Networks underpinning emotion: A systematic review and synthesis of functional and effective connectivity

Existing models of emotion processing are based almost exclusively on brain activation data, yet make assumptions about network connectivity. There is a need to integrate connectivity findings into these models. We systematically reviewed all studies of functional and effective connectivity employing tasks to investigate negative emotion processing and regulation in healthy participants. Thirty-three studies met inclusion criteria. A quality assessment tool was derived from prominent neuroimaging papers. The evidence supports existing models, with primarily limbic regions for salience and identification, and frontal areas important for emotion regulation. There was mixed support for the assumption that regulatory influences on limbic and sensory areas come predominantly from prefrontal areas. Rather, studies quantifying effective connectivity reveal context-dependent dynamic modulatory relationships between occipital, subcortical, and frontal regions, arguing against purely top-down regulatory theoretical models. Our quality assessment tool found considerable variability in study design and tasks employed. The findings support and extend those of previous syntheses focused on activation studies, and provide evidence for a more nuanced view of connectivity in networks of human emotion processing and regulation

Reversed Frontotemporal Connectivity During Emotional Face Processing in Remitted Depression

BackgroundVulnerability to relapse persists after remission of an acute episode of major depressive disorder. This has been attributed to abnormal biases in the processing of emotional stimuli in limbic circuits. However, neuroimaging studies have not so far revealed consistent evidence of abnormal responses to emotional stimuli in limbic structures, such as the amygdala, in remitted depression. This suggests the problem might lie in the integrated functioning of emotion processing circuits.MethodsWe recruited 22 unmedicated patients in remission from major depressive disorder (rMDD) and 21 age-matched healthy control subjects. Functional magnetic resonance imaging was performed during a face emotion processing task. Dynamic causal modeling was used with Bayesian model selection to determine the most likely brain networks and valence-specific modulation of connectivity in healthy control subjects and rMDD.ResultsIn healthy volunteers, sad faces modulated bi-directional connections between amygdala and orbitofrontal cortex and between fusiform gyrus and orbitofrontal cortex. Happy faces modulated unidirectional connections from fusiform gyrus to orbitofrontal cortex. In rMDD, the opposite pattern was observed, with evidence of happy faces modulating bidirectional frontotemporal connections and sad faces modulating unidirectional fusiform–orbitofrontal connections.ConclusionsParticipants with rMDD have abnormal modulation of frontotemporal effective connectivity in response to happy and sad face emotions, despite normal activations within each region. Specifically, processing of mood incongruent happy information was associated with a more richly modulated frontotemporal brain network, whereas mood congruent sad information was associated with less network modulation. This supports a hypothesis of dysfunction within cortico–limbic connections in individuals vulnerable to depression

Functional morphological imaging of autism spectrum disorders: Current position and theories proposed

AbstractAutism is a pervasive disorder of childhood development. Polymorphous clinical profiles combining various degrees of communication and social interaction with restricted and stereotyped behaviour are grouped under the heading of ‘autism spectrum disorders’ (ASD). Many teams are trying to pick out the underlying cerebral abnormalities in order to understand the neuronal networks involved in relationships with others. Here we review the morphological, spectroscopic and functional abnormalities in the amygdala-hippocampal circuit, the caudate nuclei, the cerebellum, and the frontotemporal regions, which have been described in subjects with ASD. White matter abnormalities have also been described in diffusion tensor imaging, leading to suspected damage to the subjacent neural networks, such as mirror neurones or the social brain

Flexibly adapting to emotional cues: Examining the functional and structural correlates of emotional reactivity and emotion control in healthy and depressed individuals

