olivocerebellar system response. Subjects were scanned while observing changes in stimulus timing that were presented near each subject's detection threshold such that subjects were aware of such changes in only approximately half the trials. The inferior olive and multiple areas within the cerebellar cortex showed a robust response to time changes regardless of whether the subjects were aware of these changes. Our findings provide support to the proposed role of the olivocerebellar system in encoding temporal information and further suggest that this system can operate independently of awareness and mediate implicit timing in a multitude of perceptual and motor operations, including classical conditioning and implicit learning.cerebellum | visual E ncoding the timing of events is an inherent component of perceptual and motor tasks. Such timing can be implicit or without the subject's awareness yet important for performance regardless of the goal of the task. For example, when throwing a ball at a target, the spatial accuracy relies, at least partially, on precise motor timing; however, subjects may not be explicitly aware of the timing of individual components of this complex multijoint movement (1, 2). Similarly, subjects may improve the speed and accuracy of performing a perceptual task by implicitly using temporal information to predict the timing of sensory stimuli (i.e., temporal expectancy) (3, 4). More directly, implicit timing can be conceptualized as a critical component of classical conditioning and other stimulus/response association processes such as implicit learning and automatic behavior. However, implicit timing or timing without awareness has been difficult to characterize in experimental settings, especially in animal studies, and its neural correlates remain poorly understood (5). One system that has long been implicated in event timing is the olivocerebellar system, which originates exclusively in the inferior olive (6-12). Whether the olivocerebellar system mediates timing without awareness has not been demonstrated directly to our knowledge. However, the capacity of the inferior olive and the climbing fiber system to encode temporal information independently of awareness is supported by indirect evidence from classical conditioning and single cell recording literature (10)(11)(13)(14)(15)(16). In the few imaging and lesion studies in humans that specifically addressed the cerebellar contribution to implicit timing, the term "implicit timing" has not been strictly defined as timing without awareness (5,(17)(18)(19)(2...

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Section: Discussionsupporting

confidence: 87%

mentioning

confidence: 99%

Role of olivocerebellar system in timing without awareness

Ashe²,

Bushara

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…It is noteworthy that the inferior olive and cerebellum (HV), and apparently the rubral area, are specifically recruited while encoding temporal information of "unexpected" sensory events. 39 In our study, the RN could constitute a relay for salience detection of affective/ autonomic information. Second, functional connectivity was also found between the RN and subcortical loci (hypothalamus, SN, mesencephalic tegmentum).…”

Section: Discussionmentioning

confidence: 78%

Functional Connectivity of the Human Red Nucleus in the Brain Resting State at 3T

Nioche¹,

Cabanis²,

Habas³

2008

AJNR Am J Neuroradiol

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BACKGROUND AND PURPOSE:Previous structural data obtained with diffusion tensor imaging axonal tracking have demonstrated possible in vivo connections between the human red nucleus (RN) and the sensorimotor and associative cortical areas. However, tractographic reconstructions can include false trajectories because of, for instance, the low spatial resolution of diffusion images or the inability to precisely detect fiber crossings. The rubral network was therefore reassessed by functional connectivity during the brain resting state. Because the RN is located very close to the substantia nigra (SN), the nigral network was also studied to ensure that these 2 circuits were correctly dissociated.

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“…Therefore, we performed an additional experiment in which we dissociated the temporal and non-temporal characteristics of different sensory stimuli [45]. Subjects were asked to focus on specific characteristics (orientation, color, or timing) of a visually displayed stimulus and indicate when it changed during individual trials.…”

Section: Activation In Inferior Olive Specific For Stimulus Timingmentioning

confidence: 99%

The Olivo-Cerebellar System as a Neural Clock

Ashe

Bushara

2014

Advances in Experimental Medicine and Biology

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The cerebellum, and the olivo-cerebellar system in particular, may be the central mechanism of a neural clock that provides a rhythmic neural signal used to time motor and cognitive processes. Several independent lines of evidence support this hypothesis. First, the resting membrane potential of neurons in the inferior olive oscillates at ~10 Hz and the neural input from the olive leads to rhythmic complex spikes in cerebellum Purkinje cells. Second, the repeating modular microstructure of the cerebellum is ideally suited for performing computations underlying a basic neural process such as timing. Third, damage to the cerebellum leads to deficits in the perception of time and in the production of timed movements. Fourth, functional imaging studies in human subjects have shown activation of the inferior olive specifically during time perception. However, additional data on the exact role of rhythmic cerebellar activity during basis motor and sensory processing will be necessary before the hypothesis that the cerebellum is a neural clock is more widely accepted.

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Specificity of Inferior Olive Response to Stimulus Timing

Cited by 40 publications

References 39 publications

Role of olivocerebellar system in timing without awareness

Role of olivocerebellar system in timing without awareness

Functional Connectivity of the Human Red Nucleus in the Brain Resting State at 3T

The Olivo-Cerebellar System as a Neural Clock

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