Individual differences in the evaluation of ambiguous visual and auditory threat-related expressions.

This study investigated the neural correlates of the judgement of auditory and visual ambiguous threat-related information, and the influence of state anxiety on this process. Healthy subjects were scanned using a fast, high-resolution functional magnetic resonance imaging (fMRI) multiband sequence while they performed a two-alternative forced-choice emotion judgement task on faces and vocal utterances conveying explicit anger or fear, as well as ambiguous ones. Critically, the latter was specific to each subject, obtained through a morphing procedure and selected prior to scanning following a perceptual decision-making task. Behavioural results confirmed a greater task-difficulty for subject-specific ambiguous stimuli and also revealed a judgement bias for visual fear, and, to a lesser extent, for auditory anger. Imaging results showed increased activity in regions of the salience and frontoparietal control networks (FPCNs) and deactivation in areas of the default mode network for ambiguous, relative to explicit, expressions. In contrast, the right amygdala (AMG) responded more strongly to explicit stimuli. Interestingly, its response to the same ambiguous stimulus depended on the subjective judgement of the expression. Finally, we found that behavioural and neural differences between ambiguous and explicit expressions decreased as a function of state anxiety scores. Taken together, our results show that behavioural and brain responses to emotional expressions are determined not only by emotional clarity but also modality and the subjects' subjective perception of the emotion expressed, and that some of these responses are modulated by state anxiety levels.

Human motor sequence learning drives transient changes in network topology and hippocampal connectivity early during memory consolidation.

In the last decade, the exclusive role of the hippocampus in human declarative learning has been challenged. Recently, we have shown that gains in performance observed in motor sequence learning (MSL) during the quiet rest periods interleaved with practice are associated with increased hippocampal activity, suggesting a role of this structure in motor memory reactivation. Yet, skill also develops offline as memory stabilizes after training and overnight. To examine whether the hippocampus contributes to motor sequence memory consolidation, here we used a network neuroscience strategy to track its functional connectivity offline 30 min and 24 h post learning using resting-state functional magnetic resonance imaging. Using a graph-analytical approach we found that MSL transiently increased network modularity, reflected in an increment in local information processing at 30 min that returned to baseline at 24 h. Within the same time window, MSL decreased the connectivity of a hippocampal-sensorimotor network, and increased the connectivity of a striatal-premotor network in an antagonistic manner. Finally, a supervised classification identified a low-dimensional pattern of hippocampal connectivity that discriminated between control and MSL data with high accuracy. The fact that changes in hippocampal connectivity were detected shortly after training supports a relevant role of the hippocampus in early stages of motor memory consolidation.

Overactivation of posterior insular, postcentral and temporal regions during preserved experience of envy in autism.

Social emotions are critical to successfully navigate in a complex social world because they promote self-regulation of behaviour. Difficulties in social behaviour are at the core of autism spectrum disorder (ASD). However, social emotions and their neural correlates have been scarcely investigated in this population. In particular, the experience of envy has not been addressed in ASD despite involving neurocognitive processes crucially compromised in this condition. Here, we used an fMRI adapted version of a well-validated task to investigate the subjective experience of envy and its neural correlates in adults with ASD (n = 30) in comparison with neurotypical controls (n = 28). Results revealed that both groups reported similarly intense experience of envy in association with canonical activation in the anterior cingulate cortex and the anterior insula, among other regions. However, in participants with ASD, the experience of envy was accompanied by overactivation of the posterior insula, the postcentral gyrus and the posterior superior temporal gyrus, regions subserving the processing of painful experiences and mentalizing. This pattern of results suggests that individuals with ASD may use compensatory strategies based on the embodied amplification of pain and additional mentalizing efforts to shape their subjective experience of envy. Results have relevant implications to better understand the heterogeneity of this condition and to develop new intervention targets.

Brain structural correlates of psychopathic traits in elite female combat-sports athletes.

