Functional Segregation of the Human Cerebellum in Social Cognitive Tasks Revealed by TMS.

The role of the posterior cerebellum in social cognition is well established; however, it is still unclear whether different cerebellar subregions contribute to different social cognitive processes by exerting specific functions. Here, we employed transcranial magnetic stimulation (TMS) in male and female healthy humans to test the hypothesis of the existence of a medial-to-lateral gradient in the functional organization of the posterior cerebellum, according to which the phylogenetically newer cerebellar hemispheres are involved in tasks requiring higher-level social inferences whereas vermal/medial sectors are involved in basic perceptual emotional mechanisms. We found that interfering via TMS with activity of the medial cerebellum significantly impaired basic emotional recognition/discrimination. In turn, only TMS over the lateral cerebellum affected a task requiring recognizing an emotion considering the social context in which it was experienced. Overall, our data support the existence of a medial-to-lateral gradient in the posterior cerebellum, with medial sectors supporting basic emotion recognition and lateral sectors being recruited when the task taps on higher inferential processing/mentalizing. Interestingly, the contribution of the cerebellum in these different processes seems to be restricted to negative emotional stimuli.SIGNIFICANCE STATEMENT The cerebellum has been recently recognized as a critical component of the social brain, however, the functional topography of this structure in relation to social and emotional processes is still debated. By adopting a causative approach through the use of transcranial magnetic stimulation (TMS), the present study critically insights into the functional organization of the posterior cerebellum by testing the hypothesis of a medial-to-lateral gradient that reflects increasing complexity of social cognitive processes. Our findings demonstrate that lateral and medial cerebellar regions exert partially distinguishable functions in the social cognitive domain, with the medial cerebellum that mainly mediates basic perceptual emotional mechanisms while the lateral cerebellum, although supporting more basic functions, further subserves higher-level social operations.

The Evolution of the Optimization of Cognitive and Social Functions in the Cerebellum and Thereby the Rise of Homo sapiens Through Cumulative Culture.

The evolution of the prominent role of the cerebellum in the development of composite tools, and cumulative culture, leading to the rise of Homo sapiens is examined. Following Stout and Hecht's (2017) detailed description of stone-tool making, eight key repetitive involvements of the cerebellum are highlighted. These key cerebellar learning involvements include the following: (1) optimization of cognitive-social control, (2) prediction (3) focus of attention, (4) automaticity of smoothness, appropriateness, and speed of movement and cognition, (5) refined movement and social cognition, (6) learns models of extended practice, (7) learns models of Theory of Mind (ToM) of teachers, (8) is predominant in acquisition of novel behavior and cognition that accrues from the blending of cerebellar models sent to conscious working memory in the cerebral cortex. Within this context, the evolution of generalization and blending of cerebellar internal models toward optimization of social-cognitive learning is described. It is concluded that (1) repetition of movement and social cognition involving the optimization of internal models in the cerebellum during stone-tool making was the key selection factor toward social-cognitive and technological advancement, (2) observational learning during stone-tool making was the basis for both technological and social-cognitive evolution and, through an optimizing positive feedback loop between the cerebellum and cerebral cortex, the development of cumulative culture occurred, and (3) the generalization and blending of cerebellar internal models related to the unconscious forward control of the optimization of imagined future states in working memory was the most important brain adaptation leading to intertwined advances in stone-tool technology, cognitive-social processes behind cumulative culture (including the emergence of language and art) and, thereby, with the rise of Homo sapiens.

Cerebellar Neurostimulation for Boosting Social and Affective Functions: Implications for the Rehabilitation of Hereditary Ataxia Patients.

