Amygdala functional connectivity with medial prefrontal cortex at rest predicts the positivity effect in older adults’ memory

As people get older, they tend to remember more positive than negative information. This age-by-valence interaction has been called “positivity effect.” The current study addressed the hypotheses that baseline functional connectivity at rest is predictive of older adults' brain activity when learning emotional information and their positivity effect in memory. Using fMRI, we examined the relationship among resting-state functional connectivity, subsequent brain activity when learning emotional faces, and individual differences in the positivity effect (the relative tendency to remember faces expressing positive vs. negative emotions). Consistent with our hypothesis, older adults with a stronger positivity effect had increased functional coupling between amygdala and medial PFC (MPFC) during rest. In contrast, younger adults did not show the association between resting connectivity and memory positivity. A similar age-by-memory positivity interaction was also found when learning emotional faces. That is, memory positivity in older adults was associated with (a) enhanced MPFC activity when learning emotional faces and (b) increased negative functional coupling between amygdala and MPFC when learning negative faces. In contrast, memory positivity in younger adults was related to neither enhanced MPFC activity to emotional faces, nor MPFC–amygdala connectivity to negative faces. Furthermore, stronger MPFC–amygdala connectivity during rest was predictive of subsequent greater MPFC activity when learning emotional faces. Thus, emotion–memory interaction in older adults depends not only on the task-related brain activity but also on the baseline functional connectivity

Heart rate variability is associated with amygdala functional connectivity with MPFC across younger and older adults

The ability to regulate emotion is crucial to promote well-being. Evidence suggests that the medial prefrontal cortex (mPFC) and adjacent anterior cingulate (ACC) modulate amygdala activity during emotion regulation. Yet less is known about whether the amygdala-mPFC circuit is linked with regulation of the autonomic nervous system and whether the relationship differs across the adult lifespan. The current study tested the hypothesis that heart rate variability (HRV) reflects the strength of mPFC-amygdala interaction across younger and older adults. We recorded participants’ heart rates at baseline and examined whether baseline HRV was associated with amygdala-mPFC functional connectivity during rest. We found that higher HRV was associated with stronger functional connectivity between the amygdala and the mPFC during rest across younger and older adults. In addition to this age-invariant pattern, there was an age-related change, such that greater HRV was linked with stronger functional connectivity between amygdala and ventrolateral PFC (vlPFC) in younger than in older adults. These results are in line with past evidence that vlPFC is involved in emotion regulation especially in younger adults. Taken together, our results support the neurovisceral integration model and suggest that higher heart rate variability is associated with neural mechanisms that support successful emotional regulation across the adult lifespan

Exposure to negative socio-emotional events induces sustained alteration of resting-state brain networks in older adults

Basic emotional functions seem well preserved in older adults. However, their reactivity to and recovery from socially negative events remain poorly characterized. To address this, we designed a ‘task–rest’ paradigm in which 182 participants from two independent experiments underwent functional magnetic resonance imaging while exposed to socio-emotional videos. Experiment 1 (N = 55) validated the task in young and older participants and unveiled age-dependent effects on brain activity and connectivity that predominated in resting periods after (rather than during) negative social scenes. Crucially, emotional elicitation potentiated subsequent resting-state connectivity between default mode network and amygdala exclusively in older adults. Experiment 2 replicated these results in a large older adult cohort (N = 127) and additionally showed that emotion-driven changes in posterior default mode network–amygdala connectivity were associated with anxiety, rumination and negative thoughts. These findings uncover the neural dynamics of empathy-related functions in older adults and help understand its relationship to poor social stress recovery

Exploring Age-Related Changes in Resting State Functional Connectivity of the Amygdala: From Young to Middle Adulthood

