Action and semantic tool knowledge – Effective connectivity in the underlying neural networks

Abstract

Evidence from neuropsychological and imaging studies indicate that action and semantic knowledge about tools draw upon distinct neural substrates, but little is known about the underlying interregional effective connectivity. With fMRI and dynamic causal modeling (DCM) we investigated effective connectivity in the left-hemisphere (LH) while subjects performed (i) a function knowledge and (ii) a value knowledge task, both addressing semantic tool knowledge, and (iii) a manipulation (action) knowledge task. Overall, the results indicate crosstalk between action nodes and semantic nodes. Interestingly, effective connectivity was weakened between semantic nodes and action nodes during the manipulation task. Furthermore, pronounced modulations of effective connectivity within the fronto-parietal action system of the LH (comprising lateral occipito-temporal cortex, intraparietal sulcus, supramarginal gyrus, inferior frontal gyrus) were observed in a bidirectional manner during the processing of action knowledge. In contrast, the function and value knowledge tasks resulted in a significant strengthening of the effective connectivity between visual cortex and fusiform gyrus. Importantly, this modulation was present in both semantic tasks, indicating that processing different aspects of semantic knowledge about tools evokes similar effective connectivity patterns. Data revealed that interregional effective connectivity during the processing of tool knowledge occurred in a bidirectional manner with a weakening of connectivity between areas engaged in action and semantic knowledge about tools during the processing of action knowledge. Moreover, different semantic tool knowledge tasks elicited similar effective connectivity patterns.

Gesturing tool use and tool transport actions modulates inferior parietal functional connectivity with the dorsal and ventral object processing pathways

“…For example, although the peak of our BOLD contrast‐defined left SMG was in good agreement with the Gallivan et al () peak (4.9 mm in Euclidean distance), our left middle temporal gyrus was 20.4 mm in Euclidean distance from the Gallivan et al () left posterior middle temporal gyrus peak. Nevertheless, there was strong functional connectivity for tool use epochs between our BOLD contrast‐defined left SMG and left middle temporal gyrus, replicating prior work demonstrating these regions exhibit resting state connectivity (Simmons & Martin, ) and task‐based functional connectivity driven by tool use (Garcea et al, ; Hutchison & Gallivan, ; Kleineberg et al, ). Future studies using participant‐specific ROIs derived from independent localizer tasks will be able to resolve subtle differences in peak voxels used in functional connectivity analyses.…”

“…Moreover, we extend their findings by controlling for tool viewing; this is an important control, as prior research indicates that the left SMG, middle temporal gyrus, and ventral premotor cortex exhibit increased BOLD contrast for tool stimuli in passive viewing paradigms (Chao & Martin, 2000;Garcea et al, 2016;Garcea & Mahon, 2014;Grafton et al, 1997;Mahon et al, 2007;Noppeney et al, 2006). (Simmons & Martin, 2012) and task-based functional connectivity driven by tool use Hutchison & Gallivan, 2018;Kleineberg et al, 2018). Future studies using participant-specific ROIs derived from independent localizer tasks will be able to resolve subtle differences in peak voxels used in functional connectivity analyses.…”

“…A number of fMRI studies have demonstrated there is a high degree of cross-talk between the dorsal and ventral visual pathways as a function of grasping or generating tool-directed gestures (e.g., see Budisavljevic, Dell'Acqua, & Castiello, 2018;Garcea et al, 2018;Hutchison & Gallivan, 2018) or when viewing objects or making judgments about object manipulation (e.g., Chen, Snow, Culham, & Goodale, 2018;Chen et al, 2017;Freud, Rosenthal, Ganel, & Avidan, 2015;Kleineberg et al, 2018;Sim, Helbig, Graf, & Kiefer, 2015; for discussion, see Orban & Caruana, 2014;van Polanen & Davare, 2015). Our results offer a novel interpretation of the role that the left SMG plays in tool-directed actions: Tool manipulation knowledge is not "represented" in the left SMG; rather the left SMG sits at the nexus of the dorso-dorsal and ventro-dorsal visual pathways, and serves as an intermediary or "hub" region aggregating (a) representations of object properties and conceptual knowledge in the ventral stream with (b) online sensory-motor information processed in the dorsal stream, (c) which is informed by top-down biasing signals from prefrontal cortex to resolve competition between candidate tool use actions.…”

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

“…Functional magnetic resonance imaging (fMRI) findings in neurotypical adults are consistent with the available neuropsychological data, as there is increased blood oxygen level-dependent (BOLD) contrast in the left posterior middle temporal gyrus when participants gesture tool use (Brandi et al, 2014;Johnson-Frey et al, 2005;Vry et al, 2015), view images of tools (Beauchamp et al, 2002;Chao et al, 1999;Garcea et al, 2016;Mahon et al, 2007; for review, see Lingnau & Downing, 2015;A. Martin, 2007), and make judgments about actions (Kable et al, 2005;Kable et al, 2002;Wurm & Caramazza, 2019), including tool use actions (Kleineberg et al, 2018;Valyear & Culham, 2010). Furthermore, an emerging literature demonstrates there is increased functional connectivity between the left inferior parietal lobule and left posterior middle temporal gyrus when neurotypical participants gesture the use of tools (Garcea et al, 2018;Hutchison & Gallivan, 2018;Vingerhoets & Clauwaert, 2015).…”

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

“…2016 ; for review, see Martin 2007 ; Lingnau and Downing 2015 ), and make judgments about actions ( Kable et al. 2002 , 2005 ; Wurm and Caramazza 2019 ), including tool use actions ( Valyear and Culham 2010 ; Kleineberg et al. 2018 ).…”