Sanda Dolcos

Neural correlates of emotion–cognition interactions: A review of evidence from brain imaging investigations

Complex dynamic behaviour involves reciprocal influences between emotion and cognition. On the one hand, emotion is a “double-edged sword” that may affect various aspects of our cognition and behaviour, by enhancing or hindering them and exerting both transient and long-term influences. On the other hand, emotion processing is also susceptible to cognitive influences, typically exerted in the form of emotion regulation. Noteworthy, both of these reciprocal influences are subjective to individual differences that may affect the way we perceive, experience, and eventually remember emotional experiences, or respond to emotionally challenging situations. Understanding these relationships is critical, as unbalanced emotion–cognition interactions may lead to devastating effects, such as those observed in mood and anxiety disorders. The present review analyses the reciprocal relationships between emotion and cognition, based on evidence derived from brain imaging investigations focusing on three main topics: (1) the impact of emotion on cognition, (2) the impact of cognition on emotion, and (3) the role of individual differences in emotion–cognition interactions. This evidence will be discussed in the context of identifying aspects that are fundamental to understanding the mechanisms underlying emotion–cognition interactions in healthy functioning, and to understanding changes associated with affective disorders.

Neural signatures of the response to emotional distraction: a review of evidence from brain imaging investigations

Prompt responses to emotional, potentially threatening, stimuli are supported by neural mechanisms that allow for privileged access of emotional information to processing resources. The existence of these mechanisms can also make emotional stimuli potent distracters, particularly when task-irrelevant. The ability to deploy cognitive control in order to cope with emotional distraction is essential for adaptive behavior, while reduced control may lead to enhanced emotional distractibility, which is often a hallmark of affective disorders. Evidence suggests that increased susceptibility to emotional distraction is linked to changes in the processing of emotional information that affect both the basic response to and coping with emotional distraction, but the neural correlates of these phenomena are not clear. The present review discusses emerging evidence from brain imaging studies addressing these issues, and highlights the following three aspects. First, the response to emotional distraction is associated with opposing patterns of activity in a ventral “hot” affective system (HotEmo, showing increased activity) and a dorsal “cold” executive system (ColdEx, showing decreased activity). Second, coping with emotional distraction involves top–down control in order to counteract the bottom-up influence of emotional distraction, and involves interactions between the amygdala and the prefrontal cortex. Third, both the response to and coping with emotional distraction are influenced by individual differences affecting emotional sensitivity and distractibility, which are linked to alterations of both HotEmo and ColdEx neural systems. Collectively, the available evidence identifies specific neural signatures of the response to emotional challenge, which are fundamental to understanding the mechanisms of emotion-cognition interactions in healthy functioning, and the changes linked to individual variation in emotional distractibility and susceptibility to affective disorders.

The Impact of Anxiety-Inducing Distraction on Cognitive Performance: A Combined Brain Imaging and Personality Investigation

Background Previous investigations revealed that the impact of task-irrelevant emotional distraction on ongoing goal-oriented cognitive processing is linked to opposite patterns of activation in emotional and perceptual vs. cognitive control/executive brain regions. However, little is known about the role of individual variations in these responses. The present study investigated the effect of trait anxiety on the neural responses mediating the impact of transient anxiety-inducing task-irrelevant distraction on cognitive performance, and on the neural correlates of coping with such distraction. We investigated whether activity in the brain regions sensitive to emotional distraction would show dissociable patterns of co-variation with measures indexing individual variations in trait anxiety and cognitive performance. Methodology/Principal Findings Event-related fMRI data, recorded while healthy female participants performed a delayed-response working memory (WM) task with distraction, were investigated in conjunction with behavioural measures that assessed individual variations in both trait anxiety and WM performance. Consistent with increased sensitivity to emotional cues in high anxiety, specific perceptual areas (fusiform gyrus - FG) exhibited increased activity that was positively correlated with trait anxiety and negatively correlated with WM performance, whereas specific executive regions (right lateral prefrontal cortex - PFC) exhibited decreased activity that was negatively correlated with trait anxiety. The study also identified a role of the medial and left lateral PFC in coping with distraction, as opposed to reflecting a detrimental impact of emotional distraction. Conclusions These findings provide initial evidence concerning the neural mechanisms sensitive to individual variations in trait anxiety and WM performance, which dissociate the detrimental impact of emotion distraction and the engagement of mechanisms to cope with distracting emotions. Our study sheds light on the neural correlates of emotion-cognition interactions in normal behaviour, which has implications for understanding factors that may influence susceptibility to affective disorders, in general, and to anxiety disorders, in particular.

Reliving emotional personal memories: affective biases linked to personality and sex-related differences.

