Functional MRI of cerebellar activity during eyeblink classical conditioning in children and adults

Dominic T. Cheng*, Ernesta M. Meintjes, Mark E. Stanton, John E. Desmond, Mariska Pienaar, Neil C. Dodge, John M. Power, Christopher D. Molteno, John F Disterhoft, Joseph L. Jacobson, Sandra W. Jacobson

*Corresponding author for this work

Research output: Contribution to journalArticle

24 Citations (Scopus)

Abstract

This study characterized human cerebellar activity during eyeblink classical conditioning (EBC) in children and adults using functional magnetic resonance imaging (fMRI). During fMRI, participants were administered delay conditioning trials, in which the conditioned stimulus (a tone) precedes, overlaps, and coterminates with the unconditioned stimulus (a corneal airpuff). Behavioral eyeblink responses and brain activation were measured concurrently during two phases: pseudoconditioning, involving presentations of tone alone and airpuff alone, and conditioning, during which the tone and airpuff were paired. Although all participants demonstrated significant conditioning, the adults produced more conditioned responses (CRs) than the children. When brain activations during pseudoconditioning were subtracted from those elicited during conditioning, significant activity was distributed throughout the cerebellar cortex (Crus I-II, lateral lobules IV-IX, and vermis IV-VI) in all participants, suggesting multiple sites of associative learning-related plasticity. Despite their less optimal behavioral performance, the children showed greater responding in the pons, lateral lobules VIII, IX, and Crus I, and vermis VI, suggesting that they may require greater activation and/or the recruitment of supplementary structures to achieve successful conditioning. Correlation analyses relating brain activations to behavioral CRs showed a positive association of activity in cerebellar deep nuclei (including dentate, fastigial, and interposed nuclei) and vermis VI with CRs in the children. This is the first study to compare cerebellar cortical and deep nuclei activations in children versus adults during EBC.

Original languageEnglish (US)
Pages (from-to)1390-1403
Number of pages14
JournalHuman Brain Mapping
Volume35
Issue number4
DOIs
StatePublished - Jan 1 2014

Fingerprint

Classical Conditioning
Cerebellar Nuclei
Magnetic Resonance Imaging
Brain
Cerebellar Cortex
Pons
Human Activities
Conditioning (Psychology)
Learning

Keywords

  • Cerebellum
  • Development
  • Learning
  • Memory
  • Neuroimaging

ASJC Scopus subject areas

  • Clinical Neurology
  • Anatomy
  • Neurology
  • Radiology Nuclear Medicine and imaging
  • Radiological and Ultrasound Technology
  • Medicine(all)

Cite this

Cheng, D. T., Meintjes, E. M., Stanton, M. E., Desmond, J. E., Pienaar, M., Dodge, N. C., ... Jacobson, S. W. (2014). Functional MRI of cerebellar activity during eyeblink classical conditioning in children and adults. Human Brain Mapping, 35(4), 1390-1403. https://doi.org/10.1002/hbm.22261
Cheng, Dominic T. ; Meintjes, Ernesta M. ; Stanton, Mark E. ; Desmond, John E. ; Pienaar, Mariska ; Dodge, Neil C. ; Power, John M. ; Molteno, Christopher D. ; Disterhoft, John F ; Jacobson, Joseph L. ; Jacobson, Sandra W. / Functional MRI of cerebellar activity during eyeblink classical conditioning in children and adults. In: Human Brain Mapping. 2014 ; Vol. 35, No. 4. pp. 1390-1403.
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Cheng, DT, Meintjes, EM, Stanton, ME, Desmond, JE, Pienaar, M, Dodge, NC, Power, JM, Molteno, CD, Disterhoft, JF, Jacobson, JL & Jacobson, SW 2014, 'Functional MRI of cerebellar activity during eyeblink classical conditioning in children and adults', Human Brain Mapping, vol. 35, no. 4, pp. 1390-1403. https://doi.org/10.1002/hbm.22261

Functional MRI of cerebellar activity during eyeblink classical conditioning in children and adults. / Cheng, Dominic T.; Meintjes, Ernesta M.; Stanton, Mark E.; Desmond, John E.; Pienaar, Mariska; Dodge, Neil C.; Power, John M.; Molteno, Christopher D.; Disterhoft, John F; Jacobson, Joseph L.; Jacobson, Sandra W.

