Seeing Through Each Other's Hearts: Inferring Others' Heart Rate as a Function of Own Heart Rate Perception and Perceived Social Intelligence.

Successful social interactions require a good understanding of the emotional states of other people. This information is often not directly communicated but must be inferred. As all emotional experiences are also imbedded in the visceral or interoceptive state of the body (i.e., accelerating heart rate during arousal), successfully inferring the interoceptive states of others may open a window into their emotional state. But how well can people do that? Here, we replicate recent results showing that people can discriminate between the cardiac states (i.e., the resting heartrate) of other people by simply looking at them. We further tested whether the ability to infer the interoceptive states of others depends on one's own interoceptive abilities. We measured people's performance in a cardioception task and their self-reported interoceptive accuracy. Whilst neither was directly associated to their ability to infer the heartrate of another person, we found a significant interaction. Specifically, overestimating one's own interoceptive capacities was associated with a worse performance at inferring the heartrate of others. In contrast, underestimating one's own interoceptive capacities did not have such influence. This pattern suggests that deficient beliefs about own interoceptive capacities can have detrimental effects on inferring the interoceptive states of other people. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-022-00151-4.

Active tactile discrimination is coupled with and modulated by the cardiac cycle.

Perception and cognition are modulated by the phase of the cardiac signal in which the stimuli are presented. This has been shown by locking the presentation of stimuli to distinct cardiac phases. However, in everyday life sensory information is not presented in this passive and phase-locked manner, instead we actively move and control our sensors to perceive the world. Whether active sensing is coupled and modulated with the cardiac cycle remains largely unknown. Here, we recorded the electrocardiograms of human participants while they actively performed a tactile grating orientation task. We show that the duration of subjects' touch varied as a function of the cardiac phase in which they initiated it. Touches initiated in the systole phase were held for longer periods of time than touches initiated in the diastole phase. This effect was most pronounced when elongating the duration of the touches to sense the most difficult gratings. Conversely, while touches in the control condition were coupled to the cardiac cycle, their length did not vary as a function of the phase in which these were initiated. Our results reveal that we actively spend more time sensing during systole periods, the cardiac phase associated with lower perceptual sensitivity (vs. diastole). In line with interoceptive inference accounts, these results indicate that we actively adjust the acquisition of sense data to our internal bodily cycles.

Most of what is known about human senses comes from experiments under laboratory conditions where participants stay still and stimuli are presented to them by the scientists. However, this approach does not reflect what happens in real life as we move around, changing the position of our eyes, heads and hands, to actively sense the world. Our perception also changes depending on what is going on inside our bodies and minds at any one time. For instance, our sensitivity to touch varies during the two phases of our heartbeat: people are less perceptive to being touched during systole (when the heart ejects blood), compared to when they are touched during diastole (when the heart refills with blood). But it was unclear if this relationship influences how we actively touch and sense objects. For instance, do people seek touch in a particular phase of their heartbeat, and how does this change their response to the object? To investigate, Galvez-Pol et al. traced people's heartbeats while they actively touched different objects. Without looking, the participants had to work out whether the objects had vertical or horizontal grooves. Although they did not start their touches in a specific phase of the heartbeat, their hearts did influence their behaviour. If they started the touch during systole, they held their fingers over the object for longer. The effect was especially noticeable when it was difficult to discriminate the objects' grooves. Galvez-Pol et al. reasoned that this was down to participants having to compensate for the loss in touch sensitivity during the systole phase of their heartbeat. This suggests that people actively adjust how they acquire sensory information, such as touch, based on how their bodily functions alter their senses. These findings provide a starting point for future studies investigating how internal bodily fluctuations impact how we sense and respond to things in real world scenarios. This could potentially shed light on the differences between the way neurotypical and neurodivergent individuals sense the world.

People can identify the likely owner of heartbeats by looking at individuals' faces.

