Action Observation Network Activity Related to Object-Directed and Socially-Directed Actions in Adolescents

Abstract

The human action observation network (AON) encompasses brain areas consistently engaged when we observe other's actions. Although the core nodes of the AON are present from childhood, it is not known to what extent they are sensitive to different action features during development. Because social cognitive abilities continue to mature during adolescence, the AON response to socially-oriented actions, but not to object-related actions, may differ in adolescents and adults. To test this hypothesis, we scanned with functional magnetic resonance imaging (fMRI) male and female typically-developing teenagers (n = 28; 13 females) and adults (n = 25; 14 females) while they passively watched videos of manual actions varying along two dimensions: sociality (i.e., directed toward another person or not) and transitivity (i.e., involving an object or not). We found that action observation recruited the same fronto-parietal and occipito-temporal regions in adults and adolescents. The modulation of voxel-wise activity according to the social or transitive nature of the action was similar in both groups of participants. Multivariate pattern analysis, however, revealed that decoding accuracies in intraparietal sulcus (IPS)/superior parietal lobe (SPL) for both sociality and transitivity were lower for adolescents compared with adults. In addition, in the lateral occipital temporal cortex (LOTC), generalization of decoding across the orthogonal dimension was lower for sociality only in adolescents. These findings indicate that the representation of the content of others' actions, and in particular their social dimension, in the adolescent AON is still not as robust as in adults.SIGNIFICANCE STATEMENT The activity of the action observation network (AON) in the human brain is modulated according to the purpose of the observed action, in particular the extent to which it involves interaction with an object or with another person. How this conceptual representation of actions is implemented during development is largely unknown. Here, using multivoxel pattern analysis (MVPA) of functional magnetic resonance imaging (fMRI) data, we discovered that, while the action observation network is in place in adolescence, the fine-grain organization of its posterior regions is less robust than in adults to decode the abstract social dimensions of an action. This finding highlights the late maturation of social processing in the human brain.

Keywords: action observation; adolescence; fMRI; occipito-temporal cortex; parietal cortex; social actions.

Figure 1.

A, Stimuli used in the present study. They vary along two dimensions: sociality (social, nonsocial) and transitivity (transitive, intransitive), leading to four distinct categories of actions: Social Transitive (ST), Social Intransitive (SI), Nonsocial Transitive (NT), and Nonsocial Intransitive (NI). Class of actions are defined as: Give: the actor moves an object from his/her peri-personal space toward the peri-personal space of the passive actor; Take: the reverse of Give; Open: the actor opens the notebook; Close: the reverse of Open; Rub: the actor moves the eraser on the notebook with rapid oscillatory movements; Write: the actor writes on the notebook with the pencil; Agree: the actor indicates with a gesture (i.e., thumb up) to the passive actor that he agrees with him/her; Disagree: idem with thumb down, to signify disagreement; Come: the actor indicates with his/her hand to the passive actor to come closer; Go away: the reverse of Come; Stroke: the actor strokes his/her forearm with his/her opposite hand; Scratch: the actor scratches his/her forearm with his/her opposite hand. B, Schematic depiction of the sequence of events in a representative session. C, Behavioral ratings obtained during the fMRI sessions according to the action dimension (sociality and transitivity) and the age group (adults and adolescents). D, Motion magnitude mean values for each class of action.

Figure 2.

Scatter plots of individual videos ratings along the Sociality and Transitivity dimensions. These data were obtained during the pretest phase where 126 participants (M = 33.9 years, SD = 10.2; 77 females) were recruited to rate the videos. As can be seen, the four categories of videos were well-discriminated across the two dimensions.

Figure 3.

Example of the control condition. Representation of several frames of a control video showing upward and downward movement of a pink disk. In this example, the trajectory and cinematic of the disk are matched with that of the gesture “agree” (i.e., Social Intransitive video).

Figure 4.