Psychopathy is characterized by glibness and superficial charm, as well as a lack of empathy, guilt and remorse, and is often accompanied by antisocial behaviour. The cerebral bases of this syndrome have been mostly studied in violent subjects or those with a criminal history. However, the antisocial component of psychopathy is not central to its conceptualization, and in fact, psychopathic traits are present in well-adjusted, non-criminal individuals within the general population. Interestingly, certain psychopathy characteristics appear to be particularly pronounced in some groups or professions. Importantly, as these so-called adaptive or successful psychopaths do not show antisocial tendencies or have significant psychiatric comorbidities, they may represent an ideal population to study this trait. Here, we investigated such a group, specifically elite female judo athletes, and compared them with matched non-athletes. Participants completed psychopathy, anger, perspective-taking and empathic concern questionnaires and underwent structural magnetic resonance imaging (MRI). Grey matter volume (GMV) was computed using voxel-based morphometry from the T1-weighted images. Athletes scored significantly higher in primary psychopathy and anger and lower in empathy and perspective taking. They also exhibited smaller GMV in the right temporal pole, left occipital cortex and left amygdala/hippocampus. GMV values for the latter cluster significantly correlated with primary psychopathy scores across both groups. These results confirm and extend previous findings to a little-studied population and provide support for the conceptualization of psychopathy as a dimensional personality trait which not only is not necessarily associated with antisocial behaviour but may potentially have adaptive value.

Rapid hippocampal plasticity supports motor sequence learning.

Recent evidence suggests that gains in performance observed while humans learn a novel motor sequence occur during the quiet rest periods interleaved with practice (micro-offline gains, MOGs). This phenomenon is reminiscent of memory replay observed in the hippocampus during spatial learning in rodents. Whether the hippocampus is also involved in the production of MOGs remains currently unknown. Using a multimodal approach in humans, here we show that activity in the hippocampus and the precuneus increases during the quiet rest periods and predicts the level of MOGs before asymptotic performance is achieved. These functional changes were followed by rapid alterations in brain microstructure in the order of minutes, suggesting that the same network that reactivates during the quiet periods of training undergoes structural plasticity. Our work points to the involvement of the hippocampal system in the reactivation of procedural memories.

Improving Spatial Normalization of Brain Diffusion MRI to Measure Longitudinal Changes of Tissue Microstructure in the Cortex and White Matter.

BACKGROUND: Fractional anisotropy (FA) and mean diffusivity (MD) are frequently used to evaluate longitudinal changes in white matter (WM) microstructure. Recently, there has been a growing interest in identifying experience-dependent plasticity in gray matter using MD. Improving registration has thus become a major goal to enhance the detection of subtle longitudinal changes in cortical microstructure. PURPOSE: To optimize normalization of diffusion tensor images (DTI) to improve registration in gray matter and reduce variability associated with multisession registrations. STUDY TYPE: Prospective longitudinal study. SUBJECTS: Twenty-one healthy subjects (18-31 years old) underwent nine MRI scanning sessions each. FIELD STRENGTH/SEQUENCE: 3.0T, diffusion-weighted multiband-accelerated sequence, MP2RAGE sequence. ASSESSMENT: Diffusion-weighted images were registered to standard space using different pipelines that varied in the features used for normalization, namely, the nonlinear registration algorithm (FSL vs. ANTs), the registration target (FA-based vs. T1 -based templates), and the use of intermediate individual (FA-based or T1 -based) targets. We compared the across-session test-retest reproducibility error of these normalization approaches for FA and MD in white and gray matter. STATISTICAL TESTS: Reproducibility errors were compared using a repeated-measures analysis of variance with pipeline as the within-subject factor. RESULTS: The registration of FA data to the FMRIB58 FA atlas using ANTs yielded lower reproducibility errors in white matter (P < 0.0001) with respect to FSL. Moreover, using the MNI152 T1 template as the target of registration resulted in lower reproducibility errors for MD (P < 0.0001), whereas the FMRIB58 FA template performed better for FA (P < 0.0001). Finally, the use of an intermediate individual template improved reproducibility when registration of the FA images to the MNI152 T1 was carried out within modality (FA-FA) (P < 0.05), but not via a T1 -based individual template. DATA CONCLUSION: A normalization approach using ANTs to register FA images to the MNI152 T1 template via an individual FA template minimized test-retest reproducibility errors both for gray and white matter. LEVEL OF EVIDENCE: 1 TECHNICAL EFFICACY STAGE: 1 J. Magn. Reson. Imaging 2020;52:766-775.