For more than a century it has been proposed that visceral and vasomotor changes inside the body influence and reflect our experience of the world. For instance, cardiac rhythms (heartbeats and consequent heart rate) reflect psychophysiological processes that underlie our cognition and affective experience. Yet, considering that we usually infer what others do and feel through vision, whether people can identify the most likely owner of a given bodily rhythm by looking at someone's face remains unknown. To address this, we developed a novel two-alternative forced-choice task in which 120 participants watched videos showing two people side by side and visual feedback from one of the individuals' heartbeats in the centre. Participants' task was to select the owner of the depicted heartbeats. Across five experiments, one replication, and supplementary analyses, the results show that: i) humans can judge the most likely owner of a given sequence of heartbeats significantly above chance levels, ii) that performance in such a task decreases when the visual properties of the faces are altered (inverted, masked, static), and iii) that the difference between the heart rates of the individuals portrayed in our 2AFC task seems to contribute to participants' responses. While we did not disambiguate the type of information used by the participants (e.g., knowledge about appearance and health, visual cues from heartbeats), the current work represents the first step to investigate the possible ability to infer or perceive others' cardiac rhythms. Overall, our novel observations and easily adaptable paradigm may generate hypotheses worth examining in the study of human and social cognition.

Emotional representations of space vary as a function of peoples' affect and interoceptive sensibility.

Most research on people's representation of space has focused on spatial appraisal and navigation. But there is more to space besides navigation and assessment: people have different emotional experiences at different places, which create emotionally tinged representations of space. Little is known about the emotional representation of space and the factors that shape it. The purpose of this study was to develop a graphic methodology to study the emotional representation of space and some of the environmental features (non-natural vs. natural) and personal features (affective state and interoceptive sensibility) that modulate it. We gave participants blank maps of the region where they lived and asked them to apply shade where they had happy/sad memories, and where they wanted to go after Covid-19 lockdown. Participants also completed self-reports on affective state and interoceptive sensibility. By adapting methods for analyzing neuroimaging data, we examined shaded pixels to quantify where and how strong emotions are represented in space. The results revealed that happy memories were consistently associated with similar spatial locations. Yet, this mapping response varied as a function of participants' affective state and interoceptive sensibility. Certain regions were associated with happier memories in participants whose affective state was more positive and interoceptive sensibility was higher. The maps of happy memories, desired locations to visit after lockdown, and regions where participants recalled happier memories as a function of positive affect and interoceptive sensibility overlayed significantly with natural environments. These results suggest that people's emotional representations of their environment are shaped by the naturalness of places, and by their affective state and interoceptive sensibility.

Reduced differentiation of emotion-associated bodily sensations in autism.

LAY ABSTRACT: More research has been conducted on how autistic people understand and interpret other people's emotions, than on how autistic people experience their own emotions. The experience of emotion is important however, because it can relate to difficulties like anxiety and depression, which are common in autism. In neurotypical adults and children, different emotions have been associated with unique maps of activity patterns in the body. Whether these maps of emotion are comparable in autism is currently unknown. Here, we asked 100 children and adolescents, 45 of whom were autistic, to color in outlines of the body to indicate how they experienced seven emotions. Autistic adults and children sometimes report differences in how they experience their internal bodily states, termed interoception, and so we also investigated how this related to the bodily maps of emotion. In this study, the autistic children and adolescents had comparable interoception to the non-autistic children and adolescents, but there was less variability in their maps of emotion. In other words, they showed more similar patterns of activity across the different emotions. This was not related to interoception, however. This work suggests that there are differences in how autistic people experience emotion that are not explained by differences in interoception. In neurotypical people, less variability in emotional experiences is linked to anxiety and depression, and future work should seek to understand if this is a contributing factor to the increased prevalence of these difficulties in autism.

Active sampling in visual search is coupled to the cardiac cycle.

