scholarly journals Structural Disconnection of the Tool Use Network After Left Hemisphere Stroke Predicts Limb Apraxia Severity

2020 ◽  
Author(s):  
Frank E. Garcea ◽  
Clint Greene ◽  
Scott T. Grafton ◽  
Laurel J. Buxbaum

AbstractProducing 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 between the left inferior parietal lobule, lateral temporal lobe (left middle temporal gyrus) and ventral temporal cortex (left medial fusiform gyrus) predicted the severity of tool use gesturing performance. Control analyses demonstrated that reductions in right-hand grip strength were associated with motor system disconnection, bypassing regions supporting tool use gesturing. Our findings provide causal evidence that limb apraxia may arise, in part, from disconnection of conceptual representations in the temporal lobe from mechanisms enabling skilled action production in the inferior parietal lobule.

2020 ◽  
Vol 1 (1) ◽  
Author(s):  
Frank E Garcea ◽  
Clint Greene ◽  
Scott T Grafton ◽  
Laurel J Buxbaum

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 cortices, 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 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.


2019 ◽  
Author(s):  
Frank E. Garcea ◽  
Harrison Stoll ◽  
Laurel J. Buxbaum

AbstractWhen pantomiming the use of tools, patients with limb apraxia after left hemisphere stroke (LCVA) produce more spatiotemporal hand action errors with tools associated with conflicting actions for use versus grasp-to-pick-up (e.g., corkscrew) than tools having a single action for both use and grasp (e.g., hammer). There are two possible accounts for this pattern of results. Reduced performance with ‘conflict’ tools may simply reflect weakened automaticity of use action activation, which is evident only when the use and grasp actions are not redundant. Alternatively, poor use performance may reflect reduced ability of appropriate tool use actions to compete with task-inappropriate action representations. To address this issue, we developed a Stroop-like experiment in which 21 LCVA and 8 neurotypical participants performed pantomime actions in blocks containing two tools that were similar (“neighbors”) in terms of hand action or function, or unrelated on either dimension. In a congruent condition, they pantomimed the use action associated with the visually presented tool, whereas in an incongruent condition, they pantomimed the use action for the other tool in the block. Relative to controls and other task conditions, LCVA participants showed reductions in hand action errors in incongruent relative to congruent action trials; furthermore, the degree of reduction in this incongruence effect was related to the participants’ susceptibility to grasp-on-use conflict in a separate test of pantomime to the sight of tools. Support vector regression lesion-symptom mapping analyses identified the left inferior frontal gyrus, supramarginal gyrus, and superior longitudinal fasciculus as core neuroanatomical sites associated with abnormal performance on both tasks. Collectively, the results indicate that weakened activation of tool use actions in limb apraxia gives rise to reduced ability of these actions to compete for task-appropriate selection when competition arises within single tools (grasp-on-use conflict) as well as between two tools (reduced neighborhood effects).


2012 ◽  
Vol 35 (4) ◽  
pp. 234-234 ◽  
Author(s):  
Guy A. Orban ◽  
Giacomo Rizzolatti

AbstractA comparative fMRI study by Peeters et al. (2009) provided evidence that a specific sector of left inferior parietal lobule is devoted to tool use in humans, but not in monkeys. We propose that this area represents the neural substrate of the human capacity to understand tool use by using causal reasoning.


2011 ◽  
Vol 23 (9) ◽  
pp. 2376-2386 ◽  
Author(s):  
Rutvik H. Desai ◽  
Jeffrey R. Binder ◽  
Lisa L. Conant ◽  
Quintino R. Mano ◽  
Mark S. Seidenberg

The role of sensory-motor systems in conceptual understanding has been controversial. It has been proposed that many abstract concepts are understood metaphorically through concrete sensory-motor domains such as actions. Using fMRI, we compared neural responses with literal action (Lit; The daughter grasped the flowers), metaphoric action (Met; The public grasped the idea), and abstract (Abs; The public understood the idea) sentences of varying familiarity. Both Lit and Met sentences activated the left anterior inferior parietal lobule, an area involved in action planning, with Met sentences also activating a homologous area in the right hemisphere, relative to Abs sentences. Both Met and Abs sentences activated the left superior temporal regions associated with abstract language. Importantly, activation in primary motor and biological motion perception regions was inversely correlated with Lit and Met familiarity. These results support the view that the understanding of metaphoric action retains a link to sensory-motor systems involved in action performance. However, the involvement of sensory-motor systems in metaphor understanding changes through a gradual abstraction process whereby relatively detailed simulations are used for understanding unfamiliar metaphors, and these simulations become less detailed and involve only secondary motor regions as familiarity increases. Consistent with these data, we propose that anterior inferior parietal lobule serves as an interface between sensory-motor and conceptual systems and plays an important role in both domains. The similarity of abstract and metaphoric sentences in the activation of left superior temporal regions suggests that action metaphor understanding is not completely based on sensory-motor simulations but relies also on abstract lexical-semantic codes.