Multivariate fMRI pattern analysis of fear perception across modalities.

The emotional expression of fear can be processed through a number of modalities, and of varying forms, however, much of the functional imaging literature has centered on investigating fear as expressed through faces. Findings point to an active involvement of the amygdala, and remain fairly consistent in other studies of unimodal fear perception; however, few studies have looked at within-subject cross-modal responses to fear. Thus, we approached this inquiry by testing 30 healthy young adults with fast, high-resolution fMRI, recording the neural responses of fear perception, as expressed through faces, bodies, prosody, and vocalizations. The study was analyzed using a multivariate approach (multi-voxel pattern analysis) and yielded a significant distinction in the responses associated with the perception of fearful vs. neutral emotions. Calculated weights highlighted areas in the amygdala and surrounding subcortical structures as contributing the greatest to the discrimination; however, a whole-brain analysis was necessary to obtain above-chance classification accuracy, suggesting that processing fear across modalities likely involves a broad, distributed network. Thus, our findings support a multivariate approach to studying a highly complex construct such as emotion, as it accounts for multiple voxels simultaneously and can accommodate the high subject-level variability that oftentimes comes with studying emotion perception.

Singing in the brain: Neural representation of music and voice as revealed by fMRI.

The ubiquity of music across cultures as a means of emotional expression, and its proposed evolutionary relation to speech, motivated researchers to attempt a characterization of its neural representation. Several neuroimaging studies have reported that specific regions in the anterior temporal lobe respond more strongly to music than to other auditory stimuli, including spoken voice. Nonetheless, because most studies have employed instrumental music, which has important acoustic distinctions from human voice, questions still exist as to the specificity of the observed "music-preferred" areas. Here, we sought to address this issue by testing 24 healthy young adults with fast, high-resolution fMRI, to record neural responses to a large and varied set of musical stimuli, which, critically, included a capella singing, as well as purely instrumental excerpts. Our results confirmed that music; vocal or instrumental, preferentially engaged regions in the superior STG, particularly in the anterior planum polare, bilaterally. In contrast, human voice, either spoken or sung, activated more strongly a large area along the superior temporal sulcus. Findings were consistent between univariate and multivariate analyses, as well as with the use of a "silent" sparse acquisition sequence that minimizes any potential influence of scanner noise on the resulting activations. Activity in music-preferred regions could not be accounted for by any basic acoustic parameter tested, suggesting these areas integrate, likely in a nonlinear fashion, a combination of acoustic attributes that, together, result in the perceived musicality of the stimuli, consistent with proposed hierarchical processing of complex auditory information within the temporal lobes.

Early selectivity for vocal and musical sounds: electrophysiological evidence from an adaptation paradigm.

There is growing interest in characterizing the neural basis of music perception and, in particular, assessing how similar, or not, it is to that of speech. To further explore this question, we employed an EEG adaptation paradigm in which we compared responses to short sounds belonging to the same category, either speech (pseudo-sentences) or music (piano or violin), depending on whether they were immediately preceded by a same- or different-category sound. We observed a larger reduction in the N100 component magnitude in response to musical sounds when they were preceded by music (either the same or different instrument) than by speech. In contrast, the N100 amplitude was not affected by the preceding stimulus category in the case of speech. For P200 component, we observed a diminution of amplitude when speech sounds were preceded speech, compared to music. No such decrease was found when we compared the responses to music sounds. These differences in the processing of speech and music are consistent with the proposal that some degree of category selectivity for these two classes of complex stimuli already occurs at early stages of auditory processing, possibly subserved by partly separated neuronal populations.

Human amygdala activation during rapid eye movements of rapid eye movement sleep: an intracranial study.

