Shawn Nielsen

Sympathetic arousal increases a negative memory bias in young women with low sex hormone levels

Emotionally arousing events are typically better attended to and remembered than neutral ones. Current theories propose that arousal-induced increases in norepinephrine during encoding bias attention and memory in favor of affectively salient stimuli. Here, we tested this hypothesis by manipulating levels of physiological arousal prior to encoding and examining how it influenced memory for emotionally salient images, particularly those that are negative rather than positive in valence. We also tested whether sex steroid hormones interact with noradrenergic activity to influence these emotional memory biases in women. Healthy naturally cycling women and women on hormonal contraception completed one of the following physiological arousal manipulations prior to viewing a series of negative, positive and neutral images: (1) immediate handgrip arousal-isometric handgrip immediately prior to encoding, (2) residual handgrip arousal-isometric handgrip 15min prior to encoding, or (3) no handgrip. Sympathetic arousal was measured throughout the session via pupil diameter changes. Levels of 17β-estradiol and progesterone were measured via salivary samples. Memory performance was assessed approximately 10min after encoding using a surprise free recall test. The results indicated that handgrip successfully increased sympathetic arousal compared to the control task. Under immediate handgrip arousal, women showed enhanced memory for negative images over positive images; this pattern was not observed in women assigned to the residual and no-handgrip arousal conditions. Additionally, under immediate handgrip arousal, both high estradiol and progesterone levels attenuated the memory bias for negative over positive images. Follow-up hierarchical linear models revealed consistent effects when accounting for trial-by-trial variability in normative International Affective Picture System valence and arousal ratings. These findings suggest that heightened sympathetic arousal interacts with estradiol and progesterone levels during encoding to increase the mnemonic advantage of negative over positive emotional material.

Comparison of two isometric handgrip protocols on sympathetic arousal in women

Isometric handgrip is commonly used in stress research because the task reliably increases sympathetic arousal. Various handgrip protocols have been used; they vary in handgrip strength, duration of grip, and the number of cycles of handgrip and rest. However, most protocols require the calibration of a maximum voluntary contraction (MVC) prior to the handgrip task, which is not always convenient (i.e., in a functional magnetic resonance imaging study). Here, we wanted to test whether two handgrip protocols with different strength, duration and cycle protocols would reliably elicit sympathetic arousal in the absence of calibrating an MVC. Sixty-two healthy naturally cycling women and women on hormonal contraception participated in one of the two isometric handgrip protocols using a hand therapy ball of medium resistance. Women completed one of the following handgrip protocols: 1) 30% of a perceived maximum voluntary contraction for 3 min or 2) 3 cycles of maximum voluntary contraction for 18s with a one minute rest in between. All handgrip blocks were counterbalanced with a control condition. Sympathetic arousal was measured throughout the session via pupil diameter changes and salivary alpha-amylase. Results indicate that in the absence of calibrating an MVC, the handgrip tasks elicited different changes in sympathetic arousal. Pupil dilation responses increased significantly in the handgrip versus control blocks only in participants in the 18-s protocol. Additionally, more participants exhibited a salivary alpha-amylase response to the handgrip block in the 18-s condition compared to the 3-min condition. Thus, these results suggest that neuroimaging and behavioral studies with isometric handgrip should be able to successfully induce sympathetic nervous activity with the 18-s paradigm, regardless of the handgrip device and the ability to calibrate an MVC.

Stress-induced increases in progesterone and cortisol in naturally cycling women

Studies with animals of both sexes show that the adrenal glands release progesterone in addition to cortisol in response to stress. However, little is known about the progesterone response to stress in naturally cycling women. We investigated the effect of stress on estradiol, progesterone, and cortisol levels in women during the follicular phase of the menstrual cycle. We found that physical stress (the cold pressor test) had no effect on estradiol levels, but increased progesterone and cortisol. We also found positive correlations between baseline progesterone and cortisol levels, as well as between the change in progesterone and cortisol before and after water exposure in both the stress and control sessions. Mediation analyses revealed during the stress session, the change in progesterone from baseline to 42-min post-stress onset was mediated by the magnitude of change in cortisol levels across the same time span. Overall, these findings reveal that progesterone released in response to stress as observed in animals and men extends to women during the low ovarian output follicular phase of the menstrual cycle, and that the mechanism of release may be similar to the mechanism of cortisol release.

