Does fMRI repetition suppression reveal mirror neuron activity in the human brain? Insights from univariate and multivariate analysis

Journal article


Fuelscher, Ian, Caeyenberghs, Karen, Enticott, Peter Gregory, Kirkovski, Melissa, Farquharson, Shawna, Lum, Jarrad and Hyde, Christian. (2019) Does fMRI repetition suppression reveal mirror neuron activity in the human brain? Insights from univariate and multivariate analysis. European Journal of Neuroscience. 50(5), pp. 2877 - 2892. https://doi.org/10.1111/ejn.14370
AuthorsFuelscher, Ian, Caeyenberghs, Karen, Enticott, Peter Gregory, Kirkovski, Melissa, Farquharson, Shawna, Lum, Jarrad and Hyde, Christian
Abstract

Mirror neurons (MN) have been proposed as the neural substrate for a wide range of clinical, social and cognitive phenomena. Over the last decade, a commonly used tool for investigating MN activity in the human brain has been functional magnetic resonance (f MRI ) repetition suppression (RS ) paradigms. However, the available evidence is mixed, largely owing to inconsistent application of the methodological criteria necessary to infer MN properties. This raises concerns about the degree to which one can infer the presence (or absence) of MN activity from earlier accounts that adopted RS paradigms. We aimed to clarify this issue using a well‐validated f MRI RS paradigm and tested for mirror properties by rigorously applying the widely accepted criteria necessary to demonstrate MN activity using traditional univariate techniques and Multivariate Pattern Analysis (MVPA ). While univariate whole brain analysis in healthy adults showed uni‐modal RS effects within the supplementary motor area, no evidence for cross‐modal RS effects consistent with mirror neuron activity was found. MVPA on the other hand revealed a region along the anterior intraparietal sulcus that met the criteria for MN activity. Taken together, these results clarify disparate evidence from earlier RS studies, highlighting that traditional univariate analysis of RS data may not be sensitive for detecting MN activity when rigorously applying the requisite criteria. In light of these findings, we recommend that short of increasing sample sizes substantially, future studies using RS paradigms to investigate MN s across the human brain consider the use of MVPA.

Keywordsaction execution; action observation; mirror neurons; multivariate pattern analysis
Year2019
JournalEuropean Journal of Neuroscience
Journal citation50 (5), pp. 2877 - 2892
PublisherWiley-Blackwell Publishing Ltd.
ISSN0953-816X
Digital Object Identifier (DOI)https://doi.org/10.1111/ejn.14370
Scopus EID2-s2.0-85063400580
Open accessOpen access
Page range2877 - 2892
Research GroupMary MacKillop Institute for Health Research
Author's accepted manuscript
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This is the peer reviewed version of the following article: Fuelscher, I, Caeyenberghs, K, Enticott, PG, et al. Does f MRI repetition suppression reveal mirror neuron activity in the human brain? Insights from univariate and multivariate analysis. European Journal of Neuroscience. 2019; 50: 2877– 2892, which has been published in final form at https://doi.org/10.1111/ejn.14370. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Use of Self-Archived Versions.