The amygdaloid complex plays a crucial role in processing emotional signals and in the formation of emotional memories. Neuroimaging studies have shown human amygdala activation during rapid eye movement sleep (REM). Stereotactically implanted electrodes for presurgical evaluation in epileptic patients provide a unique opportunity to directly record amygdala activity. The present study analysed amygdala activity associated with REM sleep eye movements on the millisecond scale. We propose that phasic activation associated with rapid eye movements may provide the amygdala with endogenous excitation during REM sleep. Standard polysomnography and stereo-electroencephalograph (SEEG) were recorded simultaneously during spontaneous sleep in the left amygdala of four patients. Time-frequency analysis and absolute power of gamma activity were obtained for 250 ms time windows preceding and following eye movement onset in REM sleep, and in spontaneous waking eye movements in the dark. Absolute power of the 44-48 Hz band increased significantly during the 250 ms time window after REM sleep rapid eye movements onset, but not during waking eye movements. Transient activation of the amygdala provides physiological support for the proposed participation of the amygdala in emotional expression, in the emotional content of dreams and for the reactivation and consolidation of emotional memories during REM sleep, as well as for next-day emotional regulation, and its possible role in the bidirectional interaction between REM sleep and such sleep disorders as nightmares, anxiety and post-traumatic sleep disorder. These results provide unique, direct evidence of increased activation of the human amygdala time-locked to REM sleep rapid eye movements.

Neural activity related to self-initiating elaborative semantic encoding in associative memory.

During episodic memory encoding, elaborative encoding strategies have been related to greater performance on later memory tests. However, many clinical populations display a deficit in self-initiating encoding strategies. We designed an fMRI study to examine the neural correlates of self-initiating elaborative encoding. Twenty-three healthy participants were presented triads of objects in which either neither, one or both objects in the bottom of the triad were related to the top object, and given two encoding instructions that required them to indicate the number of semantic ("related?") or physical ("smaller?") relationships in the triad. Reaction time decreased with more semantic relationships for both encoding instructions, indicating that semantic analysis was performed during the non-semantic encoding task. Recognition memory was better for the semantic encoding condition ("related?"), but there was no modulation of the number of semantic links on memory performance for either encoding condition. We performed a conjunction analysis on the fMRI data to find areas with greater activity for the non-semantic>semantic encoding tasks that were modulated by increasing semantic relationships during non-semantic encoding. Activity was found in the left dorsolateral prefrontal cortex (DLPFC) and bilaterally in the supramarginal gyrus. We suggest that the DLPFC is the most likely candidate region for the self-initiation of elaborative encoding while the supramarginal activity is likely related to attentional effects.

The effects of emotion on memory for music and vocalisations.

Music is a powerful tool for communicating emotions which can elicit memories through associative mechanisms. However, it is currently unknown whether emotion can modulate memory for music without reference to a context or personal event. We conducted three experiments to investigate the effect of basic emotions (fear, happiness, and sadness) on recognition memory for music, using short, novel stimuli explicitly created for research purposes, and compared them with nonlinguistic vocalisations. Results showed better memory accuracy for musical clips expressing fear and, to some extent, happiness. In the case of nonlinguistic vocalisations we confirmed a memory advantage for all emotions tested. A correlation between memory accuracy for music and vocalisations was also found, particularly in the case of fearful expressions. These results confirm that emotional expressions, particularly fearful ones, conveyed by music can influence memory as has been previously shown for other forms of expressions, such as faces and vocalisations.

Differential effects of trait anger on optimism and risk behaviour.

It has been proposed that angry people exhibit optimistic risk estimates about future events and, consequently, are biased towards making risk-seeking choices. The goal of this study was to directly test the hypothesised effect of trait anger on optimism and risk-taking behaviour. One hundred healthy volunteers completed questionnaires about personality traits, optimism and risk behaviour. In addition their risk tendency was assessed with the Balloon Analogue Risk Task (BART), which provides an online measure of risk behaviour. Our results partly confirmed the relation between trait anger and outcome expectations of future life events, but suggest that this optimism does not necessarily translate into actual risk-seeking behaviour.

Antisocial and impulsive personality traits are linked to individual differences in somatosensory maps of emotion.

Somatosensory experience is an important component of emotion, playing a prominent role in many traditional emotion theories. Nonetheless, and despite the extensive literature on the influence of individual differences in emotional processing, the relation between personality traits and emotion-related somatosensation has received little attention. Here, we addressed this question in a large sample of healthy individuals through the "bodily maps of emotion" behavioural paradigm, in which participants indicated the location and extent of their body sensations for the 6 basic and 4 additional social emotions (contempt, envy, pride, shame). We found that emotional somatosensation in specific body areas, including the heart, the stomach, and the head, was related to specific personality factors, particularly antisocial attitudes and impulsivity. Moreover, the similarity of individual participants' maps to the group-average was likewise negatively correlated with antisocial tendencies. Overall, our results suggest that differences in individuals' sensitivity to somatosensation from different body areas, as well as the typicality of their topographical patterns, may partly underlie variation in higher-order social and affective traits.