Noradrenergic mechanisms of arousal’s bidirectional effects on episodic memory

HighlightsBeta‐adrenoreceptor blockade attenuated arousal‐induced anterograde amnesia.Beta‐adrenoreceptor blockade attenuated arousal‐enhanced memory selectivity.Salivary alpha‐amylase change was correlated with arousal’s retrograde memory effects.This sAA‐memory relationship occurred across both the drug and placebo groups.Different noradrenergic mechanisms promote arousal’s bidirectional effects on memory. ABSTRACT Arousal’s selective effects on cognition go beyond the simple enhancement of emotional stimuli, sometimes enhancing and other times impairing processing of proximal neutral information. Past work shows that arousal impairs encoding of subsequent neutral stimuli regardless of their top‐down priority via the engagement of &bgr;‐adrenoreceptors. In contrast, retrograde amnesia induced by emotional arousal can flip to enhancement when preceding neutral items are prioritized in top‐down attention. Whether &bgr;‐adrenoreceptors also contribute to this retrograde memory enhancement of goal‐relevant neutral stimuli is unclear. In this pharmacological study, we administered 40 mg of propranolol or 40 mg of placebo to healthy young adults to examine whether emotional arousal’s bidirectional effects on declarative memory relies on &bgr;‐adrenoreceptor activation. Following pill intake, participants completed an emotional oddball task in which they were asked to prioritize a neutral object appearing just before an emotional or neutral oddball image within a sequence of 7 neutral objects. Under placebo, emotional oddballs impaired memory for lower priority oddball+1 objects but had no effect on memory for high priority oddball−1 objects. Propranolol blocked this anterograde amnesic effect of arousal. Emotional oddballs also enhanced selective memory trade‐offs significantly more in the placebo than drug condition, such that high priority oddball−1 objects were more likely to be remembered at the cost of their corresponding lower priority oddball+1 objects under arousal. Lastly, those who recalled more high priority oddball−1 objects preceding an emotional versus neutral oddball image showed greater increases in salivary alpha‐amylase, a biomarker of noradrenergic system activation, across the task. Together these findings suggest that different noradrenergic mechanisms contribute to the anterograde and retrograde mnemonic effects of arousal on proximal neutral memoranda.

Arousal amplifies biased competition between high and low priority memories more in women than in men: The role of elevated noradrenergic activity

Recent findings indicate that emotional arousal can enhance memory consolidation of goal-relevant stimuli while impairing it for irrelevant stimuli. According to one recent model, these goal-dependent memory tradeoffs are driven by arousal-induced release of norepinephrine (NE), which amplifies neural gain in target sensory and memory processing brain regions. Past work also shows that ovarian hormones modulate activity in the same regions thought to support NEs effects on memory, such as the amygdala, suggesting that men and women may be differentially susceptible to arousals dual effects on episodic memory. Here, we aimed to determine the neurohormonal mechanisms that mediate arousal-biased competition processes in memory. In a competitive visuo-attention task, participants viewed images of a transparent object overlaid on a background scene and explicitly memorized one of these stimuli while ignoring the other. Participants then heard emotional or neutral audio-clips and provided a subjective arousal rating. Hierarchical generalized linear modeling (HGLM) analyses revealed that greater pre-to-post task increases in salivary alpha-amylase (sAA), a biomarker of noradrenergic activity, was associated with significantly greater arousal-enhanced memory tradeoffs in women than in men. These sex-dependent effects appeared to result from phasic and background noradrenergic activity interacting to suppress task-irrelevant representations in women but enhancing them in men. Additionally, in naturally cycling women, low ovarian hormone levels interacted with increased noradrenergic activity to amplify memory selectivity independently of emotion-induced arousal. Together these findings suggest that increased noradrenergic transmission enhances preferential consolidation of goal-relevant memory traces according to phasic arousal and ovarian hormone levels in women.