Dissecting abstract, modality-specific and experience-dependent coding of affect in the human brain.

Emotion and perception are tightly intertwined, as affective experiences often arise from the appraisal of sensory information. Nonetheless, whether the brain encodes emotional instances using a sensory-specific code or in a more abstract manner is unclear. Here, we answer this question by measuring the association between emotion ratings collected during a unisensory or multisensory presentation of a full-length movie and brain activity recorded in typically developed, congenitally blind and congenitally deaf participants. Emotional instances are encoded in a vast network encompassing sensory, prefrontal, and temporal cortices. Within this network, the ventromedial prefrontal cortex stores a categorical representation of emotion independent of modality and previous sensory experience, and the posterior superior temporal cortex maps the valence dimension using an abstract code. Sensory experience more than modality affects how the brain organizes emotional information outside supramodal regions, suggesting the existence of a scaffold for the representation of emotional states where sensory inputs during development shape its functioning.

How Male and Female Literary Authors Write About Affect Across Cultures and Over Historical Periods.

A wealth of literature suggests the existence of sex differences in how emotions are experienced, recognized, expressed, and regulated. However, to what extent these differences result from the put in place of stereotypes and social rules is still a matter of debate. Literature is an essential cultural institution, a transposition of the social life of people but also of their intimate affective experiences, which can serve to address questions of psychological relevance. Here, we created a large corpus of literary fiction enriched by authors' metadata to measure the extent to which culture influences how men and women write about emotion. Our results show that even though before the twenty-first century and across 116 countries women more than men have written about affect, starting from 2000, this difference has diminished substantially. Also, in the past, women's narratives were more positively laden and less arousing. While the difference in arousal is ubiquitous and still present nowadays, sex differences in valence vary as a function of culture and have dissolved in recent years. Altogether, these findings suggest that historic evolution is associated with men and women writing similarly about emotions and reveal a sizable impact of culture on the affective characteristics of the lexicon. Supplementary Information: The online version contains supplementary material available at 10.1007/s42761-023-00219-9.

Information load dynamically modulates functional brain connectivity during narrative listening.

Narratives are paradigmatic examples of natural language, where nouns represent a proxy of information. Functional magnetic resonance imaging (fMRI) studies revealed the recruitment of temporal cortices during noun processing and the existence of a noun-specific network at rest. Yet, it is unclear whether, in narratives, changes in noun density influence the brain functional connectivity, so that the coupling between regions correlates with information load. We acquired fMRI activity in healthy individuals listening to a narrative with noun density changing over time and measured whole-network and node-specific degree and betweenness centrality. Network measures were correlated with information magnitude with a time-varying approach. Noun density correlated positively with the across-regions average number of connections and negatively with the average betweenness centrality, suggesting the pruning of peripheral connections as information decreased. Locally, the degree of the bilateral anterior superior temporal sulcus (aSTS) was positively associated with nouns. Importantly, aSTS connectivity cannot be explained by changes in other parts of speech (e.g., verbs) or syllable density. Our results indicate that the brain recalibrates its global connectivity as a function of the information conveyed by nouns in natural language. Also, using naturalistic stimulation and network metrics, we corroborate the role of aSTS in noun processing.

The structure underlying core affect and perceived affective qualities of human vocal bursts.

Vocal bursts are non-linguistic affectively-laden sounds with a crucial function in human communication, yet their affective structure is still debated. Studies showed that ratings of valence and arousal follow a V-shaped relationship in several kinds of stimuli: high arousal ratings are more likely to go on a par with very negative or very positive valence. Across two studies, we asked participants to listen to 1,008 vocal bursts and judge both how they felt when listening to the sound (i.e. core affect condition), and how the speaker felt when producing it (i.e. perception of affective quality condition). We show that a V-shaped fit outperforms a linear model in explaining the valence-arousal relationship across conditions and studies, even after equating the number of exemplars across emotion categories. Also, although subjective experience can be significantly predicted using affective quality ratings, core affect scores are significantly lower in arousal, less extreme in valence, more variable between individuals, and less reproducible between studies. Nonetheless, stimuli rated with opposite valence between conditions range from 11% (study 1) to 17% (study 2). Lastly, we demonstrate that ambiguity in valence (i.e. high between-participants variability) explains violations of the V-shape and relates to higher arousal.

