Neurocognitive mechanisms underlying action tool knowledge tasks: specificity of tool-tool compared to hand-tool compatibility tasks

Abstract

Action tool knowledge can be assessed mainly with two kinds of tasks: tool-tool and hand-tool compatibility tasks. While these tasks are used to assess action tool knowledge, recent data showed striking dissociations between these tasks in brain-damaged patients. In this study, we explored the neuropsychological dissociations (Experiment 1; 60 brain-damaged patients) and the potential cognitive mechanisms engaged during these two tasks (Experiment 2; 52 healthy participants). Finally, we also reanalyzed fMRI data to investigate the neural bases engaged in tool-tool and hand-tool compatibility tasks (Experiment 3; 34 healthy participants). The three experiments provide convergent arguments by showing that both tasks share common core computations supported by a left-lateralized brain network, but hand-tool compatibility task engages regions outside of this brain network and is explained by visual imagery while tool-tool task is rather explained by motor imagery. Our results shed a new light on action tool knowledge tasks.

Fig. 1. Example of items used in the action tool knowledge tasks in Experiment 1 and Experiment 2.

A Tool-tool compatibility task. B Hand-tool compatibility task. Explanations are given in the text.

Fig. 2. Correlation plots between chronological age and raw scores for controls and patients in tool-tool and hand-tool compatibility tasks.

Linear regression lines and confidence regions are presented for each plot.

Fig. 3. Effect of Task (tool-tool compatibility vs. hand-tool compatibility) and Group (LBD vs. RBD) on patients’ scores.

Barplots represent mean z-scores, and error bars represent the Standard Error from the Mean (SEM). Significance (***p < .001) denotes corrected statistics for the comparisons between each patient group and the control group based on raw scores. Colored points (green: LBD and orange: RBD) represent individual z-scores.

Fig. 4. Analysis of lesions associated with dissociations between hand-tool and tool-tool tasks.

The top left panel (A) shows the lesion overlap of all LBD and RBD patients. The bottom left panel (B) shows the lesion and disconnection patterns of LBD03 and RBD02 who showed lower scores in hand-tool task compared to tool-tool tasks. Nodes are sized and colored according to the total disconnection severity for each node. Edges are colored according to disconnection severity. Connectivity matrices were computed using the Schaefer et al. (2018) 100-region parcellation using the Lesion Quantification Toolkit (LQT; Griffis et al.). The right panel (C) shows the lesion overlap of LBD and RBD patients showing the opposite pattern of behavioral dissociations. Lesions, disconnection severity (edges and nodes) and lesion overlap are projected on an MNI152 template present in the SurfIce viewer.

Fig. 5. Multidimensional scaling of correlations between experimental tasks.

RTM: recognition of tool manipulation. Explanations are given in the text.

Fig. 6. Example of stimuli and sequence of events used in the tool-tool compatibility task (left) and in the hand-tool compatibility task (right) in the experiment 3.

Explanations are given in the text.

Fig. 7. Statistical maps for the contrasts.

A Hand-Tool > Control (threshold of spatial extent = 85), B Tool-Tool > Control (threshold of spatial extent = 185), (C) Hand-Tool > Tool-Tool (threshold of spatial extent = 70) and Tool-Tool > Hand-Tool (threshold of spatial extent = 76) are projected on an MNI template and are FWE-corrected (p < 0.05) for multiple comparisons across the whole-brain at the cluster level. IFG: inferior frontal gyrus; LOC: lateral occipitotemporal cortex; SFG: superior frontal gyrus; SPL: superior parietal lobe.