The role of the cerebellum in adaptation: ALE meta-analyses on sensory feedback error

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

It is widely accepted that unexpected sensory consequences of self-action engage the cerebellum. However, we currently lack consensus on where in the cerebellum, we find fine-grained differentiation to unexpected sensory feedback. This may result from methodological diversity in task-based human neuroimaging studies that experimentally alter the quality of self-generated sensory feedback. We gathered existing studies that manipulated sensory feedback using a variety of methodological approaches and performed activation likelihood estimation (ALE) meta-analyses. Only half of these studies reported cerebellar activation with considerable variation in spatial location. Consequently, ALE analyses did not reveal significantly increased likelihood of activation in the cerebellum despite the broad scientific consensus of the cerebellum's involvement. In light of the high degree of methodological variability in published studies, we tested for statistical dependence between methodological factors that varied across the published studies. Experiments that elicited an adaptive response to continuously altered sensory feedback more frequently reported activation in the cerebellum than those experiments that did not induce adaptation. These findings may explain the surprisingly low rate of significant cerebellar activation across brain imaging studies investigating unexpected sensory feedback. Furthermore, limitations of functional magnetic resonance imaging to probe the cerebellum could play a role as climbing fiber activity associated with feedback error processing may not be captured by it. We provide methodological recommendations that may guide future studies.

Original languageEnglish
Pages (from-to)3966-3981
Number of pages16
JournalHuman Brain Mapping
Volume40
Issue number13
Early online date2 Jun 2019
DOIs
Publication statusPublished - Sep 2019

Keywords

  • ADAPTIVE-CONTROL
  • DELAYED AUDITORY-FEEDBACK
  • EXTRASTRIATE BODY AREA
  • HUNTINGTONS-DISEASE
  • INTERNAL-MODELS
  • PREFRONTAL CORTEX
  • SENSORIMOTOR ADAPTATION
  • SPEECH PRODUCTION
  • SUPPLEMENTARY MOTOR AREA
  • VISUO-MOTOR
  • cerebellum
  • fMRI
  • forward model
  • meta-analysis
  • prediction
  • sensory feedback

Cite this

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title = "The role of the cerebellum in adaptation: ALE meta-analyses on sensory feedback error",
abstract = "It is widely accepted that unexpected sensory consequences of self-action engage the cerebellum. However, we currently lack consensus on where in the cerebellum, we find fine-grained differentiation to unexpected sensory feedback. This may result from methodological diversity in task-based human neuroimaging studies that experimentally alter the quality of self-generated sensory feedback. We gathered existing studies that manipulated sensory feedback using a variety of methodological approaches and performed activation likelihood estimation (ALE) meta-analyses. Only half of these studies reported cerebellar activation with considerable variation in spatial location. Consequently, ALE analyses did not reveal significantly increased likelihood of activation in the cerebellum despite the broad scientific consensus of the cerebellum's involvement. In light of the high degree of methodological variability in published studies, we tested for statistical dependence between methodological factors that varied across the published studies. Experiments that elicited an adaptive response to continuously altered sensory feedback more frequently reported activation in the cerebellum than those experiments that did not induce adaptation. These findings may explain the surprisingly low rate of significant cerebellar activation across brain imaging studies investigating unexpected sensory feedback. Furthermore, limitations of functional magnetic resonance imaging to probe the cerebellum could play a role as climbing fiber activity associated with feedback error processing may not be captured by it. We provide methodological recommendations that may guide future studies.",
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author = "Johnson, {Joseph F} and Michel Belyk and Michael Schwartze and Pinheiro, {Ana P} and Kotz, {Sonja A}",
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The role of the cerebellum in adaptation : ALE meta-analyses on sensory feedback error. / Johnson, Joseph F; Belyk, Michel; Schwartze, Michael; Pinheiro, Ana P; Kotz, Sonja A.

In: Human Brain Mapping, Vol. 40, No. 13, 09.2019, p. 3966-3981.

Research output: Contribution to journalArticleAcademicpeer-review

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T1 - The role of the cerebellum in adaptation

T2 - ALE meta-analyses on sensory feedback error

AU - Johnson, Joseph F

AU - Belyk, Michel

AU - Schwartze, Michael

AU - Pinheiro, Ana P

AU - Kotz, Sonja A

N1 - © 2019 The Authors. Human Brain Mapping published by Wiley Periodicals, Inc.

PY - 2019/9

Y1 - 2019/9

N2 - It is widely accepted that unexpected sensory consequences of self-action engage the cerebellum. However, we currently lack consensus on where in the cerebellum, we find fine-grained differentiation to unexpected sensory feedback. This may result from methodological diversity in task-based human neuroimaging studies that experimentally alter the quality of self-generated sensory feedback. We gathered existing studies that manipulated sensory feedback using a variety of methodological approaches and performed activation likelihood estimation (ALE) meta-analyses. Only half of these studies reported cerebellar activation with considerable variation in spatial location. Consequently, ALE analyses did not reveal significantly increased likelihood of activation in the cerebellum despite the broad scientific consensus of the cerebellum's involvement. In light of the high degree of methodological variability in published studies, we tested for statistical dependence between methodological factors that varied across the published studies. Experiments that elicited an adaptive response to continuously altered sensory feedback more frequently reported activation in the cerebellum than those experiments that did not induce adaptation. These findings may explain the surprisingly low rate of significant cerebellar activation across brain imaging studies investigating unexpected sensory feedback. Furthermore, limitations of functional magnetic resonance imaging to probe the cerebellum could play a role as climbing fiber activity associated with feedback error processing may not be captured by it. We provide methodological recommendations that may guide future studies.

AB - It is widely accepted that unexpected sensory consequences of self-action engage the cerebellum. However, we currently lack consensus on where in the cerebellum, we find fine-grained differentiation to unexpected sensory feedback. This may result from methodological diversity in task-based human neuroimaging studies that experimentally alter the quality of self-generated sensory feedback. We gathered existing studies that manipulated sensory feedback using a variety of methodological approaches and performed activation likelihood estimation (ALE) meta-analyses. Only half of these studies reported cerebellar activation with considerable variation in spatial location. Consequently, ALE analyses did not reveal significantly increased likelihood of activation in the cerebellum despite the broad scientific consensus of the cerebellum's involvement. In light of the high degree of methodological variability in published studies, we tested for statistical dependence between methodological factors that varied across the published studies. Experiments that elicited an adaptive response to continuously altered sensory feedback more frequently reported activation in the cerebellum than those experiments that did not induce adaptation. These findings may explain the surprisingly low rate of significant cerebellar activation across brain imaging studies investigating unexpected sensory feedback. Furthermore, limitations of functional magnetic resonance imaging to probe the cerebellum could play a role as climbing fiber activity associated with feedback error processing may not be captured by it. We provide methodological recommendations that may guide future studies.

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KW - PREFRONTAL CORTEX

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KW - SPEECH PRODUCTION

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KW - VISUO-MOTOR

KW - cerebellum

KW - fMRI

KW - forward model

KW - meta-analysis

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