Effects of stress and sex on acquisition and consolidation of human fear conditioning

Abstract

We examined the relationship between stress hormone (cortisol) release and acquisition and consolidation of conditioned fear learning in healthy adults. Participants underwent acquisition of differential fear conditioning, and consolidation was assessed in a 24-h delayed extinction test. The acquisition phase was immediately followed by an 11-min psychosocial stress period (arithmetic test combined with a public speech). Salivary cortisol was sampled at various time points before and after acquisition and retention of fear conditioning. Results showed two effects of endogenous cortisol. Post-acquisition cortisol correlated with fear acquisition in male but not female participants. In addition, post-acquisition cortisol correlated with consolidation of fear but only in those participants with high cortisol levels. We conclude that in the short term, a robust and sexually dimorphic relationship exists between fear learning and stress hormone levels. For those participants whose fear learning is accompanied by high stress hormone levels, a long-term relationship exists between cortisol release and memory consolidation. These short-term and long-term effects may relate to the differential involvement of mineralocorticoid and glucocorticoid receptor subtypes, respectively. The findings have implications for understanding the role of stress, sex, and hormones in different stages of fear learning and memory.

Figure 1.

(A) Mean skin conductance responses (SCR) to the reinforced CS+ and the non-reinforced CS− in females and males across different phases of conditioning and the 24-h delayed retention test. *P < 0.02 (CS+ vs. CS−). (B) Differential SCR expressed as the difference between responses to the CS+ and CS−. μS = microSiemens. Error bars reflect SEMs.

Figure 2.

Differential skin conductance responses (SCRs), expressed as the difference between CS+ and CS−, during late acquisition and the 24-h delayed retention test in females and males as a function of cortisol level. The participants were assigned to high- and low-cortisol groups according to a median split of post-acquisition salivary cortisol levels (+45 min). *P < 0.001; n.s. = not significant. Error bars represent SEMs.

Figure 3.

Correlation between differential skin conductance responses (SCRs), expressed as the difference between CS+ and CS−, during late acquisition of conditioning and post-acquisition salivary cortisol levels (+45 min) in female (A) and male (B) participants.

Figure 4.

Salivary cortisol levels of participants in Zorawski et al. (2005) and the current study at various time points on Day 1. Time points are expressed relative to the beginning of the conditioning session. *P <0.01. Error bars represent SEMs.

Figure 5.

Correlation between differential skin conductance responses (SCRs), expressed as the difference between CS+ and CS−, during the 24-h delayed retention test on Day 2 (reflecting memory consolidation) and post-acquisition salivary cortisol levels on Day 1 (+45 min) in high- (A) and low-cortisol (B) participants. Data from participants in both experiments (current study and Zorawski et al. [2005) were pooled together and assigned to high- and low-cortisol groups according to a median split of post-acquisition salivary cortisol levels (+45 min on Day 1).