Functional connectivities of the amygdala support emotional and cognitive processing. Life-span development of resting-state functional connectivities (rsFC) of the amygdala may underlie age-related differences in emotion regulatory mechanisms. To date, age-related changes in amygdala rsFC have been reported through adolescence but not as thoroughly for adulthood. This study investigated age-related differences in amygdala rsFC in 132 young and middle-aged adults (19–55 years). Data processing followed published routines. Overall, amygdala showed positive rsFC with the temporal, sensorimotor and ventromedial prefrontal cortex (vmPFC), insula and lentiform nucleus, and negative rsFC with visual, frontoparietal, and posterior cingulate cortex and caudate head. Amygdala rsFC with the cerebellum was positively correlated with age, and rsFCs with the dorsal medial prefrontal cortex (dmPFC) and somatomotor cortex were negatively correlated with age, at voxel p < 0.001 in combination with cluster p < 0.05 FWE. These age-dependent changes in connectivity appeared to manifest to a greater extent in men than in women, although the sex difference was only evident for the cerebellum in a slope test of age regressions (p = 0.0053). Previous studies showed amygdala interaction with the anterior cingulate cortex (ACC) and vmPFC during emotion regulation. In region of interest analysis, amygdala rsFC with the ACC and vmPFC did not show age-related changes. These findings suggest that intrinsic connectivity of the amygdala evolved from young to middle adulthood in selective brain regions, and may inform future studies of age-related emotion regulation and maladaptive development of the amygdala circuits as an etiological marker of emotional disorders

Age-related alterations in simple declarative memory and the effect of negative stimulus valence

Healthy aging has been shown to modulate the neural circuitry underlying simple declarative memory; however, the functional impact of negative stimulus valence on these changes has not been fully investigated. Using BOLD fMRI, we explored the effects of aging on behavioral performance, neural activity, and functional coupling during the encoding and retrieval of novel aversive and neutral scenes. Behaviorally, there was a main effect of valence with better recognition performance for aversive greater than neutral stimuli in both age groups. There was also a main effect of age with better recognition performance in younger participants compared to older participants. At the imaging level, there was a main effect of valence with increased activity in the medial-temporal lobe (amygdala and hippocampus) during both encoding and retrieval of aversive relative to neutral stimuli. There was also a main effect of age with older participants showing decreased engagement of medial-temporal lobe structures and increased engagement of prefrontal structures during both encoding and retrieval sessions. Interestingly, older participants presented with relatively decreased amygdalar-hippocampal coupling and increased amygdalar-prefrontal coupling when compared to younger participants. Furthermore, older participants showed increased activation in prefrontal cortices and decreased activation in the amygdala when contrasting the retrieval of aversive and neutral scenes. These results suggest that although normal aging is associated with a decline in declarative memory with alterations in the neural activity and connectivity of brain regions underlying simple declarative memory, memory for aversive stimuli is relatively better preserved than for neutral stimuli, possibly through greater compensatory prefrontal cortical activit

Effects of emotion and interoception on memory

Emotional events are usually remembered better than neutral events. For example, people usually remember instances of own success or failure better than mundane events. Despite the abundant literature on the interaction between emotion and memory, there are still some unanswered questions with regards to the effects of emotion on memory and moderators of emotional memory. One of these questions concerns whether and how emotion affects memory for neutral information encountered later. The second question concerns the sources of individual differences in emotional memory. There are individual differences in emotional memory; such that some individuals may be predisposed to remember negative information more than positive or vice versa. Such differences in emotional memory may be rooted in individual differences in the bodily responses (interoception) as well as brain’s functional organisation. In the present thesis, each of these questions was addressed across three studies. The first study examined how experiencing emotional arousal affects memory of neutral information encountered minutes later; and whether the goal-relevance of the information modulates the effects of emotional arousal. Using a public speech task combined with false heart rate feedback, the study found that emotional arousal does not affect memory of neutral items viewed minutes later, irrespective of their goal-relevance. The second study examined the effects of interoception on emotional memory by presenting heartbeat biofeedback while presenting emotional images. The study revealed that attending to heartbeat biofeedback leads to increased negativity bias in memory, suggesting that interoception may play key roles in individual differences in memory for emotional items concurrently presented. The third study investigated the association between resting-state functional connectivity and emotional memory in a large dataset, utilising machine learning algorithms. Yet resting-state functional connectivity was not associated with individual differences in emotional memory. In sum, the studies reported in the thesis cast doubts on some of the previous literature’s claims that a) emotional arousal affects memory for other information individuals encounter subsequently and b) resting-state connectivity is useful to predict individual differences in emotional memory or cognitive processing in general. The findings also showed the effect of attention to heartbeats on emotional memory, suggesting that interoception may be associated with individual differences in emotional memory. The research has practical implications and theoretical implications leading to better understanding of the effects and moderators of emotional memory

