Modality-specific brain representations during automatic processing of face, voice and body expressions.

A central question in affective science and one that is relevant for its clinical applications is how emotions provided by different stimuli are experienced and represented in the brain. Following the traditional view emotional signals are recognized with the help of emotion concepts that are typically used in descriptions of mental states and emotional experiences, irrespective of the sensory modality. This perspective motivated the search for abstract representations of emotions in the brain, shared across variations in stimulus type (face, body, voice) and sensory origin (visual, auditory). On the other hand, emotion signals like for example an aggressive gesture, trigger rapid automatic behavioral responses and this may take place before or independently of full abstract representation of the emotion. This pleads in favor specific emotion signals that may trigger rapid adaptative behavior only by mobilizing modality and stimulus specific brain representations without relying on higher order abstract emotion categories. To test this hypothesis, we presented participants with naturalistic dynamic emotion expressions of the face, the whole body, or the voice in a functional magnetic resonance (fMRI) study. To focus on automatic emotion processing and sidestep explicit concept-based emotion recognition, participants performed an unrelated target detection task presented in a different sensory modality than the stimulus. By using multivariate analyses to assess neural activity patterns in response to the different stimulus types, we reveal a stimulus category and modality specific brain organization of affective signals. Our findings are consistent with the notion that under ecological conditions emotion expressions of the face, body and voice may have different functional roles in triggering rapid adaptive behavior, even if when viewed from an abstract conceptual vantage point, they may all exemplify the same emotion. This has implications for a neuroethologically grounded emotion research program that should start from detailed behavioral observations of how face, body, and voice expressions function in naturalistic contexts.

Voxelwise encoding models of body stimuli reveal a representational gradient from low-level visual features to postural features in occipitotemporal cortex.

Previous research on body representation in the brain has focused on category-specific representation, using fMRI to investigate the response pattern to body stimuli in occipitotemporal cortex. But the central question of the specific computations involved in body selective regions has not been addressed so far. This study used ultra-high field fMRI and banded ridge regression to investigate the computational mechanisms of coding body images, by comparing the performance of three encoding models in predicting brain activity in occipitotemporal cortex and specifically in the extrastriate body area (EBA). Our results indicate that bodies are encoded in occipitotemporal cortex and in the EBA according to a combination of low-level visual features and postural features.

Decoding the difference between explicit and implicit body expression representation in high level visual, prefrontal and inferior parietal cortex.

Recent studies provide an increasing understanding of how visual objects categories like faces or bodies are represented in the brain and also raised the question whether a category based or more dynamic network inspired models are more powerful. Two important and so far sidestepped issues in this debate are, first, how major category attributes like the emotional expression directly influence category representation and second, whether category and attribute representation are sensitive to task demands. This study investigated the impact of a crucial category attribute like emotional expression on category area activity and whether this varies with the participants' task. Using (fMRI) we measured BOLD responses while participants viewed whole body expressions and performed either an explicit (emotion) or an implicit (shape) recognition task. Our results based on multivariate methods show that the type of task is the strongest determinant of brain activity and can be decoded in EBA, VLPFC and IPL. Brain activity was higher for the explicit task condition in VLPFC and was not emotion specific. This pattern suggests that during explicit recognition of the body expression, body category representation may be strengthened, and emotion and action related activity suppressed. Taken together these results stress the importance of the task and of the role of category attributes for understanding the functional organization of high level visual cortex.

Being the victim of virtual abuse changes default mode network responses to emotional expressions.

Recent behavioural studies have provided evidence that virtual reality (VR) experiences have an impact on socio-affective processes, and a number of findings now underscore the potential of VR for therapeutic interventions. An interesting recent result is that when male offenders experience a violent situation as a female victim of domestic violence in VR, their sensitivity for recognition of fearful facial expressions improves. A timely question now concerns the underlying brain mechanisms of these behavioural effects as these are still largely unknown. The current study used fMRI to measure the impact of a VR intervention in which participants experienced a violent aggression from the specific vantage point of the victim. We compared brain processes related to facial and bodily emotion perception before and after the VR experience. Our results show that the virtual abuse experience led to an enhancement of Default Mode Network (DMN) activity, specifically associated with changes in the processing of ambiguous emotional stimuli. In contrast, DMN activity was decreased when observing fully fearful expressions. Finally, we observed increased variability in brain activity for male versus female facial expressions. Taken together, these results suggest that the first-person perspective of a virtual violent situation impacts emotion recognition through modifications in DMN activity. Our study contributes to a better understanding of the brain mechanisms associated with the behavioural effects of VR interventions in the context of a violent confrontation with the male participant embodied as a female victim. Furthermore, this research also consolidates the use of VR embodied perspective-taking interventions for addressing socio-affective impairments.