The ability of emotionally significant stimuli to bias our behaviour is an evolutionarily adaptive phenomenon. However, sometimes emotions become excessive, inappropriate, and even pathological, like in major depressive disorder (MDD). Emotional flexibility includes both the neural processes involved in reacting to, or representing, emotional significance, and those involved in controlling emotional reactivity. MDD represents a potentially distinct form of emotion (in)flexibility, and therefore offers a unique perspective for understanding both the integration of conflicting emotional cues and the neural regions involved in actively controlling emotional systems. The present investigation of emotional flexibility began by considering the functional neural correlates of competing socio-emotional cues and effortful emotion regulation in MDD using both negative and positive emotions. Study 1 revealed greater amygdala activity in MDD relative to control participants when negative cues were centrally presented and task-relevant. No significant between-group differences were observed in the amygdala for peripheral task-irrelevant negative distracters. However, controls demonstrated greater recruitment of the ventrolateral (vlPFC) and dorsomedial prefrontal cortices (dmPFC) implicated in emotion control. Conversely, attenuated amygdala activity for task-relevant and irrelevant positive cues was observed in depressed participants. In Study 2, effortful emotion regulation using strategies adapted from cognitive behaviour therapy (CBT) revealed greater activity in regions of the dorsal and lateral prefrontal cortices in both MDD and control participants when attempting to either down-regulate negative or up-regulate positive emotions. During the down-regulation of negative cues, only controls displayed a significant reduction of amygdala activity. In Study 3, an individual differences approach using multiple regression revealed that while greater amygdala-vmPFC structural connectivity was associated with low trait-anxiety, greater connectivity between amygdala and regions of occipitotemporal and parietal cortices was associated with high trait-anxiety. These findings are discussed with respect to current models of emotional reactivity and emotion control derived from studies of both healthy individuals and those with emotional disorders, particularly depression. The focus is on amygdala variability in differing contexts, the role of the vmPFC in the modulation of amygdala activity via learning processes, and the modulation of emotion by attention or cognitive control mechanisms initiated by regions of frontoparietal cortices

Functional disconnection and social cognition in schizophrenia

Introduction Social and emotional functions play a key role in schizophrenia. Both positive symptoms, such as hallucinations and persecutory delusions, as well as negative symptoms such as social withdrawal, and flattened affect impact socioemotional function. These functions involve distributed brain networks. The ‘Disconnection Hypothesis’, a plausible unifying theory of schizophrenia, proposes connectivity within such networks as a core pathological feature of schizophrenia. Connectivity is also related to specific genetic risk factors. Therefore the present project addresses the hypothesis that individuals with schizophrenia might show disconnection within socio-emotional brain networks, and examines the effects of a functional polymorphism of the BDNF gene on connectivity within these networks. Methods Here I examined the brain activation and connectivity for implicit emotional reaction and social judgment in schizophrenia, as well as with variation in the val66met polymorphism of BDNF. Brain activation was examined with functional magnetic resonance imaging, and effective connectivity was estimated using psycho-physiological interactions, from the bilateral amygdala to the whole brain (using a facial image paradigm for explicit approachability judgement and implicit fear response respectively). Results Individuals with schizophrenia showed reduced activation in the right lingual gyrus, right superior temporal gyrus and left amygdala during fear processing, as well as reduced connectivity from the left amygdala to the right temporo-parietal junction and precuneus. During approachability judgments, patients overactivated the right inferior frontal gyrus and right precuneus and showed reduced connectivity from the bilateral amygdala to the right inferior frontal gyrus. Met allele carriers of the BDNF val66met polymorphism showed overactivation in the medial anterior cingulate cortex, and bilateral insula, as well as reduced connectivity between the anterior cingulate cortex and hippocampus. For approachability judgment, met carriers overactivated the middle occipital gyrus, and showed reduced connectivity from the left amygdala to the right parahippocampal gyrus and medial frontal gyrus, as well as the left posterior cingulate gyrus, pre and post central gyrus, middle temporal gyrus and cerebellum. Conclusion In conclusion, connectivity between the amygdala and brain regions associated with a range of socially relevant functions were found to be reduced in both patients, and met allele carriers of the BDNF val66met SNP. Given the key role of the amygdala in affective processing this diffuse disconnection in networks for socio-emotional functions might mediate the aberrant emotional and social behavior seen in individuals with schizophrenia

Neural activation of anxiety and depression in children and young people: A systematic meta-analysis of fMRI studies