The Contribution of Shape Features and Demographic Variables to Disembedding Abilities.

Humans naturally perceive visual patterns in a global manner and are remarkably capable of extracting object shapes based on properties such as proximity, closure, symmetry, and good continuation. Notwithstanding the role of these properties in perceptual grouping, studies highlighted differences in disembedding performance across individuals, which are summarized by the field dependence dimension. Evidence suggests that age and educational attainment explain part of this variability, whereas the role of sex is still highly debated. Also, which stimulus features primarily influence inter-individual variations in perceptual grouping has still to be fully determined. Building upon these premises, we assessed the role of age, education level, and sex on performance at the Leuven Embedded Figure Test-a proxy of disembedding abilities-in 391 cisgender individuals. We also investigated to what extent shape symmetry, closure, complexity, and continuation relate to task accuracy. Overall, target asymmetry, closure, and good continuation with the embedding context increase task difficulty. Simpler shapes are more difficult to detect than those with more lines, yet context complexity impairs the recognition of complex targets (i.e., those with 6 lines or more) to a greater extent. Concerning demographic data, we confirm that age and educational attainment are significantly associated with disembedding abilities and reveal a perceptual advantage in males. In summary, our study further highlights the role of shape properties in disembedding performance and unveils sex differences not reported so far.

Default and control network connectivity dynamics track the stream of affect at multiple timescales.

In everyday life, the stream of affect results from the interaction between past experiences, expectations and the unfolding of events. How the brain represents the relationship between time and affect has been hardly explored, as it requires modeling the complexity of everyday life in the laboratory setting. Movies condense into hours a multitude of emotional responses, synchronized across subjects and characterized by temporal dynamics alike real-world experiences. Here, we use time-varying intersubject brain synchronization and real-time behavioral reports to test whether connectivity dynamics track changes in affect during movie watching. The results show that polarity and intensity of experiences relate to the connectivity of the default mode and control networks and converge in the right temporoparietal cortex. We validate these results in two experiments including four independent samples, two movies and alternative analysis workflows. Finally, we reveal chronotopic connectivity maps within the temporoparietal and prefrontal cortex, where adjacent areas preferentially encode affect at specific timescales.

Emotion Regulation Failures Are Preceded by Local Increases in Sleep-like Activity.

Emotion self-regulation relies both on cognitive and behavioral strategies implemented to modulate the subjective experience and/or the behavioral expression of a given emotion. Although it is known that a network encompassing fronto-cingulate and parietal brain areas is engaged during successful emotion regulation, the functional mechanisms underlying failures in emotion suppression (ES) are still unclear. In order to investigate this issue, we analyzed video and high-density EEG recordings of 20 healthy adult participants during an ES and a free expression task performed on two consecutive days. Changes in facial expression during ES, but not free expression, were preceded by local increases in sleep-like activity (1-4 Hz) in brain areas responsible for emotional suppression, including bilateral anterior insula and anterior cingulate cortex, and in right middle/inferior frontal gyrus (p < .05, corrected). Moreover, shorter sleep duration the night before the ES experiment correlated with the number of behavioral errors (p = .03) and tended to be associated with higher frontal sleep-like activity during ES failures (p = .09). These results indicate that local sleep-like activity may represent the cause of ES failures in humans and may offer a functional explanation for previous observations linking lack of sleep, changes in frontal activity, and emotional dysregulation.

The case for preregistering all region of interest (ROI) analyses in neuroimaging research.

In neuroimaging studies, small sample sizes and the resultant reduced statistical power to detect effects that are not large, combined with inadequate analytic choices, concur to produce inflated or false-positive findings. To mitigate these issues, researchers often restrict analyses to specific brain areas, using the region of interest (ROI) approach. Crucially, ROI analysis assumes the a priori justified definition of the target region. Nonetheless, reports often lack details about where in the timeline, ranging from study conception to the data analysis and interpretation of findings, were ROIs selected. Frequently, the rationale for ROI selection is vague or inadequately founded on the existing literature. These shortcomings have important implications for ROI-based studies, augmenting the risk that observed effects are inflated or even false positives. Tools like preregistration and registered reports could address this problem, ensuring the validity of ROI-based studies. The benefits could be enhanced by additional practices such as selection of ROIs using quantitative methods (i.e., meta-analysis) and the sharing of whole-brain unthresholded maps of effect size, as well as of binary ROIs, in publicly accessible repositories.

