The basal ganglia in perceptual timing: Timing performance in Multiple System Atrophy and Huntington's disease ^☆

Abstract

The timing of perceptual events depends on an anatomically and functionally connected network comprising basal ganglia, cerebellum, pre-frontal cortex and supplementary motor area. Recent studies demonstrate the cerebellum to be involved in absolute, duration-based timing, but not in relative timing based on a regular beat. Conversely, functional involvement of the striatum is observed in relative timing, but its role in absolute timing is unclear.

This work tests the specific role of the basal ganglia in the perceptual timing of auditory events. It aims to distinguish the hypothesised unified model of time perception ( Teki, Grube, & Griffiths, 2012), in which the striatum is a mandatory component for all timing tasks, from a modular system in which they subserve relative timing, with absolute timing processed by the cerebellum.

Test groups comprised individuals with Multiple System Atrophy, a disorder in which similar pathology can produce clinical deficits associated with dysfunction of the cerebellum (MSA-C, n=8) or striatum (MSA-P, n=10), and early symptomatic Huntington's disease (HD, n=14). Individuals with chronic autoimmune peripheral neuropathy ( n=11) acted as controls.

Six adaptive tasks were carried out to assess perceptual thresholds for absolute timing through duration discrimination for sub- and supra-second time intervals, and relative timing through the detection of beat-based regularity and irregularity, detection of a delay within an isochronous sequence, and the discrimination of sequences with metrical structure.

All three patient groups exhibited impairments in performance in comparison with the control group for all tasks, and severity of impairment was significantly correlated with disease progression. No differences were demonstrated between MSA-C and MSA-P, and the most severe impairments were observed in those with HD.

The data support an obligatory role for the basal ganglia in all tested timing tasks, both absolute and relative, as predicted by the unified model. The results are not compatible with models of a brain timing network based upon independent modules.

Graphical abstract

Ninety five percent confidence intervals for mean group performance by task. Var: sub-second variable-interval discrimination. Sup: supra-second variable-interval discrimination. Pul: detection of regularity (pulse or beat) within an irregular sequence. Iso: detection of deviation from isochrony. Irr: detection of irregularity within a regular sequence. Met: detection of distortion of a sequence with strong metrical structure.

Highlights

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  Patients with basal ganglia disease undertook a battery of perceptual timing tasks.

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  All patients displayed poorer performance than neurological control participants.

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  Performance in Huntington's disease was worse than Multiple System Atrophy.

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  Poorer performance was significantly correlated with disease progression.

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  These findings support the hypothesised unified model of time perception.