Anatomo-functional basis of emotional and motor resonance elicited by facial expressions.

Simulation theories predict that the observation of other's expressions modulates neural activity in the same centers controlling their production. This hypothesis has been developed by two models, postulating that the visual input is directly projected either to the motor system for action recognition (motor resonance) or to emotional/interoceptive regions for emotional contagion and social synchronization (emotional resonance). Here we investigated the role of frontal/insular regions in the processing of observed emotional expressions by combining intracranial recording, electrical stimulation and effective connectivity. First, we intracranially recorded from prefrontal, premotor or anterior insular regions of 44 patients during the passive observation of emotional expressions, finding widespread modulations in prefrontal/insular regions (anterior cingulate cortex, anterior insula, orbitofrontal cortex and inferior frontal gyrus) and motor territories (rolandic operculum and inferior frontal junction). Subsequently, we electrically stimulated the activated sites, finding that (a) in the anterior cingulate cortex and anterior insula, the stimulation elicited emotional/interoceptive responses, as predicted by the 'emotional resonance model', (b) in the rolandic operculum it evoked face/mouth sensorimotor responses, in line with the 'motor resonance' model, and (c) all other regions were unresponsive or revealed functions unrelated to the processing of facial expressions. Finally, we traced the effective connectivity to sketch a network-level description of these regions, finding that the anterior cingulate cortex and the anterior insula are reciprocally interconnected while the rolandic operculum is part of the parieto-frontal circuits and poorly connected with the formers. These results support the hypothesis that the pathways hypothesized by the 'emotional resonance' and the 'motor resonance' models work in parallel, differing in terms of spatio-temporal fingerprints, reactivity to electrical stimulation and connectivity patterns.

Architectural experience influences the processing of others' body expressions.

The interplay between space and cognition is a crucial issue in Neuroscience leading to the development of multiple research fields. However, the relationship between architectural space and the movement of the inhabitants and their interactions has been too often neglected, failing to provide a unifying view of architecture's capacity to modulate social cognition broadly. We bridge this gap by requesting participants to judge avatars' emotional expression (high vs. low arousal) at the end of their promenade inside high- or low-arousing architectures. Stimuli were presented in virtual reality to ensure a dynamic, naturalistic experience. High-density electroencephalography (EEG) was recorded to assess the neural responses to the avatar's presentation. Observing highly aroused avatars increased Late Positive Potentials (LPP), in line with previous evidence. Strikingly, 250 ms before the occurrence of the LPP, P200 amplitude increased due to the experience of low-arousing architectures, reflecting an early greater attention during the processing of body expressions. In addition, participants stared longer at the avatar's head and judged the observed posture as more arousing. Source localization highlighted a contribution of the dorsal premotor cortex to both P200 and LPP. In conclusion, the immersive and dynamic architectural experience modulates human social cognition. In addition, the motor system plays a role in processing architecture and body expressions suggesting that the space and social cognition interplay is rooted in overlapping neural substrates. This study demonstrates that the manipulation of mere architectural space is sufficient to influence human social cognition.

Language lateralization mapping (reversibly) masked by non-dominant focal epilepsy: a case report.

Language lateralization in patients with focal epilepsy frequently diverges from the left-lateralized pattern that prevails in healthy right-handed people, but the mechanistic explanations are still a matter of debate. Here, we debate the complex interaction between focal epilepsy, language lateralization, and functional neuroimaging techniques by introducing the case of a right-handed patient with unaware focal seizures preceded by aphasia, in whom video-EEG and PET examination suggested the presence of focal cortical dysplasia in the right superior temporal gyrus, despite a normal structural MRI. The functional MRI for language was inconclusive, and the neuropsychological evaluation showed mild deficits in language functions. A bilateral stereo-EEG was proposed confirming the right superior temporal gyrus origin of seizures, revealing how ictal aphasia emerged only once seizures propagated to the left superior temporal gyrus and confirming, by cortical mapping, the left lateralization of the posterior language region. Stereo-EEG-guided radiofrequency thermocoagulations of the (right) focal cortical dysplasia not only reduced seizure frequency but led to the normalization of the neuropsychological assessment and the "restoring" of a classical left-lateralized functional MRI pattern of language. This representative case demonstrates that epileptiform activity in the superior temporal gyrus can interfere with the functioning of the contralateral homologous cortex and its associated network. In the case of presurgical evaluation in patients with epilepsy, this interference effect must be carefully taken into consideration. The multimodal language lateralization assessment reported for this patient further suggests the sensitivity of different explorations to this interference effect. Finally, the neuropsychological and functional MRI changes after thermocoagulations provide unique cues on the network pathophysiology of focal cortical dysplasia and the role of diverse techniques in indexing language lateralization in complex scenarios.