Place of publicationUnited Kingdom
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Drijkoningen, David, Caeyenberghs, Karen, Leunissen, Inge, Vander Linden, Catharine, Leemans, Alexander, Sunaert, Stefan, Duysens, Jacques and Swinnen, Stephen. (2015) Training-induced improvements in postural control are accompanied by alterations in cerebellar white matter in brain injured patients. NeuroImage: Clinical. 7, pp. 240 - 251. https://doi.org/10.1016/j.nicl.2014.12.006
Resonance: An interactive tabletop artwork for co-located group rehabilitation and play
Duckworth, Jonathan, Mumford, Nick, Caeyenberghs, Karen, Eldridge, Ross Michael, Mayson, Scott, Thomas, Patrick R., Shum, David, Williams, Gavin and Wilson, Peter Henry. (2015) Resonance: An interactive tabletop artwork for co-located group rehabilitation and play. Universal Access in Human-Computer Interaction. Germany: Springer Verlag. pp. 420 - 431 https://doi.org/10.1007/978-3-319-20684-4_41
Neural correlates of motor deficits in young patients with traumatic brain injury
Caeyenberghs, Karen and Swinnen, Stephen. (2015) Neural correlates of motor deficits in young patients with traumatic brain injury. In In A. W. Toga (Ed.). Brain mapping: An encyclopedic reference Volume 2 pp. 461 - 468 Academic Press. https://doi.org/10.1016/B978-0-12-397025-1.00025-7
Neural correlates of motor deficits in young patients with traumatic brain injury
Caeyenberghs, Karen and Swinnen, Stephen. (2015) Neural correlates of motor deficits in young patients with traumatic brain injury. In In A. W. Toga (Ed.). Brain mapping: An encyclopedic reference Volume 2 pp. 461 - 468 Academic Press. https://doi.org/10.1016/B978-0-12-397025-1.00025-7
Coupling online control and inhibitory systems in children with Developmental Coordination Disorder : Goal-directed reaching
Ruddock, Scott, Piek, Jan, Sugden, David, Morris, Sue, Hyde, Christian, Caeyenberghs, Karen and Wilson, Peter. (2015) Coupling online control and inhibitory systems in children with Developmental Coordination Disorder : Goal-directed reaching. Research in Developmental Disabilities. 36, pp. 244 - 255. https://doi.org/10.1016/j.ridd.2014.10.013
Schizophrenia-like topological changes in the structural connectome of individuals with subclinical psychotic experiences
Drakesmith, Mark, Caeyenberghs, Karen, Dutt, Anirban, Zammit, Stanley, Evans, C John, Reichenberg, Abraham, Lewis, Glyn, David, Anthony and Jones, Derek. (2015) Schizophrenia-like topological changes in the structural connectome of individuals with subclinical psychotic experiences. Human Brain Mapping. 36(7), pp. 2629 - 2643. https://doi.org/10.1002/hbm.22796
Associations between muscle strength asymmetry and impairments in gait and posture in young brain-injured patients
Drijkoningen, David, Caeyenberghs, Karen, Vander Linden, Catharine, Van Herpe, Katrin, Duysens, Jacques and Swinnen, Stephan P.. (2015) Associations between muscle strength asymmetry and impairments in gait and posture in young brain-injured patients. Journal of Neurotrauma. 32(17), pp. 1324 - 1332. https://doi.org/10.1089/neu.2014.3787
Dynamics of the connectome in Huntington's disease: A longitudinal diffusion MRI study
Odish, Omar F. F., Caeyenberghs, Karen, Hosseini, Hadi, van den Bogaard, Simon J.A., Roos, Raymund A.C. and Leemans, Alexander. (2015) Dynamics of the connectome in Huntington's disease: A longitudinal diffusion MRI study. NeuroImage: Clinical. 9, pp. 32 - 43. https://doi.org/10.1016/j.nicl.2015.07.003