Computation-Based Feature Representation of Body Expressions in the Human Brain.

Humans and other primate species are experts at recognizing body expressions. To understand the underlying perceptual mechanisms, we computed postural and kinematic features from affective whole-body movement videos and related them to brain processes. Using representational similarity and multivoxel pattern analyses, we showed systematic relations between computation-based body features and brain activity. Our results revealed that postural rather than kinematic features reflect the affective category of the body movements. The feature limb contraction showed a central contribution in fearful body expression perception, differentially represented in action observation, motor preparation, and affect coding regions, including the amygdala. The posterior superior temporal sulcus differentiated fearful from other affective categories using limb contraction rather than kinematics. The extrastriate body area and fusiform body area also showed greater tuning to postural features. The discovery of midlevel body feature encoding in the brain moves affective neuroscience beyond research on high-level emotion representations and provides insights in the perceptual features that possibly drive automatic emotion perception.

The role of computational and subjective features in emotional body expressions.

Humans are experts at recognizing intent and emotion from other people's body movements; however, the underlying mechanisms are poorly understood. Here, we computed quantitative features of body posture and kinematics and acquired behavioural ratings of these feature descriptors to investigate their role in affective whole-body movement perception. Representational similarity analyses and classification regression trees were used to investigate the relation of emotional categories to both the computed features and behavioural ratings. Overall, postural rather than kinematic features discriminated better between emotional movements for the computed as well as for the behavioural features. In particular, limb angles and symmetry appeared to be the most relevant ones. This was observed independently of whether or not the time-related information was preserved in the computed features. Interestingly, the behavioural ratings showed a clearer distinction between affective movements than the computed counterparts. Finally, the perceived directionality of the movement (i.e. towards or away from the observer) was found to be critical for the recognition of fear and anger.

Threat Anticipation in Pulvinar and in Superficial Layers of Primary Visual Cortex (V1). Evidence from Layer-Specific Ultra-High Field 7T fMRI.

The perceptual system gives priority to threat-relevant signals with survival value. In addition to the processing initiated by sensory inputs of threat signals, prioritization of threat signals may also include processes related to threat anticipation. These neural mechanisms remain largely unknown. Using ultra-high-field 7 tesla (7T) fMRI, we show that anticipatory processing takes place in the early stages of visual processing, specifically in the pulvinar and V1. When anticipation of a threat-relevant fearful face target triggered false perception of not-presented target, there was enhanced activity in the pulvinar as well as in the V1 superficial-cortical-depth (layers 1-3). The anticipatory activity was absent in the LGN or higher visual cortical areas (V2-V4). The effect in V1 was specific to the perception of fearful face targets and did not generalize to happy face targets. A preliminary analysis showed that the connectivity between the pulvinar and V1 superficial-cortical-depth was enhanced during false perception of threat, indicating that the pulvinar and V1 may interact in preparation of anticipated threat. The anticipatory processing supported by the pulvinar and V1 may play an important role in non-sensory-input-driven anxiety states.

Anterior and posterior commissures in agenesis of the corpus callosum: Alternative pathways for attention processes?