Beyond motor deficits, spinocerebellar ataxia (SCA) patients also suffer cognitive decline and show socio-affective difficulties, negatively impacting on their social functioning. The possibility to modulate cerebello-cerebral networks involved in social cognition through cerebellar neurostimulation has opened up potential therapeutic applications for ameliorating social and affective difficulties. The present review offers an overview of the research on cerebellar neurostimulation for the modulation of socio-affective functions in both healthy individuals and different clinical populations, published in the time period 2000-2022. A total of 25 records reporting either transcranial magnetic stimulation (TMS) or transcranial direct current stimulation (tDCS) studies were found. The investigated clinical populations comprised different pathological conditions, including but not limited to SCA syndromes. The reviewed evidence supports that cerebellar neurostimulation is effective in improving social abilities in healthy individuals and reducing social and affective symptoms in different neurological and psychiatric populations associated with cerebellar damage or with impairments in functions that involve the cerebellum. These findings encourage to further explore the rehabilitative effects of cerebellar neurostimulation on socio-affective deficits experienced by patients with cerebellar abnormalities, as SCA patients. Nevertheless, conclusions remain tentative at this stage due to the heterogeneity characterizing stimulation protocols, study methodologies and patients' samples.

Direct reciprocity and reputation shape trust decisions similarly in blind and sighted individuals.

This study addresses the effects of blindness on trust. Using an auditory version of the multi-round Trust Game, we investigated the effect of reputation and reciprocity on trust decisions in early blind and sighted participants. During each round of the game, participants were endowed with a sum of money and had to decide how much they wanted to invest in their partners, who were manipulated as a function of their good or bad reputation and individualistic or cooperative behavior. The data showed that negative first impression about the partner (bad reputation and/or selfish behavior) impacted more blind participants than sighted ones. However, following repeated interactions with the partners, the overall mean investment aligned between the blind and sighted groups. We interpret these findings as suggesting that blindness may guide participants to a more cautionary behavior when dealing with partners with negative initial characteristics.

Social perception in deaf individuals: A meta-analysis of neuroimaging studies.

Deaf individuals may report difficulties in social interactions. However, whether these difficulties depend on deafness affecting social brain circuits is controversial. Here, we report the first meta-analysis comparing brain activations of hearing and (prelingually) deaf individuals during social perception. Our findings showed that deafness does not impact on the functional mechanisms supporting social perception. Indeed, both deaf and hearing control participants recruited regions of the action observation network during performance of different social tasks employing visual stimuli, and including biological motion perception, face identification, action observation, viewing, identification and memory for signs and lip reading. Moreover, we found increased recruitment of the superior-middle temporal cortex in deaf individuals compared with hearing participants, suggesting a preserved and augmented function during social communication based on signs and lip movements. Overall, our meta-analysis suggests that social difficulties experienced by deaf individuals are unlikely to be associated with brain alterations but may rather depend on non-supportive environments.

Cerebellar Contribution to Emotional Body Language Perception.

Body language is a powerful form of non-verbal communication providing important information about the emotions and intentions of others. The ability to infer other's emotions from their bodily movements and postures recruits an extended network in the brain that encompasses both cortical and subcortical regions. In this chapter, we review recent evidence suggesting that the cerebellum is a critical node of this network. Specifically, we present convergent findings from patients', neuroimaging and non-invasive brain stimulation studies that have shown that the cerebellum is involved in both biological motion perception and in discrimination of bodily emotional expressions. We discuss the potential underlying mechanisms that drive the recruitment of the sensorimotor (anterior) and cognitive (posterior) cerebellum in inferring others' emotions through their bodily movements and postures and how the cerebellum may exert these functions within different cortico-cerebellar and limbic-cerebellar networks dedicated to body language perception.

The Cerebellum and Beauty: The Impact of the Cerebellum in Art Experience and Creativity.

