It takes two to pantomime: Communication meets motor cognition

For over a century, pantomime of tool use has been employed to diagnose limb apraxia, a disorder of motor cognition primarily induced by left brain damage. While research consistently implicates damage to a left fronto-temporo-parietal network in limb apraxia, findings are inconsistent regarding the...

Full description

Bibliographic Details
Main Authors: Lisa Finkel, Katharina Hogrefe, Scott H. Frey, Georg Goldenberg, Jennifer Randerath
Format: Article
Language:English
Published: Elsevier 2018-01-01
Series:NeuroImage: Clinical
Online Access:http://www.sciencedirect.com/science/article/pii/S221315821830202X
_version_ 1828394002196463616
author Lisa Finkel
Katharina Hogrefe
Scott H. Frey
Georg Goldenberg
Jennifer Randerath
author_facet Lisa Finkel
Katharina Hogrefe
Scott H. Frey
Georg Goldenberg
Jennifer Randerath
author_sort Lisa Finkel
collection DOAJ
description For over a century, pantomime of tool use has been employed to diagnose limb apraxia, a disorder of motor cognition primarily induced by left brain damage. While research consistently implicates damage to a left fronto-temporo-parietal network in limb apraxia, findings are inconsistent regarding the impact of damage to anterior versus posterior nodes within this network on pantomime. Complicating matters is the fact that tool use pantomime can be affected and evaluated at multiple levels. For instance, the production of tool use gestures requires the consideration of semantic characteristics (e.g. how to communicate the action intention) as well as motor features (e.g. forming grip and movement). Together, these factors may contribute substantially to apparent discrepancies in previously reported findings regarding neural correlates of tool use pantomime.In the current study, 67 stroke patients with unilateral left-brain damage performed a classic pantomime task. In order to analyze different error characteristics, we evaluated the proper use of grip and movement for each pantomime. For certain objects, healthy subjects may use body parts as representative for the object, e.g. use of the fingers to indicate scissors blades. To specify the pathological use of body parts as the object (BPO) we only assessed pantomime items that were not prone to this response in healthy participants. We performed modern voxel-based lesion analyses on MRI or CT data to determine associations between brain injury and the frequency of the specific types of pantomime errors.Our results support a model in which anterior and posterior nodes of the left fronto-temporo-parietal network contribute differentially to pantomime of tool use. More precisely, damage in the inferior frontal cortex reaching to the temporal pole is associated with an increased frequency of BPO errors, whereas damage to the inferior parietal lobe is predominantly linked to an increased frequency of movement and/or grip errors. Our work suggests that the validity of attempts to specify the neural correlates of limb apraxia based on tool use pantomime depends on differentiating the specific types of errors committed. We conclude that successful tool use pantomime involves dissociable functions with communicative aspects represented in more anterior (rather ventral) regions and motor-cognitive aspects in more posterior (rather dorsal) nodes of a left fronto-temporo-parietal network. Keywords: Pantomime, BPO, Motor cognition, Communication, Dual routes, Neural correlates
first_indexed 2024-12-10T07:48:52Z
format Article
id doaj.art-e1c7220a743f4d079f4b0b01ec15937c
institution Directory Open Access Journal
issn 2213-1582
language English
last_indexed 2024-12-10T07:48:52Z
publishDate 2018-01-01
publisher Elsevier
record_format Article
series NeuroImage: Clinical
spelling doaj.art-e1c7220a743f4d079f4b0b01ec15937c2022-12-22T01:57:07ZengElsevierNeuroImage: Clinical2213-15822018-01-011910081017It takes two to pantomime: Communication meets motor cognitionLisa Finkel0Katharina Hogrefe1Scott H. Frey2Georg Goldenberg3Jennifer Randerath4Department of Psychology, University of Konstanz, Germany; Lurija Institute for Rehabilitation Science and Health Research, Kliniken Schmieder, Allensbach, GermanyLudwig-Maximilians-Universität München, GermanyDepartment of Psychological Sciences, University of Missouri, USATechnical University Munich, Germany; Medical Practice for Cognitive Neurology, Vienna, AustriaDepartment of Psychology, University of Konstanz, Germany; Lurija Institute for Rehabilitation Science and Health Research, Kliniken Schmieder, Allensbach, Germany; Corresponding author at: Department of Psychology, University of Konstanz, Germany.For over a century, pantomime of tool use has been employed to diagnose limb apraxia, a disorder of motor cognition primarily induced by left brain damage. While research consistently implicates damage to a left fronto-temporo-parietal network in limb apraxia, findings are inconsistent regarding the impact of damage to anterior versus posterior nodes within this network on pantomime. Complicating matters is the fact that tool use pantomime can be affected and evaluated at multiple levels. For instance, the production of tool use gestures requires the consideration of semantic characteristics (e.g. how to communicate the action intention) as well as motor features (e.g. forming grip and movement). Together, these factors may contribute substantially to apparent discrepancies in previously reported findings regarding neural correlates of tool use pantomime.In the current study, 67 stroke patients with unilateral left-brain damage performed a classic pantomime task. In order to analyze different error characteristics, we evaluated the proper use of grip and movement for each pantomime. For certain objects, healthy subjects may use body parts as representative for the object, e.g. use of the fingers to indicate scissors blades. To specify the pathological use of body parts as the object (BPO) we only assessed pantomime items that were not prone to this response in healthy participants. We performed modern voxel-based lesion analyses on MRI or CT data to determine associations between brain injury and the frequency of the specific types of pantomime errors.Our results support a model in which anterior and posterior nodes of the left fronto-temporo-parietal network contribute differentially to pantomime of tool use. More precisely, damage in the inferior frontal cortex reaching to the temporal pole is associated with an increased frequency of BPO errors, whereas damage to the inferior parietal lobe is predominantly linked to an increased frequency of movement and/or grip errors. Our work suggests that the validity of attempts to specify the neural correlates of limb apraxia based on tool use pantomime depends on differentiating the specific types of errors committed. We conclude that successful tool use pantomime involves dissociable functions with communicative aspects represented in more anterior (rather ventral) regions and motor-cognitive aspects in more posterior (rather dorsal) nodes of a left fronto-temporo-parietal network. Keywords: Pantomime, BPO, Motor cognition, Communication, Dual routes, Neural correlateshttp://www.sciencedirect.com/science/article/pii/S221315821830202X
spellingShingle Lisa Finkel
Katharina Hogrefe
Scott H. Frey
Georg Goldenberg
Jennifer Randerath
It takes two to pantomime: Communication meets motor cognition
NeuroImage: Clinical
title It takes two to pantomime: Communication meets motor cognition
title_full It takes two to pantomime: Communication meets motor cognition
title_fullStr It takes two to pantomime: Communication meets motor cognition
title_full_unstemmed It takes two to pantomime: Communication meets motor cognition
title_short It takes two to pantomime: Communication meets motor cognition
title_sort it takes two to pantomime communication meets motor cognition
url http://www.sciencedirect.com/science/article/pii/S221315821830202X
work_keys_str_mv AT lisafinkel ittakestwotopantomimecommunicationmeetsmotorcognition
AT katharinahogrefe ittakestwotopantomimecommunicationmeetsmotorcognition
AT scotthfrey ittakestwotopantomimecommunicationmeetsmotorcognition
AT georggoldenberg ittakestwotopantomimecommunicationmeetsmotorcognition
AT jenniferranderath ittakestwotopantomimecommunicationmeetsmotorcognition