Developmental absence (agenesis) of the corpus callosum (AgCC) is a congenital brain malformation resulting from disruption of corpus callosum formation, a structure that is crucial for the transfer and integration of information, including attention processes, across the brain. This study aimed to investigate previously proposed candidates for alternative inter-hemispheric pathways in AgCC by examining (1) white matter volume and microstructure of the anterior and posterior commissures in children with AgCC compared to typically developing controls (TDC), and (2) in children with AgCC, examine the associations of white matter volume and microstructure of the anterior and posterior commissures and any remaining corpus callosum with attention processes. Participants were 21 children with AgCC (13 complete, 8 partial) recruited from The Royal Children's Hospital, Melbourne, and 30 TDC aged 8-17 years. T1-and diffusion-weighted MR sequences were used to calculate volume and microstructural parameters. Neuropsychological testing assessed attention processes. We found the anterior commissure was significantly larger in volume in children with AgCC than TDC (p = .027), with reduced mean FA (p = .001) associated with increased mean RD (p < .001). In children with AgCC, we found microstructural properties of the anterior commissure associated with attentional processes, specifically, mean FA of the anterior commissure was associated with better divided attention (p = .03), and the association between alerting attention and mean AD and RD was found to be moderated by age (p = .027, p = .008) and the degree of corpus callosum agenesis (p = .025, p = .016). Furthermore, in partial AgCC, larger posterior commissure volume was associated with better orienting attention (p = .035). In conclusion, we provide evidence that the volume and microstructure of the anterior commissure are altered in children with AgCC, and this neuroplastic response might have an influence on attention processes.

Computational Feature Analysis of Body Movements Reveals Hierarchical Brain Organization.

Social species spend considerable time observing the body movements of others to understand their actions, predict their emotions, watch their games, or enjoy their dance movements. Given the important information obtained from body movements, we still know surprisingly little about the details of brain mechanisms underlying movement perception. In this fMRI study, we investigated the relations between movement features obtained from automated computational analyses of video clips and the corresponding brain activity. Our results show that low-level computational features map to specific brain areas related to early visual- and motion-sensitive regions, while mid-level computational features are related to dynamic aspects of posture encoded in occipital-temporal cortex, posterior superior temporal sulcus and superior parietal lobe. Furthermore, behavioral features obtained from subjective ratings correlated with activity in higher action observation regions. Our computational feature-based analysis suggests that the neural mechanism of movement encoding is organized in the brain not so much by semantic categories than by feature statistics of the body movements.

Confidence of emotion expression recognition recruits brain regions outside the face perception network.

Metacognitive beliefs about emotions expressed by others are crucial to social life, yet very little studied. To what extent does our confidence in emotion expression recognition depend on perceptual or other non-perceptual information? We obtained behavioral and magnetic resonance imaging measures while participants judged either the emotion in ambiguous faces or the size of two lines flanking these faces, and then rated their confidence on decision accuracy. Distinct behavioral and neural mechanisms were identified for confidence and perceptual decision in both tasks. Participants overestimated their emotion recognition (ER) accuracy, unlike visual size judgments. Whereas expression discrimination recruited several areas in the face-processing network, confidence for ER uniquely engaged the bilateral retrosplenial/posterior cingulate complex and left parahippocampal gyrus. Further, structural white matter connectivity of the former region predicted metacognitive sensitivity. These results highlight a key role for brain mechanisms integrating perception with contextual mnemonic information in the service of confidence during ER.

Classical paintings may trigger pain and pleasure in the gendered brain.

The human body is the most common object of pictorial representation in western art and its representations trigger a vast range of experiences from pain to pleasure. The goal of this study was to investigate brain activity triggered by paintings of male and female body images exemplifying conditions associated with pleasure or pain. Our findings show participant-general as well as gender specific brain activity for either the pain or the pleasure conditions. Although our participants were fully aware that they were viewing artworks, the inferior parietal lobule - known for its role in the perception of emotional body images - and the somatosensory cortex related to touch were selectively active for female body paintings in all participants in the pleasure conditions. As regards gender we observed that the sight of female bodies activated the subgenual anterior cingulate cortex in males, an area known to subserve autonomic arousal. In contrast, in females the sight of the male body activated reward and control related parts of the dorsal anterior cingulate cortex. This study supports the notion that some basic evolutionary processes operate when we view body images, also when they are cultural heritage paintings far removed from daily experience.

Looking at the face and seeing the whole body. Neural basis of combined face and body expressions.

