Manual praxis and language-production networks, and their links to handedness

Gregory Kroliczak,Mikolaj Buchwald,Pawel Kleka,Michal Klichowski,Weronika Potok,Agnieszka M Nowik,Jennifer Randerath,Brian J Piper

doi:10.1016/j.cortex.2021.03.022

Abstract

While Liepmann was one of the first researchers to consider a relationship between skilled manual actions (praxis) and language for tasks performed “freely from memory”, his primary focus was on the relations between the organization of praxis and left-hemisphere dominance. Subsequent attempts to apply his apraxia model to all cases he studied – including his first patient, a “non-pure right-hander” treated as an exception – left the praxis-handedness issue unresolved. Modern neuropsychological and recent neuroimaging evidence either showed closer associations of praxis and language, than between handedness and any of these two functions, or focused on their dissociations. Yet, present-day developments in neuroimaging and statistics allow us to overcome the limitations of the earlier work on praxis-language-handedness links, and to better quantify their interrelationships. Using functional magnetic resonance imaging (fMRI), we studied tool use pantomimes and subvocal word generation in 125 participants, including righthanders (NRH = 52), ambidextrous individuals (mixedhanders; NMH = 31), and lefthanders (NLH = 42). Laterality indices were calculated both in two critical cytoarchitectonic maps, and 180 multi-modal parcellations of the human cerebral cortex, using voxel count and signal intensity, and the most relevant regions of interest and their networks were further analyzed. We found that atypical organization of praxis was present in all handedness groups (RH = 25.0%, MH = 22.6%; LH = 45.2%), and was about two and a half times as common as atypical organization of language (RH = 3.8%; MH = 6.5%; LH = 26.2%), contingent on ROI selection/LI-calculation method. Despite strong associations of praxis and language, regardless of handedness and typicality, dissociations of atypically represented praxis from typical left-lateralized language were common (~20% of cases), whereas the inverse dissociations of atypically represented language from typical left-lateralized praxis were very rare (in ~2.5% of all cases). The consequences of the existence of such different phenotypes for theoretical accounts of manual praxis, and its links to language and handedness are modeled and discussed.

Highlights

Skillful use of hands for complex movements and handling of tools, as well as the ability to communicate using language are some of the most fundamental human traits
Liepmann was among the first researchers to consider links between praxis and language for tasks performed “freely from memory” (Liepmann, 1912), as the control of movements performed without objects could be similar to the control of spoken language, he eventually abandoned this notion
Not being impressed by the observations that both praxis and language typically depend on the left hemisphere resources (Liepmann, 1908), and being able to demonstrate that apraxia is not a result of lost comprehension, his primary focus diverted from any putative praxis-language links

Summary

Introduction

Skillful use of hands for complex movements and handling of tools, as well as the ability to communicate using language are some of the most fundamental human traits. Liepmann was among the first researchers to consider links between praxis and language for tasks performed “freely from memory” (Liepmann, 1912), as the control of movements performed without objects could be similar to the control of spoken language, he eventually abandoned this notion Instead, he postulated that apraxia is a result of disrupted connections between intact (tool/action) concepts and motor centers (i.e., the concepts could not be reliably retrieved or transmitted, especially from one hemisphere to the other). Not being impressed by the observations that both praxis and language typically depend on the left hemisphere resources (Liepmann, 1908), and being able to demonstrate that apraxia is not a result of lost comprehension, his primary focus diverted from any putative praxis-language links He focused on the more apparent and, potentially, more important relations between the general organization of manual praxis and hemisphere dominance. While developing his disparate apraxia concepts (e.g., Liepmann, 1908; 1920; 1925), he did not explore the issue of praxislanguage relationships any further

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