Using multi-level Bayesian lesion-symptom mapping to probe the body-part-specificity of gesture imitation skills

Abstract Past attempts to identify the neural substrates of hand and finger imitation skills in the left hemisphere of the brain have yielded inconsistent results. Here, we analyse those associations in a large sample of 257 left hemisphere stroke patients. By introducing novel Bayesian methods, we characterise lesion symptom associations at three levels: the voxel‐level, the single‐region level (using anatomically defined regions), and the region‐pair level. The results are inconsistent across those three levels and we argue that each level of analysis makes assumptions which constrain the results it can produce. Regardless of the inconsistencies across levels, and contrary to past studies which implicated differential neural substrates for hand and finger imitation, we find no consistent voxels or regions, where damage affects one imitation skill and not the other, at any of the three analysis levels. Our novel Bayesian approach indicates that any apparent differences appear to be driven by an increased sensitivity of hand imitation skills to lesions that also impair finger imitation. In our analyses, the results of the highest level of analysis (region‐pairs) emphasise a role of the primary somatosensory and motor cortices, and the occipital lobe in imitation. We argue that this emphasis supports an account of both imitation tasks based on direct sensor‐motor connections, which throws doubt on past accounts which imply the need for an intermediate (e.g. body‐part‐coding) system of representation. HighlightsNovel Bayesian lesion‐symptom analyses are proposed.Different levels of analysis emphasise different lesion sites for gesture imitation deficits.All levels argue against the body‐part‐specificity of gesture imitation skills.A direct sensor‐to‐motor pathway model of gesture imitation is supported.

[1]  A. Meltzoff,et al.  Explaining Facial Imitation: A Theoretical Model. , 1997, Early development & parenting.

[2]  Gereon R Fink,et al.  The somatotopic organization of cytoarchitectonic areas on the human parietal operculum. , 2007, Cerebral cortex.

[3]  A. Dovern,et al.  Effect of meaning on apraxic finger imitation deficits , 2016, Neuropsychologia.

[4]  K. Heilman,et al.  A Cognitive Neuropsychological Model of Limb Praxis , 1991 .

[5]  Gottfried Schlaug,et al.  Impairment of Speech Production Predicted by Lesion Load of the Left Arcuate Fasciculus , 2011, Stroke.

[6]  P. Szeszko,et al.  MRI atlas of human white matter , 2006 .

[7]  Joana C Carmo,et al.  Neuropsychological perspectives on the mechanisms of imitation , 2009, Philosophical Transactions of the Royal Society B: Biological Sciences.

[8]  A. Dovern,et al.  Diagnosis and treatment of upper limb apraxia , 2012, Journal of Neurology.

[9]  K. Zilles,et al.  Human Somatosensory Area 2: Observer-Independent Cytoarchitectonic Mapping, Interindividual Variability, and Population Map , 2001, NeuroImage.

[10]  G. Goldenberg,et al.  Hemisphere asymmetries for imitation of novel gestures , 2002, Neurology.

[11]  Cathy J. Price,et al.  Comparing language outcomes in monolingual and bilingual stroke patients , 2015, Brain : a journal of neurology.

[12]  J. Dekker,et al.  Prevalence of apraxia among patients with a first left hemisphere stroke in rehabilitation centres and nursing homes , 2000, Clinical rehabilitation.

[13]  Cornelius Weiller,et al.  Neural bases of imitation and pantomime in acute stroke patients: distinct streams for praxis. , 2014, Brain : a journal of neurology.

[14]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[15]  Georg Goldenberg,et al.  The Neural Basis of Imitation is Body Part Specific , 2006, The Journal of Neuroscience.

[16]  Angela R. Laird,et al.  ALE meta-analysis of action observation and imitation in the human brain , 2010, NeuroImage.

[17]  James M Shine,et al.  The Next Step , 2016, The Neuroscientist : a review journal bringing neurobiology, neurology and psychiatry.

[18]  Gereon R Fink,et al.  Apraxia Impairs Intentional Retrieval of Incidentally Acquired Motor Knowledge , 2011, The Journal of Neuroscience.

[19]  L. Vriens,et al.  The Difference Between , 2018 .

[20]  S. Wakana,et al.  MRI Atlas of Human White Matter , 2005 .

[21]  M. Wyke,et al.  The effects of brain lesions on the performance of bilateral arm movements. , 1971, Neuropsychologia.

[22]  G. Goldenberg Defective imitation of gestures in patients with damage in the left or right hemispheres. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[23]  A. Meltzoff,et al.  Imitation of Facial and Manual Gestures by Human Neonates , 1977, Science.

