Hypothalamic neurons that mirror aggression.

Social interactions require awareness and understanding of the behavior of others. Mirror neurons, cells representing an action by self and others, have been proposed to be integral to the cognitive substrates that enable such awareness and understanding. Mirror neurons of the primate neocortex represent skilled motor tasks, but it is unclear if they are critical for the actions they embody, enable social behaviors, or exist in non-cortical regions. We demonstrate that the activity of individual VMHvlPR neurons in the mouse hypothalamus represents aggression performed by self and others. We used a genetically encoded mirror-TRAP strategy to functionally interrogate these aggression-mirroring neurons. We find that their activity is essential for fighting and that forced activation of these cells triggers aggressive displays by mice, even toward their mirror image. Together, we have discovered a mirroring center in an evolutionarily ancient region that provides a subcortical cognitive substrate essential for a social behavior.

Neural Circuits for Emotion.

Emotions are fundamental to our experience and behavior, affecting and motivating all aspects of our lives. Scientists of various disciplines have been fascinated by emotions for centuries, yet even today vigorous debates abound about how to define emotions and how to best study their neural underpinnings. Defining emotions from an evolutionary perspective and acknowledging their important functional roles in supporting survival allows the study of emotion states in diverse species. This approach enables taking advantage of modern tools in behavioral, systems, and circuit neurosciences, allowing the precise dissection of neural mechanisms and behavior underlying emotion processes in model organisms. Here we review findings about the neural circuit mechanisms underlying emotion processing across species and try to identify points of convergence as well as important next steps in the pursuit of understanding how emotions emerge from neural activity.

Breathing Rhythm and Pattern and Their Influence on Emotion.

Breathing is a vital rhythmic motor behavior with a surprisingly broad influence on the brain and body. The apparent simplicity of breathing belies a complex neural control system, the breathing central pattern generator (bCPG), that exhibits diverse operational modes to regulate gas exchange and coordinate breathing with an array of behaviors. In this review, we focus on selected advances in our understanding of the bCPG. At the core of the bCPG is the preBötzinger complex (preBötC), which drives inspiratory rhythm via an unexpectedly sophisticated emergent mechanism. Synchronization dynamics underlying preBötC rhythmogenesis imbue the system with robustness and lability. These dynamics are modulated by inputs from throughout the brain and generate rhythmic, patterned activity that is widely distributed. The connectivity and an emerging literature support a link between breathing, emotion, and cognition that is becoming experimentally tractable. These advances bring great potential for elucidating function and dysfunction in breathing and other mammalian neural circuits.

Reward Contributions to Serotonergic Functions.

The brain serotonin systems participate in numerous aspects of reward processing, although it remains elusive how exactly serotonin signals regulate neural computation and reward-related behavior. The application of optogenetics and imaging techniques during the last decade has provided many insights. Here, we review recent progress on the organization and physiology of the dorsal raphe serotonin neurons and the relationships between their activity and behavioral functions in the context of reward processing. We also discuss several interesting theories on serotonin's function and how these theories may be reconciled by the possibility that serotonin, acting in synergy with coreleased glutamate, tracks and calculates the so-called beneficialness of the current state to guide an animal's behavior in dynamic environments.

Bodily maps of musical sensations across cultures.

Emotions, bodily sensations and movement are integral parts of musical experiences. Yet, it remains unknown i) whether emotional connotations and structural features of music elicit discrete bodily sensations and ii) whether these sensations are culturally consistent. We addressed these questions in a cross-cultural study with Western (European and North American, n = 903) and East Asian (Chinese, n = 1035). We precented participants with silhouettes of human bodies and asked them to indicate the bodily regions whose activity they felt changing while listening to Western and Asian musical pieces with varying emotional and acoustic qualities. The resulting bodily sensation maps (BSMs) varied as a function of the emotional qualities of the songs, particularly in the limb, chest, and head regions. Music-induced emotions and corresponding BSMs were replicable across Western and East Asian subjects. The BSMs clustered similarly across cultures, and cluster structures were similar for BSMs and self-reports of emotional experience. The acoustic and structural features of music were consistently associated with the emotion ratings and music-induced bodily sensations across cultures. These results highlight the importance of subjective bodily experience in music-induced emotions and demonstrate consistent associations between musical features, music-induced emotions, and bodily sensations across distant cultures.

Live music stimulates the affective brain and emotionally entrains listeners in real time.