Emotionotopy in the human right temporo-parietal cortex.

Humans use emotions to decipher complex cascades of internal events. However, which mechanisms link descriptions of affective states to brain activity is unclear, with evidence supporting either local or distributed processing. A biologically favorable alternative is provided by the notion of gradient, which postulates the isomorphism between functional representations of stimulus features and cortical distance. Here, we use fMRI activity evoked by an emotionally charged movie and continuous ratings of the perceived emotion intensity to reveal the topographic organization of affective states. Results show that three orthogonal and spatially overlapping gradients encode the polarity, complexity and intensity of emotional experiences in right temporo-parietal territories. The spatial arrangement of these gradients allows the brain to map a variety of affective states within a single patch of cortex. As this organization resembles how sensory regions represent psychophysical properties (e.g., retinotopy), we propose emotionotopy as a principle of emotion coding.

Brain Hemodynamic Intermediate Phenotype Links Vitamin B12 to Cognitive Profile of Healthy and Mild Cognitive Impaired Subjects.

Vitamin B12, folate, and homocysteine are implicated in pivotal neurodegenerative mechanisms and partake in elders' mental decline. Findings on the association between vitamin-related biochemistry and cognitive abilities suggest that the structural and functional properties of the brain may represent an intermediate biomarker linking vitamin concentrations to cognition. Despite this, no previous study directly investigated whether vitamin B12, folate, and homocysteine levels are sufficient to explain individual neuropsychological profiles or, alternatively, whether the activity of brain regions modulated by these compounds better predicts cognition in elders. Here, we measured the relationship between vitamin blood concentrations, scores at seventeen neuropsychological tests, and brain activity of sixty-five elders spanning from normal to Mild Cognitive Impairment. We then evaluated whether task-related brain responses represent an intermediate phenotype, providing a better prediction of subjects' neuropsychological scores, as compared to the one obtained considering blood biochemistry only. We found that the hemodynamic activity of the right dorsal anterior cingulate cortex was positively associated (p value < 0.05 cluster corrected) with vitamin B12 concentrations, suggesting that elders with higher B12 levels had a more pronounced recruitment of this salience network region. Crucially, the activity of this area significantly predicted subjects' visual search and attention abilities (p value = 0.0023), whereas B12 levels per se failed to do so. Our results demonstrate that the relationship between blood biochemistry and elders' cognitive abilities is revealed when brain activity is included into the equation, thus highlighting the role of brain imaging as intermediate phenotype.

Predictive value of electroencephalography connectivity measures for motor training outcome in multiple sclerosis: an observational longitudinal study.

BACKGROUND: Neurophysiological investigations represent powerful tools to shed light on brain plasticity in multiple sclerosis (MS) patients. AIM: We investigated the relationship between electroencephalography (EEG)-based connectivity, the extent of brain lesions and changes in motor performance after an intensive task-oriented circuit training (TOCT). DESIGN: Observational longitudinal study. SETTING: Outpatients training program. POPULATION: Sixteen MS patients (10F; mean age =51.4 years; range: 27-67; mean disease duration =15.1 years; range: 2-26; mean Expanded Disability Status Scale 4.4; range: 3.5-5.5), were included in our study. METHODS: MS patients with mild gait impairment were evaluated through functional scales and submitted to TOCT. Resting-state EEG was performed before (T0) and after (T1) rehabilitation. Alpha-band weighted Phase Lag Index (wPLI) and broadband weighted Symbolic Mutual Information (wSMI) connectivity analyses were performed. White matter lesion load was measured using MRI prior to the TOCT. Neurophysiological and structural parameters were then related to behavioral changes. RESULTS: Dynamic Gait Index significantly improved after TOCT (F(1,14) =13.10, P=0.003). Moreover, the interaction between TOCT and age was observed for changes in Timed Up and Go (TUG) performance (F(1,14) = 7.75, P=0.015), indicating that older patients only benefited in this measure. Regarding the relationship between EEG connectivity and TOCT outcome, we observed positive correlations between changes in TUG and strength (P=0.017) and efficiency (Pone-tail =0.029) of alpha-band wPLI connectivity at T0. Such correlation was mainly driven by antero-posterior regional interactions (P=0.038), rather than by inter-hemispheric connectivity (P=0.089). Moreover, we observed a positive correlation between performance improvements and wSMI connectivity at T1 (P=0.001) as well as the difference between T0 and T1 (P=0.005). Lesion load percentage was not related to functional improvement after TOCT (Pone-tail=0.137). CONCLUSIONS: Results of the current study demonstrated that baseline alpha-band wPLI connectivity predicts TOCT outcome in MS patients. Moreover, broadband wSMI tracks neural changes that accompany treatment-related variations in motor performance. CLINICAL REHABILITATION IMPACT: Our findings suggest that EEG-based connectivity measures may represent a potential tool for customizing rehabilitative management of the disease.