2018 ◽  
Vol 8 (12) ◽  
pp. 206 ◽  
Author(s):  
Brenda Hanna-Pladdy ◽  
Hyun Choi ◽  
Brian Herman ◽  
Spenser Haffey

Binding sensory features of multiple modalities of what we hear and see allows formation of a coherent percept to access semantics. Previous work on object naming has focused on visual confrontation naming with limited research in nonverbal auditory or multisensory processing. To investigate neural substrates and sensory effects of lexical retrieval, we evaluated healthy adults (n = 118) and left hemisphere stroke patients (LHD, n = 42) in naming manipulable objects across auditory (sound), visual (picture), and multisensory (audiovisual) conditions. LHD patients were divided into cortical, cortical–subcortical, or subcortical lesions (CO, CO–SC, SC), and specific lesion location investigated in a predictive model. Subjects produced lower accuracy in auditory naming relative to other conditions. Controls demonstrated greater naming accuracy and faster reaction times across all conditions compared to LHD patients. Naming across conditions was most severely impaired in CO patients. Both auditory and visual naming accuracy were impacted by temporal lobe involvement, although auditory naming was sensitive to lesions extending subcortically. Only controls demonstrated significant improvement over visual naming with the addition of auditory cues (i.e., multisensory condition). Results support overlapping neural networks for visual and auditory modalities related to semantic integration in lexical retrieval and temporal lobe involvement, while multisensory integration was impacted by both occipital and temporal lobe lesion involvement. The findings support modality specificity in naming and suggest that auditory naming is mediated by a distributed cortical–subcortical network overlapping with networks mediating spatiotemporal aspects of skilled movements producing sound.


2021 ◽  
Author(s):  
Nicholas E. Souter ◽  
Xiuyi Wang ◽  
Hannah Thompson ◽  
Katya Krieger-Redwood ◽  
Ajay D. Halai ◽  
...  

AbstractPatients with semantic aphasia have impaired control of semantic retrieval, often accompanied by executive dysfunction following left hemisphere stroke. Many but not all of these patients have damage to the left inferior frontal gyrus, important for semantic and cognitive control. Yet semantic and cognitive control networks are highly distributed, including posterior as well as anterior components. Accordingly, semantic aphasia might not only reflect local damage but also white matter structural and functional disconnection. Here we characterise the lesions and predicted patterns of structural and functional disconnection in individuals with semantic aphasia and relate these effects to semantic and executive impairment. Impaired semantic cognition was associated with infarction in distributed left- hemisphere regions, including in the left anterior inferior frontal and posterior temporal cortex. Lesions were associated with executive dysfunction within a set of adjacent but distinct left frontoparietal clusters. Performance on executive tasks was also associated with interhemispheric structural disconnection across the corpus callosum. Poor semantic cognition was associated with small left-lateralized structurally disconnected clusters, including in the left posterior temporal cortex. These results demonstrate that while left- lateralized semantic and executive control regions are often damaged together in stroke aphasia, these deficits are associated with distinct patterns of structural disconnection, consistent with the bilateral nature of executive control and the left-lateralized yet distributed semantic control network.


2020 ◽  
Author(s):  
Elisabeth Rounis ◽  
Ajay Halai ◽  
Gloria Pizzamiglio ◽  
Matthew A. Lambon Ralph

AbstractLimb apraxia, a disorder of skilled action not consequent on primary motor or sensory deficits, has traditionally been defined according to errors patients make on neuropsychological tasks. Previous models of the disorder have failed to provide a unified account of patients’ deficits, due to heterogeneity in the patients and tasks used. In this study we implemented principal component analysis (PCA) to elucidate core factors of the disorder in a cohort of 41 unselected left hemisphere chronic stroke patients who were tested on a comprehensive and validated apraxia screen. Three principal components were identified: posture selection, semantic control and multi-demand sequencing. These were submitted to a lesion symptom mapping (VBCM) analysis in a subset of 24 patients, controlled for lesion volume, age and time post-stroke. Although the first component revealed no significant structural correlates, the second and third components were related to regions in the ‘ventro-dorsal’ and ‘ventral’ and ‘dorsal’ pathways, respectively. These results challenge the previously reported distinction between ideomotor and ideational deficits and highlight a significant role of common cognitive functions in the disorder, which include action selection, semantic retrieval, sequencing and response inhibition. Further research using this technique would help elucidate the cognitive processes underlying limb apraxia and their relationship with other cognitive disorders.


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