Developmental changes of bodily self-consciousness in adolescent girls.

The body and the self change markedly during adolescence, but how does bodily self-consciousness, the pre-reflexive experience of being a bodily subject, change? We addressed this issue by studying embodiment towards virtual avatars in 70 girls aged 10-17 years. We manipulated the synchrony between participants' and avatars' touch or movement, as well as the avatar visual shape or size relative to each participant's body. A weaker avatar's embodiment in case of mismatch between the body seen in virtual reality and the real body is indicative of a more robust bodily self-consciousness. In both the visuo-tactile and the visuo-motor experiments, asynchrony decreased ownership feeling to the same extent for all participants, while the effect of asynchrony on agency feeling increased with age. In the visuo-tactile experiment, incongruence in visual appearance did not affect agency feeling but impacted ownership, especially in older teenage girls. These findings highlight the higher malleability of bodily self-consciousness at the beginning of adolescence and suggest some independence between body ownership and agency.

Relating different dimensions of bodily experiences: Review and proposition of an integrative model relying on phenomenology, predictive brain and neuroscience of the self.

How we mentally experience our body has been studied in a variety research domains. Each of these domains focuses in its own ways on different aspects of the body, namely the neurophysiological, perceptual, affective or social components, and proposes different conceptual taxonomies. It is therefore difficult to find one's way through this vast literature and to grasp the relationships between the different dimensions of bodily experiences. In this narrative review, we summarize the existing research directions and present their limits. We propose an integrative framework, grounded in studies on phenomenal consciousness, self-consciousness and bodily self-consciousness, that can provide a common basis for evaluating findings on different dimensions of bodily experiences. We review the putative mechanisms, relying on predictive processes, and neural substrates that support this model. We discuss how this model enables a conceptual assessment of the interrelationships between multiple dimensions of bodily experiences and potentiate interdisciplinary approaches.

Behavioural synchronization and social referencing of dogs and humans: walking in dyad vs in group.

Recent studies have demonstrated that dogs synchronize their locomotor behaviour with that of their owners. The present study aims to improve our understanding of the sensorimotor processes underlying interspecific behavioural synchronization by testing the influence of the number of humans on dogs' behavioural synchronization. We used Global Positioning System (GPS) devices in an outdoor environment to measure dogs' behavioural synchronization to humans during a locomotor activity involving three speeds (static, slow walking and fast walking). For half of the dogs, only their owner was walking, while for the other half, the owner walked with two familiar people. We also tested the effect of dog breeds by involving 30 shepherd dogs and 30 molossoids. Our results showed that dogs exhibited the same level of behavioural synchronization with their owner if alone or if surrounded by two familiar people. Though the presence of a group of humans did not strengthen the dogs' locomotor synchronization, it did produce another effect: dogs gazed at their owners more frequently in the presence of a group compared to their owner alone. This result suggests the same level of locomotor social entrainment but a difference in social referencing depending on the number of humans.

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

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.

Brain Activity During Antisaccades to Faces in Adolescence.

Cognitive control and social perception both change during adolescence, but little is known of the interaction of these 2 processes. We aimed to characterize developmental changes in brain activity related to the influence of a social stimulus on cognitive control and more specifically on inhibitory control. Children (age 8-11, n = 19), adolescents (age 12-17, n = 20), and adults (age 24-40, n = 19) performed an antisaccade task with either faces or cars as visual stimuli, during functional magnetic resonance brain imaging. We replicate the finding of the engagement of the core oculomotor and face perception brain regions in all age-groups, with increased involvement of frontoparietal oculomotor regions and fusiform face regions with age. The antisaccade-related activity was modulated by stimulus category significantly only in adolescents. This interaction was observed mainly in occipitotemporal regions as well as in supplementary motor cortex and postcentral gyrus. These results indicate a special treatment of social stimuli during adolescence.

Developmental trajectory of interpersonal motor alignment: Positive social effects and link to social cognition.