Second generation system development and multi-centre studies of the Elements VR-rehab system
Mumford, Nick, Shum, David, Thomas, Patrick, Steenbergen, Bert, Duckworth, Jonathan, Eldridge, Ross, Williams, Gavin, Green, Dido, Rogers, Jeff, Caeyenberghs, Karen and Wilson, Peter H.. (2015) Second generation system development and multi-centre studies of the Elements VR-rehab system. 2015 International Conference on Virtual Rehabilitation. Spain: IEEE Computer Society. pp. 164 - 165 https://doi.org/10.1109/ICVR.2015.7358601
Resting-state functional connectivity of the sensorimotor network in individuals with nonspecific low back pain and the association with the sit-to-stand-to-sit task
Pijnenburg, Madelon, Brumagne, Simon, Caeyenberghs, Karen, Janssens, Lotte, Goossens, Nina, Marinazzo, Daniele, Swinnen, Stephen P., Claeys, Kurt and Siugzdaite, Roma. (2015) Resting-state functional connectivity of the sensorimotor network in individuals with nonspecific low back pain and the association with the sit-to-stand-to-sit task. Brain Connectivity. 5(5), pp. 303 - 311. https://doi.org/10.1089/brain.2014.0309
Abnormal wiring of the connectome in adults with high-functioning autism spectrum disorder
Roine, Ulrika, Roine, Timo, Salmi, Juha, Nieminen-von Wendt, Taina, Tani, Pekka, Leppämäki, Sami, Rintahaka, Pertti, Caeyenberghs, Karen, Leemans, Alexander and Sams, Mikko. (2015) Abnormal wiring of the connectome in adults with high-functioning autism spectrum disorder. Molecular Autism. 6(1), pp. 1 - 11. https://doi.org/10.1186/s13229-015-0058-4
The vulnerability to suicidal behavior is associated with reduced connectivity strength
Bijttebier, Stijn, Caeyenberghs, Karen, van den Ameele, Hans, Achten, Eric, Rujescu, Dan, Titeca, Koen and van Heeringen, Kees. (2015) The vulnerability to suicidal behavior is associated with reduced connectivity strength. Frontiers in Human Neuroscience (online). 9, pp. 1 - 11. https://doi.org/10.3389/fnhum.2015.00632
Overcoming the effects of false positives and threshold bias in graph theoretical analyses of neuroimaging data
Drakesmith, M., Caeyenberghs, Karen, Dutt, A., Lewis, G., David, A. and Jones, D.. (2015) Overcoming the effects of false positives and threshold bias in graph theoretical analyses of neuroimaging data. NeuroImage. 118, pp. 313 - 333. https://doi.org/10.1016/j.neuroimage.2015.05.011
Functional connectivity density and balance in young patients with traumatic axonal injury
Caeyenberghs, Karen, Siugzdaite, Roma, Drijkoningen, David, Marinazzo, Daniele and Swinnen, Stephen P.. (2015) Functional connectivity density and balance in young patients with traumatic axonal injury. Brain Connectivity. 5(7), pp. 423 - 432. https://doi.org/10.1089/brain.2014.0293
Hyperconnectivity in juvenile myoclonic epilepsy: A network analysis
Caeyenberghs, Karen, Powell, H., Thomas, Rhys, Brindley, Lisa, Church, Carla, Evans, John, Muthukumaraswamy, Suresh, Jones, Derek and Hamandi, Khalid. (2015) Hyperconnectivity in juvenile myoclonic epilepsy: A network analysis. NeuroImage: Clinical. 7, pp. 98 - 104. https://doi.org/10.1016/j.nicl.2014.11.018
Assessing motor imagery using the hand rotation task: Does performance change across childhood?
