Influence of the stress hormone cortisol on fear conditioning in humans: Evidence for sex differences in the response of the prefrontal cortex

Stark, Rudolf; Wolf, Oliver T.; Tabbert, Katharina; Kagerer, Sabine; Zimmermann, Mark; Kirsch, Peter; Schienle, Anne; Vaitl, Dieter

doi:10.1016/j.neuroimage.2006.05.046

Cited by 154 publications

(106 citation statements)

References 67 publications

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“…Other sex differences in learning are mediated by the presence of sex hormones and sex differences in the structure of the brain (27,28,(39)(40)(41). As presented here, the total volume of the dentate gyrus is greater in males than in females (27,42).…”

Section: Discussionmentioning

confidence: 49%

Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi

Dalla

Papachristos

Whetstone

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

108

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Learning increases the survival of new cells that are generated in the hippocampal formation before the training experience, especially if the animal learns to associate stimuli across time [Gould E, Beylin A, Tanapat P, Reeves A, Shors TJ (1999) Nat Neurosci 2:260 -265]. All relevant studies have been conducted on male rats, despite evidence for sex differences in this type of learning. In the present study, we asked whether sex differences in learning influence the survival of neurons generated in the adult hippocampus. Male and female adult rats were injected with one dose of bromodeoxyuridine (BrdU; 200 mg/kg), to label one population of dividing cells. One week later, half of the animals were trained with a temporal learning task of trace eyeblink conditioning, while the other half were not trained. Animals were killed 1 day after training (12 days after the BrdU injection). Hippocampal tissue was stained for BrdU and a marker of immature neurons, doublecortin. Both sexes learned to emit the conditioned eyeblink response during the trace interval. As a consequence, more new neurons remained in their hippocampi than in sex-matched controls. In individual animals, the number of surviving cells correlated positively with asymptotic performance; those that expressed more learned responses retained more new neurons. However, animals that learned very well retained even more new cells if they required many trials to do so. Because females emitted more learned responses than males did, they retained nearly twice as many new cells per unit volume of tissue. This effect was most evident in the ventral region of the hippocampal formation. Thus, sex differences in learning alter the anatomical structure of the hippocampus. As a result, male and female brains continue to differentiate in adulthood.eyeblink conditioning ͉ learning ͉ neurogenesis ͉ sex differences ͉ stem cell

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Section: Discussionmentioning

confidence: 49%

Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi

Dalla

Papachristos

Whetstone

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

108

View full text Add to dashboard Cite

show abstract

“…Previous studies have reported substantial gender differences for the relationship between cortisol and memory (Andreano & Cahill, 2006;Jackson, Payne, Nadel, & Jacobs, 2006;Stark et al, 2006;Zorawski, Blanding, Kuhn, & LaBar, 2006;Wolf, Schommer, Hellhammer, McEwen, & Kirschbaum, 2001). We did not find substantial differences between men and women.…”

Section: Discussionmentioning

confidence: 99%

Associations between Basal Cortisol Levels and Memory Retrieval in Healthy Young Individuals

Ackermann

Hartmann

Papassotiropoulos

et al. 2013

Journal of Cognitive Neuroscience

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Cortisol is known to affect memory processes. On the one hand, stress-induced or pharmacologically induced elevations of cortisol levels enhance memory consolidation. On the other hand, such experimentally induced elevations of cortisol levels have been shown to impair memory retrieval. However, the effects of individual differences in basal cortisol levels on memory processes remain largely unknown. Here we tested whether individual differences in cortisol levels predict picture learning and recall in a large sample. A total of 1225 healthy young women and men viewed two different sets of emotional and neutral pictures on two consecutive days. Both sets were recalled after a short delay (10 min). On Day 2, the pictures seen on Day 1 were additionally recalled, resulting in a long-delay (20 hr) recall condition. Cortisol levels were measured three times on Days 1 and 2 via saliva samples before encoding, between encoding and recall as well as after recall testing. We show that stronger decreases in cortisol levels during retrieval testing were associated with better recall performance of pictures, regardless of emotional valence of the pictures or length of the retention interval (i.e., 10 min vs. 20 hr). In contrast, average cortisol levels during retrieval were not related to picture recall. Remarkably during encoding, individual differences in average cortisol levels as well as changes in cortisol did not predict memory recall. Our results support previous findings indicating that higher cortisol levels during retrieval testing hinders recall of episodic memories and extend this view onto interindividual changes in basal cortisol levels. However, the effects of individual differences in basal cortisol levels on memory processes remain largely unknown. Here we tested whether individual differences in cortisol levels predict picture learning and recall in a large sample. A total of 1225 healthy young women and men viewed two different sets of emotional and neutral pictures on two consecutive days. Both sets were recalled after a short delay (10 min). On Day 2, the pictures seen on Day 1 were additionally recalled, resulting in a long-delay (20 hr) recall condition.Cortisol levels were measured three times on Days 1 and 2 via saliva samples before encoding, between encoding and recall as well as after recall testing. We show that stronger decreases in cortisol levels during retrieval testing were associated with better recall performance of pictures, regardless of emotional valence of the pictures or length of the retention interval (i.e., 10 min vs. 20 hr). In contrast, average cortisol levels during retrieval were not related to picture recall. Remarkably during encoding, individual differences in average cortisol levels as well as changes in cortisol did not predict memory recall. Our results support previous findings indicating that higher cortisol levels during retrieval testing hinders recall of episodic memories and extend this view onto interindividual changes in basal cortisol levels. ■

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“…Studies have shown that glucocorticoid administration alters metabolism and blood flow in the prefrontal cortex and several other regions (de Quervain et al, 2003;Stark et al, 2006). Pruessner et al (2004) showed that ventral striatal DA release was increased in response to a psychosocial stressor in humans who reported insufficient early life maternal care.…”

Section: Discussionmentioning

confidence: 99%

Association of Amphetamine-Induced Striatal Dopamine Release and Cortisol Responses to Psychological Stress

Wand

Oswald

McCaul

et al. 2007

Neuropsychopharmacol

146

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Preclinical studies have shown that stress and glucocorticoids increase mesolimbic dopamine (DA) and thereby facilitate psychostimulant self-administration. The relationship between stress-induced cortisol and mesolimbic DA responses to psychostimulants has not been studied in humans. To test the hypotheses that glucocorticoid responses to psychological stress are correlated with DA and subjective responses to psychostimulants in humans, 25 healthy adults (18-29 years) completed the Trier Social Stress Test (TSST) and two positron emission tomography (PET) scans with high-specific [ 11 C]raclopride. The first scan was preceded by intravenous saline and the second by amphetamine (AMPH). Findings showed that stress-induced cortisol levels were positively associated with AMPH-induced DA release in the ventral striatum and other striatal regions. Subjects with higher cortisol responses to stress also reported more positive subjective drug effects with AMPH than subjects with lower responses. The results are consistent with preclinical findings showing an interrelationship between glucocorticoids and mesolimbic DA dynamics, which may influence psychostimulant self-administration in humans.

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Influence of the stress hormone cortisol on fear conditioning in humans: Evidence for sex differences in the response of the prefrontal cortex

Cited by 154 publications

References 67 publications

Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi

Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi

Associations between Basal Cortisol Levels and Memory Retrieval in Healthy Young Individuals

Association of Amphetamine-Induced Striatal Dopamine Release and Cortisol Responses to Psychological Stress

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