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. 2021 Aug 15:237:118220.
doi: 10.1016/j.neuroimage.2021.118220. Epub 2021 May 28.

The unique role of parietal cortex in action observation: Functional organization for communicative and manipulative actions

Burcu A Urgen  1 , Guy A Orban  2
Affiliations

The unique role of parietal cortex in action observation: Functional organization for communicative and manipulative actions

Burcu A Urgen et al. Neuroimage. .

Abstract

Action observation is supported by a network of regions in occipito-temporal, parietal, and premotor cortex in primates. Recent research suggests that the parietal node has regions dedicated to different action classes including manipulation, interpersonal interactions, skin displacement, locomotion, and climbing. The goals of the current study consist of: 1) extending this work with new classes of actions that are communicative and specific to humans, 2) investigating how parietal cortex differs from the occipito-temporal and premotor cortex in representing action classes. Human subjects underwent fMRI scanning while observing three action classes: indirect communication, direct communication, and manipulation, plus two types of control stimuli, static controls which were static frames from the video clips, and dynamic controls consisting of temporally-scrambled optic flow information. Using univariate analysis, MVPA, and representational similarity analysis, our study presents several novel findings. First, we provide further evidence for the anatomical segregation in parietal cortex of different action classes: We have found a new site that is specific for representing human-specific indirect communicative actions in cytoarchitectonic parietal area PFt. Second, we found that the discriminability between action classes was higher in parietal cortex than the other two levels suggesting the coding of action identity information at this level. Finally, our results advocate the use of the control stimuli not just for univariate analysis of complex action videos but also when using multivariate techniques.