Butson, Michael Lloyd, Hyde, Christian, Steenbergen, Bert and Williams, Jacqueline Louise. (2014) Assessing motor imagery using the hand rotation task: Does performance change across childhood? Human Movement Science. 35, pp. 50 - 65. https://doi.org/10.1016/j.humov.2014.03.013
Subcortical volume analysis in traumatic brain injury: The importance of the fronto-striato-thalamic circuit in task switching
Leunissen, Inge, Coxon, James P., Caeyenberghs, Karen, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephan P.. (2014) Subcortical volume analysis in traumatic brain injury: The importance of the fronto-striato-thalamic circuit in task switching. Cortex. 51(1), pp. 67 - 81. https://doi.org/10.1016/j.cortex.2013.10.009
Microstructural integrity of the superior cerebellar peduncle is associated with an impaired proprioceptive weighting capacity in individuals with non-specific low back pain
Pijnenburg, Madelon, Caeyenberghs, Karen, Janssens, Lotte, Goossens, Nina, Swinnen, Stephen P., Sunaert, Stefan and Brumagne, Simon. (2014) Microstructural integrity of the superior cerebellar peduncle is associated with an impaired proprioceptive weighting capacity in individuals with non-specific low back pain. PLoS ONE. 9(6), pp. 1 - 7. https://doi.org/10.1371/journal.pone.0100666
Hemispheric lateralization of topological organization in structural brain networks
Caeyenberghs, Karen and Leemans, Alexander. (2014) Hemispheric lateralization of topological organization in structural brain networks. Human Brain Mapping. 35(9), pp. 4944 - 4957. https://doi.org/10.1002/hbm.22524
Deficient motor timing in children with neurofibromatosis type 1
Debrabant, Julie, Plasschaert, Ellen, Caeyenberghs, Karen, Vingerhoets, Guy, Legius, Eric, Janssens, Sandra and Van Waelvelde, Hilde. (2014) Deficient motor timing in children with neurofibromatosis type 1. Research in Developmental Disabilities. 35(11), pp. 3131 - 3138. https://doi.org/10.1016/j.ridd.2014.07.059
White matter organization in relation to upper limb motor control in healthy subjects: exploring the added value of diffusion kurtosis imaging
Gooijers, J., Leemans, A., Van Cauter, S., Sunaert, S., Swinnen, S. P. and Caeyenberghs, K.. (2014) White matter organization in relation to upper limb motor control in healthy subjects: exploring the added value of diffusion kurtosis imaging. Brain Structure and Function. 219(5), pp. 1627 - 1638. https://doi.org/10.1007/s00429-013-0590-y
Altered structural networks and executive deficits in traumatic brain injury patients
Caeyenberghs, K., Leemans, A., Leunissen, I., Gooijers, J., Michiels, K., Sunaert, S. and Swinnen, S. P.. (2014) Altered structural networks and executive deficits in traumatic brain injury patients. Brain Structure and Function. 219(1), pp. 193 - 209. https://doi.org/10.1007/s00429-012-0494-2
Executive systems constrain the flexibility of online control in children during goal-directed reaching
Ruddock, Scott, Hyde, Christian, Piek, Jan, Sugden, David, Morris, Susan and Wilson, Peter. (2014) Executive systems constrain the flexibility of online control in children during goal-directed reaching. Developmental Neuropsychology. 39(1), pp. 51 - 68. https://doi.org/10.1080/87565641.2013.855215
Task switching in traumatic brain injury relates to cortico-subcortical integrity
Leunissen, Inge, Coxon, James P., Caeyenberghs, Karen, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephen P.. (2014) Task switching in traumatic brain injury relates to cortico-subcortical integrity. Human Brain Mapping. 35(5), pp. 2459 - 2469. https://doi.org/10.1002/hbm.22341
Neural underpinnings of impaired predictive motor timing in children with Developmental Coordination Disorder
Debrabant, Julie, Gheysen, Freja, Caeyenberghs, Karen, Waelvelde, Hilde Van and Vingerhoets, Guy. (2013) Neural underpinnings of impaired predictive motor timing in children with Developmental Coordination Disorder. Research in Developmental Disabilities. 34(5), pp. 1478 - 1487. https://doi.org/10.1016/j.ridd.2013.02.008