Interpersonal motor alignment is a ubiquitous behavior in daily social life. It is a building block for higher social cognition, including empathy and mentalizing and promotes positive social effects. It can be observed as mimicry, synchrony and automatic imitation, to name a few. These phenomena rely on motor resonance processes, i.e., a direct link between the perception of an action and its execution. While a considerable literature debates its underlying mechanisms and measurement methods, the question of how motor alignment comes about and changes in ontogeny all the way until adulthood, is rarely discussed specifically. In this review we will focus on the link between interpersonal motor alignment, positive social effects and social cognition in infants, children, and adolescents, demonstrating that this link is present early on in development. Yet, in reviewing the existing literature pertaining to social psychology and developmental social cognitive neuroscience, we identify a knowledge gap regarding the healthy developmental changes in interpersonal motor alignment especially in adolescence.

A dynamic body-selective area localizer for use in fMRI.

Functional localizers allow the definition of regions of interest in the human brain that cannot be delineated by anatomical markers alone. To date, when localizing the body-selective areas of the visual cortex using fMRI, researchers have used static images of bodies and objects. However, there are other relevant brain areas involved in the processing of moving bodies and action interpretation that are missed by these techniques. Typically, these biological motion areas are localized separately using whole and scrambled point-light display stimuli. Currently, one can only localize either the static body-selective areas or the biological motion areas, but not both together. Here, for the first time, using motion-controlled dynamic body and object stimuli, we describe a method for localizing the full dynamic body-selective network of the human brain in one experimental run. •The method uses dynamic body and object stimuli.•Low-level local motion information is added as a covariate into the fMRI analysis.•This localizes the full dynamic body-selective network of the human brain.

Emotion modulation of the body-selective areas in the developing brain.

Emotions are strongly conveyed by the human body and the ability to recognize emotions from body posture or movement is still developing through childhood and adolescence. To date, very few studies have explored how these behavioural observations are paralleled by functional brain development. Furthermore, currently no studies have explored the development of emotion modulation in these areas. In this study, we used functional magnetic resonance imaging (fMRI) to compare the brain activity of 25 children (age 6-11), 18 adolescents (age 12-17) and 26 adults while they passively viewed short videos of angry, happy or neutral body movements. We observed that when viewing dynamic bodies generally, adults showed higher activity than children bilaterally in the body-selective areas; namely the extra-striate body area (EBA), fusiform body area (FBA), posterior superior temporal sulcus (pSTS), as well as the amygdala (AMY). Adults also showed higher activity than adolescents, but only in the right hemisphere. Crucially, however, we found that there were no age differences in the emotion modulation of activity in these areas. These results indicate, for the first time, that despite activity selective to body perception increasing across childhood and adolescence, emotion modulation of these areas in adult-like from 7 years of age.

Categorical emotion recognition from voice improves during childhood and adolescence.

Converging evidence demonstrates that emotion processing from facial expressions continues to improve throughout childhood and part of adolescence. Here we investigated whether this is also the case for emotions conveyed by non-linguistic vocal expressions, another key aspect of social interactions. We tested 225 children and adolescents (age 5-17) and 30 adults in a forced-choice labeling task using vocal bursts expressing four basic emotions (anger, fear, happiness and sadness). Mixed-model logistic regressions revealed a small but highly significant change with age, mainly driven by changes in the ability to identify anger and fear. Adult-level of performance was reached between 14 and 15 years of age. Also, across ages, female participants obtained better scores than male participants, with no significant interaction between age and sex effects. These results expand the findings showing that affective prosody understanding improves during childhood; they document, for the first time, continued improvement in vocal affect recognition from early childhood to mid- adolescence, a pivotal period for social maturation.

Brain network connectivity associated with anticipatory postural control in children and adults.

Internal models provide a coherent framework for understanding motor behavior. Examples for the use of internal models include anticipatory postural adjustments (APAs), where the individual anticipates and cancels out the destabilizing effect of movement on body posture. Yet little is known about the functional changes in the brain supporting the development of APAs. Here, we addressed this issue by relating individual differences in APAs as assessed during bimanual load lifting to interindividual variation in brain network interactions at rest. We showed that the strength of the connectivity between three main canonical brain networks, namely the cingulo-opercular, the fronto-parietal and the somatosensory-motor networks, is an index of the ability to implement APAs from late childhood (9- to 11-year-old children). We also found an effect of age on the relationship between APAs and coupling strength between these networks, consistent with the notion that APAs are near but not yet fully mature in children. We discuss the implications of these findings for our understanding of learning disorders with impairment in predictive motor control.

