Structural Disconnection of the Tool Use Network after Left Hemisphere Stroke Predicts Limb Apraxia Severity

Abstract

Producing a tool use gesture is a complex process drawing upon the integration of stored knowledge of tools and their associated actions with sensory-motor mechanisms supporting the planning and control of hand and arm actions. Understanding how sensory-motor systems in parietal cortex interface with semantic representations of actions and objects in the temporal lobe remains a critical issue, and is hypothesized to be a key determinant of the severity of limb apraxia, a deficit in producing skilled action after left hemisphere stroke. We used voxel-based and connectome-based lesion symptom mapping with data from 57 left hemisphere stroke participants to assess the lesion sites and structural disconnection patterns associated with poor tool use gesturing. We found that structural disconnection among the left inferior parietal lobule, lateral and ventral temporal cortex, and middle and superior frontal gyri predicted the severity of tool use gesturing performance. Control analyses demonstrated that reductions in right-hand grip strength were associated with motor system disconnection, largely bypassing regions supporting tool use gesturing. Our findings provide causal evidence that limb apraxia may arise, in part, from a disconnection between conceptual representations in the temporal lobe and mechanisms enabling skilled action production in the inferior parietal lobule.

Atypical Organization of Praxis and Language: A Look Back

“…Yet, the argument presented above can be weakened by additional positive interpretations stemming from comparisons of group averages for atypically represented praxis. Figures 1C and 1E, as well as 2C and 2E show numerous common components of the core praxis network or praxis-related areas, regardless of whether they come from individuals with right-lateralized, bilateral or typical left-lateralized activity in the praxis hub-i.e., the supramarginal gyrus (Bohlhalter et al, 2009;Króliczak & Frey, 2009;Biduła & Króliczak, 2015;Chen et al, 2016;Buchwald et al, 2018;Potok et al, 2019;Garcea et al, 2020;Amaral et al, 2021;Króliczak et al, 2021a; see also Lesourd et al, 2021). By looking at all these results, one can argue that except for the supramarginal gyrus itself, and its immediate vicinity (i.e., areas PF and PFt, and PFcm or AIP), numerous areas of the praxis network contribute to the task in a bilateral or mixed manner, regardless of the lateralization of activity in its main hub (Binkofski & Buxbaum, 2013; see also Garcea & Buxbaum, 2019;Malfatti & Turella, 2021;Amaral et al, 2021;cf.…”

Single-Case Disconnectome Lesion-symptom Mapping: Identifying Two Subtypes of Limb Apraxia

“…For each participant we derived a whole-brain disconnectome, representing structural disconnection among cortical and Disconnectome Lesion-Symptom Mapping of Apraxia 15 subcortical nodes. Structural connectivity was inferred on the basis of stroke lesion location using a cohort of normal diffusion scans from The Human Connectome Project (HCP) database (for methodological detail, see Greene et al, 2019; for prior work in the investigation of apraxia severity, see Garcea et al, 2020). First, each LCVA participant's stroke lesion was drawn on their corresponding native T1-weighted structural MRI volume and then normalized to a custom T1weighted template constructed from 40 participants of the Human Connectome Project (HCP; Greene et al, 2018) using cost function masking in ANTS (Avants et al, 2008).…”

“…The copyright holder for this preprint this version posted February 25, 2022. ; https://doi.org/10.1101/2022.02.22.481524 doi: bioRxiv preprint Disconnectome Lesion-Symptom Mapping of Apraxia 26 gyrus and the left inferior parietal lobule (e.g., see Garcea et al, 2020;Watson et al, 2019). By hypothesis, the left posterior middle temporal gyrus is involved in the retrieval of the visual appearance of a tool use action, and the left inferior parietal lobule aggregates visual attributes of a tool and its associated action (e.g., that a hammer is swung along a particular trajectory to pound in a nail) with fronto-parietal visuomotor circuits that support the programming and implementation of tool use actions (for discussion, see Finkel et al, 2018;Frey, 2007;Kroliczak et al, 2016).…”

“…For example, Watson and colleagues (2019) found that in a group of LCVA participants, lower tool use pantomiming accuracy was associated with reduced resting state functional connectivity between the left inferior parietal lobule and left middle temporal gyrus (see also Garcea, Almeida, et al, 2019). Garcea and colleagues (2020) showed that after controlling for shared variance with MGI performance, reduced PTU performance was associated with the degree of white matter structural disconnection between the left inferior parietal lobule and left middle temporal gyrus, and between the left inferior parietal lobule and left middle frontal gyrus (see also Bi et al, 2015). These findings suggest that distinct aspects of praxis are supported by distinct cortical nodes and white matter pathways.…”

Brain intrinsic connection patterns underlying tool processing in human adults are present in neonates and not in macaques

“…These regions are preferentially activated when human adults view pictures of tools relative to other types of objects (e.g., faces, animals, and large, non-manipulable objects), listen to tool names, imagine tool use, or pantomime tool use (Chao and Martin, 2000;Chouinard and Goodale, 2012;Lewis, 2006;Peelen et al, 2013;Wang et al, 2018). Also, they have been observed to be both structurally and functionally connected (Bi et al, 2015;Konkle and Caramazza, 2017;Peelen et al, 2013) and lesions to these regions and/or to their underlying white matter connections can lead to deficits in tool understanding and use (Bi et al, 2015;Buxbaum et al, 2014;Garcea et al, 2020;Tarhan et al, 2015). It is assumed that each of these regions contributes distinct computations to tool processing, with the LOTC, as part of the ventral visual pathway, involved in visual shape analysis and, optimally connected to the parietal and frontal regions to support grasping and manipulating tools (Mahon, 2020).…”