Recent research has demonstrated that perception and reasoning vary according to the phase of internal bodily signals such as heartbeat. This has been shown by locking the presentation of sensory events to distinct phases of the cardiac cycle. However, task-relevant information is not usually encountered in such a phase-locked manner nor passively accessed, but rather actively sampled at one's own pace. Moreover, if the phase of the cardiac cycle is an important modulator of perception and cognition, as previously proposed, then the way in which we actively sample the world should be similarly modulated by the phase of the cardiac cycle. Here we tested this by coregistration of eye movements and heartbeat signals while participants freely compared differences between two visual arrays. Across three different analyses, we found a significant coupling of saccades, subsequent fixations, and blinks with the cardiac cycle. More eye movements were generated during the systolic phase of the cardiac cycle, which has been reported as the period of maximal effect of the baroreceptors' activity upon cognition. Conversely, more fixations were found during the diastole phase (quiescent baroreceptors). Lastly, more blinks were generated in the later period of the cardiac cycle. These results suggest that interoceptive and exteroceptive processing do adjust to each other; in our case, by sampling the outer environment during quiescent periods of the inner organism.

Dopaminergic Modulation of Sensory Attenuation in Parkinson's Disease: Is There an Underlying Modulation of Beta Power?

Background and Aims: Pathological high amplitude of beta oscillations is thought as the underlying mechanism of motor symptoms in Parkinson's disease (PD), in particular with regard to bradykinesia. In addition, abnormality in a neurophysiological phenomenon labeled sensory attenuation has been found in patients with PD. The current study explored the hypothesis that the abnormal sensory attenuation has a causal link with the typical abnormality in beta oscillations in PD. Methods: The study tested sixteen right-handed patients with a diagnosis of PD and 22 healthy participants, which were matched by age and gender. Somatosensory evoked potentials were elicited through electrical stimulation of the median nerve at the wrist. Electrical activity was recorded at the scalp using a 128 channels EEG. Somatosensory evoked potentials were recorded in 2 conditions: at rest and at the onset of a voluntary movement, which was a self-paced abduction movement of the right thumb. Results: Healthy participants showed a reduction of the N20-P25 amplitude at the onset of the right thumb abduction compared to the rest condition (P < 0.05). When patients were OFF medication, they showed mild reduction of the N20-P25 component at movement onset (P < 0.05). On the contrary, they did show greater attenuation of the N20-P25 component at the onset of movement compared to the rest condition when ON medication (P < 0.05). There was no significant evidence of a link between the degree of sensory attenuation and the change in beta oscillations in our cohort of patients. Conclusion: These results confirmed a significant link between dopaminergic modulation and sensory attenuation. However, the sensory attenuation and beta oscillations were found as two independent phenomena.

Voluntary tic suppression and the normalization of motor cortical beta power in Gilles de la Tourette syndrome: an EEG study.

Gilles de la Tourette syndrome (GTS) is a neurological condition characterized by motor and vocal tics. Previous studies suggested that this syndrome is associated with abnormal sensorimotor cortex activity at rest, as well as during the execution of voluntary movements. It has been hypothesized that this abnormality might be interpreted as a form of increased tonic inhibition, probably to suppress tics; however, this hypothesis has not been tested so far. The present study was designed to formally test how voluntary tic suppression in GTS influences the activity of the sensorimotor cortex during the execution of a motor task. We used EEG to record neural activity over the contralateral sensorimotor cortex during a finger movement task in adult GTS patients, in both free ticcing and tic suppression conditions; these data were then compared with those collected during the same task in age-matched healthy subjects. We focused on the levels of activity in the beta frequency band, which is typically associated with the activation of the motor system, during three different phases: a pre-movement, a movement, and a post-movement phase. GTS patients showed decreased levels of beta modulation with respect to the healthy controls, during the execution of the task; however, this abnormal pattern returned to be normal when they were explicitly asked to suppress their tics while moving. This is the first demonstration that voluntary tic suppression in GTS operates through the normalization of the EEG rhythm in the beta frequency range during the execution of a voluntary finger movement.

The functional neuroanatomy of emotion processing in frontotemporal dementias.