[24]  Cathy J. Price,et al.  Distinguishing the effect of lesion load from tract disconnection in the arcuate and uncinate fasciculi , 2016, NeuroImage.

[25]  A. Gelman,et al.  The Difference Between “Significant” and “Not Significant” is not Itself Statistically Significant , 2006 .

[26]  G. Rees,et al.  Human brain lesion-deficit inference remapped , 2014, Brain : a journal of neurology.

[27]  Paul Cisek,et al.  Neural activity in primary motor and dorsal premotor cortex in reaching tasks with the contralateral versus ipsilateral arm. , 2003, Journal of neurophysiology.

[28]  H Spinnler,et al.  Upper and lower face apraxia: role of the right hemisphere. , 2000, Brain : a journal of neurology.

[29]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[30]  Gereon R. Fink,et al.  Transcranial Direct Current Stimulation (tDCS) of Left Parietal Cortex Facilitates Gesture Processing in Healthy Subjects , 2013, The Journal of Neuroscience.

[31]  Peter A. Calabresi,et al.  Tract probability maps in stereotaxic spaces: Analyses of white matter anatomy and tract-specific quantification , 2008, NeuroImage.

[32]  Chris Rorden,et al.  Multivariate Connectome-Based Symptom Mapping in Post-Stroke Patients: Networks Supporting Language and Speech , 2016, The Journal of Neuroscience.

[33]  M. Brass,et al.  Imitation: is cognitive neuroscience solving the correspondence problem? , 2005, Trends in Cognitive Sciences.

[34]  E Capitani,et al.  Recovery from ideomotor apraxia. A study on acute stroke patients. , 1987, Brain : a journal of neurology.

[35]  Maurizio Filippone,et al.  Decoding post-stroke motor function from structural brain imaging , 2016, NeuroImage: Clinical.

[36]  A. Schleicher,et al.  Areas 3a, 3b, and 1 of Human Primary Somatosensory Cortex 1. Microstructural Organization and Interindividual Variability , 1999, NeuroImage.

[37]  Karl J. Friston,et al.  Classical and Bayesian Inference in Neuroimaging: Applications , 2002, NeuroImage.

[38]  Sung Ho Jang,et al.  Relation between aphasia and arcuate fasciculus in chronic stroke patients , 2014, BMC Neurology.

[39]  Chris Rorden,et al.  Improving Lesion-Symptom Mapping , 2007, Journal of Cognitive Neuroscience.

[40]  K. Amunts,et al.  The human inferior parietal lobule in stereotaxic space , 2008, Brain Structure and Function.

[41]  E. Wagenmakers,et al.  A Default Bayesian Hypothesis Test for ANOVA Designs , 2012 .

[42]  H. Freund,et al.  Recognition and imitation of pantomimed motor acts after unilateral parietal and premotor lesions: a perspective on apraxia , 2001, Neuropsychologia.

[43]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[44]  David Rudrauf,et al.  What affects detectability of lesion–deficit relationships in lesion studies? , 2014, NeuroImage: Clinical.

[45]  E. Wagenmakers,et al.  A default Bayesian hypothesis test for correlations and partial correlations , 2012, Psychonomic bulletin & review.

[46]  Norman Relkin,et al.  Exploring the brain's structural connectome: A quantitative stroke lesion‐dysfunction mapping study , 2015, Human brain mapping.

[47]  F. Dick,et al.  Voxel-based lesion–symptom mapping , 2003, Nature Neuroscience.

[48]  L. M. M.-T. Theory of Probability , 1929, Nature.

[49]  J. Hermsdörfer,et al.  Cortical Correlates of Gesture Processing: Clues to the Cerebral Mechanisms Underlying Apraxia during the Imitation of Meaningless Gestures , 2001, NeuroImage.

[50]  R T Knight,et al.  Neural representations of skilled movement. , 2000, Brain : a journal of neurology.

[51]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[52]  J. Ferro,et al.  Lesion size and location in ideomotor apraxia. , 1984, Brain : a journal of neurology.

[53]  E. Kaplan,et al.  Neuropsychological and neuroanatomical dimensions of ideomotor apraxia. , 1992, Brain : a journal of neurology.

[54]  Cathy J. Price,et al.  Predicting outcome and recovery after stroke with lesions extracted from MRI images , 2013, NeuroImage: Clinical.

[55]  Hans-Otto Karnath,et al.  The next step in modern brain lesion analysis: multivariate pattern analysis. , 2014, Brain : a journal of neurology.