70 Years of Human Cingulate Cortex Stimulation. Functions and Dysfunctions Through the Lens of Electrical Stimulation.

SUMMARY: In this review, we retrace the results of 70 years of human cingulate cortex (CC) intracerebral electrical stimulation and discuss its contribution to our understanding of the anatomofunctional and clinical aspects of this wide cortical region. The review is divided into three main sections. In the first section, we report the results obtained by the stimulation of the anterior, middle, and posterior CC, in 30 studies conducted on approximately 1,000 patients from the 1950s to the present day. These studies show that specific manifestations can be reliably associated with specific cingulate subfields, with autonomic, interoceptive, and emotional manifestations clustered in the anterior cingulate, goal-oriented motor behaviors elicited from the anterior midcingulate and a variety of sensory symptoms characterizing the posterior cingulate regions. In the second section, we compare the effect of CC intracerebral electrical stimulation with signs and manifestations characterizing cingulate epilepsy, showing that the stimulation mapping of CC subfields provides precious information for understanding cingulate epileptic manifestations. The last section tackles the issue of the discrepancy emerging when comparing the results of clinical (electrical stimulation, epilepsy) studies-revealing the quintessential affective and motor nature of the CC-with that reported by neuroimaging studies-which focus on high-level cognitive functions. Particular attention will be paid to the hypothesis that CC hosts a "Pain Matrix" specifically involved in pain perception, which we will discuss in the light of the fact that the stimulation of CC (as well as cingulate epileptic seizures) does not induce nociceptive effects.

The naturalistic approach to laughter in humans and other animals: towards a unified theory.

This opinion piece aims to tackle the biological, psychological, neural and cultural underpinnings of laughter from a naturalistic and evolutionary perspective. A naturalistic account of laughter requires the revaluation of two dogmas of a longstanding philosophical tradition, that is, the quintessential link between laughter and humour, and the uniquely human nature of this behaviour. In the spirit of Provine's and Panksepp's seminal studies, who firstly argued against the anti-naturalistic dogmas, here we review compelling evidence that (i) laughter is first and foremost a social behaviour aimed at regulating social relationships, easing social tensions and establishing social bonds, and that (ii) homologue and homoplasic behaviours of laughter exist in primates and rodents, who also share with humans the same underpinning neural circuitry. We make a case for the hypothesis that the contagiousness of laughter and its pervasive social infectiousness in everyday social interactions is mediated by a specific mirror mechanism. Finally, we argue that a naturalistic account of laughter should not be intended as an outright rejection of classic theories; rather, in the last part of the piece we argue that our perspective is potentially able to integrate previous viewpoints-including classic philosophical theories-ultimately providing a unified evolutionary explanation of laughter. This article is part of the theme issue 'Cracking the laugh code: laughter through the lens of biology, psychology and neuroscience'.

Measuring arousal and valence generated by the dynamic experience of architectural forms in virtual environments.

The built environment represents the stage surrounding our everyday life activities. To investigate how architectural design impacts individuals' affective states, we measured subjective judgments of perceived valence (pleasant and unpleasant) and arousal after the dynamic experience of a progressive change of macro visuospatial dimensions of virtual spaces. To this aim, we developed a parametric model that allowed us to create 54 virtual architectural designs characterized by a progressive change of sidewalls distance, ceiling and windows height, and color of the environment. Decreasing sidewalls distance, ceiling height variation, and increasing windows height significantly affected the participants' emotional state within virtual environments. Indeed, such architectural designs generated high arousing and unpleasant states according to subjective judgment. Overall, we observed that valence and arousal scores are affected by all the dynamic form factors which modulated the spaciousness of the surrounding. Showing that the dynamic experience of virtual environments enables the possibility of measuring the emotional impact of macro spatial architectural features, the present findings may lay the groundwork for future experiments investigating the effects that the architectural design has on individuals' mental state as a fundamental factor for the creation of future spaces.

The Avatar's Gist: How to Transfer Affective Components From Dynamic Walking to Static Body Postures.

Dynamic virtual representations of the human being can communicate a broad range of affective states through body movements, thus effectively studying emotion perception. However, the possibility of modeling static body postures preserving affective information is still fundamental in a broad spectrum of experimental settings exploring time-locked cognitive processes. We propose a novel automatic method for creating virtual affective body postures starting from kinematics data. Exploiting body features related to postural cues and movement velocity, we transferred the affective components from dynamic walking to static body postures of male and female virtual avatars. Results of two online experiments showed that participants coherently judged different valence and arousal levels in the avatar's body posture, highlighting the reliability of the proposed methodology. In addition, esthetic and postural cues made women more emotionally expressive than men. Overall, we provided a valid methodology to create affective body postures of virtual avatars, which can be used within different virtual scenarios to understand better the way we perceive the affective state of others.

Facial impression of trustworthiness biases statement credibility unless suppressed by facemask.