In the natural world, faces are not isolated objects but are rather encountered in the context of the whole body. Previous work has studied the perception of combined faces and bodies using behavioural and electrophysiological measurements, but the neural correlates of emotional face-body perception still remain unexplored. Here, we combined happy and fearful faces and bodies to investigate the influence of body expressions on the neural processing of the face, the effect of emotional ambiguity between the two and the role of the amygdala in this process. Our functional magnetic resonance imaging analyses showed that the activity in motor, prefrontal and visual areas increases when facial expressions are presented together with bodies rather than in isolation, consistent with the notion that seeing body expressions triggers both emotional and action-related processes. In contrast, psychophysiological interaction analyses revealed that amygdala modulatory activity increases after the presentation of isolated faces when compared to combined faces and bodies. Furthermore, a facial expression combined with a congruent body enhanced both cortical activity and amygdala functional connectivity when compared to an incongruent face-body compound. Finally, the results showed that emotional body postures influence the processing of facial expressions, especially when the emotion conveyed by the body implies danger.

Examining distinct working memory processes in children and adolescents using fMRI: Results and validation of a modified Brown-Peterson paradigm.

Verbal working memory (WM) comprises different processes (encoding, maintenance, retrieval) that are often compromised in brain diseases, but their neural correlates have not yet been examined in childhood and adolescence. To probe WM processes and associated neural correlates in developmental samples, and obtain comparable effects across different ages and populations, we designed an adapted Brown-Peterson task (verbal encoding and retrieval combined with verbal and visual concurrent tasks during maintenance) to implement during functional magnetic resonance imaging (fMRI). In a sample of typically developing children and adolescents (n = 16), aged 8 to 16 years, our paradigm successfully identified distinct patterns of activation for encoding, maintenance, and retrieval. While encoding activated perceptual systems in posterior and ventral visual regions, retrieval activated fronto-parietal regions associated with executive control and attention. We found a different impact of verbal versus visual concurrent processing during WM maintenance: at retrieval, the former condition evoked greater activations in visual cortex, as opposed to selective involvement of language-related areas in left temporal cortex in the latter condition. These results are in accord with WM models, suggesting greater competition for processing resources when retrieval follows within-domain compared with cross-domain interference. This pattern was found regardless of age. Our study provides a novel paradigm to investigate distinct WM brain systems with reliable results across a wide age range in developmental populations, and suitable for participants with different WM capacities.

Structural white-matter connections mediating distinct behavioral components of spatial neglect in right brain-damaged patients.

Spatial neglect is a neuropsychological syndrome in which patients fail to perceive and orient to stimuli located in the space contralateral to the lesioned hemisphere. It is characterized by a wide heterogeneity in clinical symptoms which can be grouped into distinct behavioral components correlating with different lesion sites. Moreover, damage to white-matter (WM) fiber tracts has been suggested to disconnect brain networks that mediate different functions associated with spatial cognition and attention. However, it remains unclear what WM pathways are associated with functionally dissociable neglect components. In this study we examined nine patients with a focal right hemisphere stroke using a series of neuropsychological tests and diffusion tensor imaging (DTI) in order to disentangle the role of specific WM pathways in neglect symptoms. First, following previous work, the behavioral test scores of patients were factorized into three independent components reflecting perceptual, exploratory, and object-centered deficits in spatial awareness. We then examined the structural neural substrates of these components by correlating indices of WM integrity (fractional anisotropy) with the severity of deficits along each profile. Several locations in the right parietal and frontal WM correlated with neuropsychological scores. Fiber tracts projecting from these locations indicated that posterior parts of the superior longitudinal fasciculus (SLF), as well as nearby callosal fibers connecting ipsilateral and contralateral parietal areas, were associated with perceptual spatial deficits, whereas more anterior parts of SLF and inferior fronto-occipital fasciculus (IFOF) were predominantly associated with object-centered deficits. In addition, connections between frontal areas and superior colliculus were found to be associated with the exploratory deficits. Our results provide novel support to the view that neglect may result from disconnection lesions in distributed brain networks, but also extend these notions by highlighting the role of dissociable circuits in different functional components of the neglect syndrome. However these preliminary findings require replication with larger samples of patients.

Spatial heterogeneity analysis of brain activation in fMRI.

