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

Abstract

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.

Keywords: BANE; Emotional memory; GANE; Hormones; Pupil dilation; Sympathetic arousal.

Fig 1

Experiment timeline by physiological arousal condition.

Fig 2

Pupil dilation response to task immediately prior to image encoding. The increase in pupil dilation was significantly greater in the immediate handgrip condition compared to either the residual or no-handgrip conditions.*p <.05

Fig 3

The relationship between physiological arousal conditions and memory for negative and positive images. Only women in the immediate handgrip-induced physiologicalarousal showed enhanced memory for negative images over positive images, *p < .01

Fig 4

Recall of positive and negative images as a function of estradiol, progesterone, and physiological arousal. There was a negativity bias in women with low levels of estradiol and progesterone. Under immediate physiological arousal, but not residual or no handgrip-related physiological arousal, women with low levels of estradiol and progesterone recalled significantly more negative compared to positive images. *p < .05.

Fig 5

Correlations between sex steroid hormone levels and memory difference score (% negative images recalled - % positive images recalled) in the immediate handgrip condition. a) Average progesterone levels trended toward a significant negative correlation with memory difference score. b) Average estradiol levels were significantly negatively correlated with memory difference score; higher levels of estradiol a predicted greater negativity bias in memory performance.