Sex, stress, and fear: Individual differences in conditioned learning

Zorawski, Michael; Cook, Craig A.; Kuhn, Cynthia M.; LaBar, Kevin S.

doi:10.3758/cabn.5.2.191

Cited by 99 publications

(90 citation statements)

References 106 publications

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“…This finding is consistent with animal data (Shors 2001) and with human studies showing improved performance in other forms of associative learning paradigms after exposure to acute stress (Zorawski et al 2005;Jackson et al 2006). Results from animal studies indicate that the stress-induced facilitation of eyeblink conditioning might be mediated by a circuit including basolateral amygdala (Shors and Mathew 1998), bed nucleus of the stria terminalis (Bangasser et al 2005), and hippocampus (Shors 2001;Shors et al 2001;Weiss et al 2005).…”

Section: Discussionsupporting

confidence: 78%

“…Results are often contradictory, which may in part be due to differences in stress exposure (acute versus repeated) (Wolf 2003) and different components of memory analyzed (consolidation or short-term memory versus retrieval or long-term memory) (Roozendaal 2002;Het et al 2005). Acute stress seems to facilitate memory formation when the learning procedure itself is arousing or emotionally valenced, or when learning takes place in a stressful context (Shors 2001;Bemelmans et al 2003;Akirav et al 2004;Jelici et al 2004;Putman et al 2004;Zorawski et al 2005;Abercrombie et al 2006;Andreano and Cahill 2006;Jackson et al 2006;Steidl et al 2006), but usually impairs retrieval (de Quervain et al 1998;Domes et al 2004). Repeated, or chronic, stress exposure is usually associated with deleterious effects on both memory consolidation and retrieval (Luine et al 1994;Newcomer et al 1999;Park et al 2001;Wright and Conrad 2005).…”

mentioning

confidence: 99%

“…In animals, learning performance is frequently assessed with classical conditioning (Shors 2001) and spatial navigation tests (Diamond et al 1996;Woodson et al 2003;Yang et al 2003;Akirav et al 2004), whereas only a few studies have applied learning paradigms based on object recognition (Baker and Kim 2002). Learning and memory studies in humans have typically involved the use of word lists, picture sets, or short stories (Kirschbaum et al 1996;Lupien et al 1997;Bemelmans et al 2003;Jelici et al 2004;Putman et al 2004;Takahashi 2005;Abercrombie et al 2006;Andreano and Cahill 2006), but only rarely have they applied paradigms that directly translate to those used in animal studies (Zorawski et al 2005;Jackson et al 2006). Accordingly, the primary aim of the present study was to evaluate the acute effect of stress exposure on learning performance in human analogs of two paradigms frequently used in animals, eyeblink conditioning, and spatial navigation.…”

mentioning

confidence: 99%

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Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men

Dunčko¹,

Cornwell²,

Cui³

et al. 2007

Learn. Mem.

115

100

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The present study investigated the effects of acute stress exposure on learning performance in humans using analogs of two paradigms frequently used in animals. Healthy male participants were exposed to the cold pressor test (CPT) procedure, i.e., insertion of the dominant hand into ice water for 60 sec. Following the CPT or the control procedure, participants completed a trace eyeblink conditioning task followed by a virtual navigation Morris water task (VNMWT). Hypothalamic-pituitary-adrenocortical (HPA) axis and sympathetic autonomic system (SAS) activity were assessed by measuring salivary cortisol, heart rate, and skin conductance at selected timepoints. Results revealed positive effects of stress on performance in both tasks. The stress group showed significantly more conditioned blinks than the control group during acquisition of trace eyeblink conditioning. The stress group also performed significantly better in the VNMWT than the control group, with the former showing significantly fewer failures to locate the hidden platform in the allotted time and smaller heading errors than the latter. Regression analyses revealed positive relationships between HPA axis and SAS activity during stress and eyeblink conditioning performance. Our results directly extend findings from animal studies and suggest potential physiological mechanisms underlying stress and learning.

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Section: Discussionsupporting

confidence: 78%

mentioning

confidence: 99%

mentioning

confidence: 99%

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Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men

Dunčko¹,

Cornwell²,

Cui³

et al. 2007

Learn. Mem.