Music is powerful in conveying emotions and triggering affective brain mechanisms. Affective brain responses in previous studies were however rather inconsistent, potentially because of the non-adaptive nature of recorded music used so far. Live music instead can be dynamic and adaptive and is often modulated in response to audience feedback to maximize emotional responses in listeners. Here, we introduce a setup for studying emotional responses to live music in a closed-loop neurofeedback setup. This setup linked live performances by musicians to neural processing in listeners, with listeners' amygdala activity was displayed to musicians in real time. Brain activity was measured using functional MRI, and especially amygdala activity was quantified in real time for the neurofeedback signal. Live pleasant and unpleasant piano music performed in response to amygdala neurofeedback from listeners was acoustically very different from comparable recorded music and elicited significantly higher and more consistent amygdala activity. Higher activity was also found in a broader neural network for emotion processing during live compared to recorded music. This finding included observations of the predominance for aversive coding in the ventral striatum while listening to unpleasant music, and involvement of the thalamic pulvinar nucleus, presumably for regulating attentional and cortical flow mechanisms. Live music also stimulated a dense functional neural network with the amygdala as a central node influencing other brain systems. Finally, only live music showed a strong and positive coupling between features of the musical performance and brain activity in listeners pointing to real-time and dynamic entrainment processes.

Disadvantaged group members are prouder of their group when using the language of the dominant group compared to their native language.

In ethnically and linguistically diverse societies, disadvantaged groups often face pressures to acquire and speak the advantaged group's language to achieve social inclusion and economic mobility. This work investigates how using the advantaged group's language affects disadvantaged group members' in-group pride and collective self-esteem, relative to using their native language. Across six experimental studies involving Palestinian citizens of Israel (total N = 1,348), we test two competing hypotheses: Disadvantaged group members may experience greater in-group pride when using a) their native language, due to its emotional significance (the nativity hypothesis), or b) the language of the advantaged group, due to activation of habituated compensatory responses to dominance relations (the identity enhancement hypothesis). We found that respondents reported significantly higher in-group pride when responding to a Hebrew survey when compared to performing the same activity in Arabic (Studies 1a and 1b), regardless of whether the researchers administering the survey were identified as Jewish or Arab (Studies 2a and 2b). Study 3 replicated this effect while employing the "bogus pipeline" technique, suggesting the pride expression was authentic, not merely driven by social desirability. Finally, Study 4 (pre-registered) examined additional measures of positive regard for the in-group, finding that participants described their group more positively in an attribute selection task, and reported greater collective self-esteem, when surveyed in Hebrew, rather than in Arabic. Taken together, these findings suggest that language use influences disadvantaged group members' perceptions and feelings concerning their group when those languages are associated with relative position in an intergroup hierarchy.

Automating the analysis of facial emotion expression dynamics: A computational framework and application in psychotic disorders.

Facial emotion expressions play a central role in interpersonal interactions; these displays are used to predict and influence the behavior of others. Despite their importance, quantifying and analyzing the dynamics of brief facial emotion expressions remains an understudied methodological challenge. Here, we present a method that leverages machine learning and network modeling to assess the dynamics of facial expressions. Using video recordings of clinical interviews, we demonstrate the utility of this approach in a sample of 96 people diagnosed with psychotic disorders and 116 never-psychotic adults. Participants diagnosed with schizophrenia tended to move from neutral expressions to uncommon expressions (e.g., fear, surprise), whereas participants diagnosed with other psychoses (e.g., mood disorders with psychosis) moved toward expressions of sadness. This method has broad applications to the study of normal and altered expressions of emotion and can be integrated with telemedicine to improve psychiatric assessment and treatment.

The role of positive emotion in harmful health behavior: Implications for theory and public health campaigns.

Meta-analyses have concluded that positive emotions do not reduce appetitive risk behaviors (risky behaviors that fulfill appetitive or craving states, such as smoking and excessive alcohol use). We propose that this conclusion is premature. Drawing on the Appraisal Tendency Framework and related theories of emotion and decision-making, we hypothesized that gratitude (a positive emotion) can decrease cigarette smoking, a leading cause of premature death globally. A series of multimethod studies provided evidence supporting our hypothesis (collective N = 34,222). Using nationally representative US samples and an international sample drawn from 87 countries, Studies 1 and 2 revealed that gratitude was inversely associated with likelihood of smoking, even after accounting for numerous covariates. Other positive emotions (e.g., compassion) lacked such consistent associations, as expected. Study 3, and its replication, provided further support for emotion specificity: Experimental induction of gratitude, unlike compassion or sadness, reduced cigarette craving compared to a neutral state. Study 4, and its replication, showed that inducing gratitude causally increased smoking cessation behavior, as evidenced by enrollment in a web-based cessation intervention. Self-reported gratitude mediated the effects in both experimental studies. Finally, Study 5 found that current antismoking messaging campaigns by the US Centers for Disease Control and Prevention primarily evoked sadness and compassion, but seldom gratitude. Together, our studies advance understanding of positive emotion effects on appetitive risk behaviors; they also offer practical implications for the design of public health campaigns.