Impaired processing of emotional signals is a core feature of frontotemporal dementia syndromes, but the underlying neural mechanisms have proved challenging to characterize and measure. Progress in this field may depend on detecting functional changes in the working brain, and disentangling components of emotion processing that include sensory decoding, emotion categorization and emotional contagion. We addressed this using functional MRI of naturalistic, dynamic facial emotion processing with concurrent indices of autonomic arousal, in a cohort of patients representing all major frontotemporal dementia syndromes relative to healthy age-matched individuals. Seventeen patients with behavioural variant frontotemporal dementia [four female; mean (standard deviation) age 64.8 (6.8) years], 12 with semantic variant primary progressive aphasia [four female; 66.9 (7.0) years], nine with non-fluent variant primary progressive aphasia [five female; 67.4 (8.1) years] and 22 healthy controls [12 female; 68.6 (6.8) years] passively viewed videos of universal facial expressions during functional MRI acquisition, with simultaneous heart rate and pupillometric recordings; emotion identification accuracy was assessed in a post-scan behavioural task. Relative to healthy controls, patient groups showed significant impairments (analysis of variance models, all P < 0.05) of facial emotion identification (all syndromes) and cardiac (all syndromes) and pupillary (non-fluent variant only) reactivity. Group-level functional neuroanatomical changes were assessed using statistical parametric mapping, thresholded at P < 0.05 after correction for multiple comparisons over the whole brain or within pre-specified regions of interest. In response to viewing facial expressions, all participant groups showed comparable activation of primary visual cortex while patient groups showed differential hypo-activation of fusiform and posterior temporo-occipital junctional cortices. Bi-hemispheric, syndrome-specific activations predicting facial emotion identification performance were identified (behavioural variant, anterior insula and caudate; semantic variant, anterior temporal cortex; non-fluent variant, frontal operculum). The semantic and non-fluent variant groups additionally showed complex profiles of central parasympathetic and sympathetic autonomic involvement that overlapped signatures of emotional visual and categorization processing and extended (in the non-fluent group) to brainstem effector pathways. These findings open a window on the functional cerebral mechanisms underpinning complex socio-emotional phenotypes of frontotemporal dementia, with implications for novel physiological biomarker development.

Sensorimotor beta power reflects the precision-weighting afforded to sensory prediction errors.

It has been proposed that accurate motor control relies on Bayesian inference that integrates sensory input with prior contextual knowledge (Bays and Wolpert, 2007; Körding and Wolpert, 2004; Wolpert et al., 1995). Recent evidence has suggested that modulations in beta power (∼12-30 Hz) measured over sensorimotor cortices using electroencephalography (EEG) may represent parameters of Bayesian inference. While the well characterised post-movement beta synchronisation has been shown to correlate with prediction error (H. Tan, Jenkinson, & Brown, 2014; Huiling Tan, Wade, & Brown, 2016), recent evidence suggests that beta power may also represent uncertainty measures (Tan et al., 2016; Tzagarakis et al., 2015). The current study aimed to measure the neurophysiological correlates of uncertainty mediating Bayesian updating during a visuomotor adaptation paradigm in healthy human participants. In particular, sensory uncertainty was directly modulated to measure its effect on sensorimotor beta power. Participant's behaviour was modelled using the Hierarchical Gaussian Filter (HGF) in order to extract the latent variables involved in learning actions required by the task and correlate these with the measured EEG. We found that sensorimotor beta power correlated with inverse uncertainty afforded to sensory prediction errors both prior to and following a movement. This suggests that sensorimotor beta oscillations may more readily represent relative uncertainty within the sensorimotor system rather than error. Neurophysiological models describing the generation of beta oscillations offer a potential mechanism by which this neural signature may encode latent uncertainty parameters. This is essential for understanding how the brain controls behaviour.

Emotional facedness in Parkinson's disease.

People with Parkinson's disease (PD) have a deficit of facial expression. Previous studies indicate that hemispheric dominance for emotional processing can give rise to an asymmetric pattern of facial expression of emotion. In this study, we aimed to evaluate possible asymmetry in facial emotion expressivity in PD. Twenty PD patients and twenty healthy controls were video-recorded while posing the 6 basic emotions. The most expressive pictures were derived from the videos and chimeric faces were created. Nine healthy raters were asked to judge which of the two chimeras looked more expressive. Chosen responses, reaction times and confidence levels were the main outcome measures. We evaluated possible differences in these measures within each group and between groups (PD, healthy controls). We assessed possible correlations between a global facial laterality index (pooling all emotions together) as well as facial laterality indexes for each emotion and the body laterality index, accounting for the predominant side of limb bradykinesia in patients. There was no difference in outcome measures when evaluating the two hemifaces within PD patients and healthy controls or between the two groups (all Ps > 0.05). In PD patients there was a correlation between the global facial laterality index and the body laterality index (R = - 0.39, P = 0.01), suggesting that the most expressive hemiface corresponded to the less affected body side. The results of our study do not support the hypothesis of hemisphere predominance in regulating facial emotion expressions and provides novel information on altered facial emotion expression in PD.