The vocal side of empathy: neural correlates of pain perception in spoken complaints.

In the extensive neuroimaging literature on empathy for pain, few studies have investigated how this phenomenon may relate to everyday social situations such as spoken interactions. The present study used functional Magnetic Resonance Imaging (fMRI) to assess how complaints, as vocal expressions of pain, are empathically processed by listeners and how these empathic responses may vary based on speakers' vocal expression and cultural identity. Twenty-four French participants listened to short utterances describing a painful event, which were either produced in a neutral-sounding or complaining voice by both in-group (French) and out-group (French Canadian) speakers. Results suggest that the perception of suffering from a complaining voice increased activity in the emotional voice areas, composed of voice-sensitive temporal regions interacting with prefrontal cortices and the amygdala. The Salience and Theory of Mind networks, associated with affective and cognitive aspects of empathy, also showed prosody-related activity and specifically correlated with behavioral evaluations of suffering by listeners. Complaints produced by in- vs out-group speakers elicited sensorimotor and default mode activity, respectively, suggesting accent-based changes in empathic perspective. These results, while reaffirming the role of key networks in tasks involving empathy, highlight the importance of vocal expression information and social categorization processes when perceiving another's suffering during social interactions.

Emotion regulation in bipolar disorder type-I: multivariate analysis of fMRI data.

BACKGROUND: Bipolar disorder type-I (BD-I) patients are known to show emotion regulation abnormalities. In a previous fMRI study using an explicit emotion regulation paradigm, we compared responses from 19 BD-I patients and 17 matched healthy controls (HC). A standard general linear model-based univariate analysis revealed that BD patients showed increased activations in inferior frontal gyrus when instructed to decrease their emotional response as elicited by neutral images. We implemented multivariate pattern recognition analyses on the same data to examine if we could classify conditions within-group as well as HC versus BD. METHODS: We reanalyzed explicit emotion regulation data using a multivariate pattern recognition approach, as implemented in PRONTO software. The original experimental paradigm consisted of a full 2 × 2 factorial design, with valence (Negative/Neutral) and instruction (Look/Decrease) as within subject factors. RESULTS: The multivariate models were able to accurately classify different task conditions when HC and BD were analyzed separately (63.24%-75.00%, p = 0.001-0.012). In addition, the models were able to correctly classify HC versus BD with significant accuracy in conditions where subjects were instructed to downregulate their felt emotion (59.60%-60.84%, p = 0.014-0.018). The results for HC versus BD classification demonstrated contributions from the salience network, several occipital and frontal regions, inferior parietal lobes, as well as other cortical regions, to achieve above-chance classifications. CONCLUSIONS: Our multivariate analysis successfully reproduced some of the main results obtained in the previous univariate analysis, confirming that these findings are not dependent on the analysis approach. In particular, both types of analyses suggest that there is a significant difference of neural patterns between conditions within each subject group. The multivariate approach also revealed that reappraisal conditions provide the most informative activity for differentiating HC versus BD, irrespective of emotional valence (negative or neutral). The current results illustrate the importance of investigating the cognitive control of emotion in BD. We also propose a set of candidate regions for further study of emotional control in BD.

Emotional descriptions increase accidental harm punishment and its cortico-limbic signatures during moral judgment in autism.