The development of rapid online control in children aged 6 - 12 years : Reaching performance
Wilson, Peter and Hyde, Christian. (2013) The development of rapid online control in children aged 6 - 12 years : Reaching performance. Human Movement Science. https://doi.org/10.1016/j.humov.2013.02.008
Bimanual motor coordination in older adults is associated with increased functional brain connectivity: A graphceoretical analysis
Heitger, Marcus H., Goble, Daniel J., Dhollander, Thijs, Dupont, Patrick, Caeyenberghs, Karen, Leemans, Alexander, Sunaert, Stefan and Swinnen, Stephen P.. (2013) Bimanual motor coordination in older adults is associated with increased functional brain connectivity: A graphceoretical analysis. PLoS ONE. 8(4), pp. 1 - 17. https://doi.org/10.1371/journal.pone.0062133
Impaired online control in children with developmental coordination disorder reflects developmental immaturity
Hyde, Christian and Wilson, Peter. (2013) Impaired online control in children with developmental coordination disorder reflects developmental immaturity. Developmental Neuropsychology. https://doi.org/10.1080/87565641.2012.718820
Diffusion tensor imaging metrics of the corpus callosum in relation to bimanual coordination: Effect of task complexity and sensory feedback
Gooijers, Jolien, Caeyenberghs, Karen, Sisti, Helene M., Geurts, Monique, Heitger, Marcus H., Leemans, Alexander and Swinnen, Stephen P.. (2013) Diffusion tensor imaging metrics of the corpus callosum in relation to bimanual coordination: Effect of task complexity and sensory feedback. Human Brain Mapping. 34(1), pp. 241 - 252. https://doi.org/10.1002/hbm.21429
Topological correlations of structural and functional networks in patients with traumatic brain injury
Caeyenberghs, Karen, Leemans, Alexander, Leunissen, Inge, Michiels, Karla and Swinnen, Stephen P.. (2013) Topological correlations of structural and functional networks in patients with traumatic brain injury. Frontiers in Human Neuroscience. 7, pp. 1 - 11. https://doi.org/10.3389/fnhum.2013.00726
Disruption of cerebral networks and cognitive impairment in Alzheimer disease
Reijmer, Yael D., Leemans, Alexander, Caeyenberghs, Karen, Heringa, Sophie M. and Biessels, Geert J.. (2013) Disruption of cerebral networks and cognitive impairment in Alzheimer disease. Neurology. 80(15), pp. 1370 - 1377. https://doi.org/10.1212/WNL.0b013e31828c2ee5
Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury
Leunissen, Inge, Coxon, James P., Geurts, Monique, Caeyenberghs, Karen, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephen P.. (2013) Disturbed cortico-subcortical interactions during motor task switching in traumatic brain injury. Human Brain Mapping. 34(6), pp. 1254 - 1271. https://doi.org/10.1002/hbm.21508
Graph analysis of functional brain networks for cognitive control of action in traumatic brain injury
Caeyenberghs, Karen, Leemans, Alexander, Heitger, Marcus H., Leunissen, Inge, Dhollander, Thijs, Sunaert, Stefan, Dupont, Patrick and Swinnen, Stephen P.. (2012) Graph analysis of functional brain networks for cognitive control of action in traumatic brain injury. Brain. 135(4), pp. 1293 - 1307. https://doi.org/10.1093/brain/aws048
Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning
Sisti, Helene M., Geurts, Monique, Gooijers, Jolien, Heitger, Marcus H., Caeyenberghs, Karen, Beets, Iseult A. M., Serbruyns, Leen, Leemans, Alexander and Swinnen, Stephen P.. (2012) Microstructural organization of corpus callosum projections to prefrontal cortex predicts bimanual motor learning. Learning and Memory. 19(8), pp. 351 - 357. https://doi.org/10.1101/lm.026534.112
Brain connectivity and postural control in young traumatic brain injury patients: A diffusion MRI based network analysis
