Role of olivocerebellar system in timing without awareness

Abstract

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...

Electrical Coupling and Synchronized Subthreshold Oscillations in the Inferior Olive of the Rhesus Macaque

“…The finding supports models of sensory-motor timing in humans that propose that the IO provides information for monitoring absolute time (Teki et al, 2012;Ashe and Bushara, 2014). Those models are based on the findings of strong IO activation triggered by deviations in the expected timing of sensory events (Teki et al, 2011;Wu et al, 2011). An internal clock-like mechanism could be ideal in tasks requiring discrimination of absolute duration and STOs in the human IO synchronized by strong electrical coupling provide an attractive neurophysiological substrate.…”

Meta-analytic connectivity and behavioral parcellation of the human cerebellum

“…The most widely accepted current structural parcellation of the cerebellum is a normalized probabilistic atlas consisting of 28 structures (Diedrichsen et al, 2009) (Figure 1) based on the Schmahmann cerebellum parcellation strategy (Schmahmann et al, 2000). This atlas has been used in various ways including confirmation and comparison of anatomical connectivity patterns (Rosch et al, 2010), identification of structural contributions across diverse tasks (Vahdat et al, 2012; Wu et al, 2011; Wildenberg et al, 2011; Moulton et al, 2011), examination of differential cortico-cerebellar co-activation (Balsters et al, 2014) and the longitudinal investigation of cerebellar morphometry (Tiemeier et al, 2010). Images delineating the volume of each cerebellar structure were obtained according to the Diedrichsen parcellation strategy in MNI space (http://www.icn.ucl.ac.uk/motorcontrol/imaging/propatlas.htm), with left and right structures treated independently (Diedrichsen et al, 2009).…”

The Olivo-Cerebellar System as a Neural Clock

“…It had long been assumed, using indirect evidence from classical conditioning and neural recording studies [46][47][48][49] that the olivo-cerebellar system mediated implicit timing. To directly test this hypothesis in human subjects, we used a temporal 'odd-ball' paradigm during event-related functional imaging [50]. We first measured the ability of each subject to detect an asynchronous stimulus with~50 % probability (temporal detection threshold) within a series of otherwise synchronous visual stimuli (Fig.…”