Alexithymia mediates the relationship between interoceptive sensibility and anxiety.

A number of empirical and theoretical reports link altered interoceptive processing to anxiety. However, the mechanistic understanding of the relationship between the two remains poor. We propose that a heightened sensibility for interoceptive signals, combined with a difficulty in attributing these sensations to emotions, increases an individual's vulnerability to anxiety. In order to investigate this, a large sample of general population adults were recruited and completed self-report measures of interoceptive sensibility, trait anxiety and alexithymia. Results confirmed that the positive association between interoceptive sensibility and trait anxiety was partially mediated by alexithymia, such that those most at risk for clinically significant levels of trait anxiety have both significantly higher levels of interoceptive sensibility and alexithymia. A subsequent factor analysis confirmed the independence of the three measures. Altered interoceptive processing in combination with alexithymia, increased the risk for anxiety above and beyond altered interoceptive processing alone. We suggest that a heightened sensibility for interoceptive signals, combined with a difficulty in attributing these sensations to emotions, leaves these sensations vulnerable to catastrophizing interpretation. Interventions that target the attribution of bodily sensations may prove valuable in reducing anxiety.

High-frequency peripheral vibration decreases completion time on a number of motor tasks.

A recent theoretical account of motor control proposes that modulation of afferent information plays a role in affecting how readily we can move. Increasing the estimate of uncertainty surrounding the afferent input is a necessary step in being able to move. It has been proposed that an inability to modulate the gain of this sensory information underlies the cardinal symptoms of Parkinson's disease (PD). We aimed to test this theory by modulating the uncertainty of the proprioceptive signal using high-frequency peripheral vibration, to determine the subsequent effect on motor performance. We investigated if this peripheral stimulus might modulate oscillatory activity over the sensorimotor cortex in order to understand the mechanism by which peripheral vibration can change motor performance. We found that 80 Hz peripheral vibration applied to the right wrist of a total of 54 healthy human participants reproducibly improved performance across four separate randomised experiments on a number of motor control tasks (nine-hole peg task, box and block test, reaction time task and finger tapping). Improved performance on all motor tasks (except the amplitude of finger tapping) was also seen for a sample of 18PD patients ON medication. EEG data investigating the effect of vibration on oscillatory activity revealed a significant decrease in beta power (15-30 Hz) over the contralateral sensorimotor cortex at the onset and offset of 80 Hz vibration. This finding is consistent with a novel theoretical account of motor initiation, namely that modulating uncertainty of the proprioceptive afferent signal improves motor performance potentially by gating the incoming sensory signal and allowing for top-down proprioceptive predictions.

Cardiac responses to viewing facial emotion differentiate frontotemporal dementias.

OBJECTIVE: To establish proof-of-principle for the use of heart rate responses as objective measures of degraded emotional reactivity across the frontotemporal dementia spectrum, and to demonstrate specific relationships between cardiac autonomic responses and anatomical patterns of neurodegeneration. METHODS: Thirty-two patients representing all major frontotemporal dementia syndromes and 19 healthy older controls performed an emotion recognition task, viewing dynamic, naturalistic videos of facial emotions while ECG was recorded. Cardiac reactivity was indexed as the increase in interbeat interval at the onset of facial emotions. Gray matter associations of emotional reactivity were assessed using voxel-based morphometry of patients' brain MR images. RESULTS: Relative to healthy controls, all patient groups had impaired emotion identification, whereas cardiac reactivity was attenuated in those groups with predominant fronto-insular atrophy (behavioral variant frontotemporal dementia and nonfluent primary progressive aphasia), but preserved in syndromes focused on the anterior temporal lobes (right temporal variant frontotemporal dementia and semantic variant primary progressive aphasia). Impaired cardiac reactivity correlated with gray matter atrophy in a fronto-cingulo-insular network that overlapped correlates of cognitive emotion processing. INTERPRETATION: Autonomic indices of emotional reactivity dissociate from emotion categorization ability, stratifying frontotemporal dementia syndromes and showing promise as novel biomarkers. Attenuated cardiac responses to the emotions of others suggest a core pathophysiological mechanism for emotional blunting and degraded interpersonal reactivity in these diseases.