Although available evidence suggests that the emotional valence and recollective properties of autobiographical memories (AMs) may be influenced by personality- and sex-related differences, overall these relationships remain poorly understood. The present study investigated these issues by comparing the effect of general personality traits (extraversion and neuroticism) and specific traits linked to emotion regulation (ER) strategies (reappraisal and suppression) on the retrieval of emotional AMs and on the associated postretrieval emotional states, in men and women. First, extraversion predicted recollection of positive AMs in both men and women, whereas neuroticism predicted the proportion of negative AMs in men and the frequency of rehearsing negative AMs in women. Second, reappraisal predicted positive AMs in men, and suppression predicted negative AMs in women. Third, while reliving of positive memories had an overall indirect effect on postretrieval positive mood through extraversion, reliving of negative AMs had a direct effect on postretrieval negative mood, which was linked to inefficient engagement of suppression in women. Our findings suggest that personality traits associated with positive affect predict recollection of positive AMs and maintenance of a positive mood, whereas personality traits associated with negative affect, along with differential engagement of habitual ER strategies in men and women, predict sex-related differences in the recollection and experiencing of negative AMs. These findings provide insight into the factors that influence affective biases in reliving AMs, and into their possible link to sex-related differences in the susceptibility to affective disorders.

The role of arousal in the spontaneous regulation of emotions in healthy aging: a fMRI investigation

Despite ample support for enhanced affective well-being and emotional stability in healthy aging, the role of potentially important dimensions, such as the emotional arousal, has not been systematically investigated in neuroimaging studies. In addition, the few behavioral studies that examined effects of arousal have produced inconsistent findings. The present study manipulated the arousal of pictorial stimuli to test the hypothesis that preserved emotional functioning in aging is modulated by the level of arousal, and to identify the associated neural correlates. Young and older healthy participants were presented with negative and neutral pictures, which they rated for emotional content, while fMRI data were recorded. There were three main novel findings regarding the neural mechanisms underlying the processing of negative pictures with different levels of arousal in young and older adults. First, the common engagement of the right amygdala in young and older adults was driven by high arousing negative stimuli. Second, complementing an age-related reduction in the subjective ratings for low arousing negative pictures, there were opposing patterns of activity in the rostral/ventral anterior cingulate cortex (ACC) and the amygdala, which showed increased vs. decreased responses, respectively, to low arousing negative pictures. Third, increased spontaneous activity in the ventral ACC/ventromedial prefrontal cortex (vmPFC) in older adults was linked to reduced ratings for low arousing negative pictures. Overall, these findings advance our understanding of the neural correlates underlying processing of negative emotions with different levels of arousal in the context of enhanced emotional functioning in healthy aging. Notably, the results support the idea that older adults have emotion regulation networks chronically activated, in the absence of explicit induction of the goal to regulate emotions, and that this effect is specific to low arousing negative emotions.

Reappraisal and Suppression Mediate the Contribution of Regulatory Focus to Anxiety in Healthy Adults

Theory and research link regulatory focus (RF) in the form of promotion and prevention goal orientation with internalizing symptoms (e.g., anxiety), but the relevant mechanisms are not well understood. This study investigated the role of two emotion regulation (ER) strategies (cognitive reappraisal and expressive suppression) as possible mediators. Path analysis using data from 179 healthy young participants (110 women, 69 men) revealed that stronger promotion orientation was significantly associated with less anxiety, and that the use of reappraisal and suppression partially mediated this association. Prevention was associated with more suppression but was not directly associated with anxiety. There were no gender differences in these effects. Collectively, these findings suggest that effective ER, through heightened use of reappraisal and dampened use of suppression, serves as a mechanism through which promotion confers protection against anxiety. This research provides empirical support to initiatives aimed at promoting healthy psychological adjustment and preventing anxiety, by optimizing ER strategies with respect to RF goal orientations.

Sex differences in the response to emotional distraction: an event-related fMRI investigation

Evidence has suggested that women have greater emotional reactivity than men. However, it is unclear whether these differences in basic emotional responses are also associated with differences in emotional distractibility, and what the neural mechanisms that implement differences in emotional distractibility between women and men are. Functional MRI recording was used in conjunction with a working memory (WM) task, with emotional distraction (angry faces) presented during the interval between the memoranda and the probes. First, we found an increased impact of emotional distraction among women in trials associated with high-confidence responses, in the context of overall similar WM performance in women and men. Second, women showed increased sensitivity to emotional distraction in brain areas associated with “hot” emotional processing, whereas men showed increased sensitivity in areas associated with “cold” executive processing, in the context of overall similar patterns of response to emotional distraction in women and men. Third, a sex-related dorsal–ventral hemispheric dissociation emerged in the lateral PFC related to coping with emotional distraction, with women showing a positive correlation with WM performance in left ventral PFC, and men showing similar effects in the right dorsal PFC. In addition to extending to men results that have previously been reported in women, by showing that both sexes engage mechanisms that are similar overall in response to emotional distraction, the present study identifies sex differences in both the response to and coping with emotional distraction. These results have implications for understanding sex differences in the susceptibility to affective disorders, in which basic emotional responses, emotional distractibility, and coping abilities are altered.