Functional magnetic resonance imaging (fMRI) studies consistently demonstrate altered neural activation in youth experiencing anxiety and depression in a way that is distinct from adult-onset disorders. However, there is a paucity of research systematically reviewing this, and no meta-analyses have been conducted using Activation Likelihood Estimation (ALE). The present study conducted a systematic literature search to identify fMRI studies in youth (age 4-18) with depression or anxiety disorders. 48 studies with over 2000 participants were identified that met the inclusion criteria. Significant foci were extracted. Five ALE meta-analyses were conducted: a) activation for both anxiety disorders and depression; b) activation for anxiety disorders only; c) activation for depression only; d) deactivation for both anxiety disorders and depression; e) deactivation for depression. Results indicated significant clusters of increased activation in the bilateral amygdala for youth with internalising disorders, and specifically for those with anxiety disorders. Significant increased activation extended into the dorsal anterior cingulate, entorhinal cortex, the putamen, and the medial and lateral globus pallidus in youth with anxiety disorders. These findings help to detail the nature of anxiety being an amygdala hyperactivity disorder, whilst also defining the distinction between neural activation patterns in anxiety and depression

Expressive and response dimensions of human emotion.

This thesis is about the neural mechanisms that underpin the expression of emotion in the human face and emotional modulation of behavioural responses. I designed 5 integrated studies and used functional magnetic resonance imaging (fMRI) to address specifically the neural mechanisms underlying human facial expression and emotional response. This work complements studies of emotion perception and subjective affective experience to provide a more comprehensive understanding of human emotions. I examined the neural underpinnings of emotional facial expression in three studies. I first demonstrated that emotional (compared to non-emotional) facial expression is not a purely motoric process but engages affective centres, including amygdala and rostral cingulate gyrus. In a second study I developed the concept of emotion contagion to demonstrate and verify a new interference effect (emotion expression interference, EEI). There is a cost (in reaction time and effort) to over-riding pre-potent tendency to mirror the emotional expressions of others. Several neural centres supporting EEI were identified (inferior frontal gyrus, superior temporal sulcus and insula), with their activity across subject predicting individual differences in personal empathy and emotion regulation. In a third study I examined an interesting phenomenon in our daily social life: how our own emotional facial expressions influence our judgment of the emotional signals of other people I explored this issue experimentally to examine the behavioural and neural consequences of posing positive (smiling) and negative (frowning) emotional expressions on judgments of perceived facial expressions. Reciprocal interactions between an emotion centre (amygdala) and a social signal processing region (superior temporal sulcus) were quantified. My analysis further revealed that the biasing of emotion judgments by one's own facial expression works through changes in connectivity between posterior brain regions (specifically from superior temporal sulcus to post-central cortex). I further developed two versions of an emotion GO/NOGO task to probe the impact of affective processing on behavioural responses. GO represents response execution and NOGO represents response inhibition. I therefore investigated how different emotions modulate both these complementary response dimensions (i.e. execution and inhibition). This research line is pertinent to a major theme within emotion theory, in which emotion is defined in terms of response patterns (e.g. approach and withdrawal). My results confirmed that both emotional processing and induced emotional states have robust modulatory effects on neural centres supporting response execution and response inhibition. Importantly, my results argue for emotion as a context for response control. My work extends our understanding of human emotion in terms of the nature and effect of its expression and its influence on response system

Hierarchical Brain Network for Face and Voice Integration of Emotion Expression

The brain has separate specialized computational units to process faces and voices located in occipital and temporal cortices. However, humans seamlessly integrate signals from the faces and voices of others for optimal social interaction. How are emotional expressions, when delivered by different sensory modalities (faces and voices), integrated in the brain? In this study, we characterized the brains' response to faces, voices, and combined face-voice information (congruent, incongruent), which varied in expression (neutral, fearful). Using a whole-brain approach, we found that only the right posterior superior temporal sulcus (rpSTS) responded more to bimodal stimuli than to face or voice alone but only when the stimuli contained emotional expression. Face- and voice-selective regions of interest, extracted from independent functional localizers, similarly revealed multisensory integration in the face-selective rpSTS only; further, this was the only face-selective region that also responded significantly to voices. Dynamic causal modeling revealed that the rpSTS receives unidirectional information from the face-selective fusiform face area, and voice-selective temporal voice area, with emotional expression affecting the connection strength. Our study promotes a hierarchical model of face and voice integration, with convergence in the rpSTS, and that such integration depends on the (emotional) salience of the stimuli