115

100

View full text Add to dashboard Cite

show abstract

“…Men tend to show a greater cortisol stress response than women in laboratory studies (Kirschbaum, Kudielka, Gaab, Schommer, & Hellhammer, 1999). Studies examining sex differences have shown that men are more affected by stress than women on both declarative memory retrieval (Wolf, Schommer, Hellhammer, McEwen, & Kirschbaum, 2001) as well as in fear conditioning (Jackson, Payne, Nadel, & Jacobs, 2006;Zorawski, Blanding, Kuhn, & LaBar, 2006;Zorawski, Cook, Kuhn, & LaBar, 2005). The reason for this sex difference is unclear, although there has been speculation on the potential beneficial effects of female sex hormones (Wolf, 2006) and sex differences in cortisol response to stress (Kudielka & Kirschbaum, 2005).…”

Section: Introductionmentioning

confidence: 99%

Stress and emotional memory retrieval: Effects of sex and cortisol response

Buchanan

Tranel

2008

Neurobiology of Learning and Memory

158

118

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In some situations, memory is enhanced by stressful experience, while in others, it is impaired. The specific components of the stress-response that may result in these differing effects remain unclear, and the current study sought to address this knowledge gap. Forty healthy participants (20 women, 20 men) were exposed to emotionally arousing and neutral pictures. Twenty-four hours later, 20 participants underwent a social stressor (speech and math tests), and 20 underwent a control reading task, both followed by a delayed recall task. Cortisol responders to the stress condition (5 men and 1 woman) showed reduced memory retrieval for both neutral and emotionally arousing pictures. Men and women in the stress condition who did not produce a cortisol response showed increased retrieval of unpleasant pictures compared to controls. The results provide further evidence that cortisol is a primary effector in the stress-induced memory retrieval deficit. At the same time, stress can enhance memory retrieval performance, especially for emotional stimuli, when the cortisol response is absent.

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“…Studies in both humans and experimental animals have found that high endogenous baseline levels or exogenous administration of cortisol or stress prior to a memory task is associated with better immediate performance, implying beneficial effects on memory acquisition or encoding (Wilson et al 1975;Beckwith et al 1986;Shors et al 1992;Fehm-Wolfsdorf et al 1993;Bemelsmans et al 2002;Domes et al 2002;Lupien et al 2002a,b;Abercrombie et al 2003;Akirav et al 2004;Putman et al 2004;Maheu et al 2005b;Zorawski et al 2005). However, the issue is not unequivocal, and contradictory results have been reported (Wolkowitz et al 1990;Kirschbaum et al 1996;Lupien et al , 1999Wolf et al 2001a,b;Maheu et al 2004).…”

mentioning

confidence: 99%

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

Zorawski¹,

Blanding²,

Kuhn³

et al. 2006

Learn. Mem.

104

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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.Fear conditioning constitutes an adaptive cognitive mechanism in most organisms, allowing them to effectively learn about danger-relevant relationships in the environment and thus enhancing their survival chances. In a typical fear conditioning procedure in the laboratory, a previously neutral conditioned stimulus (CS) predicts the occurrence of an aversive unconditioned stimulus (US) and, as a result, acquires emotional properties. Conditioning is established when the CS triggers a conditioned response in the form of arousal reactions. An increased release of adrenocortical stress hormones-glucocorticoids-through activation of the hypothalamic-pituitary-adrenal (HPA) axis represents an important physiologic component of such arousal responses to fearful stimuli. The principal glucocorticoid in humans is cortisol.Basal and stress levels of glucocorticoids vary across individuals (Piazza et al. 1991;Meaney et al. 1993;Cools and Gingras 1998;Kirschbaum et al. 1999;Kabbaj et al. 2000;Stone et al. 2001;Bartels et al. 2003;Rohleder et al. 2003;Steptoe et al. 2003) and play an important but complex role in learning and memory (McEwen and Sapolsky 1995;Roozendaal 2003;Wolf 2003). While cortisol may be detrimental to memory function under some circumstances-i.e., when levels are elevated chronically (Starkman et al. 1992;Luine et al. 1993Luine et al. , 1994Arbel et al. 1994;Bodnoff et al. 1995;Conrad et al. 1996;Newcomer et al. 1999;Park et al. 2001) or during memory retrieval (De Quervain et al. 1998Buss et al. 2004)-they also have acute facilitative effects, presumably constituting part of the underlying neurobiological m...

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Sex, stress, and fear: Individual differences in conditioned learning

Cited by 99 publications

References 106 publications

Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men

Acute exposure to stress improves performance in trace eyeblink conditioning and spatial learning tasks in healthy men

Stress and emotional memory retrieval: Effects of sex and cortisol response

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

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