The impression of trustworthiness based on someone's facial appearance biases our subsequent behavior toward that subject in a variety of contexts. In this study, we investigated whether facial trustworthiness also biases the credibility of utterances associated with that face (H1). We explored whether this bias is mitigated by utterances eliciting reasoning, i.e. explanations (as opposed to factual statements; H2). Moreover, we hypothesized that overimposing facemasks on those faces could enhance/reduce utterance credibility due to social value of mask-wearing (H3), and that facemasks could counter the putative credibility bias introduced by facial trustworthiness (H4). If so, this may be either because facemasks remove the visual information necessary for trustworthiness impression (H4a), or because information is less salient, although it can be retrieved under different circumstances (H4b). An online study (N = 159) was conducted to test these hypotheses. In the first task, subjects saw 48 facial pictures coupled with one utterance and judged the truthfulness/falsity of this utterance. In the second task, they saw again 16 of the faces from the previous tasks and were asked to recall whether the associated utterance was true or false. Findings from the first task support H1 and H4, but not H2 and H3. However, in the second task, where the face is the only available cue, the credibility-mitigation bias exerted by facemask disappears, supporting H4b over H4a. Our results confirm the pervasivity of facial trustworthiness impressions in social cognition, and suggest that facemask can mitigate them, or at least their salience. Supplementary information: The online version contains supplementary material available at 10.1007/s12144-022-03277-7.

Association Between Semiology and Anatomo-functional Localization in Patients With Cingulate Epilepsy: A Cohort Study.

BACKGROUND AND OBJECTIVES: Cingulate epilepsy (CE) is a rare type of focal epilepsy that is challenging to diagnose because of the polymorphic semiology of the seizures, mimicking other types of epilepsy, and the limited utility of scalp EEG. METHODS: We selected consecutive patients with drug-resistant CE who were seizure-free after surgery, with seizure onset zone (SOZ) confirmed in the cingulate cortex (CC) by histology or stereo EEG. We analyzed subjective and objective ictal manifestations using video recordings and correlated semiology with anatomical CC subregion (anterior, anterior middle, posterior middle, and posterior) localization of SOZ. RESULTS: We analyzed 122 seizures in 57 patients. Seizures were globally characterized by complex behaviors, typically natural seeming and often accompanied by emotional components. All objective ictal variables considered (pronation of the body or arising from a lying/sitting position, tonic/dystonic posturing, hand movements, asymmetry, vocalizations, fluidity and repetitiveness of motor manifestations, awareness, and emotional and autonomic components) were differently distributed among CC subregions (p < 0.05). Along the rostro-caudal axis, fluidity and repetitiveness of movement, vocalizations, body pronation, and emotional components decreased anterior-posteriorly, whereas tonic/dystonic postures, signs of lateralization, and awareness increased. Vestibular and asymmetric somatosensory, somatosensory, and epigastric and enteroceptive/autonomic symptoms were distributed differently among CC subregions (p < 0.05). Along the rostro-caudal axis, vestibular, somatosensory, and somatosensory asymmetric symptoms increased anterior-posteriorly. DISCUSSION: CE is characterized by a spectrum of semiologic manifestations with a topographic distribution. CE semiology could indicate which cingulate sector is primarily involved.

Tonic somatosensory responses and deficits of tactile awareness converge in the parietal operculum.

Although clinical neuroscience and the neuroscience of consciousness have long sought mechanistic explanations of tactile-awareness disorders, mechanistic insights are rare, mainly because of the difficulty of depicting the fine-grained neural dynamics underlying somatosensory processes. Here, we combined the stereo-EEG responses to somatosensory stimulation with the lesion mapping of patients with a tactile-awareness disorder, namely tactile extinction. Whereas stereo-EEG responses present different temporal patterns, including early/phasic and long-lasting/tonic activities, tactile-extinction lesion mapping co-localizes only with the latter. Overlaps are limited to the posterior part of the perisylvian regions, suggesting that tonic activities may play a role in sustaining tactile awareness. To assess this hypothesis further, we correlated the prevalence of tonic responses with the tactile-extinction lesion mapping, showing that they follow the same topographical gradient. Finally, in parallel with the notion that visuotactile stimulation improves detection in tactile-extinction patients, we demonstrated an enhancement of tonic responses to visuotactile stimuli, with a strong voxel-wise correlation with the lesion mapping. The combination of these results establishes tonic responses in the parietal operculum as the ideal neural correlate of tactile awareness.

The impact of facemasks on emotion recognition, trust attribution and re-identification.