Do moral values change with the seasons?

Moral values guide consequential attitudes and actions. Here, we report evidence of seasonal variation in Americans' endorsement of some-but not all-moral values. Studies 1 and 2 examined a decade of data from the United States (total N = 232,975) and produced consistent evidence of a biannual seasonal cycle in values pertaining to loyalty, authority, and purity ("binding" moral values)-with strongest endorsement in spring and autumn and weakest endorsement in summer and winter-but not in values pertaining to care and fairness ("individualizing" moral values). Study 2 also provided some evidence that the summer decrease, but not the winter decrease, in binding moral value endorsement was stronger in regions with greater seasonal extremity. Analyses on an additional year of US data (study 3; n = 24,199) provided further replication and showed that this biannual seasonal cycle cannot be easily dismissed as a sampling artifact. Study 4 provided a partial explanation for the biannual seasonal cycle in Americans' endorsement of binding moral values by showing that it was predicted by an analogous seasonal cycle in Americans' experience of anxiety. Study 5 tested the generalizability of the primary findings and found similar seasonal cycles in endorsement of binding moral values in Canada and Australia (but not in the United Kingdom). Collectively, results from these five studies provide evidence that moral values change with the seasons, with intriguing implications for additional outcomes that can be affected by those values (e.g., intergroup prejudices, political attitudes, legal judgments).

Emotions and courtship help bonded pairs cooperate, but emotional agents are vulnerable to deceit.

Coordinated pair bonds are common in birds and also occur in many other taxa. How do animals solve the social dilemmas they face in coordinating with a partner? We developed an evolutionary model to explore this question, based on observations that a) neuroendocrine feedback provides emotional bookkeeping which is thought to play a key role in vertebrate social bonds and b) these bonds are developed and maintained via courtship interactions that include low-stakes social dilemmas. Using agent-based simulation, we found that emotional bookkeeping and courtship sustained cooperation in the iterated prisoner's dilemma in noisy environments, especially when combined. However, when deceitful defection was possible at low cost, courtship often increased cooperation, whereas emotional bookkeeping decreased it.

Collective events and individual affect shape autobiographical memory.

How do collective events shape how we remember our lives? We leveraged advances in natural language processing as well as a rich, longitudinal assessment of 1,000 Americans throughout 2020 to examine how memory is influenced by two prominent factors: surprise and emotion. Autobiographical memory for 2020 displayed a unique signature: There was a substantial bump in March, aligning with pandemic onset and lockdowns, consistent across three memory collections 1 y apart. We further investigated how emotion, using both immediate and retrieved measures, predicted the amount and content of autobiographical memory: Negative affect increased recall across all measures, whereas its more clinical indices, depression and posttraumatic stress disorder, selectively increased nonepisodic recall. Finally, in a separate cohort, we found pandemic news to be better remembered, surprising, and negative, while lockdowns compressed remembered time. Our work connects laboratory findings to the real world and delineates the effects of acute versus clinical signatures of negative emotion on memory.

Curiosity evolves as information unfolds.

When people feel curious, they often seek information to resolve their curiosity. Reaching resolution, however, does not always occur in a single step but instead may follow the accumulation of information over time. Here, we investigated changes in curiosity over a dynamic information-gathering process and how these changes related to affective and cognitive states as well as behavior. Human participants performed an Evolving Line Drawing Task, during which they reported guesses about the drawings' identities and made choices about whether to keep watching. In Study 1, the timing of choices was predetermined and externally imposed, while in Study 2, participants had agency in the timing of guesses and choices. Using this dynamic paradigm, we found that even within a single information-gathering episode, curiosity evolved in concert with other emotional states and with confidence. In both studies, we showed that the relationship between curiosity and confidence depended on stimulus entropy (unique guesses across participants) and on guess accuracy. We demonstrated that curiosity is multifaceted and can be experienced as either positive or negative depending on the state of information gathering. Critically, even when given the choice to alleviate uncertainty immediately (i.e., view a spoiler), higher curiosity promoted continuing to engage in the information-gathering process. Collectively, we show that curiosity changes over information accumulation to drive engagement with external stimuli, rather than to shortcut the path to resolution, highlighting the value inherent in the process of discovery.