Patterns of Activity in the Human Frontal and Parietal Cortex Differentiate Large and Small Saccades.

A vast literature indicates that small and large saccades, respectively, subserve different perceptual and cognitive strategies and may rely on different programming modes. While it is well-established that in monkeys' main oculomotor brain regions small and large eye movements are controlled by segregated neuronal populations, the representation of saccade amplitude in the human brain remains unclear. To address this question we used functional magnetic resonance imaging to scan participants while they performed saccades toward targets at either short (4°) or large (30°) eccentricity. A regional multivoxel pattern analysis reveals that patterns of activity in the frontal eye-field and parietal eye fields discriminate between the execution of large or small saccades. This was not the case in the supplementary eye-fields nor in the inferior precentral cortex. These findings provide the first evidence of a representation of saccadic eye movement size in the fronto-parietal occulomotor circuit. They shed light on the respective roles of the different cortical oculomotor regions with respect to space perception and exploration, as well as on the homology of eye movement control between human and non-human primates.

Mirror Neurons System Engagement in Late Adolescents and Adults While Viewing Emotional Gestures.

Observing others' actions enhances muscle-specific cortico-spinal excitability, reflecting putative mirror neurons activity. The exposure to emotional stimuli also modulates cortico-spinal excitability. We investigated how those two phenomena might interact when they are combined, i.e., while observing a gesture performed with an emotion, and whether they change during the transition between adolescence and adulthood, a period of social and brain maturation. We delivered single-pulse transcranial magnetic stimulation (TMS) over the hand area of the left primary motor cortex of 27 healthy adults and adolescents and recorded their right first dorsal interossus (FDI) muscle activity (i.e., motor evoked potential - MEP), while they viewed either videos of neutral or angry hand actions and facial expressions, or neutral objects as a control condition. We reproduced the motor resonance and the emotion effects - hand-actions and emotional stimuli induced greater cortico-spinal excitability than the faces/control condition and neutral videos, respectively. Moreover, the influence of emotion was present for faces but not for hand actions, indicating that the motor resonance and the emotion effects might be non-additive. While motor resonance was observed in both groups, the emotion effect was present only in adults and not in adolescents. We discuss the possible neural bases of these findings.

Pros and Cons of Using the Informed Basis Set to Account for Hemodynamic Response Variability with Developmental Data.

Conventional analysis of functional magnetic resonance imaging (fMRI) data using the general linear model (GLM) employs a neural model convolved with a canonical hemodynamic response function (HRF) peaking 5 s after stimulation. Incorporation of a further basis function, namely the canonical HRF temporal derivative, accounts for delays in the hemodynamic response to neural activity. A population that may benefit from this flexible approach is children whose hemodynamic response is not yet mature. Here, we examined the effects of using the set based on the canonical HRF plus its temporal derivative on both first- and second-level GLM analyses, through simulations and using developmental data (an fMRI dataset on proprioceptive mapping in children and adults). Simulations of delayed fMRI first-level data emphasized the benefit of carrying forward to the second-level a derivative boost that combines derivative and nonderivative beta estimates. In the experimental data, second-level analysis using a paired t-test showed increased mean amplitude estimate (i.e., increased group contrast mean) in several brain regions related to proprioceptive processing when using the derivative boost compared to using only the nonderivative term. This was true especially in children. However, carrying forward to the second-level the individual derivative boosts had adverse consequences on random-effects analysis that implemented one-sample t-test, yielding increased between-subject variance, thus affecting group-level statistic. Boosted data also presented a lower level of smoothness that had implication for the detection of group average activation. Imposing soft constraints on the derivative boost by limiting the time-to-peak range of the modeled response within a specified range (i.e., 4-6 s) mitigated these issues. These findings support the notion that there are pros and cons to using the informed basis set with developmental data.

