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

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

Cerebellar contribution to emotional body language perception: A TMS study

Consistent evidence suggests that the cerebellum contributes to the processing of emotional facial expressions. However, it is not yet known whether the cerebellum is recruited when emotions are expressed by body postures or movements, or whether it is recruited differently for positive and negative emotions. In this study, we asked healthy participants to discriminate between body postures (with masked face) expressing emotions of opposite valence (happiness vs anger, Experiment 1), or of the same valence (negative: anger vs sadness; positive: happiness vs surprise, Experiment 2). While performing the task, participants received online transcranial magnetic stimulation (TMS) over a region of the posterior left cerebellum and over two control sites (early visual cortex and vertex). We found that TMS over the cerebellum affected participants' ability to discriminate emotional body postures, but only when one of the emotions was negatively valenced (i.e. anger). These findings suggest that the cerebellar region we stimulated is involved in processing the emotional content conveyed by body postures and gestures. Our findings complement prior evidence on the role of the cerebellum in emotional face processing and have important implications from a clinical perspective, where non-invasive cerebellar stimulation is a promising tool for the treatment of motor, cognitive and affective deficits

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 Impact of the Perception of Primary Facial Emotions on Corticospinal Excitability

The link between emotional experience and motor body responses has long been acknowledged. A well-established approach to exploring the effect of the perception of emotional stimuli on the motor system is measuring variations in the excitability of the corticospinal tract (CSE) through motor-evoked potentials (MEP) elicited via transcranial magnetic stimulation (TMS). Previous evidence has indicated a selective increase in MEP amplitude while participants view emotional stimuli, such as emotional facial expressions, compared to neutral cues. However, it is still not clear whether this effect depends on the specific emotional meaning conveyed by the stimulus. In the present study, we explored whether viewing faces expressing the primary emotions compared to faces with a neutral expression affects individuals’ CSE, measured using TMS-elicited MEPs. Specifically, we elicited MEPs from the left motor cortex (M1) while participants passively viewed the same faces expressing either anger, fear, disgust, happiness, sadness, surprise, and no emotion (in different blocks). We found that the observation of fearful, angry, disgusted, and happy facial expressions was associated with a significant increase in the MEPs’ amplitude compared to neutral facial expressions, with a comparable enhancement in the CSE occurring across these emotions. In turn, viewing sad and surprised faces did not modulate the CSE. Overall, our findings suggest that only facial expressions that signal (real or potential) danger or a rewarding stimulus, but not emotional facial expressions per se, are capable of activating action-related mechanisms

The left posterior cerebellum is involved in orienting attention along the mental number line: An online-TMS study

Although converging evidence suggests that the posterior cerebellum is involved in visuospatial functions and in the orienting of attention, a clear topography of cerebellar regions causally involved in the control of spatial attention is still missing. In this study, we aimed to shed light on this issue by using online neuronavigated transcranial magnetic stimulation (TMS) to temporarily interfere with posterior medial (Vermis lobule VII) and left lateral (Crus I/II) cerebellar activity during a task measuring visuospatial (landmark task, Experiment 1 and 2) and representational (number bisection task, Experiment 2) asymmetries in the orienting of attention. At baseline, participants showed attentional biases consistent with the literature, that is a leftward and upward bias with horizontal and vertical lines, respectively, and a leftward bias in number bisection. Critically, TMS over the left cerebellar hemisphere significantly counteracted pseudoneglect in the number bisection task, whilst not affecting attentional biases in the landmark task. In turn, TMS over the posterior vermis did not affect performance in either task. Taken together, our findings suggest that the left posterior cerebellar hemisphere (but not the posterior vermis) is a critical node of an extended brain network subtending the control of spatial attention, at least when attention needs to be allocated to an internal representational space and a certain degree of mental manipulation is required (as in the number bisection task)

The effect of cognitive load on horizontal and vertical spatial asymmetries

Healthy individuals typically show a leftward attentional bias in the allocation of spatial attention along the horizontal plane, a phenomenon known as pseudoneglect, which relies on a right hemispheric dominance for visuospatial processing. Also, healthy individuals tend to overestimate the upper hemispace when orienting attention along the vertical plane, a phenomenon that may depend on asymmetric ventral and dorsal visual streams activation. Previous research has demonstrated that when attentional resources are reduced due to increased cognitive load, pseudoneglect is attenuated (or even reversed), due to decreased right-hemispheric activations. Critically, whether and how the reduction of attentional resources under load modulates vertical spatial asymmetries has not been addressed before. We asked participants to perform a line bisection task both with and without the addition of a concurrent auditory working memory task with lines oriented either horizontally or vertically. Results showed that increasing cognitive load reduced the typical leftward/upward bias with no difference between orientations. Our data suggest that the degree of cognitive load affects spatial attention not only in the horizontal but also in the vertical plane. Lastly, the similar effect of load on horizontal and vertical judgements suggests these biases may be related to only partially independent mechanisms.Andrea Ciricugno, Megan L. Bartlett, Owen S. Gwinn, Daniel J. Carragher and Michael E.R. Nicholl

Distinct cerebellar regions for body motion discrimination

Visual processing of human movements is critical for adaptive social behavior. Cerebellar activations have been observed during biological motion discrimination in prior neuroimaging studies, and cerebellar lesions may be detrimental for this task. However, whether the cerebellum plays a causal role in biological motion discrimination has never been tested. Here, we addressed this issue in three different experiments by interfering with the posterior cerebellar lobe using transcranial magnetic stimulation (TMS) during a biological discrimination task. In Experiments 1 and 2, we found that TMS delivered at onset of the visual stimuli over the vermis (vermal lobule VI), but not over the left cerebellar hemisphere (left lobule VI/Crus I), interfered with participants' ability to distinguish biological from scrambled motion compared to stimulation of a control site (vertex). Interestingly, when stimulation was delivered at a later time point (300 ms after stimulus onset), participants performed worse when TMS was delivered over the left cerebellar hemisphere compared to the vermis and the vertex (Experiment 3). Our data show that the posterior cerebellum is causally involved in biological motion discrimination and suggest that different sectors of the posterior cerebellar lobe may contribute to the task at different time points

The effect of blindness on spatial asymmetries

The human cerebral cortex is asymmetrically organized with hemispheric lateralization pervading nearly all neural systems of the brain. Whether the lack of normal visual development affects hemispheric specialization subserving the deployment of visuospatial attention asymmetries is controversial. In principle, indeed, the lack of early visual experience may affect the lateralization of spatial functions, and the blind may rely on a different sensory input compared to the sighted. In this review article, we thus present a current state-of-the-art synthesis of empirical evidence concerning the effects of visual deprivation on the lateralization of various spatial processes (i.e., including line bisection, mirror symmetry, and localization tasks). Overall, the evidence reviewed indicates that spatial processes are supported by a right hemispheric network in the blind, hence, analogously to the sighted. Such a right-hemisphere dominance, however, seems more accentuated in the blind as compared to the sighted as indexed by the greater leftward bias shown in different spatial tasks. This is possibly the result of the more pronounced involvement of the right parietal cortex during spatial tasks in blind individuals compared to the sighted, as well as of the additional recruitment of the right occipital cortex, which would reflect the cross-modal plastic phenomena that largely characterize the blind brain