Individuals with autism spectrum disorder (ASD) present difficulties in integrating mental state information in complex moral tasks. Yet, ASD research has not examined whether this process is influenced by emotions, let alone while capturing its neural bases. We investigated how language-induced emotions modulate intent-based moral judgment in ASD. In a fMRI task, 30 adults with ASD and 27 neurotypical controls read vignettes whose protagonists commit harm either accidentally or intentionally, and then decided how much punishment the protagonist deserved. Emotional content was manipulated across scenarios through the use of graphic language (designed to trigger arousing negative responses) vs. plain (just-the-facts, emotionless) language. Off-line functional connectivity correlates of task performance were also analyzed. In ASD, emotional (graphic) descriptions amplified punishment ratings of accidental harms, associated with increased activity in fronto-temporo-limbic, precentral, and postcentral/supramarginal regions (critical for emotional and empathic processes), and reduced connectivity among the orbitofrontal cortex and the angular gyrus (involved in mentalizing). Language manipulation did not influence intentional harm processing in ASD. In conclusion, in arousing and ambiguous social situations that lack intentionality clues (i.e. graphic accidental harm scenarios), individuals with ASD would misuse their emotional responses as the main source of information to guide their moral decisions. Conversely, in face of explicit harmful intentions, they would be able to compensate their socioemotional alterations and assign punishment through non-emotional pathways. Despite limitations, such as the small sample size and low ecological validity of the task, results of the present study proved reliable and have relevant theoretical and translational implications.

Morphology-based hypothesis testing in discrete random fields: a non-parametric method to address the multiple-comparison problem in neuroimaging.

A new method for detecting activations in random fields, which may be useful for addressing the issue of multiple comparisons in neuroimaging, is presented. This method is based on some constructs of mathematical morphology--specifically, morphological erosions and dilations--that enable the detection of active regions in random fields possessing moderate activation levels and relatively large spatial extension, which may not be detected by the standard methods that control the family-wise error rate. The method presented here permits an appropriate control of the false positive errors, without having to adjust any threshold values, other than the significance level. The method is easily adapted to permutation-based procedures (with the usual restrictions), and therefore does not require strong assumptions about the distribution and spatio-temporal correlation structure of the data. Some examples of applications to synthetic data, including realistic fMRI simulations, as well as to real fMRI and electroencephalographic data are presented, illustrating the power of the presented technique. Comparisons with other methods that combine voxel intensity and cluster size, as well as some extensions of the method presented here based on their basic ideas are presented as well.

Intra-individual Reliability of Voice- and Music-elicited Responses and their Modulation by Expertise.

A growing number of functional neuroimaging studies have identified regions within the temporal lobe, particularly along the planum polare and planum temporale, that respond more strongly to music than other types of acoustic stimuli, including voice. This "music preferred" regions have been reported using a variety of stimulus sets, paradigms and analysis approaches and their consistency across studies confirmed through meta-analyses. However, the critical question of intra-subject reliability of these responses has received less attention. Here, we directly assessed this important issue by contrasting brain responses to musical vs. vocal stimuli in the same subjects across three consecutive fMRI runs, using different types of stimuli. Moreover, we investigated whether these music- and voice-preferred responses were reliably modulated by expertise. Results demonstrated that music-preferred activity previously reported in temporal regions, and its modulation by expertise, exhibits a high intra-subject reliability. However, we also found that activity in some extra-temporal regions, such as the precentral and middle frontal gyri, did depend on the particular stimuli employed, which may explain why these are less consistently reported in the literature. Taken together, our findings confirm and extend the notion that specific regions in the brain consistently respond more strongly to certain socially-relevant stimulus categories, such as faces, voices and music, but that some of these responses appear to depend, at least to some extent, on the specific features of the paradigm employed.

Morphology-based hypothesis testing in discrete random fields: a non-parametric method to address the multiple-comparison problem in neuroimaging.

A new method for detecting activations in random fields, which may be useful for addressing the issue of multiple comparisons in neuroimaging, is presented. This method is based on some constructs of mathematical morphology - specifically, morphological erosions and dilations - that enable the detection of active regions in random fields possessing moderate activation levels and relatively large spatial extension, which may not be detected by the standard methods that control the family-wise error rate. The method presented here permits an appropriate control of the false positive errors, without having to adjust any threshold values, other than the significance level. The method is easily adapted to permutation-based procedures (with the usual restrictions), and therefore does not require strong assumptions about the distribution and spatio-temporal correlation structure of the data. Some examples of applications to synthetic data, including realistic fMRI simulations, as well as to real fMRI and electroencephalographic data are presented, illustrating the power of the presented technique. Comparisons with other methods that combine voxel intensity and cluster size, as well as some extensions of the method presented here based on their basic ideas are presented as well.