Co-ordinated structural and functional covariance in the adolescent brain underlies face processing performance.

Our ability to process complex social cues presented by faces improves during adolescence. Using multivariate analyses of neuroimaging data collected longitudinally from a sample of 38 adolescents (17 males) when they were 10, 11.5, 13 and 15 years old, we tested the possibility that there exists parallel variations in the structural and functional development of neural systems supporting face processing. By combining measures of task-related functional connectivity and brain morphology, we reveal that both the structural covariance and functional connectivity among 'distal' nodes of the face-processing network engaged by ambiguous faces increase during this age range. Furthermore, we show that the trajectory of increasing functional connectivity between the distal nodes occurs in tandem with the development of their structural covariance. This demonstrates a tight coupling between functional and structural maturation within the face-processing network. Finally, we demonstrate that increased functional connectivity is associated with age-related improvements of face-processing performance, particularly in females. We suggest that our findings reflect greater integration among distal elements of the neural systems supporting the processing of facial expressions. This, in turn, might facilitate an enhanced extraction of social information from faces during a time when greater importance is placed on social interactions.

Dorsal and Ventral Pathways for Prosody.

Our vocal tone--the prosody--contributes a lot to the meaning of speech beyond the actual words. Indeed, the hesitant tone of a "yes" may be more telling than its affirmative lexical meaning. The human brain contains dorsal and ventral processing streams in the left hemisphere that underlie core linguistic abilities such as phonology, syntax, and semantics. Whether or not prosody--a reportedly right-hemispheric faculty--involves analogous processing streams is a matter of debate. Functional connectivity studies on prosody leave no doubt about the existence of such streams, but opinions diverge on whether information travels along dorsal or ventral pathways. Here we show, with a novel paradigm using audio morphing combined with multimodal neuroimaging and brain stimulation, that prosody perception takes dual routes along dorsal and ventral pathways in the right hemisphere. In experiment 1, categorization of speech stimuli that gradually varied in their prosodic pitch contour (between statement and question) involved (1) an auditory ventral pathway along the superior temporal lobe and (2) auditory-motor dorsal pathways connecting posterior temporal and inferior frontal/premotor areas. In experiment 2, inhibitory stimulation of right premotor cortex as a key node of the dorsal stream decreased participants' performance in prosody categorization, arguing for a motor involvement in prosody perception. These data draw a dual-stream picture of prosodic processing that parallels the established left-hemispheric multi-stream architecture of language, but with relative rightward asymmetry.

TMS over V5 disrupts motion prediction.

Given the vast amount of sensory information the brain has to deal with, predicting some of this information based on the current context is a resource-efficient strategy. The framework of predictive coding states that higher-level brain areas generate a predictive model to be communicated via feedback connections to early sensory areas. Here, we directly tested the necessity of a higher-level visual area, V5, in this predictive processing in the context of an apparent motion paradigm. We flashed targets on the apparent motion trace in-time or out-of-time with the predicted illusory motion token. As in previous studies, we found that predictable in-time targets were better detected than unpredictable out-of-time targets. However, when we applied functional magnetic resonance imaging-guided, double-pulse transcranial magnetic stimulation (TMS) over left V5 at 13-53 ms before target onset, the detection advantage of in-time targets was eliminated; this was not the case when TMS was applied over the vertex. Our results are causal evidence that V5 is necessary for a prediction effect, which has been shown to modulate V1 activity (Alink et al. 2010). Thus, our findings suggest that information processing between V5 and V1 is crucial for visual motion prediction, providing experimental support for the predictive coding framework.

Body-selective areas in the visual cortex are less active in children than in adults.