Neurophysiological Changes Measured Using Somatosensory Evoked Potentials.

Measurements of somatosensory evoked potentials (SEPs), recorded using electroencephalography during different phases of movement, have been fundamental in understanding the neurophysiological changes related to motor control. SEP recordings have also been used to investigate adaptive plasticity changes in somatosensory processing related to active and observational motor learning tasks. Combining noninvasive brain stimulation with SEP recordings and intracranial SEP depth recordings, including recordings from deep brain stimulation electrodes, has been critical in identifying neural areas involved in specific temporal stages of somatosensory processing. Consequently, this fundamental information has furthered our understanding of the maladaptive plasticity changes related to pathophysiology of diseases characterized by abnormal movements, such as Parkinson's disease, dystonia, and functional movement disorders.

Motor signatures of emotional reactivity in frontotemporal dementia.

Automatic motor mimicry is essential to the normal processing of perceived emotion, and disrupted automatic imitation might underpin socio-emotional deficits in neurodegenerative diseases, particularly the frontotemporal dementias. However, the pathophysiology of emotional reactivity in these diseases has not been elucidated. We studied facial electromyographic responses during emotion identification on viewing videos of dynamic facial expressions in 37 patients representing canonical frontotemporal dementia syndromes versus 21 healthy older individuals. Neuroanatomical associations of emotional expression identification accuracy and facial muscle reactivity were assessed using voxel-based morphometry. Controls showed characteristic profiles of automatic imitation, and this response predicted correct emotion identification. Automatic imitation was reduced in the behavioural and right temporal variant groups, while the normal coupling between imitation and correct identification was lost in the right temporal and semantic variant groups. Grey matter correlates of emotion identification and imitation were delineated within a distributed network including primary visual and motor, prefrontal, insular, anterior temporal and temporo-occipital junctional areas, with common involvement of supplementary motor cortex across syndromes. Impaired emotional mimesis may be a core mechanism of disordered emotional signal understanding and reactivity in frontotemporal dementia, with implications for the development of novel physiological biomarkers of socio-emotional dysfunction in these diseases.

Impaired Interoceptive Accuracy in Semantic Variant Primary Progressive Aphasia.

BACKGROUND: Interoception (the perception of internal bodily sensations) is strongly linked to emotional experience and sensitivity to the emotions of others in healthy subjects. Interoceptive impairment may contribute to the profound socioemotional symptoms that characterize frontotemporal dementia (FTD) syndromes, but remains poorly defined. METHODS: Patients representing all major FTD syndromes and healthy age-matched controls performed a heartbeat counting task as a measure of interoceptive accuracy. In addition, patients had volumetric MRI for voxel-based morphometric analysis, and their caregivers completed a questionnaire assessing patients' daily-life sensitivity to the emotions of others. RESULTS: Interoceptive accuracy was impaired in patients with semantic variant primary progressive aphasia relative to healthy age-matched individuals, but not in behavioral variant frontotemporal dementia and nonfluent variant primary progressive aphasia. Impaired interoceptive accuracy correlated with reduced daily-life emotional sensitivity across the patient cohort, and with atrophy of right insula, cingulate, and amygdala on voxel-based morphometry in the impaired semantic variant group, delineating a network previously shown to support interoceptive processing in the healthy brain. CONCLUSION: Interoception is a promising novel paradigm for defining mechanisms of reduced emotional reactivity, empathy, and self-awareness in neurodegenerative syndromes and may yield objective measures for these complex symptoms.