Covid-19 pandemics has fostered a pervasive use of facemasks all around the world. While they help in preventing infection, there are concerns related to the possible impact of facemasks on social communication. The present study investigates how emotion recognition, trust attribution and re-identification of faces differ when faces are seen without mask, with a standard medical facemask, and with a transparent facemask restoring visual access to the mouth region. Our results show that, in contrast to standard medical facemasks, transparent masks significantly spare the capability to recognize emotional expressions. Moreover, transparent masks spare the capability to infer trustworthiness from faces with respect to standard medical facemasks which, in turn, dampen the perceived untrustworthiness of faces. Remarkably, while transparent masks (unlike standard masks) do not impair emotion recognition and trust attribution, they seemingly do impair the subsequent re-identification of the same, unmasked, face (like standard masks). Taken together, this evidence supports a dissociation between mechanisms sustaining emotion and identity processing. This study represents a pivotal step in the much-needed analysis of face reading when the lower portion of the face is occluded by a facemask.

Mirroring other's laughter. Cingulate, opercular and temporal contributions to laughter expression and observation.

Simulation theories predict that the observation of other's laughter modulates activity in the same centers controlling its production. Investigating this issue is particularly challenging, given the technical difficulties of studying laughter production. Previous observations from surgical patients reported laughter production following the electrical stimulation (ES) of the pregenual anterior cingulate (pACC), the frontal operculum (FO) and the temporal pole (TP), deemed to control emotional, communicative and cognitive aspects of laughter, respectively. Here we investigated which region is recruited during laughter observation and production, by adopting a twofold strategy which combines ES and intracranial recording in the same patients. We identified nine sites equally distributed in the pACC, FO and TP, where ES elicited laughter. Subsequently, we presented the patients with visual stimuli depicting dynamic (video) and static (pictures) expressions of laughter, along with emotional and neutral controls, while intracranially recording high-frequency gamma activity (50-150 Hz) from the same sites. pACC sites showed a selective activation during laughter observation, but only if laughter is presented in a dynamical fashion. FO and TP failed to respond during both dynamic and static expressions. We conclude that pACC host a mirror mechanism directly mapping other's laughter onto the neural substrate responsible for the production of emotional laughter.

Action execution and action observation elicit mirror responses with the same temporal profile in human SII.

The properties of the secondary somatosensory area (SII) have been described by many studies in monkeys and humans. Recent studies on monkeys, however, showed that beyond somatosensory stimuli, SII responds to a wider number of stimuli, a finding requiring a revision that human SII is purely sensorimotor. By recording cortical activity with stereotactic electroencephalography (stereo-EEG), we examined the properties of SI and SII in response to a motor task requiring reaching, grasping and manipulation, as well as the observation of the same actions. Furthermore, we functionally characterized this area with a set of clinical tests, including tactile, acoustical, and visual stimuli. The results showed that only SII activates both during execution and observation with a common temporal profile, whereas SI response were limited to execution. Together with their peculiar response to tactile stimuli, we conclude that the role of SII is pivotal also in the observation of actions involving haptic control.

Pathways for smiling, disgust and fear recognition in blindsight patients.

The aim of the present review is to discuss the localization of circuits that allow recognition of emotional facial expressions in blindsight patients. Because recognition of facial expressions is function of different centers, and their localization is not always clear, we decided to discuss here three emotional facial expression - smiling, disgust, and fear - whose anatomical localization in the pregenual sector of the anterior cingulate cortex (pACC), anterior insula (AI), and amygdala, respectively, is well established. We examined, then, the possible pathways that may convey affective visual information to these centers following lesions of V1. We concluded that the pathway leading to pACC, AI, and amygdala involves the deep layers of the superior colliculus, the medial pulvinar, and the superior temporal sulcus region. We suggest that this visual pathway provides an image of the observed affective faces, which, although deteriorated, is sufficient to determine some overt behavior, but not to provide conscious experience of the presented stimuli.

Ipsilateral somatosensory responses in humans: the tonic activity of SII and posterior insular cortex.

In the present study, we mapped the spatio-temporal dynamics of cortical responses to ipsilateral median nerve stimulation using intracerebral recordings (stereo-EEG) in 38 drug-resistant epileptic patients. Furthermore, we compared the pattern of responsiveness obtained in the same leads across ipsilateral and contralateral stimulations. Ipsilateral responses were found mostly confined to SII and posterior insula, while no activity was found in ipsilateral SI. By examining the temporal profiles of activation, ipsilateral SII showed a prominent tonic pattern, while contralateral SII exhibited both phasic and tonic responses. Beyond the localization of the active cortical nodes, these data contributed to identify the cortico-cortical connections carrying the somatosensory information to the ipsilateral hemisphere, with a major role of transcallosal projections from contralateral SII. In light of previous literature and of its localization, the functional role possibly covered by long lasting discharge in SII and insular cortex is also discussed. Overall, the presence of tonic activities was neglected so far due to the impossibility to identify deep sources along with a resolved description of their time course. The use of stereo-EEG, instead, allows one to achieve a four-dimensional characterization, complementing the classical view about the somatosensory system organization.