Neural correlates of emotion-attention interactions: from perception, learning, and memory to social cognition, individual differences, and training interventions

Due to their ability to capture attention, emotional stimuli tend to benefit from enhanced perceptual processing, which can be helpful when such stimuli are task-relevant but hindering when they are task-irrelevant. Altered emotion-attention interactions have been associated with symptoms of affective disturbances, and emerging research focuses on improving emotion-attention interactions to prevent or treat affective disorders. In line with the Human Affectome Project’s emphasis on linguistic components, we also analyzed the language used to describe attention-related aspects of emotion, and highlighted terms related to domains such as conscious awareness, motivational effects of attention, social attention, and emotion regulation. These terms were discussed within a broader review of available evidence regarding the neural correlates of (1) Emotion-Attention Interactions in Perception, (2) Emotion-Attention Interactions in Learning and Memory, (3) Individual Differences in Emotion-Attention Interactions, and (4) Training and Interventions to Optimize Emotion-Attention Interactions. This comprehensive approach enabled an integrative overview of the current knowledge regarding the mechanisms of emotion-attention interactions at multiple levels of analysis, and identification of emerging directions for future investigations

Emotional valence and arousal affect reading in an interactive way: neuroimaging evidence for an approach-withdrawal framework

A growing body of literature shows that the emotional content of verbal material affects reading, wherein emotional words are given processing priority compared to neutral words. Human emotions can be conceptualised within a two-dimensional model comprised of emotional valence and arousal (intensity). These variables are at least in part distinct, but recent studies report interactive effects during implicit emotion processing and relate these to stimulus-evoked approach-withdrawal tendencies. The aim of the present study was to explore how valence and arousal interact at the neural level, during implicit emotion word processing. The emotional attributes of written word stimuli were orthogonally manipulated based on behavioural ratings from a corpus of emotion words. Stimuli were presented during an fMRI experiment while 16 participants performed a lexical decision task, which did not require explicit evaluation of a word's emotional content. Results showed greater neural activation within right insular cortex in response to stimuli evoking conflicting approach-withdrawal tendencies (i.e., positive high-arousal and negative low-arousal words) compared to stimuli evoking congruent approach vs. withdrawal tendencies (i.e., positive low-arousal and negative high-arousal words). Further, a significant cluster of activation in the left extra-striate cortex was found in response to emotional than neutral words, suggesting enhanced perceptual processing of emotionally salient stimuli. These findings support an interactive two-dimensional approach to the study of emotion word recognition and suggest that the integration of valence and arousal dimensions recruits a brain region associated with interoception, emotional awareness and sympathetic functions

The Effect of Negative and Positive Emotionality on Associative Memory: An fMRI Study

In general, emotion is known to enhance memory processes. However, the effect of emotion on associative memory and the underling neural mechanisms remains largely unexplored. In this study, we explored brain activation during an associative memory task that involved the encoding and retrieval of word and face pairs. The word and face pairs consisted of either negative or positive words with neutral faces. Significant hippocampal activation was observed during both encoding and retrieval, regardless of whether the word was negative or positive. Negative and positive emotionality differentially affected the hemodynamic responses to encoding and retrieval in the amygdala, with increased responses during encoding negative word and face pairs. Furthermore, activation of the amygdala during encoding of negative word and neutral face pairs was inversely correlated with subsequent memory retrieval. These findings suggest that activation of the amygdala induced by negative emotion during encoding may disrupt associative memory performance

Age-Related Attenuation of Dominant Hand Superiority

The decline of motor performance of the human hand-arm system with age is well-documented. While dominant hand performance is superior to that of the non-dominant hand in young individuals, little is known of possible age-related changes in hand dominance. We investigated age-related alterations of hand dominance in 20 to 90 year old subjects. All subjects were unambiguously right-handed according to the Edinburgh Handedness Inventory. In Experiment 1, motor performance for aiming, postural tremor, precision of arm-hand movement, speed of arm-hand movement, and wrist-finger speed tasks were tested. In Experiment 2, accelerometer-sensors were used to obtain objective records of hand use in everyday activities

Neural correlates of enhanced visual short-term memory for angry faces: An fMRI study

Copyright: © 2008 Jackson et al.Background: Fluid and effective social communication requires that both face identity and emotional expression information are encoded and maintained in visual short-term memory (VSTM) to enable a coherent, ongoing picture of the world and its players. This appears to be of particular evolutionary importance when confronted with potentially threatening displays of emotion - previous research has shown better VSTM for angry versus happy or neutral face identities.Methodology/Principal Findings: Using functional magnetic resonance imaging, here we investigated the neural correlates of this angry face benefit in VSTM. Participants were shown between one and four to-be-remembered angry, happy, or neutral faces, and after a short retention delay they stated whether a single probe face had been present or not in the previous display. All faces in any one display expressed the same emotion, and the task required memory for face identity. We find enhanced VSTM for angry face identities and describe the right hemisphere brain network underpinning this effect, which involves the globus pallidus, superior temporal sulcus, and frontal lobe. Increased activity in the globus pallidus was significantly correlated with the angry benefit in VSTM. Areas modulated by emotion were distinct from those modulated by memory load.Conclusions/Significance: Our results provide evidence for a key role of the basal ganglia as an interface between emotion and cognition, supported by a frontal, temporal, and occipital network.The authors were supported by a Wellcome Trust grant (grant number 077185/Z/05/Z) and by BBSRC (UK) grant BBS/B/16178