Our ability to read other people's non-verbal signals gets refined throughout childhood and adolescence. How this is paralleled by brain development has been investigated mainly with regards to face perception, showing a protracted functional development of the face-selective visual cortical areas. In view of the importance of whole-body expressions in interpersonal communication it is important to understand the development of brain areas sensitive to these social signals. Here we used functional magnetic resonance imaging (fMRI) to compare brain activity in a group of 24 children (age 6-11) and 26 adults while they passively watched short videos of body or object movements. We observed activity in similar regions in both groups; namely the extra-striate body area (EBA), fusiform body area (FBA), posterior superior temporal sulcus (pSTS), amygdala and premotor regions. Adults showed additional activity in the inferior frontal gyrus (IFG). Within the main body-selective regions (EBA, FBA and pSTS), the strength and spatial extent of fMRI signal change was larger in adults than in children. Multivariate Bayesian (MVB) analysis showed that the spatial pattern of neural representation within those regions did not change over age. Our results indicate, for the first time, that body perception, like face perception, is still maturing through the second decade of life.

Biasing the perception of ambiguous vocal affect: a TMS study on frontal asymmetry.

Several sources of evidence point toward a link between asymmetry of prefrontal brain activity and approach-withdrawal tendencies. Here, we tested the causal nature of this link and examined if the categorization of an ambiguous approach- or withdrawal-related vocal signal can be biased by manipulating left and right frontal neural activity. We used voice morphing of affective non-verbal vocalizations to create individually tailored affectively ambiguous stimuli on an Anger-Fear continuum-two emotions that represent extremes on the approach-withdrawal dimension. We tested perception of these stimuli after 10 min of low-frequency repetitive transcranial magnetic stimulation over left or right dorsolateral prefrontal cortex or over the vertex (control), a technique that has transient inhibitory effects on the targeted brain region. As expected, ambiguous stimuli were more likely perceived as expressing Anger (approach) than Fear (withdrawal) after right prefrontal compared with left prefrontal or control stimulation. These results provide the first evidence that the manipulation of asymmetrical activity in prefrontal cortex can change the explicit categorization of ambiguous emotional signals.

Parieto-occipital cortex shows early target selection to faces in a reflexive orienting task.

It is well established that human faces induce stronger involuntary orienting responses than other visual objects. Yet, the timing of this preferential orienting response at the neural level is still unknown. Here, we used an antisaccade paradigm to investigate the neural dynamics preceding the onset of reflexive and voluntary saccades elicited by human faces and nonface visual objects, normalized for their global low-level visual properties. High-density event-related potentials (ERPs) were recorded in observers as they performed interleaved pro- and antisaccades toward a lateralized target. For reflexive saccades, we report an ERP modulation specific to faces as early as 40-60 ms following stimulus onset over parieto-occipital sites, further predicting the speed of saccade execution. This was not linked to differences in the programming of the saccadic eye movements, as it occurred early in time. For the first time, we present electrophysiological evidence of early target selection to faces in reflexive orienting responses over parieto-occipital cortex that facilitates the triggering of saccades toward faces. We argue for a 2-stage process in the representation of a face in involuntary spatial orienting with an initial, rapid implicit processing of the visual properties of a face, followed by subsequent stimulus categorization depicted by the N170 component.

Uni- and multisensory brain areas are synchronised across spectators when watching unedited dance recordings.

The superior temporal sulcus (STS) and gyrus (STG) are commonly identified to be functionally relevant for multisensory integration of audiovisual (AV) stimuli. However, most neuroimaging studies on AV integration used stimuli of short duration in explicit evaluative tasks. Importantly though, many of our AV experiences are of a long duration and ambiguous. It is unclear if the enhanced activity in audio, visual, and AV brain areas would also be synchronised over time across subjects when they are exposed to such multisensory stimuli. We used intersubject correlation to investigate which brain areas are synchronised across novices for uni- and multisensory versions of a 6-min 26-s recording of an unfamiliar, unedited Indian dance recording (Bharatanatyam). In Bharatanatyam, music and dance are choreographed together in a highly intermodal-dependent manner. Activity in the middle and posterior STG was significantly correlated between subjects and showed also significant enhancement for AV integration when the functional magnetic resonance signals were contrasted against each other using a general linear model conjunction analysis. These results extend previous studies by showing an intermediate step of synchronisation for novices: while there was a consensus across subjects' brain activity in areas relevant for unisensory processing and AV integration of related audio and visual stimuli, we found no evidence for synchronisation of higher level cognitive processes, suggesting these were idiosyncratic.