Acetylcholine Engages Distinct Amygdala Microcircuits to Gate Internal Theta Rhythm.

Acetylcholine (ACh) is released from basal forebrain cholinergic neurons in response to salient stimuli and engages brain states supporting attention and memory. These high ACh states are associated with theta oscillations, which synchronize neuronal ensembles. Theta oscillations in the basolateral amygdala (BLA) in both humans and rodents have been shown to underlie emotional memory, yet their mechanism remains unclear. Here, using brain slice electrophysiology in male and female mice, we show large ACh stimuli evoke prolonged theta oscillations in BLA local field potentials that depend upon M3 muscarinic receptor activation of cholecystokinin (CCK) interneurons (INs) without the need for external glutamate signaling. Somatostatin (SOM) INs inhibit CCK INs and are themselves inhibited by ACh, providing a functional SOM→CCK IN circuit connection gating BLA theta. Parvalbumin (PV) INs, which can drive BLA oscillations in baseline states, are not involved in the generation of ACh-induced theta, highlighting that ACh induces a cellular switch in the control of BLA oscillatory activity and establishes an internally BLA-driven theta oscillation through CCK INs. Theta activity is more readily evoked in BLA over the cortex or hippocampus, suggesting preferential activation of the BLA during high ACh states. These data reveal a SOM→CCK IN circuit in the BLA that gates internal theta oscillations and suggest a mechanism by which salient stimuli acting through ACh switch the BLA into a network state enabling emotional memory.

Synaptic Connectivity and Electrophysiological Properties of the Nucleus of the Lateral Olfactory Tract.

The sense of smell is tightly linked to emotions, a link that is thought to rely on the direct synaptic connections between the olfactory bulb (OB) and nuclei of the amygdala. However, there are multiple pathways projecting olfactory information to the amygdala, and their unique functions are unknown. The pathway via the nucleus of the lateral olfactory tract (NLOT) that receives input from olfactory regions and projects to the basolateral amygdala (BLA) is among them. NLOT has been very little studied, and consequentially its function is unknown. Furthermore, formulation of informed hypotheses about NLOT function is at this stage limited by the lack of knowledge about its connectivity and physiological properties. Here, we used virus-based tracing methods to systematically reveal inputs into NLOT, as well as NLOT projection targets in mice of both sexes. We found that the NLOT is interconnected with several olfactory brain regions and with the BLA. Some of these connections were reciprocal, and some showed unique interhemispheric patterns. We tested the excitable properties of NLOT neurons and the properties of each of the major synaptic inputs. We found that the NLOT receives powerful input from the piriform cortex, tenia tecta, and the BLA but only very weak input from the OB. When input crosses threshold, NLOT neurons respond with calcium-dependent bursts of action potentials. We hypothesize that this integration of olfactory and amygdalar inputs serves behaviors that combine smell and emotion.

Reconfiguration of Behavioral Signals in the Anterior Cingulate Cortex Based on Emotional State.

Behaviors and their execution depend on the context and emotional state in which they are performed. The contextual modulation of behavior likely relies on regions such as the anterior cingulate cortex (ACC) that multiplex information about emotional/autonomic states and behaviors. The objective of the present study was to understand how the representations of behaviors by ACC neurons become modified when performed in different emotional states. A pipeline of machine learning techniques was developed to categorize and classify complex, spontaneous behaviors in male rats from the video. This pipeline, termed Hierarchical Unsupervised Behavioural Discovery Tool (HUB-DT), discovered a range of statistically separable behaviors during a task in which motivationally significant outcomes were delivered in blocks of trials that created three unique "emotional contexts." HUB-DT was capable of detecting behaviors specific to each emotional context and was able to identify and segregate the portions of a neural signal related to a behavior and to emotional context. Overall, ∼10× as many neurons responded to behaviors in a contextually dependent versus a fixed manner, highlighting the extreme impact of emotional state on representations of behaviors that were precisely defined based on detailed analyses of limb kinematics. This type of modulation may be a key mechanism that allows the ACC to modify the behavioral output based on emotional states and contextual demands.

Re-examining the Mysterious Role of the Cerebellum in Pain.