There is growing interest in the cerebellum's contributions to higher order functions of the human brain. When considering specific activities of the human cerebellum related to art, we differentiate two broad areas. Neural activity within different locations of the cerebellum is involved in art perception and in artistic creativity. The cerebellum plays an underappreciated role in neuroaesthetics, including the perception and evaluation of art objects, their appreciation and affective aesthetic experience. Certain areas of the cerebellum presumably are of particular relevance, incorporating cognitive and affective issues within large-scaled neural networks in perceiving and appraising artworks. For art creativity, many investigations report cerebellar implementations. Important areas in these domains are evolutionary younger parts of the cerebellar hemispheres, in particular the lobule VII with its Crus I and II, influencing crucial networks such as the Default Mode Network in optimizing creativity. These structures help guide pattern recognition and in art appreciation as they may play a role in predicting ongoing neural network activities through a crucial frontoparietal axis. In this chapter, we consider how our current neuroscientific understanding of cerebellar functions point to a likely role of the cerebellum in art appreciation and creativity.

TMS over the posterior cerebellum modulates motor cortical excitability in response to facial emotional expressions.

Evidence suggests that the posterior cerebellum is involved in emotional processing. Specific mechanisms by which the cerebellum contributes to the perception of and reaction to the emotional state of others are not well-known. It is likely that perceived emotions trigger anticipatory/preparatory motor changes. However, the extent to which the cerebellum modulates the activity of the motor cortex to contribute to emotional processing has not been directly investigated. In this study, we assessed whether the activity of the posterior cerebellum influences the modulation of motor cortical excitability in response to emotional stimuli. To this end, we transiently disrupted the neural activity of the left posterior cerebellum using 1 Hz repetitive transcranial magnetic stimulation (rTMS) and examined its effect on motor cortical excitability witnessed during emotional face processing (in comparison to the effects of sham rTMS). Motor excitability was measured as TMS-based motor evoked potentials (MEPs) recorded from bilateral first dorsal interosseous (FDI) muscles during the viewing of negative emotional (i.e. fearful) and neutral facial expressions. In line with previous evidence, we found that MEP amplitude was increased during the viewing of fearful compared to neutral faces. Critically, when left posterior cerebellar activity was transiently inhibited with 1 Hz rTMS, we observed a reduction in amplitude of MEPs recorded from the contralateral (right) motor cortex during the viewing of emotional (but not neutral) faces. In turn, inhibition of the left posterior cerebellum did not affect the amplitude of MEPs recorded from the ipsilateral motor cortex. Our findings suggest that the posterolateral (left) cerebellum modulates motor cortical response to negative emotional stimuli and may serve as an interface between limbic, cognitive, and motor systems.

Overlapping and specific neural correlates for empathizing, affective mentalizing, and cognitive mentalizing: A coordinate-based meta-analytic study.

While the discussion on the foundations of social understanding mainly revolves around the notions of empathy, affective mentalizing, and cognitive mentalizing, their degree of overlap versus specificity is still unclear. We took a meta-analytic approach to unveil the neural bases of cognitive mentalizing, affective mentalizing, and empathy, both in healthy individuals and pathological conditions characterized by social deficits such as schizophrenia and autism. We observed partially overlapping networks for cognitive and affective mentalizing in the medial prefrontal, posterior cingulate, and lateral temporal cortex, while empathy mainly engaged fronto-insular, somatosensory, and anterior cingulate cortex. Adjacent process-specific regions in the posterior lateral temporal, ventrolateral, and dorsomedial prefrontal cortex might underpin a transition from abstract representations of cognitive mental states detached from sensory facets to emotionally-charged representations of affective mental states. Altered mentalizing-related activity involved distinct sectors of the posterior lateral temporal cortex in schizophrenia and autism, while only the latter group displayed abnormal empathy related activity in the amygdala. These data might inform the design of rehabilitative treatments for social cognitive deficits.

Social cognition in the blind brain: A coordinate-based meta-analysis.

