Competition between tool and hand motion impairs movement planning in limb apraxia.

Abstract

Tool use is a complex motor planning problem. Prior research suggests that planning to use tools involves resolving competition between different tool-related action representations. We therefore reasoned that competition may also be exacerbated with tools for which the motions of the tool and the hand are incongruent (e.g., pinching the fingers to open a clothespin). If this hypothesis is correct, we should observe marked deficits in planning the use of incongruent as compared to congruent tools in individuals with limb apraxia following left-hemisphere stroke (LCVA), a disorder associated with abnormal action competition. We asked 34 individuals with chronic LCVA (14 females) and 16 matched neurotypical controls (8 females) to use novel tools in which the correspondence between the motions of the hand and tool-tip were either congruent or incongruent. Individuals with LCVA also completed background assessments to quantify apraxia severity. We observed increased planning time for incongruent as compared to congruent tools as a function of apraxia severity. Further analysis revealed that this impairment predominantly occurred early in the task when the tools were first introduced. Lesion-symptom mapping analyses revealed that lesions to posterior temporal and inferior parietal areas were associated with impaired planning for incongruent tools. A second experiment on the same individuals with LCVA revealed that the ability to gesture the use of conventional tools was impaired for tools rated as more incongruent by a normative sample. These findings suggest that tool-hand incongruence evokes action competition and influences the tool-use difficulties experienced by people with apraxia.Significance Statement Prior research indicates that competition between different representations associated with moving or using tools must be resolved to enable tool use. We demonstrated that competition may be exacerbated when tool and hand motions are incongruent (e.g., pinching the hand opens a clothespin), resulting in tool-use impairments particularly for individuals with greater severity of limb apraxia, a disorder known to be associated with action competition abnormalities. Lesions in posterior portions of the brain's tool use network were associated with impairments in planning incongruent tool actions. This study thus demonstrates that tool-hand incongruence may invoke competition between motions of the hand and tool-tip, which individuals with limb apraxia have difficulty resolving to properly use tools.