A rightward shift in the visuospatial attention vector with healthy aging

The study of lateralised visuospatial attention bias in non-clinical samples has revealed a systematic group-level leftward bias (pseudoneglect), possibly as a consequence of right hemisphere dominance for visuospatial attention. Pseudoneglect appears to be modulated by age, with a reduced or even reversed bias typically present in elderly participants. It has been suggested that this shift in bias may arise due to disproportionate aging of the right hemisphere and/or an increase in complementary functional recruitment of the left hemisphere for visuospatial processing. In this study, we report rightward shifts in subjective midpoint judgement relative to healthy young participants whilst elderly participants performed a computerized version of the landmark task (in which they had to judge whether a transection mark appeared closer to the right or left end of a line) on three different line lengths. This manipulation of stimulus properties led to a similar behavioural pattern in both the young and the elderly: a rightward shift in subjective midpoint with decreasing line length, which even resulted in a systematic rightward bias in elderly participants for the shortest line length (1.98° of visual angle). Overall performance precision for the task was lower in the elderly participants regardless of line length, suggesting reduced landmark task discrimination sensitivity with healthy aging. This rightward shift in the attentional vector with healthy aging is likely to result from a reduction in right hemisphere resources/dominance for attentional processing in elderly participants. The significant rightward bias in the elderly for short lines may even suggest a reversal of hemisphere dominance in favour of the left hemisphere/right visual field under specific conditions

Serotonin transporter gene polymorphisms and brain function during emotional distraction from cognitive processing in posttraumatic stress disorder

BACKGROUND: Serotonergic system dysfunction has been implicated in posttraumatic stress disorder (PTSD). Genetic polymorphisms associated with serotonin signaling may predict differences in brain circuitry involved in emotion processing and deficits associated with PTSD. In healthy individuals, common functional polymorphisms in the serotonin transporter gene (SLC6A4) have been shown to modulate amygdala and prefrontal cortex (PFC) activity in response to salient emotional stimuli. Similar patterns of differential neural responses to emotional stimuli have been demonstrated in PTSD but genetic factors influencing these activations have yet to be examined. METHODS: We investigated whether SLC6A4 promoter polymorphisms (5-HTTLPR, rs25531) and several downstream single nucleotide polymorphisms (SNPs) modulated activity of brain regions involved in the cognitive control of emotion in post-9/11 veterans with PTSD. We used functional MRI to examine neural activity in a PTSD group (n = 22) and a trauma-exposed control group (n = 20) in response to trauma-related images presented as task-irrelevant distractors during the active maintenance period of a delayed-response working memory task. Regions of interest were derived by contrasting activation for the most distracting and least distracting conditions across participants. RESULTS: In patients with PTSD, when compared to trauma-exposed controls, rs16965628 (associated with serotonin transporter gene expression) modulated task-related ventrolateral PFC activation and 5-HTTLPR tended to modulate left amygdala activation. Subsequent to combat-related trauma, these SLC6A4 polymorphisms may bias serotonin signaling and the neural circuitry mediating cognitive control of emotion in patients with PTSD. CONCLUSIONS: The SLC6A4 SNP rs16965628 and 5-HTTLPR are associated with a bias in neural responses to traumatic reminders and cognitive control of emotions in patients with PTSD. Functional MRI may help identify intermediate phenotypes and dimensions of PTSD that clarify the functional link between genes and disease phenotype, and also highlight features of PTSD that show more proximal influence of susceptibility genes compared to current clinical categorizations

How Emotion Strengthens the Recollective Experience: A Time-Dependent Hippocampal Process

Emotion significantly strengthens the subjective recollective experience even when objective accuracy of the memory is not improved. Here, we examine if this modulation is related to the effect of emotion on hippocampal-dependent memory consolidation. Two critical predictions follow from this hypothesis. First, since consolidation is assumed to take time, the enhancement in the recollective experience for emotional compared to neutral memories should become more apparent following a delay. Second, if the emotion advantage is critically dependent on the hippocampus, then the effects should be reduced in amnesic patients with hippocampal damage. To test these predictions we examined the recollective experience for emotional and neutral photos at two retention intervals (Experiment 1), and in amnesics and controls (Experiment 2). Emotional memories were associated with an enhancement in the recollective experience that was greatest after a delay, whereas familiarity was not influenced by emotion. In amnesics with hippocampal damage the emotion effect on recollective experience was reduced. Surprisingly, however, these patients still showed a general memory advantage for emotional compared to neutral items, but this effect was manifest primarily as a facilitation of familiarity. The results support the consolidation hypothesis of recollective experience, but suggest that the effects of emotion on episodic memory are not exclusively hippocampally mediated. Rather, emotion may enhance recognition by facilitating familiarity when recollection is impaired due to hippocampal damage

Differential effects of emotional cues on components of prospective memory: an ERP study

So far, little is known about the neurocognitive mechanisms associated with emotion effects on prospective memory (PM) performance. Thus, this study aimed at disentangling possible mechanisms for the effects of emotional valence of PM cues on the distinct phases composing PM by investigating event-related potentials (ERPs). Participants were engaged in an ongoing N-back task while being required to perform a PM task. The emotional valence of both the ongoing pictures and the PM cues was manipulated (pleasant, neutral, unpleasant). ERPs were recorded during the PM phases, such as encoding, maintenance, and retrieval of the intention. A recognition task including PM cues and ongoing stimuli was also performed at the end of the sessions. ERP results suggest that emotional PM cues not only trigger an automatic, bottom-up, capture of attention, but also boost a greater allocation of top-down processes. These processes seem to be recruited to hold attention toward the emotional stimuli and to retrieve the intention from memory, likely because of the motivational significance of the emotional stimuli. Moreover, pleasant PM cues seemed to modulate especially the prospective component, as revealed by changes in the amplitude of the ERP correlates of strategic monitoring as a function of the relevance of the valence for the PM task. Unpleasant pictures seemed to modulate especially the retrospective component, as revealed by the largest old/new effect being elicited by unpleasant PM pictures in the recognition task