Graphical representation of the ROIs used in the MVPA. Individual MNI coordinates (red: adults; blue: adolescents) used as sphere centers to construct the ROIs are mapped on PALS-B12 atlas surface configurations (Van Essen, 2005). Regions colored in light white represent the union of all individual ROIs projected on the flat map for LOTC, IPS/SPL, and PMv. PrCS: precentral sulcus; CS: central sulcus; PoCS: postcentral sulcus; IPS: intraparietal sulcus; STS: superior temporal sulcus; ITS: inferior temporal sulcus; OTS: occipital temporal sulcus.

Figure 5.

Schematic representation of the MVPA. A parameter (β) estimate was first extracted for each trial using a GLM. The SVM classification was performed using a leave-one-out cross-validation scheme. For within category decoding, to decode along sociality, the SVM classifier was trained to discriminate between ST versus NT (56 β) and tested on ST versus NT (8 β). In another step, the SVM classifier was trained to discriminate between SI versus NI (56 β) and tested on SI versus NI (8 β). Then the mean accuracies were averaged. For the across category decoding, to decode along sociality, the SVM classifier was trained to discriminate between ST versus NT (56 β) and tested on SI versus NI (8 β). Classification accuracies were averaged across iterations (8 iterations) and across the two generalization directions (e.g., Transitive to Intransitive, and vice versa). Mean classification accuracies were then entered in a three-way ANOVA with Age group (adolescents and adults) as between factor and hemisphere (left and right) and Action (sociality and transitivity) as within factors, for each level of decoding separately.

Figure 6.

Brain activation associated with main effect of (A) Sociality, (B) Transitivity, and (C) Age group. Activations are projected on PALS-B12 atlas surface configurations (Van Essen, 2005): lateral fiducial surfaces. Statistical maps are FWE-corrected for multiple comparisons across the whole-brain at the cluster level; FWE, p < 0.05). AIPS: anterior intraparietal sulcus; SPL: superior parietal lobe; pSTS: posterior superior temporal sulcus; MTG: middle temporal gyrus; STS: superior temporal sulcus; iLOC: inferior lateral occipital cortex; Occ fusif G: occipital fusiform gyrus; Intracal: intracalcarine cortex; SMG: supramarginal gyrus; AG: angular gyrus; PostG: postcentral gyrus; dPMC: dorsal premotor cortex; LOC: lateral occipital cortex; TP: temporal pole; TOf: temporo-occipital fusiform gyrus; Lingual G: Lingual gyrus; EBA: extrastriate body area; FBA: fusiform body area; EVC: extrastriate visual cortex; vMPFC: ventral medial prefrontal cortex; TPJ: temporoparietal junction.

Figure 7.

ROI MVPA results. Bar graphs show group averaged decoding accuracies for within (top) and across (bottom) category decoding for social versus nonsocial actions (blue) and transitive versus intransitive actions (red) for the two groups (adolescents = dark and adults = light). Error bars indicate SD. Asterisks represent statistical significance (FDR-corrected for the number of tests). Dotted line indicates decoding accuracy at chance-level (50%). ***p < 0.001, **p < 0.01, *p < 0.05.

Figure 8.

Four-way mean classification accuracies for each action class (NI, NT, SI, and ST) in adolescents (dark green) and adults (light green) for each ROI (LOTC, PMv, and IPS/SPL). Error bars indicate SD. Asterisks indicate statistical significance with one-tailed t tests (different from chance level = 25%) after FDR correction for multiple comparisons. ***p < 0.001.

Figure 9.

Representation of individual mean classification accuracies for within and across decoding levels for decoding social versus nonsocial and transitive versus intransitive actions, in each ROI. Significant classification accuracies following permutation testing (p < 0.05) are indicated in green and nonsignificant classification accuracies following permutation testing (p > 0.05) are indicated in red. Dashed lines represent chance level (50%).

Figure 10.

MVPA searchlight analyses. Mean accuracy maps and statistical maps of the searchlight within and across decoding for Social versus Nonsocial actions (chance level = 50%) and for Transitive versus Intransitive actions (chance level = 50%) for adults and adolescents. Corrections for multiple comparisons were applied at the voxel level (FWE, p < 0.05).

Figure 11.

Contrasts of searchlight accuracy maps between adults and adolescents for within and across decoding for sociality and transitivity. Corrections for multiple comparisons were.