In: Human Brain Mapping, Vol. 35, No. 4, 01.01.2014, p. 1390-1403.

Research output: Contribution to journalArticle

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T1 - Functional MRI of cerebellar activity during eyeblink classical conditioning in children and adults

AU - Cheng, Dominic T.

AU - Meintjes, Ernesta M.

AU - Stanton, Mark E.

AU - Desmond, John E.

AU - Pienaar, Mariska

AU - Dodge, Neil C.

AU - Power, John M.

AU - Molteno, Christopher D.

AU - Disterhoft, John F

AU - Jacobson, Joseph L.

AU - Jacobson, Sandra W.

PY - 2014/1/1

Y1 - 2014/1/1

N2 - This study characterized human cerebellar activity during eyeblink classical conditioning (EBC) in children and adults using functional magnetic resonance imaging (fMRI). During fMRI, participants were administered delay conditioning trials, in which the conditioned stimulus (a tone) precedes, overlaps, and coterminates with the unconditioned stimulus (a corneal airpuff). Behavioral eyeblink responses and brain activation were measured concurrently during two phases: pseudoconditioning, involving presentations of tone alone and airpuff alone, and conditioning, during which the tone and airpuff were paired. Although all participants demonstrated significant conditioning, the adults produced more conditioned responses (CRs) than the children. When brain activations during pseudoconditioning were subtracted from those elicited during conditioning, significant activity was distributed throughout the cerebellar cortex (Crus I-II, lateral lobules IV-IX, and vermis IV-VI) in all participants, suggesting multiple sites of associative learning-related plasticity. Despite their less optimal behavioral performance, the children showed greater responding in the pons, lateral lobules VIII, IX, and Crus I, and vermis VI, suggesting that they may require greater activation and/or the recruitment of supplementary structures to achieve successful conditioning. Correlation analyses relating brain activations to behavioral CRs showed a positive association of activity in cerebellar deep nuclei (including dentate, fastigial, and interposed nuclei) and vermis VI with CRs in the children. This is the first study to compare cerebellar cortical and deep nuclei activations in children versus adults during EBC.

AB - This study characterized human cerebellar activity during eyeblink classical conditioning (EBC) in children and adults using functional magnetic resonance imaging (fMRI). During fMRI, participants were administered delay conditioning trials, in which the conditioned stimulus (a tone) precedes, overlaps, and coterminates with the unconditioned stimulus (a corneal airpuff). Behavioral eyeblink responses and brain activation were measured concurrently during two phases: pseudoconditioning, involving presentations of tone alone and airpuff alone, and conditioning, during which the tone and airpuff were paired. Although all participants demonstrated significant conditioning, the adults produced more conditioned responses (CRs) than the children. When brain activations during pseudoconditioning were subtracted from those elicited during conditioning, significant activity was distributed throughout the cerebellar cortex (Crus I-II, lateral lobules IV-IX, and vermis IV-VI) in all participants, suggesting multiple sites of associative learning-related plasticity. Despite their less optimal behavioral performance, the children showed greater responding in the pons, lateral lobules VIII, IX, and Crus I, and vermis VI, suggesting that they may require greater activation and/or the recruitment of supplementary structures to achieve successful conditioning. Correlation analyses relating brain activations to behavioral CRs showed a positive association of activity in cerebellar deep nuclei (including dentate, fastigial, and interposed nuclei) and vermis VI with CRs in the children. This is the first study to compare cerebellar cortical and deep nuclei activations in children versus adults during EBC.

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KW - Development

KW - Learning

KW - Memory

KW - Neuroimaging

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Cheng DT, Meintjes EM, Stanton ME, Desmond JE, Pienaar M, Dodge NC et al. Functional MRI of cerebellar activity during eyeblink classical conditioning in children and adults. Human Brain Mapping. 2014 Jan 1;35(4):1390-1403. https://doi.org/10.1002/hbm.22261