Optimism and the brain: trait optimism mediates the protective role of the orbitofrontal cortex gray matter volume against anxiety

Converging evidence identifies trait optimism and the orbitofrontal cortex (OFC) as personality and brain factors influencing anxiety, but the nature of their relationships remains unclear. Here, the mechanisms underlying the protective role of trait optimism and of increased OFC volume against symptoms of anxiety were investigated in 61 healthy subjects, who completed measures of trait optimism and anxiety, and underwent structural scanning using magnetic resonance imaging. First, the OFC gray matter volume (GMV) was associated with increased optimism, which in turn was associated with reduced anxiety. Second, trait optimism mediated the relation between the left OFC volume and anxiety, thus demonstrating that increased GMV in this brain region protects against symptoms of anxiety through increased optimism. These results provide novel evidence about the brain-personality mechanisms protecting against anxiety symptoms in healthy functioning, and identify potential targets for preventive and therapeutic interventions aimed at reducing susceptibility and increasing resilience against emotional disturbances.

The effect of retrieval focus and emotional valence on the medial temporal lobe activity during autobiographical recollection

Laboratory-based episodic memory studies, using micro-events (pictures/words), point to a role of the amygdala (AMY), an emotion-based region, in the encoding and retrieval of emotionally valenced memories. However, autobiographical memory (AM) studies, using real-life personal events, do not conclusively support AMY’s involvement in AM recollection. This could be due to differences in instructions across the AM studies – i.e., whether emotional aspects were explicitly emphasized or not. The present study investigated the effect of retrieval focus on activity in emotion (AMY) and memory (hippocampus – HC) based regions of the medial temporal lobe in 17 subjects, who remembered emotional AMs while event-related fMRI data were recorded. The retrieval focus was manipulated by instructions to focus either on emotional (Emotion condition) or on other contextual (Context condition) details of the recollected AMs. The effect of retrieval focus according to the valence of AMs was also investigated by involving an equal proportion of positive and negative AMs. There were four main findings, showing both similarities and differences in retrieving positive and negative AMs. Regarding similarities, (1) focusing on Emotion was associated with increased scores of subjective re-experience of emotion and increased activity in the left AMY, for both positive and negative AMs, compared to focusing on Context; (2) the subjective emotional ratings were also positively correlated with bilateral AMY activity for both positive and negative AMs. Regarding differences, (3) focusing on Emotion was associated with increased activity for positive but not for negative AMs in the right AMY, and with (4) opposing patterns of activity linked to the valence of AMs in the left HC – i.e., increased activity for positive and decreased activity for negative AMs. These findings shed light on the role of AMY and HC in emotional AM recollection, linked to the retrieval focus and the valence of memories.

The Effect of Retrieval Focus and Emotional Valence on the Inferior Frontal Cortex Activity during Autobiographical Recollection

Although available evidence points to a role of the inferior frontal cortex (IFC) in both emotion processing and autobiographical memory (AM) recollection, it is unclear what the role of this region is in emotional AM recollection. The present study investigated whether IFC activity can be influenced by manipulations of the retrieval focus (emotional vs. non-emotional) and whether this influence is similar for AMs with positive and negative emotional valence. Participants were asked to focus either on emotional (Emotion condition) or on non-emotional contextual (Context condition) details during the elaboration of positive and negative AMs, while fMRI data were collected. The study yielded two main findings: (1) Focusing on Emotion compared to Context during AM recollection was associated with increased activity in bilateral IFC, for positive AMs, whereas negative AMs produced similarly high IFC activity during Emotion and Context conditions; (2) There was a hemispheric dissociation in the IFC linked to the experiencing of emotion and the focus of AM recollection, such that the left IFC activity correlated positively with the subjective re-experience of emotion during the Emotion condition, whereas the right IFC activity correlated negatively with the subjective re-experience of emotion during the Context condition, for both positive and negative AMs. Overall, the present findings suggest that IFC’s involvement during the recollection of emotional AMs is susceptible to manipulations of the retrieval focus only in the case of positive AMs, and that this region plays a role in both the enhancement and inhibition of emotional experience during AM recollection.