Spontaneous, synchronized, and corrective timing behavior in cerebellar lesion patients

Research output: Contribution to journalArticleAcademicpeer-review

4 Citations (Scopus)

Abstract

To successfully navigate through and interact with a dynamic environment it is necessary to acquire and use adequate temporal information to guide behavior. Apart from several areas in the cerebral cortex and cortico-striatal networks, the cerebellum has been proposed to engage in the processing of temporal information. Damage to the cerebellum can impair precise event-based temporal processing in motor and non-motor behavior. To further substantiate cerebellar contributions to temporal processing and to explore its specific role in adapting to a dynamic environment, we investigated sensorimotor temporal processing in ten patients with cerebellar lesions and a corresponding number of healthy matched controls. Experimental tasks included simple self-paced repetitive finger-tapping (spontaneous motor tempo), temporally non-adaptive (isochronous pacing) and adaptive (tempo-changing pacing) sensorimotor synchronization with auditory sequences (synchronization-continuation tapping), and a perceptual tempo judgment. The results indicate that patients' performance diverges systematically from controls on several measures. Cerebellar patients demonstrate more variable self-paced tapping, larger negative asynchronies when synchronizing with isochronous pacing sequences, altered automatic error correction responses to tempo changes (phase correction), and decreased perceptual sensitivity to these perturbations, especially for small accelerations. These findings confirm imprecise temporal processing in cerebellar patients, and hint at a specific impairment in the tenth-of-milliseconds range preceding critical events, in line with a temporally predictive account of cerebellar function. Moreover, this cerebellar profile complements previous findings concerning dysfunctional temporal processing in basal ganglia patients assessed with the same experimental setup, suggesting structural and functional differentiation within an integrative temporal processing network.

Original languageEnglish
Pages (from-to)285–293
Number of pages9
JournalBehavioural Brain Research
Volume312
DOIs
Publication statusPublished - 1 Oct 2016

Keywords

  • Brain injury
  • Sensorimotor synchronization
  • Adaptation
  • Temporal processing
  • Prediction
  • BASAL GANGLIA LESIONS
  • SENSORIMOTOR SYNCHRONIZATION
  • MOTOR CONTROL
  • PERCEPTUAL CENTER
  • PHASE CORRECTION
  • DENTATE NUCLEUS
  • TEMPO CHANGES
  • TIME
  • REPRESENTATION
  • INVOLVEMENT

Cite this

@article{9d0f22c49f0548318deaa8b8831c3cc1,
title = "Spontaneous, synchronized, and corrective timing behavior in cerebellar lesion patients",
abstract = "To successfully navigate through and interact with a dynamic environment it is necessary to acquire and use adequate temporal information to guide behavior. Apart from several areas in the cerebral cortex and cortico-striatal networks, the cerebellum has been proposed to engage in the processing of temporal information. Damage to the cerebellum can impair precise event-based temporal processing in motor and non-motor behavior. To further substantiate cerebellar contributions to temporal processing and to explore its specific role in adapting to a dynamic environment, we investigated sensorimotor temporal processing in ten patients with cerebellar lesions and a corresponding number of healthy matched controls. Experimental tasks included simple self-paced repetitive finger-tapping (spontaneous motor tempo), temporally non-adaptive (isochronous pacing) and adaptive (tempo-changing pacing) sensorimotor synchronization with auditory sequences (synchronization-continuation tapping), and a perceptual tempo judgment. The results indicate that patients' performance diverges systematically from controls on several measures. Cerebellar patients demonstrate more variable self-paced tapping, larger negative asynchronies when synchronizing with isochronous pacing sequences, altered automatic error correction responses to tempo changes (phase correction), and decreased perceptual sensitivity to these perturbations, especially for small accelerations. These findings confirm imprecise temporal processing in cerebellar patients, and hint at a specific impairment in the tenth-of-milliseconds range preceding critical events, in line with a temporally predictive account of cerebellar function. Moreover, this cerebellar profile complements previous findings concerning dysfunctional temporal processing in basal ganglia patients assessed with the same experimental setup, suggesting structural and functional differentiation within an integrative temporal processing network.",
keywords = "Brain injury, Sensorimotor synchronization, Adaptation, Temporal processing, Prediction, BASAL GANGLIA LESIONS, SENSORIMOTOR SYNCHRONIZATION, MOTOR CONTROL, PERCEPTUAL CENTER, PHASE CORRECTION, DENTATE NUCLEUS, TEMPO CHANGES, TIME, REPRESENTATION, INVOLVEMENT",
author = "Michael Schwartze and Keller, {Peter E} and Kotz, {Sonja A}",
note = "Copyright {\circledC} 2016 Elsevier B.V. All rights reserved.",
year = "2016",
month = "10",
day = "1",
doi = "10.1016/j.bbr.2016.06.040",
language = "English",
volume = "312",
pages = "285–293",
journal = "Behavioural Brain Research",
issn = "0166-4328",
publisher = "Elsevier Science",

}

Spontaneous, synchronized, and corrective timing behavior in cerebellar lesion patients. / Schwartze, Michael; Keller, Peter E; Kotz, Sonja A.