Pain is considered a multidimensional experience that embodies not merely sensation, but also emotion and perception. As is appropriate for this complexity, pain is represented and processed by an extensive matrix of cortical and subcortical structures. Of these structures, the cerebellum is gaining increasing attention. Although association between the cerebellum and both acute and chronic pain have been extensively detailed in electrophysiological and neuroimaging studies, a deep understanding of what functions are mediated by these associations is lacking. Nevertheless, the available evidence implies that lobules IV-VI and Crus I are especially pertinent to pain processing, and anatomical studies reveal that these regions connect with higher-order structures of sensorimotor, emotional, and cognitive function. Therefore, we speculate that the cerebellum exerts a modulatory role in pain via its communication with sites of sensorimotor, executive, reward, and limbic function. On this basis, in this review, we propose numerous ways in which the cerebellum might contribute to both acute and chronic pain, drawing particular attention to emotional and cognitive elements of pain. In addition, we emphasise the importance of advancing our knowledge about the relationship between the cerebellum and pain by discussing novel therapeutic opportunities that capitalize on this association.

Ultrahigh Field fMRI Reveals Different Roles of the Temporal and Frontoparietal Cortices in Subjective Awareness.

A central question in consciousness theories is whether one is dealing with a dichotomous ("all-or-none") or a gradual phenomenon. In this 7T fMRI study, we investigated whether dichotomy or gradualness in fact depends on the brain region associated with perceptual awareness reports. Both male and female human subjects performed an emotion discrimination task (fear vs neutral bodies) presented under continuous flash suppression with trial-based perceptual awareness measures. Behaviorally, recognition sensitivity increased linearly with increased stimuli awareness and was at chance level during perceptual unawareness. Physiologically, threat stimuli triggered a slower heart rate than neutral ones during "almost clear" stimulus experience, indicating freezing behavior. Brain results showed that activity in the occipitotemporal, parietal, and frontal regions as well as in the amygdala increased with increased stimulus awareness while early visual areas showed the opposite pattern. The relationship between temporal area activity and perceptual awareness best fitted a gradual model while the activity in frontoparietal areas fitted a dichotomous model. Furthermore, our findings illustrate that specific experimental decisions, such as stimulus type or the approach used to evaluate awareness, play pivotal roles in consciousness studies and warrant careful consideration.

Integration of Prior Expectations and Suppression of Prediction Errors During Expectancy-Induced Pain Modulation: The Influence of Anxiety and Pleasantness.

Pain perception arises from the integration of prior expectations with sensory information. Although recent work has demonstrated that treatment expectancy effects (e.g., placebo hypoalgesia) can be explained by a Bayesian integration framework incorporating the precision level of expectations and sensory inputs, the key factor modulating this integration in stimulus expectancy-induced pain modulation remains unclear. In a stimulus expectancy paradigm combining emotion regulation in healthy male and female adults, we found that participants' voluntary reduction in anticipatory anxiety and pleasantness monotonically reduced the magnitude of pain modulation by negative and positive expectations, respectively, indicating a role of emotion. For both types of expectations, Bayesian model comparisons confirmed that an integration model using the respective emotion of expectations and sensory inputs explained stimulus expectancy effects on pain better than using their respective precision. For negative expectations, the role of anxiety is further supported by our fMRI findings that (1) functional coupling within anxiety-processing brain regions (amygdala and anterior cingulate) reflected the integration of expectations with sensory inputs and (2) anxiety appeared to impair the updating of expectations via suppressed prediction error signals in the anterior cingulate, thus perpetuating negative expectancy effects. Regarding positive expectations, their integration with sensory inputs relied on the functional coupling within brain structures processing positive emotion and inhibiting threat responding (medial orbitofrontal cortex and hippocampus). In summary, different from treatment expectancy, pain modulation by stimulus expectancy emanates from emotion-modulated integration of beliefs with sensory evidence and inadequate belief updating.

Emotion recognition and regulation in males: Role of sex and stress steroids.

Understanding emotions in males is crucial given their higher susceptibility to substance use, interpersonal violence, and suicide compared to females. Steroid hormones are assumed to be critical biological factors that affect and modulate emotion-related behaviors, together with psychological and social factors. This review explores whether males' abilities to recognize emotions of others and regulate their own emotions are associated with testosterone, cortisol, and their interaction. Higher levels of testosterone were associated with improved recognition and heightened sensitivity to threatening faces. In contrast, higher cortisol levels positively impacted emotion regulation ability. Indirect evidence from neuroimaging research suggested a link between higher testosterone levels and difficulties in cognitive emotion regulation. However, this notion must be investigated in future studies using different emotion regulation strategies and considering social status. The present review contributes to the understanding of how testosterone and cortisol affect psychological well-being and emotional behavior in males.