Social cognition skills are typically acquired on the basis of visual information (e.g., the observation of gaze, facial expressions, gestures). In light of this, a critical issue is whether and how the lack of visual experience affects neurocognitive mechanisms underlying social skills. This issue has been largely neglected in the literature on blindness, despite difficulties in social interactions may be particular salient in the life of blind individuals (especially children). Here we provide a meta-analysis of neuroimaging studies reporting brain activations associated to the representation of self and others' in early blind individuals and in sighted controls. Our results indicate that early blindness does not critically impact on the development of the "social brain," with social tasks performed on the basis of auditory or tactile information driving consistent activations in nodes of the action observation network, typically active during actual observation of others in sighted individuals. Interestingly though, activations along this network appeared more left-lateralized in the blind than in sighted participants. These results may have important implications for the development of specific training programs to improve social skills in blind children and young adults.

Consensus Paper: Cerebellum and Social Cognition.

The traditional view on the cerebellum is that it controls motor behavior. Although recent work has revealed that the cerebellum supports also nonmotor functions such as cognition and affect, only during the last 5 years it has become evident that the cerebellum also plays an important social role. This role is evident in social cognition based on interpreting goal-directed actions through the movements of individuals (social "mirroring") which is very close to its original role in motor learning, as well as in social understanding of other individuals' mental state, such as their intentions, beliefs, past behaviors, future aspirations, and personality traits (social "mentalizing"). Most of this mentalizing role is supported by the posterior cerebellum (e.g., Crus I and II). The most dominant hypothesis is that the cerebellum assists in learning and understanding social action sequences, and so facilitates social cognition by supporting optimal predictions about imminent or future social interaction and cooperation. This consensus paper brings together experts from different fields to discuss recent efforts in understanding the role of the cerebellum in social cognition, and the understanding of social behaviors and mental states by others, its effect on clinical impairments such as cerebellar ataxia and autism spectrum disorder, and how the cerebellum can become a potential target for noninvasive brain stimulation as a therapeutic intervention. We report on the most recent empirical findings and techniques for understanding and manipulating cerebellar circuits in humans. Cerebellar circuitry appears now as a key structure to elucidate social interactions.

Neural correlates of visual aesthetic appreciation: insights from non-invasive brain stimulation.

During the last decade, non-invasive brain stimulation techniques have been increasingly employed in the field of neuroaesthetics research to shed light on the possible causal role of different brain regions contributing to aesthetic appreciation. Here, I review studies that have employed transcranial magnetic stimulation (TMS) and transcranial direct current stimulation (tDCS) to investigate neurocognitive mechanisms mediating visual aesthetic appreciation for different stimuli categories (faces, bodies, paintings). The review first considers studies that have assessed the possible causal contribution of cortical regions in mediating aesthetic appreciation along the visual ventral and dorsal pathways (i.e., the extrastriate body area, the motion-sensitive region V5/MT+ , the lateral occipital complex and the posterior parietal cortex). It then considers TMS and tDCS studies that have targeted premotor and motor regions, as well as other areas involved in body and facial expression processing (such as the superior temporal sulcus and the somatosensory cortex) to assess their role in aesthetic evaluation. Finally, it discusses studies that have targeted medial and dorsolateral prefrontal regions leading to significant changes in aesthetic appreciation for both biological stimuli (faces and bodies) and artworks. Possible mechanisms mediating stimulation effects on aesthetic judgments are discussed. A final section considers both methodological limitations of the reviewed studies (including levels of statistical power and the need for further replication) and the future potential for non-invasive brain stimulation to significantly contribute to the understanding of the neural bases of visual aesthetic experiences.

Medial prefrontal cortex involvement in aesthetic appreciation of paintings: a tDCS study.

Among the brain regions involved in the aesthetic evaluation of paintings, the prefrontal cortex seems to play a pivotal role. In particular, consistent neuroimaging evidence indicates that activity in the dorsolateral prefrontal cortex (mainly in the left hemisphere) and in medial and orbital sectors of the prefrontal cortex is linked to viewing aesthetically pleasing images. In this study, we focused on the contribution of the medial prefrontal cortex (mPFC) in mediating aesthetic decisions about paintings. We found that enhancing excitability in this region via anodal tDCS led participants to judge paintings as more beautiful. Although significant, the effects were moderate, possibly due to the neutral affective value of the artworks we used, suggesting that activity in mPFC may be critically dependent on the affective impact of the paintings.