In many brain diseases it can be qualitatively observed that spatial patterns in blood oxygenation level dependent (BOLD) activation maps appear more (diffusively) distributed than in healthy controls. However, measures that can quantitatively characterize this spatial distributiveness in individual subjects are lacking. In this study, we propose a number of spatial heterogeneity measures to characterize brain activation maps. The proposed methods focus on different aspects of heterogeneity, including the shape (compactness), complexity in the distribution of activated regions (fractal dimension and co-occurrence matrix), and gappiness between activated regions (lacunarity). To this end, functional MRI derived activation maps of a language and a motor task were obtained in language impaired children with (Rolandic) epilepsy and compared to age-matched healthy controls. Group analysis of the activation maps revealed no significant differences between patients and controls for both tasks. However, for the language task the activation maps in patients appeared more heterogeneous than in controls. Lacunarity was the best measure to discriminate activation patterns of patients from controls (sensitivity 74%, specificity 70%) and illustrates the increased irregularity of gaps between activated regions in patients. The combination of heterogeneity measures and a support vector machine approach yielded further increase in sensitivity and specificity to 78% and 80%, respectively. This illustrates that activation distributions in impaired brains can be complex and more heterogeneous than in normal brains and cannot be captured fully by a single quantity. In conclusion, heterogeneity analysis has potential to robustly characterize the increased distributiveness of brain activation in individual patients.

Functional and structural network impairment in childhood frontal lobe epilepsy.

In childhood frontal lobe epilepsy (FLE), cognitive impairment and educational underachievement are serious, well-known co-morbidities. The broad scale of affected cognitive domains suggests wide-spread network disturbances that not only involves, but also extends beyond the frontal lobe. In this study we have investigated whole brain connectional properties of children with FLE in relation to their cognitive impairment and compared them with healthy controls. Functional connectivity (FC) of the networks was derived from dynamic fluctuations of resting state fMRI and structural connectivity (SC) was obtained from fiber tractograms of diffusion weighted MRI. The whole brain network was characterized with graph theoretical metrics and decomposed into modules. Subsequently, the graph metrics and the connectivity within and between modules were related to cognitive performance. Functional network disturbances in FLE were related to increased clustering, increased path length, and stronger modularity compared to healthy controls, which was accompanied by stronger within- and weaker between-module functional connectivity. Although structural path length and clustering appeared normal in children with FLE, structural modularity increased with stronger cognitive impairment. It is concluded that decreased coupling between large-scale functional network modules is a hallmark for impaired cognition in childhood FLE.

Frontal lobe connectivity and cognitive impairment in pediatric frontal lobe epilepsy.

PURPOSE: Cognitive impairment is frequent in children with frontal lobe epilepsy (FLE), but its etiology is unknown. With functional magnetic resonance imaging (fMRI), we have explored the relationship between brain activation, functional connectivity, and cognitive functioning in a cohort of pediatric patients with FLE and healthy controls. METHODS: Thirty-two children aged 8-13 years with FLE of unknown cause and 41 healthy age-matched controls underwent neuropsychological assessment and structural and functional brain MRI. We investigated to which extent brain regions activated in response to a working memory task and assessed functional connectivity between distant brain regions. Data of patients were compared to controls, and patients were grouped as cognitively impaired or unimpaired. KEY FINDINGS: Children with FLE showed a global decrease in functional brain connectivity compared to healthy controls, whereas brain activation patterns in children with FLE remained relatively intact. Children with FLE complicated by cognitive impairment typically showed a decrease in frontal lobe connectivity. This decreased frontal lobe connectivity comprised both connections within the frontal lobe as well as connections from the frontal lobe to the parietal lobe, temporal lobe, cerebellum, and basal ganglia. SIGNIFICANCE: Decreased functional frontal lobe connectivity is associated with cognitive impairment in pediatric FLE. The importance of impairment of functional integrity within the frontal lobe network, as well as its connections to distant areas, provides new insights in the etiology of the broad-range cognitive impairments in children with FLE.

Microstructural and functional MRI studies of cognitive impairment in epilepsy.