The relation between structural and functional connectivity depends on age and on task goals

The last decade has seen an increase in neuroimaging studies examining structural (i.e., structural integrity of white matter tracts) and functional connectivity (e.g., correlations in neural activity throughout the brain). Although structural and functional connectivity changes have often been measured independently, examining the relation between these two measures is critical to understanding the specific function of neural networks and the ways they may differ across tasks and individuals. The current study addressed this question by examining the effect of age (treated as a continuous variable) and emotional valence on the relation between functional and structural connectivity. As prior studies have suggested that prefrontal regions may guide and regulate emotional memory search via functional connections with the amygdala, the current analysis focused on functional connectivity between the left amygdala and the left prefrontal cortex, and structural integrity of the uncinate fasciculus, a white matter tract connecting prefrontal and temporal regions.Participants took part in a scanned retrieval task in which they recalled positive, negative, and neutral images associated with neutral titles. Aging was associated with a significant increase in the relation between measures of structural integrity (specifically, fractional anisotropy, or FA) along the uncinate fasciculus and functional connectivity between the left ventral prefrontal cortex and amygdala during positive event retrieval, but not negative or neutral retrieval. Notably, during negative event retrieval, age was linked to stronger structure-function relations between the amygdala and the dorsal anterior cingulate cortex, such that increased structural integrity predicted strong negative functional connectivity in older adults only. These findings are consistent with theories that older adults may engage regulatory strategies if they have the structural pathways to allow them to do so

Age-related alterations in functional connectivity patterns during working memory encoding of emotional items

Previous findings indicate age-related differences in frontal-amygdala connectivity during emotional processing. However, direct evidence for age differences in brain functional activation and connectivity during emotional processing and concomitant behavioral implications is lacking. In the present study, we examined the impact of aging on the neural signature of selective attention to emotional information during working memory (WM) encoding. Participants completed an emotional WM task in which they were asked to attend to emotional targets and ignore irrelevant distractors. Despite an overall reduction in accuracy for older relative to younger adults, no behavioral age effect was observed as a function of emotional valence. The functional connectivity patterns of left ventrolateral prefrontal cortex showed that younger adults recruited one network for encoding of both positive and negative emotional targets and this network contributed to higher memory accuracy in this cohort. Older adults, on the other hand, engaged two distinct networks for encoding of positive and negative targets. The functional connectivity analysis using left amygdala further demonstrated that older adults recruited one single network during encoding of positive as well as negative targets whereas younger adults recruited this network only for encoding of negative items. The engagement of amygdala functional network also contributed to higher memory performance and faster response times in older adults. Our findings provide novel insights into the differential roles of functional brain networks connected to the medial PFC and amygdala during encoding of emotionally-valenced items with advancing age

Exposure to negative socio-emotional events induces sustained alteration of resting-state brain networks in older adults.

peer reviewedBasic emotional functions seem well preserved in older adults. However, their reactivity to and recovery from socially negative events remain poorly characterized. To address this, we designed a 'task-rest' paradigm in which 182 participants from two independent experiments underwent functional magnetic resonance imaging while exposed to socio-emotional videos. Experiment 1 (N = 55) validated the task in young and older participants and unveiled age-dependent effects on brain activity and connectivity that predominated in resting periods after (rather than during) negative social scenes. Crucially, emotional elicitation potentiated subsequent resting-state connectivity between default mode network and amygdala exclusively in older adults. Experiment 2 replicated these results in a large older adult cohort (N = 127) and additionally showed that emotion-driven changes in posterior default mode network-amygdala connectivity were associated with anxiety, rumination and negative thoughts. These findings uncover the neural dynamics of empathy-related functions in older adults and help understand its relationship to poor social stress recovery