skip to main content

Title: Distinct stress‐related changes in intrinsic amygdala connectivity predict subsequent positive and negative memory performance

Experiencing stress before an event can influence how that event is later remembered. In the current study, we examine how individual differences in one's physiological response to a stressor are related to changes to underlying brain states and memory performance. Specifically, we examined how changes in intrinsic amygdala connectivity relate to positive and negative memory performance as a function of stress response, defined as a change in cortisol. Twenty‐five participants underwent a social stressor before an incidental emotional memory encoding task. Cortisol samples were obtained before and after the stressor to measure individual differences in stress response. Three resting state scans (pre‐stressor, post‐stressor/pre‐encoding and post‐encoding) were conducted to evaluate pre‐ to post‐stressor and pre‐ to post‐encoding changes to intrinsic amygdala connectivity. Analyses examined relations between greater cortisol changes and connectivity changes. Greater cortisol increases were associated with a greaterdecreasein prefrontal‐amygdala connectivity following the stressor and a reversal in the relation between prefrontal‐amygdala connectivity and negative vs. positive memory performance. Greater cortisol increases were also associated with a greaterincreasein amygdala connectivity with a number of posterior sensory regions following encoding. Consistent with prior findings in non‐stressed individuals, pre‐ to post‐encoding increases in amygdala‐posterior connectivity were associated with greater negative relative to positive memory performance, although this was specific to lateral rather than medial posterior regions and to participants with the greatest cortisol changes. These findings suggest that stress response is associated with changes in intrinsic connectivity that have downstream effects on the valence of remembered emotional content.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
European Journal of Neuroscience
Page Range / eLocation ID:
p. 4744-4765
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Sleep and stress independently enhance emotional memory consolidation. In particular, theta oscillations (4–7 Hz) during rapid eye movement (REM) sleep increase coherence in an emotional memory network (i.e., hippocampus, amygdala, and prefrontal cortex) and enhance emotional memory. However, little is known about how stress during learning mightinteractwith subsequent REM theta activity to affect emotional memory. In the current study, we examined whether the relationship between REM theta activity and emotional memory differs as a function of pre‐encoding stress exposure and reactivity. Participants underwent a psychosocial stressor (the Trier Social Stress Task;n= 32) or a comparable control task (n= 32) prior to encoding. Task‐evoked cortisol reactivity was assessed by salivary cortisol rise from pre‐ to post‐stressor, and participants in the stress condition were additionally categorized as high or low cortisol responders via a median split. During incidental encoding, participants studied 150 line drawings of negative, neutral, and positive images, followed by the complete color photo. All participants then slept overnight in the lab with polysomnographic recording. The next day, they were given a surprise recognition memory task. Results showed that memory was better for emotional relative to neutral information. Critically, these findings were observed only in the stress condition. No emotional memory benefit was observed in the control condition. In stressed participants, REM theta power significantly predicted memory for emotional information, specifically for positive items. This relationship was observed only in high cortisol responders. For low responders and controls, there was no relationship between REM theta and memory of any valence. These findings provide evidence that elevated stress at encoding, and accompanying changes in neuromodulators such as cortisol, may interact with theta activity during REM sleep to promote selective consolidation of emotional information.

    more » « less
  2. Abstract

    Both stress and sleep enhance emotional memory. They also interact, with the largest effect of sleep on emotional memory being seen when stress occurs shortly before or after encoding. Slow wave sleep (SWS) is critical for long‐term episodic memory, facilitated by the temporal coupling of slow oscillations and sleep spindles. Prior work in humans has shown these associations for neutral information in non‐stressed participants. Whether coupling interacts with stress to facilitate emotional memory formation is unknown. Here, we addressed this question by reanalyzing an existing dataset of 64 individuals. Participants underwent a psychosocial stressor (32) or comparable control (32) prior to the encoding of 150‐line drawings of neutral, positive, and negative images. All participants slept overnight with polysomnography, before being given a surprise memory test the following day. In the stress group, time spent in SWS was positively correlated with memory for images of all valences. Results were driven by those who showed a high cortisol response to the stressor, compared to low responders. The amount of slow oscillation‐spindle coupling during SWS was negatively associated with neutral and emotional memory in the stress group only. The association with emotional memory was significantly stronger than for neutral memory within the stress group. These results suggest that stress around the time of initial memory formation impacts the relationship between slow wave sleep and memory.