The role of the cerebellum in explicit and incidental processing of facial emotional expressions: A study with transcranial magnetic stimulation.

Growing evidence suggests that the cerebellum plays a critical role in non-motor functions, contributing to cognitive and affective processing. In particular, the cerebellum might represent an important node of the "limbic" network, underlying not only emotion regulation but also emotion perception and recognition. Here, we used transcranial magnetic stimulation (TMS) to shed further light on the role of the cerebellum in emotional perception by specifically testing cerebellar contribution to explicit and incidental emotional processing. In particular, in three different experiments, we found that TMS over the (left) cerebellum impaired participants' ability to categorize facial emotional expressions (explicit task) and to classify the gender of emotional faces (incidental emotional processing task), but not the gender of neutral faces. Overall, our results indicate that the cerebellum is involved in perceiving the emotional content of facial stimuli, even when this is task irrelevant.

Early blindness is associated with increased volume of the uncinate fasciculus.

Growing evidence demonstrates dramatic structural and functional neuroplastic changes in individuals born with early-onset blindness. For example, cross-modal sensory processing at the level of the occipital cortex appears to be associated with adaptive behaviors in the blind. However, detailed studies examining the structural properties of key white matter pathways in other regions of the brain remain limited. Given that blind individuals rely heavily on their sense of hearing, we examined the structural properties of two important pathways involved with auditory processing, namely the uncinate and arcuate fasciculi. High angular resolution diffusion imaging (HARDI) tractography was used to examine structural parameters (i.e., tract volume and quantitative anisotropy, or QA) of these two fasciculi in a sample of 13 early blind individuals and 14 normally sighted controls. Compared to controls, early blind individuals showed a significant increase in the volume of the left uncinate fasciculus. A small area of increased QA was also observed halfway along the right arcuate fasciculus in the blind group. These findings contribute to our knowledge regarding the broad neuroplastic changes associated with profound early blindness.

TMS over the superior temporal sulcus affects expressivity evaluation of portraits.

When viewing a portrait, we are often captured by its expressivity, even if the emotion depicted is not immediately identifiable. If the neural mechanisms underlying emotion processing of real faces have been largely clarified, we still know little about the neural basis of evaluation of (emotional) expressivity in portraits. In this study, we aimed at assessing-by means of transcranial magnetic stimulation (TMS)-whether the right superior temporal sulcus (STS) and the right somatosensory cortex (SC), that are important in discriminating facial emotion expressions, are also causally involved in the evaluation of expressivity of portraits. We found that interfering via TMS with activity in (the face region of) right STS significantly reduced the extent to which portraits (but not other paintings depicting human figures with faces only in the background) were perceived as expressive, without, though, affecting their liking. In turn, interfering with activity of the right SC had no impact on evaluating either expressivity or liking of either paintings' category. Our findings suggest that evaluation of emotional cues in artworks recruit (at least partially) the same neural mechanisms involved in processing genuine biological others. Moreover, they shed light on the neural basis of liking decisions in art by art-naïve people, supporting the view that aesthetic appreciation relies on a multitude of factors beyond emotional evaluation.

Dorsomedial prefrontal cortex and cerebellar contribution to in-group attitudes: a transcranial magnetic stimulation study.

We tend to express more positive judgments and behaviors toward individuals belonging to our own group compared to other (out-) groups. In this study, we assessed the role of the cerebellum and of the dorsomedial prefrontal cortex (dmPFC) - two regions critically implicated in social cognition processes - in mediating implicit valenced attitudes toward in-group and out-group individuals. To this aim, we used transcranial magnetic stimulation (TMS) in combination with a standard attitude priming task, in which Caucasian participants had to categorize the valence of a series of adjectives primed by either an in-group or an out-group face. In two behavioral experiments, we found an in-group bias (i.e. faster categorization of positive adjectives when preceded by in-group faces) but no evidence of an out-group bias. Interestingly, TMS over both the dmPFC and over the (right) cerebellum significantly interfered with the modulation exerted by group membership on adjective valence classification, abolishing the in-group bias observed at baseline. Overall, our data suggest that both the dmPFC and the cerebellum play a causal role in mediating implicit social attitudes.