ROI and phobias: The effect of ROI approach on an ALE meta-analysis of specific phobias.

About 90% of fMRI findings on specific phobias (SP) include analysis of region of interest (ROI). This approach characterized by higher sensitivity may produce inflated results, particularly when findings are aggregated in meta-analytic maps. Here, we conducted a systematic review and activation likelihood estimation (ALE) meta-analysis on SP, testing the impact of the inclusion of ROI-based studies. ALE meta-analyses were carried out either including ROI-based results or focusing on whole-brain voxelwise studies exclusively. To assess the risk of bias in the neuroimaging field, we modified the Newcastle-Ottawa Scale (NOS) and measured the reliability of fMRI findings. Of the 31 selected investigations (564 patients and 485 controls) one-third did not motivate ROI selection: five studies did not report an explicit rationale, whereas four did not cite any specific reference in this regard. Analyses including ROI-based studies revealed differences between phobics and healthy subjects in several regions of the limbic circuit. However, when focusing on whole-brain analysis, only the anterior midcingulate cortex differentiated SP from controls. Notably, 13 studies were labeled with low risk of bias according to the adapted NOS. The inclusion of ROI-based results artificially inflates group differences in fMRI meta-analyses. Moreover, a priori, well-motivated selection of ROIs is desirable to improve quality and reproducibility in SP neuroimaging studies. Lastly, the use of modified NOS may represent a valuable way to assess and evaluate biases in fMRI studies: "low risk" of bias was reported for less than half of the included studies, indicating the need for better practices in fMRI.

Different FDG-PET metabolic patterns at single-subject level in the behavioral variant of fronto-temporal dementia.

BACKGROUND: The diagnosis of probable behavioral variant of fronto-temporal dementia (bvFTD) according to current criteria requires the imaging evidence of frontal and/or anterior temporal atrophy or hypoperfusion/hypometabolism. Different variants of this pattern of brain involvement may, however, be found in individual cases, supporting the presence of heterogeneous phenotypes. OBJECTIVE: We examined in a case-by-case approach the FDG-PET metabolic patterns of patients fulfilling clinical criteria for probable bvFTD, assessing the presence and frequency of specific FDG-PET features. MATERIALS AND METHODS: Fifty two FDG-PET scans of probable bvFTD patients were retrospectively analyzed together with clinical and neuropsychological data. Neuroimaging experts rated the FDG-PET hypometabolism maps obtained at the single-subject level with optimized voxel-based Statistical Parametric Mapping (SPM). The functional metabolic heterogeneity was further tested by hierarchical cluster analysis and principal component analysis (PCA). RESULTS: Both the SPM maps and cluster analysis identified two major variants of cerebral hypometabolism, namely the "frontal" and the "temporo-limbic", which were correlated with different cognitive profiles. Executive and language deficits were the cognitive hallmark in the "frontal" subgroup, while poor encoding and recall on long-term memory tasks was typical of the "temporo-limbic" subgroup. DISCUSSION: SPM single-subject analysis indicates distinct patterns of brain dysfunction in bvFTD, coupled with specific clinical features, suggesting different profiles of neurodegenerative vulnerability. These findings have important implications for the early diagnosis of bvFTD and for the application of the recent international consensus criteria.

Differential Impairment of Cognitive and Affective Mentalizing Abilities in Neurodegenerative Dementias: Evidence from Behavioral Variant of Frontotemporal Dementia, Alzheimer's Disease, and Mild Cognitive Impairment.