    more » « less
  3. null (Ed.)
    Despite the well-defined behavioral criteria for posttraumatic stress disorder (PTSD), clinical care is com- plicated by the heterogeneity of biological factors underly- ing impairment. Eye movement tasks provide an opportunity to assess the relationships between aberrant neurobiological function and non-volitional performance metrics that are not dependent on self-report. A recent study using an emotional variant of the antisaccade task demonstrated attentional control biases that interfered with task performance in Veterans with PTSD. Here we present a neuroanatomically-inspired com- putational model based on gated attractor networks that is designed to replicate oculomotor behavior on an affective anti- saccade task. The model includes the putative neural circuitry underlying fear response (amygdala) and top-down inhibitory control (prefrontal cortex), and is capable of generating testable predictions about the causal implications of changes in this circuitry on task performance and neural activation associated with PTSD. Calibrating the model with the results of behavioral and neuroimaging studies on patient populations yields a pattern of connectivity changes characterized by increased amygdala sensitivity and reduced top-down prefrontal control that is consistent with the fear conditioning model of PTSD. In addition, the model makes experimentally verifiable predictions about the consequences of increased prefrontal connectivity associated with cognitive reappraisal training. Keywords: posttraumatic stress disorder, antisaccade task, inhibitory control deficits, attentional bias, cognitive control. 
    more » « less
  4. null (Ed.)
    Models of episodic emotional memory typically concern why emotional events are more likely to be remembered than neutral events, focusing on interactions between the amygdala and other medial temporal lobe regions. But memories of emotional events can be distinguished by their affective tone and framing. We propose that the dorsomedial prefrontal cortex (dmPFC), a region that is increasingly recognized to crosscut socio-affective and cognitive domains, plays a key role in this aspect of emotional memory. After briefly reviewing the role of the dmPFC in the control of behaviors ranging from actions to emotions to social cognition, we delve into the accumulating evidence that its functions also subserve the abstraction of meaning from events and the control of memories, particularly emotional memories. Its role begins during the encoding of emotional experiences, continues through their stabilization, and endures during the retrieval of memory content. At each phase, the dmPFC participates in the integration of affective and cognitive components of memories, setting up networks and framings that either emphasize or de-emphasize emotional content. Incorporating the dmPFC into models of episodic emotional memory should provide leverage in understanding the affective tone with which experiences are brought to memory. 
    more » « less
  5. Abstract

    Infancy is marked by rapid neural and emotional development. The relation between brain function and emotion in infancy, however, is not well understood. Methods for measuring brain function predominantly rely on the BOLD signal; however, interpretation of the BOLD signal in infancy is challenging because the neuronal‐hemodynamic relation is immature. Regional cerebral blood flow (rCBF) provides a context for the infant BOLD signal and can yield insight into the developmental maturity of brain regions that may support affective behaviors. This study aims to elucidate the relations among rCBF, age, and emotion in infancy. One hundred and seven mothers reported their infants' (infant ageM ± SD = 6.14 ± 0.51 months) temperament. A subsample of infants completed MRI scans, 38 of whom produced usable perfusion MRI during natural sleep to quantify rCBF. Mother‐infant dyads completed the repeated Still‐Face Paradigm, from which infant affect reactivity and recovery to stress were quantified. We tested associations of infant age at scan, temperament factor scores, and observed affect reactivity and recovery with voxel‐wise rCBF. Infant age was positively associated with CBF in nearly all voxels, with peaks located in sensory cortices and the ventral prefrontal cortex, supporting the formulation that rCBF is an indicator of tissue maturity. Temperamental Negative Affect and recovery of positive affect following a stressor were positively associated with rCBF in several cortical and subcortical limbic regions, including the orbitofrontal cortex and inferior frontal gyrus. This finding yields insight into the nature of affective neurodevelopment during infancy. Specifically, infants with relatively increased prefrontal cortex maturity may evidence a disposition toward greater negative affect and negative reactivity in their daily lives yet show better recovery of positive affect following a social stressor.

    more » « less