Caeyenberghs, Karen, Leemans, A., De Decker, C., Heitger, Marcus H., Drijkoningen, David, Linden, C. Vander, Sunaert, S. and Swinnen, Stephen P.. (2012) Brain connectivity and postural control in young traumatic brain injury patients: A diffusion MRI based network analysis. NeuroImage. 1(1), pp. 106 - 115. https://doi.org/10.1016/j.nicl.2012.09.011
Motor learning-induced changes in functional brain connectivity as revealed by means of graphceoretical network analysis
Heitger, Marcus H., Ronsse, R., Dhollander, Thijs, Dupont, Patrick, Caeyenberghs, Karen and Swinnen, Stephen P.. (2012) Motor learning-induced changes in functional brain connectivity as revealed by means of graphceoretical network analysis. NeuroImage. 61(3), pp. 633 - 650. https://doi.org/10.1016/j.neuroimage.2012.03.067
Testing multiple coordination constraints with a novel bimanual visuomotor task
Sisti, Helene M., Geurts, Monique, Clerckx, Rene´, Gooijers, Jolien, Coxon, James P., Heitger, Marcus H., Caeyenberghs, Karen, Beets, Iseult A., Serbruyns, Leen and Swinnen, Stephen P.. (2011) Testing multiple coordination constraints with a novel bimanual visuomotor task. PLoS ONE. 6(8), pp. 1 - 11. https://doi.org/10.1371/journal.pone.0023619
Keeping an eye on imagery: The role of eye movements during motor imagery training
Heremans, E., Smits-Engelsman, Bouwien, Caeyenberghs, Karen, Vercruysse, S., Nieuwboer, A., Feys, P. and Helsen, W. F.. (2011) Keeping an eye on imagery: The role of eye movements during motor imagery training. Neuroscience. 195, pp. 37 - 44. https://doi.org/10.1016/j.neuroscience.2011.07.030
Correlations between white matter integrity and motor function in traumatic brain injury patients
Caeyenberghs, Karen, Leemans, Alexander, Geurts, Monique, Vander Linden, Catharine, Smits-Engelsman, Bouwien C. M., Sunaert, Stefan and Swinnen, Stephen P.. (2011) Correlations between white matter integrity and motor function in traumatic brain injury patients. Neurorehabilitation and Neural Repair. 25(6), pp. 492 - 502. https://doi.org/10.1177/1545968310394870
Dissecting online control in Developmental Coordination Disorder :A kinematic analysis of double-step reaching
Hyde, Christian and Wilson, Peter Henry. (2011) Dissecting online control in Developmental Coordination Disorder :A kinematic analysis of double-step reaching. Brain and Cognition. 75(3), pp. 232 - 241. https://doi.org/10.1016/j.bandc.2010.12.004
Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: A diffusion tensor imaging study
Caeyenberghs, Karen, Leemans, Alexander, Coxon, James P., Leunissen, Inge, Drijkoningen, David, Geurts, Monique, Gooijers, Jolien, Michiels, Karla, Sunaert, Stefan and Swinnen, Stephen P.. (2011) Bimanual coordination and corpus callosum microstructure in young adults with traumatic brain injury: A diffusion tensor imaging study. Journal of Neurotrauma. 28(6), pp. 897 - 913. https://doi.org/10.1089/neu.2010.1721
Online motor control in children with developmental coordination disorder :chronometric analysis of double-step reaching performance
Hyde, Christian and Wilson, Peter Henry. (2011) Online motor control in children with developmental coordination disorder :chronometric analysis of double-step reaching performance. Child: Care, Health and Development. 37(1), pp. 111 - 122. https://doi.org/10.1111/j.1365-2214.2010.01131.x
Motor imagery development in primary school children
Caeyenberghs, Karen, Tsoupas, Jenny, Wilson, Peter and Smits-Engelsman, Bouwein C. M.. (2009) Motor imagery development in primary school children. Developmental Neuropsychology. 34(1), pp. 103 - 121. https://doi.org/10.1080/87565640802499183
Increasing convergence between imagined and executed movement across development: Evidence for the emergence of movement representations
Caeyenberghs, Karen, Wilson, Peter, Van Roon, Dominique, Swinnen, Stephen and Smits-Engelsman, Bouwein C. M.. (2009) Increasing convergence between imagined and executed movement across development: Evidence for the emergence of movement representations. Developmental Science. 12(3), pp. 474 - 483. https://doi.org/10.1111/j.1467-7687.2008.00803.x