Cognitive and affective theory of mind (ToM) can be impaired in the course of neurodegenerative dementias. Experimental tests based on different task conditions and/or complexity may fail to capture disease-specific patterns of impairments. In this study, we assessed with a single task both the affective and the cognitive facets of ToM ability in a sample of 47 patients (i.e., 12 AD, 20 bvFTD, and 15 aMCI fulfilling IWG criteria for AD in predementia phase) and 65 healthy controls. Subjects were administered the Story-based Empathy task (SET), a non-verbal task measuring the ability to infer others' intentions (IA) and emotions (EA) compared to a control condition (causal inferences, CI). Global and single sub-condition scores were evaluated with a vectorial method, analyzing the relationship between social abilities and basic cognitive functioning by means of two indices representing the basic ability to perform the task and the balance between basic functions and ToM skills.Dementia (AD and bvFTD) patients showed impaired performances on all SET sub-conditions, whereas aMCI subjects' performance was not different from healthy controls. Vectorial analysis revealed a specific change in the balance between EA and CI conditions only in the bvFTD group, supporting a disproportionate deficit in mental states attribution based on affective cues. The overall deficit in the task in AD appears to be more general and related to the severity of dementia. This latter finding is further supported by the normal performance of the prodromal AD group.

Right Limbic FDG-PET Hypometabolism Correlates with Emotion Recognition and Attribution in Probable Behavioral Variant of Frontotemporal Dementia Patients.

The behavioural variant of frontotemporal dementia (bvFTD) is a rare disease mainly affecting the social brain. FDG-PET fronto-temporal hypometabolism is a supportive feature for the diagnosis. It may also provide specific functional metabolic signatures for altered socio-emotional processing. In this study, we evaluated the emotion recognition and attribution deficits and FDG-PET cerebral metabolic patterns at the group and individual levels in a sample of sporadic bvFTD patients, exploring the cognitive-functional correlations. Seventeen probable mild bvFTD patients (10 male and 7 female; age 67.8±9.9) were administered standardized and validated version of social cognition tasks assessing the recognition of basic emotions and the attribution of emotions and intentions (i.e., Ekman 60-Faces test-Ek60F and Story-based Empathy task-SET). FDG-PET was analysed using an optimized voxel-based SPM method at the single-subject and group levels. Severe deficits of emotion recognition and processing characterized the bvFTD condition. At the group level, metabolic dysfunction in the right amygdala, temporal pole, and middle cingulate cortex was highly correlated to the emotional recognition and attribution performances. At the single-subject level, however, heterogeneous impairments of social cognition tasks emerged, and different metabolic patterns, involving limbic structures and prefrontal cortices, were also observed. The derangement of a right limbic network is associated with altered socio-emotional processing in bvFTD patients, but different hypometabolic FDG-PET patterns and heterogeneous performances on social tasks at an individual level exist.

A novel task assessing intention and emotion attribution: Italian standardization and normative data of the Story-based Empathy Task.

Theory of Mind (ToM), the process by which an individual imputes mental states to himself and others, is presently considered as a multidimensional cognitive domain, with two main facets (i.e., cognitive and affective ToM) accounting, respectively, for the ability to understand others' intention (intention attribution-IA) and emotions (emotion attribution-EA). Despite the large amount of literature investigating the behavioural and neural bases of mentalizing abilities in neurological conditions, there is still a lack of validated neuropsychological tools specifically designed to assess such skills. Here, we report the normative data of the Story-Based Empathy Task (SET), a non-verbal test developed for the assessment of intention and emotion attribution in the neurodegenerative conditions characterized by the impairment of social-emotional abilities. It is an easy-to-administer task including 18 stimuli, sub-grouped into two experimental conditions assessing, respectively, the ability to infer others' intentions (SET-IA) and emotions (SET-EA), compared to a control condition of causal inference (SET-CI). Normative data were collected in 136 Italian subjects pooled across subgroups homogenous for age (range 20-79 years), sex, and education (at least 5 years). The results show a detrimental effect of age and a beneficial effect of education on both the global score and each subscale, for which we provide correction grids. This new task could be a useful tool to investigate both affective and cognitive aspects of ToM in the course of disorders of socio-emotional behaviour, such as the fronto-temporal dementia spectrum.