In: Behavioural Brain Research, Vol. 312, 01.10.2016, p. 285–293.

Research output: Contribution to journalArticleAcademicpeer-review

TY - JOUR

T1 - Spontaneous, synchronized, and corrective timing behavior in cerebellar lesion patients

AU - Schwartze, Michael

AU - Keller, Peter E

AU - Kotz, Sonja A

N1 - Copyright © 2016 Elsevier B.V. All rights reserved.

PY - 2016/10/1

Y1 - 2016/10/1

N2 - To successfully navigate through and interact with a dynamic environment it is necessary to acquire and use adequate temporal information to guide behavior. Apart from several areas in the cerebral cortex and cortico-striatal networks, the cerebellum has been proposed to engage in the processing of temporal information. Damage to the cerebellum can impair precise event-based temporal processing in motor and non-motor behavior. To further substantiate cerebellar contributions to temporal processing and to explore its specific role in adapting to a dynamic environment, we investigated sensorimotor temporal processing in ten patients with cerebellar lesions and a corresponding number of healthy matched controls. Experimental tasks included simple self-paced repetitive finger-tapping (spontaneous motor tempo), temporally non-adaptive (isochronous pacing) and adaptive (tempo-changing pacing) sensorimotor synchronization with auditory sequences (synchronization-continuation tapping), and a perceptual tempo judgment. The results indicate that patients' performance diverges systematically from controls on several measures. Cerebellar patients demonstrate more variable self-paced tapping, larger negative asynchronies when synchronizing with isochronous pacing sequences, altered automatic error correction responses to tempo changes (phase correction), and decreased perceptual sensitivity to these perturbations, especially for small accelerations. These findings confirm imprecise temporal processing in cerebellar patients, and hint at a specific impairment in the tenth-of-milliseconds range preceding critical events, in line with a temporally predictive account of cerebellar function. Moreover, this cerebellar profile complements previous findings concerning dysfunctional temporal processing in basal ganglia patients assessed with the same experimental setup, suggesting structural and functional differentiation within an integrative temporal processing network.

AB - To successfully navigate through and interact with a dynamic environment it is necessary to acquire and use adequate temporal information to guide behavior. Apart from several areas in the cerebral cortex and cortico-striatal networks, the cerebellum has been proposed to engage in the processing of temporal information. Damage to the cerebellum can impair precise event-based temporal processing in motor and non-motor behavior. To further substantiate cerebellar contributions to temporal processing and to explore its specific role in adapting to a dynamic environment, we investigated sensorimotor temporal processing in ten patients with cerebellar lesions and a corresponding number of healthy matched controls. Experimental tasks included simple self-paced repetitive finger-tapping (spontaneous motor tempo), temporally non-adaptive (isochronous pacing) and adaptive (tempo-changing pacing) sensorimotor synchronization with auditory sequences (synchronization-continuation tapping), and a perceptual tempo judgment. The results indicate that patients' performance diverges systematically from controls on several measures. Cerebellar patients demonstrate more variable self-paced tapping, larger negative asynchronies when synchronizing with isochronous pacing sequences, altered automatic error correction responses to tempo changes (phase correction), and decreased perceptual sensitivity to these perturbations, especially for small accelerations. These findings confirm imprecise temporal processing in cerebellar patients, and hint at a specific impairment in the tenth-of-milliseconds range preceding critical events, in line with a temporally predictive account of cerebellar function. Moreover, this cerebellar profile complements previous findings concerning dysfunctional temporal processing in basal ganglia patients assessed with the same experimental setup, suggesting structural and functional differentiation within an integrative temporal processing network.

KW - Brain injury

KW - Sensorimotor synchronization

KW - Adaptation

KW - Temporal processing

KW - Prediction

KW - BASAL GANGLIA LESIONS

KW - SENSORIMOTOR SYNCHRONIZATION

KW - MOTOR CONTROL

KW - PERCEPTUAL CENTER

KW - PHASE CORRECTION

KW - DENTATE NUCLEUS

KW - TEMPO CHANGES

KW - TIME

KW - REPRESENTATION

KW - INVOLVEMENT

U2 - 10.1016/j.bbr.2016.06.040

DO - 10.1016/j.bbr.2016.06.040

M3 - Article

C2 - 27345424

VL - 312

SP - 285

EP - 293

JO - Behavioural Brain Research

JF - Behavioural Brain Research

SN - 0166-4328

ER -