Deciphering the impact of cerebellar and basal ganglia dysfunction in accuracy and variability of motor timing

Claassen, Daniel O.; Jones, Catherine R. G.; Yu, Minhong; Dirnberger, Georg; Malone, Tim; Parkinson, Michael; Giunti, Paola; Kubovy, Michael; Jahanshahi, Marjan

doi:10.1016/j.neuropsychologia.2012.09.018

Cited by 27 publications

(14 citation statements)

References 49 publications

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“…Older healthy controls show a similar pattern only at the slower 750 ms interval, but even here PD-Cs and PD-FOGs show a larger hastening effect than controls. This unidirectional nature—ahead of the established cue frequency—fits with our a priori hypothesis that festinating movements are globally manifest (i.e., not confined to the lower extremities) and worse in PD patients who freeze (Claassen et al, 2013; Jones et al, 2011). …”

Section: Discussionsupporting

confidence: 82%

Dysrhythmia of timed movements in Parkinson׳s disease and freezing of gait

et al. 2015

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A well-established motor timing paradigm, the Synchronization-Continuation Task (SCT), quantifies how accurately participants can time finger tapping to a rhythmic auditory beat (synchronization phase) then maintain this rhythm after the external auditory cue is extinguished, where performance depends on an internal representation of the beat (continuation phase). In this study, we investigated the hypothesis that Parkinson’s disease (PD) patients with clinical symptoms of freezing of gait (FOG) exhibit exaggerated motor timing deficits. We predicted that dysrhythmia is exacerbated when finger tapping is stopped temporarily and then reinitiated under the guidance of an internal representation of the beat. Healthy controls and PD patients with and without FOG performed the SCT with and without the insertion of a 7-second cessation of motor tapping between synchronization and continuation phases. With no interruption between synchronization and continuation phases, PD patients, especially those with FOG, showed pronounced motor timing hastening at the slowest inter stimulus intervals during the continuation phase. The introduction of a gap prior to the continuation phase had a beneficial effect for healthy controls and PD patients without FOG, although patients with FOG continued to show pronounced and persistent motor timing hastening. Ratings of freezing of gait severity across the entire sample of PD tracked closely with the magnitude of hastening during the continuation phase. These results suggest that PD is accompanied by a unique dysrhythmia of measured movements, with FOG reflecting a particularly pronounced disruption to internal rhythmic timing.

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Section: Discussionsupporting

confidence: 82%

Dysrhythmia of timed movements in Parkinson׳s disease and freezing of gait

et al. 2015

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“…Thus, a functional connectivity in a variety of tasks, from sensory processing to motor control to cognitive functions has been hypothesized. In particular, this concept has been expanded to physiology of the processing of timing information and indeed evidence suggests that both basal ganglia and cerebellum are involved in this process [202][203][204].…”

Section: Laura Avanzinomentioning

confidence: 99%

Consensus paper: Decoding the Contributions of the Cerebellum as a Time Machine. From Neurons to Clinical Applications

et al. 2018

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Time perception is an essential element of conscious and subconscious experience, coordinating our perception and interaction with the surrounding environment. In recent years, major technological advances in the field of neuroscience have helped foster new insights into the processing of temporal information, including extending our knowledge of the role of the cerebellum as one of the key nodes in the brain for this function. This consensus paper provides a state-of-the-art picture from the experts in the field of the cerebellar research on a variety of crucial issues related to temporal processing, drawing on recent anatomical, neurophysiological, behavioral, and clinical research.The cerebellar granular layer appears especially well-suited for timing operations required to confer millisecond precision for cerebellar computations. This may be most evident in the manner the cerebellum controls the duration of the timing of agonist-antagonist EMG bursts associated with fast goal-directed voluntary movements. In concert with adaptive processes, interactions within the cerebellar cortex are sufficient to support sub-second timing. However, supra-second timing seems to require cortical and basal ganglia networks, perhaps operating in concert with Cerebellum.Additionally, sensory information such as an unexpected stimulus can be forwarded to the cerebellum via the climbing fiber system, providing a temporally constrained mechanism to adjust on-going behavior and modify future processing. Patients with cerebellar disorders exhibit impairments on a range of tasks that require precise timing, and recent evidence suggest that timing problems observed in other neurological conditions such as Parkinson's disease, essential tremor, and dystonia, may reflect disrupted interactions between the basal ganglia and cerebellum.The complex concepts emerging from this consensus paper should provide a foundation for further discussion, helping identify basic research questions required to understand how the brain represents and utilizes time, as well as delineating ways in which this knowledge can help improve the lives of those with neurological conditions that disrupt this most elemental sense. The panel of experts agrees that timing control in the brain is a complex concept in whom cerebellar circuitry is deeply involved. The concept of a timing machine has now expanded to clinical disorders. The Cerebellum Represents Isolated Temporal Intervals Across Task Domains Assaf Breska and Richard B. IvryIt is widely accepted that the cerebellum contributes, in some manner, to temporal processing, but the functional domain and computational mechanisms remain the subject of considerable debate. An early hypothesis was that the cerebellum served as a centralized, dedicated timing system [6,7].

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“…Both levodopa and stimulation of the subthalamic nucleus improved time reproduction (Torta et al, 2010). PD patients can also have deficits in processing temporal information at sub-second time scales (Harrington et al, 1998; Riesen and Schnider, 2001), but there is significant variability in timing at this scale (Merchant et al, 2008; Jones et al, 2011; Claassen et al, 2013). The consistency of PD timing deficits at seconds and inconsistency below milliseconds may be related to the memory and attentional load of longer time intervals (Koch et al, 2008).…”

Section: Dopamine and Interval Timingmentioning

confidence: 99%

Executive dysfunction in Parkinson’s disease and timing deficits

Parker

Lamichhane

Caetano

et al. 2013

Front. Integr. Neurosci.

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Patients with Parkinson’s disease (PD) have deficits in perceptual timing, or the perception and estimation of time. PD patients can also have cognitive symptoms, including deficits in executive functions such as working memory, planning, and visuospatial attention. Here, we discuss how PD-related cognitive symptoms contribute to timing deficits. Timing is influenced by signaling of the neurotransmitter dopamine in the striatum. Timing also involves the frontal cortex, which is dysfunctional in PD. Frontal cortex impairments in PD may influence memory subsystems as well as decision processes during timing tasks. These data suggest that timing may be a type of executive function. As such, timing can be used to study the neural circuitry of cognitive symptoms of PD as they can be studied in animal models. Performance of timing tasks also maybe a useful clinical biomarker of frontal as well as striatal dysfunction in PD.

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Deciphering the impact of cerebellar and basal ganglia dysfunction in accuracy and variability of motor timing

Cited by 27 publications

References 49 publications

Dysrhythmia of timed movements in Parkinson׳s disease and freezing of gait

Dysrhythmia of timed movements in Parkinson׳s disease and freezing of gait

Consensus paper: Decoding the Contributions of the Cerebellum as a Time Machine. From Neurons to Clinical Applications

Executive dysfunction in Parkinson’s disease and timing deficits

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