Cognitive impairment is the most common comorbidity in children with epilepsy, but its pathophysiology and predisposing conditions remain unknown. Clinical epilepsy characteristics are not conclusive in determining cognitive outcome. Because many children with epilepsy do not have macrostructural magnetic resonance imaging (MRI) abnormalities, the underlying substrate for cognitive impairment may be found at the microstructural or functional level. In the last two decades, new MRI techniques have been developed that have the potential to visualize microstructural or functional abnormalities associated with cognitive impairment. These include volumetric MRI, voxel-based morphometry (VBM), diffusion tensor imaging (DTI), MR spectroscopy (MRS), and functional MRI (fMRI). All of these techniques have shed new light on various aspects associated with, or underlying, cognitive impairment, although their use in epilepsy has been limited and focused mostly on adults. Therefore, in this review, the use of all these different MRI techniques to unravel cognitive impairment in epilepsy is discussed both in adults and children with epilepsy. Volumetric MRI and VBM have revealed significant volume losses in the area of the seizure focus as well as in distant areas. DTI adds evidence of loss of integrity of connections from the seizure focus to distant areas as well as between distant areas. MRS and fMRI have shown impaired function both in the area of the seizure focus as well as in distant structures. For this review we have compiled and compared findings from the various techniques to conclude that cognitive impairment in epilepsy results from a network disorder in which the (micro)structures as well as the functionality can be disturbed.

Cognitive and behavioural findings in children with frontal lobe epilepsy.

BACKGROUND: Frontal Lobe Epilepsy (FLE) is the second most frequent type of partial epilepsy and its onset is generally in childhood. Though cognitive and behavioural impairments have been described as co-morbid disorders in epilepsy, their extent in FLE, particularly in children, remains unknown. AIMS: In this study, we assess cognitive skills and behaviour in a cohort of paediatric FLE patients. METHODS: We measured the performance of 71 children with cryptogenic FLE on intelligence tests, neuropsychological tests, and behavioural questionnaires. Age-dependent normative values were used for reference. Results were related to epilepsy-factors including age at epilepsy onset, duration of epilepsy, seizure frequency, localisation of the epileptic focus and drug load. RESULTS: Paediatric FLE patients performed worse on intellectual and neuropsychological tests compared to reference values, and had a delay in school achievement. The performance of patients was typically worse on tasks measuring visual-spatial functions, memory, psychomotor speed and alertness. High seizure frequency was associated with lower scores on the arithmetic subtest of the intelligence scale; the other epilepsy-factors had no statistically significant influence on intelligence test or neuropsychological test outcome. Behavioural problems included attention problems, anxiety and internalising behaviour. These were not significantly related to epilepsy-factors. CONCLUSIONS: Children with cryptogenic FLE show a broad range of cognitive and behavioural impairments, compared to reference values. While high seizure frequency may affect performance on selected cognitive measures, other epilepsy-factors do not seem to influence cognition and behaviour. Study of micro-structural or functional brain abnormalities that underlie these cognitive and behavioural impairments are warranted.

Tract specific reproducibility of tractography based morphology and diffusion metrics.

INTRODUCTION: The reproducibility of tractography is important to determine its sensitivity to pathological abnormalities. The reproducibility of tract morphology has not yet been systematically studied and the recently developed tractography contrast Tract Density Imaging (TDI) has not yet been assessed at the tract specific level. MATERIALS AND METHODS: Diffusion tensor imaging (DTI) and probabilistic constrained spherical deconvolution (CSD) tractography are performed twice in 9 healthy subjects. Tractography is based on common space seed and target regions and performed for several major white matter tracts. Tractograms are converted to tract segmentations and inter-session reproducibility of tract morphology is assessed using Dice similarity coefficient (DSC). The coefficient of variation (COV) and intraclass correlation coefficient (ICC) are calculated of the following tract metrics: fractional anisotropy (FA), apparent diffusion coefficient (ADC), volume, and TDI. Analyses are performed both for proximal (deep white matter) and extended (including subcortical white matter) tract segmentations. RESULTS: Proximal DSC values were 0.70-0.92. DSC values were 5-10% lower in extended compared to proximal segmentations. COV/ICC values of FA, ADC, volume and TDI were 1-4%/0.65-0.94, 2-4%/0.62-0.94, 3-22%/0.53-0.96 and 8-31%/0.48-0.70, respectively, with the lower COV and higher ICC values found in the proximal segmentations. CONCLUSION: For all investigated metrics, reproducibility depended on the segmented tract. FA and ADC had relatively low COV and relatively high ICC, indicating clinical potential. Volume had higher COV but its moderate to high ICC values in most tracts still suggest subject-differentiating power. Tract TDI had high COV and relatively low ICC, which reflects unfavorable reproducibility.