Common framework for "virtual lesion" and state-dependent TMS: The facilitatory/suppressive range model of online TMS effects on behavior.

The behavioral effects of Transcranial Magnetic Stimulation (TMS) are often nonlinear; factors such as stimulation intensity and brain state can modulate the impact of TMS on observable behavior in qualitatively different manner. Here we propose a theoretical framework to account for these effects. In this model, there are distinct intensity ranges for facilitatory and suppressive effects of TMS - low intensities facilitate neural activity and behavior whereas high intensities induce suppression. The key feature of the model is that these ranges are shifted by changes in neural excitability: consequently, a TMS intensity, which normally induces suppression, can have a facilitatory effect if the stimulated neurons are being inhibited by ongoing task-related processes or preconditioning. For example, adaptation reduces excitability of adapted neurons; the outcome is that TMS intensities which inhibit non-adapted neurons induce a facilitation on adapted neural representations, leading to reversal of adaptation effects. In conventional "virtual lesion" paradigms, similar effects occur because neurons not involved in task-related processes are inhibited by the ongoing task. The resulting reduction in excitability can turn high intensity "inhibitory" TMS to low intensity "facilitatory" TMS for these neurons, and as task-related neuronal representations are in the inhibitory range, the outcome is a reduction in signal-to-noise ratio and behavioral impairment.

The Dorsomedial Prefrontal Cortex Plays a Causal Role in Integrating Social Impressions from Faces and Verbal Descriptions.

Several neuroimaging studies point to a key role of the dorsomedial prefrontal cortex (dmPFC) in the formation of socially relevant impressions. In 3 different experiments, participants were required to form socially relevant impressions about other individuals on the basis of text descriptions of their social behaviors, and to decide whether a face alone, a trait adjective (e.g., "selfish"), or a face presented with a trait adjective was consistent or inconsistent with the impression they had formed. Before deciding whether the target stimulus matched the impression they had previously formed, participants received transcranial magnetic stimulation (TMS) over the dmPFC, the inferior frontal gyrus (IFG, also implicated in social impression formation), or over a control site (vertex). Results from the 3 experiments converged in showing that interfering with dmPFC activity significantly delayed participants in responding whether a face-adjective pair was consistent with the impression they had formed. No effects of TMS were observed following stimulation of the IFG or when evaluations had to be made on faces or trait adjectives presented alone. Our findings critically extend previous neuroimaging evidence by indicating a causal role of the dmPFC in creating coherent impressions based on the integration of face and verbal description of social behaviors.

The causal role of the occipital face area (OFA) and lateral occipital (LO) cortex in symmetry perception.

Symmetry is an important cue in face and object perception. Here we used fMRI-guided transcranial magnetic stimulation (TMS) to shed light on the role of the occipital face area (OFA), a key region in face processing, and the lateral occipital (LO) cortex, a key area in object processing, in symmetry detection. In the first experiment, we applied TMS over the rightOFA, its left homolog (leftOFA), rightLO, and vertex (baseline) while participants were discriminating between symmetric and asymmetric dot patterns. Stimulation of rightOFA and rightLO impaired performance, causally implicating these two regions in detection of symmetry in low-level dot configurations. TMS over rightLO but not rightOFA also significantly impaired detection of nonsymmetric shapes defined by collinear Gabor patches, demonstrating that rightOFA responds to symmetry but not to all cues mediating figure-ground segregation. The second experiment showed a causal role for rightOFA but not rightLO in facial symmetry detection. Overall, our results demonstrate that both the rightOFA and rightLO are sensitive to symmetry in dot patterns, whereas only rightOFA is causally involved in facial symmetry detection.