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Figures

Fig. 1
Fig. 1
Static frames from the videos of the three action classes and their four exemplars in the experiment. (A) Indirect communication, (B) Direct communication, (C) Manipulation.
Fig. 2
Fig. 2
ROIs included in the three levels of the Action Observation Network (occipito-temporal, parietal, and premotor) displayed on surface maps (upper panel) and flat maps (lower panel) for the left (LH) and right hemispheres (RH). Anatomical landmarks are marked in black: CS - Central sulcus, PreCS – Precentral sulcus, PostCS – Postcentral sulcus, IPS – Intraparietal sulcus, POS – Parieto-occipital sulcus, STS – Superior temporal culcus, ITS – Inferior temporal sulcus, OTS – Occipito-temporal sulcus. ROI abbreviations are as follows: MTG - middle temporal gyrus, OTS - occipito-temporal sulcus, DIPSM - dorsal intraparietal sulcus medial, DIPSA - dorsal intraparietal sulcus anterior, phAIP - putative human AIP.
Fig. 3
Fig. 3
Activation maps for each action class. The white lines indicate the borders of the ROIs included in the study as shown in Fig. 2. The anatomical landmarks are marked as in Fig. 2. The activation map for each action class was defined by the contrast [Action – (0.5*DC + 0.5*SC)] and masked inclusively by [Action - Fixation] at p<0.01, where DC and SC in each contrast refer to the dynamic and static controls of the respective action. (A) Activation map for Indirect communication (p<0.05 FWE corrected at peak level). Local maxima were labeled with numbers whose coordinates were listed in Table 2. Color bar shows the t-values. (B) Activation map for Direct communication (p<0.05 FWE corrected at peak level). Local maxima were labeled with numbers whose coordinates were listed in Table 2. (C) Activation map for Manipulation (p<0.05 FWE corrected at peak level). Local maxima were labeled with numbers whose coordinates were listed in Table 2.
Fig. 4
Fig. 4
Specific map and Common activation map. (A) Specific map for Indirect communication (p<0.001). The specific map for Indirect Communication was defined by the conjunction of the two contrasts 1) [(Indirect Communication - (0.5*DC + 0.5*SC)) – (Direct Communication - (0.5*DC + 0.5*SC)], 2) [(Indirect Communication - (0.5*DC + 0.5*SC)) – (Manipulation - (0.5*DC + 0.5*SC)], masked inclusively by the activation map of the action class of interest (Indirect Communication) at p<0.01, and the contrast [Indirect Communication - Fixation] at p<0.01, and exclusively by the activation maps of the other two action classes also at p<0.01. (B) Common activation map of all three action classes, Indirect communication, Direct communication, and Manipulation (p<0.001). The common map was defined by the conjunction of three contrasts 1) [Indirect Communication - (0.5*DC + 0.5*SC)], 2) [(Direct Communication - (0.5*DC + 0.5*SC))], and 3) [Manipulation - (0.5*DC + 0.5*SC)] with a conjunction threshold of p<0.001 (uncorrected), where DC and SC in each contrast refer to the dynamic and static controls of the respective action. The blue and green dots represent the coordinates from previous studies: observed manipulation actions (Ferri et al., 2015) and observed vocal communication actions (Corbo and Orban 2017). Same ROI and anatomical landmark conventions as in Fig. 2 and Fig. 3.
Fig. 5
Fig. 5
Activity profiles of the three action classes and their static and dynamic controls in ROIs in the occipito-temporal and premotor cortex. Video refers to the action stimulus. SC – Static control, DC – Dynamic control, LH – Left hemisphere, RH – Right hemisphere. Error bars show the standard error. (A) Left OTS and right OTS. (B) Left MTG and right MTG. (C) Left premotor and right premotor. ROI abbreviations are as follows: MTG - middle temporal gyrus, OTS - occipito-temporal sulcus.
Fig. 6
Fig. 6
Activity profiles of the three action classes and their static and dynamic controls in ROIs in the parietal cortex. Video refers to the action stimulus. SC – Static control, DC – Dynamic control, LH – Left hemisphere, RH – Right hemisphere. Error bars show the standard error. (A) Left DIPSM and right DIPSM. (B) Left DIPSA and right DIPSA. (C) Left phAIP and right phAIP. (D) Left PFt and right PFt. (E) Left PFcm and right PFcm. ROI abbreviations are as follows: DIPSM - dorsal intraparietal sulcus medial, DIPSA - dorsal intraparietal sulcus anterior, phAIP - putative human AIP.
Fig. 7
Fig. 7
Activity profiles of the exemplars for all action classes in PFt. LH – Left hemisphere, RH – Right hemisphere. Error bars show the standard error.
Fig. 8
Fig. 8
The mean prediction accuracy of between-action class classifications (3-way MVPA between Indirect, Direct, and Manipulation) for video, static control (SC), and dynamic control (DC) conditions in all levels of the Action Observation Network across 27 subjects. The results of left hemisphere are presented in the left panel and those of the right hemisphere in the right panel. The error bars show the standard error. ROI abbreviations are as follows: MTG - middle temporal gyrus, OTS - occipito-temporal sulcus, DIPSM - dorsal intraparietal sulcus medial, DIPSA - dorsal intraparietal sulcus anterior, phAIP - putative human AIP.
Fig. 9
Fig. 9
Representational similarity of action classes at the three levels of the Action Observation Network: A-C similarity for video condition in sample ROIs from each level: Left MTG from occipito-temporal, left phAIP from parietal, and left premotor from premotor cortex; D: similarity for all ROI and all presentation modes. (A) Representational similarity matrices for action videos in MTG, phAIP, and premotor. Similarity metric was correlation. Color bar shows the correlation strength. (B) Dendrograms obtained by applying hierarchical clustering to the dissimilarity matrices (1-similarity matrix, from panel A) (Left panel MTG, middle panel phAIP, right panel premotor). Each action class was marked with a different color following the conventions in Fig. 5-6: Red shows the exemplars of Indirect Communication, green shows the exemplars of Direct Communication, and blue shows the exemplars of Manipulation. (C) Distance plots obtained by applying multidimensional scaling (MDS) to the dissimilarity matrices (Left panel MTG, middle panel phAIP, right panel premotor). (D) Sum of pair-wise distances between the three action classes for videos, static controls and dynamic controls on the MDS as in Panel (C) across all ROIs (LH: left hemisphere, RH: right hemisphere). ROI abbreviations are as follows: MTG - middle temporal gyrus, OTS - occipito-temporal sulcus, DIPSM - dorsal intraparietal sulcus medial, DIPSA - dorsal intraparietal sulcus anterior, phAIP - putative human AIP.
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