The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning males versus females.

Wood, Gwendolyn E.; Beylin, Anna V.; Shors, Tracey J.

doi:10.1037/0735-7044.115.1.175

Cited by 199Memory and Neural MechanismsStress Responses and CortisolMemory Processes and Influences

The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning males versus females.

Wood, Gwendolyn E., Beylin, Anna V., Shors, Tracey J.·2001·Behavioral Neuroscience

DOI 10.1037/0735-7044.115.1.175

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Abstract

Exposure to an acute stressful experience facilitates classical conditioning in male rats but impairs conditioning in female rats (T. J. Shors, C. Lewczyk, M. Paczynski, P. R. Mathew, & J. Pickett, 1998; G. E. Wood & T. J. Shors, 1998). The authors report that these effects extend to performance on the hippocampal-dependent task of trace conditioning. The stress-induced impairment of conditioning in females was evident immediately, 24 hr and 48 hr after stress, depending on the stage of estrus. Moreover, the effect could be reactivated days later by reexposure to the stressful context. Corticosterone levels correlated with overall performance in males but not in females. Unlike the effect seen in males, adrenalectomy did not prevent the stress-induced effect on conditioning in females. These data indicate that exposure to the same experience can have opposite effects on learning in males versus females and that these opposing effects are mediated by differing hormonal systems.

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In tests of acute stress or aversive conditioning, stress enhances learning in males and impairs it in females.
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Brain Corticosteroid Receptors: Studies on the Mechanism, Function, and Neurotoxicity of Corticosteroid Action
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(1997) · doi:10.1002/(sici)1096-9861(19971201)388:4

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Stress Effects on Neuronal Structure: Hippocampus, Amygdala, and Prefrontal Cortex
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“In contrast, acute tail shock stress during classical eyeblink conditioning improves performance in males, but suppresses it in females(100) by mechanisms influenced by gonadal hormones in development and in adult life.(101,102) However, giving male and female rats control over the shock abolishes both the stress effe…”
Background
Neurogenesis may relate to some but not all types of hippocampal‐dependent learning
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Strategies and Methods for Research on Sex Differences in Brain and Behavior
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Is there a link between adult neurogenesis and learning?
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Sex Differences and Opposite Effects of Stress on Dendritic Spine Density in the Male Versus Female Hippocampus
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Serotonergic vulnerability and depression: assumptions, experimental evidence and implications
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Estrogens and progestins enhance spatial learning of intact and ovariectomized rats in the object placement task
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Learning During Stressful TimesPreprint
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Adult hippocampal neurogenesis and related neurotrophic factors
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Ovarian steroids enhance object recognition in naturally cycling and ovariectomized, hormone-primed rats
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Genomic and epigenomic mechanisms of glucocorticoids in the brain
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HPA axis and memory
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Sensitivity to the depressogenic effect of stress and HPA-axis reactivity in adolescence: a review of gender differences
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Stressful Experience and Learning Across the Lifespan
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Sex differences in spatial and non-spatial Y-maze performance after chronic stress
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Influence of predator stress on the consolidation versus retrieval of long-term spatial memory and hippocampal spinogenesis
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Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle
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Relevance of Stress and Female Sex Hormones for Emotion and Cognition
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When is a sex difference not a sex difference?
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Chronic stress and sex differences on the recall of fear conditioning and extinction
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Stress, Glucocorticoids, and Memory: A Meta-analytic Review
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Stress Differentially Modulates Fear Conditioning in Healthy Men and Women
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Estrogen-mediated effects on depression and memory formation in females
Shors, T. J. (2003) · Journal of Affective Disorders · doi:10.1016/s0165-0327(02)00428-7 · Cited by 180 · see citing works
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Antianxiety and Antidepressive Behavior Produced by Physiological Estradiol Regimen may be Modulated by Hypothalamic–Pituitary–Adrenal Axis Activity
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Menstrual cycle modulation of the relationship between cortisol and long-term memory
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Proestrous compared to diestrous wildtype, but not estrogen receptor beta knockout, mice have better performance in the spontaneous alternation and object recognition tasks and reduced anxiety-like behavior in the elevated plus and mirror maze
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Growth hormone is produced within the hippocampus where it responds to age, sex, and stress
Donahue, C. P., Kosik, K. S., & Shors, T. J. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0507776103 · Cited by 143 · see citing works
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Acute and chronic restraint stress alter the incidence of social conflict in male rats
Wood, G. E., Young, L. T., Reagan, L. P., & McEwen, B. S. (2003) · Hormones and Behavior · doi:10.1016/s0018-506x(02)00026-0 · Cited by 141 · see citing works
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Interaction of age and chronic estradiol replacement on memory and markers of brain aging
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Social cognition under stress: Differential effects of stress-induced cortisol elevations in healthy young men and women
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New Spines, New Memories
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Rapid Estrogen Signaling in the Brain: Implications for the Fine-Tuning of Neuronal Circuitry
Srivastava, D. P., Waters, E. M., Mermelstein, P. G., Kramár, E. A., Shors, T. J., & Liu, F. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4097-11.2011 · Cited by 137 · see citing works
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Cortisol and memory retrieval in women: influence of menstrual cycle and oral contraceptives
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Implications of psychosocial stress on memory formation in a typical male versus female student sample.
Cornelisse, S., van Stegeren, A. H., & Joëls, M. (2011) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2010.09.002 · Cited by 133 · see citing works
Glucocorticoids are necessary for enhancing the acquisition of associative memories after acute stressful experience
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Estrous cycle, pregnancy, and parity enhance performance of rats in object recognition or object placement tasks
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Effects of stress and sex on acquisition and consolidation of human fear conditioningPreprint
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Sex differences in anxiety, sensorimotor gating and expression of the α4 subunit of the GABAAreceptor in the amygdala after progesterone withdrawal
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Sex-dependent changes in anxiety, memory, and monoamines following one week of stress
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Expression of c-fos and BDNF mRNA in subregions of the prefrontal cortex of male and female rats after acute uncontrollable stress.
Bland, S. T., Schmid, M. J., Der-Avakian, A., Watkins, L., Spencer, R. L., & Maier, S. (2005) · Brain Research · doi:10.1016/j.brainres.2005.05.065 · Cited by 115 · see citing works
Distinctive stress effects on learning during puberty
Hodes, G. E., & Shors, T. J. (2005) · Hormones and Behavior · doi:10.1016/j.yhbeh.2005.02.008 · Cited by 109 · see citing works
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Sex, stress, and fear: Individual differences in conditioned learning
Zorawski, M., Cook, C. A., Kuhn, C. M., & LaBar, K. S. (2005) · Cognitive Affective & Behavioral Neuroscience · doi:10.3758/cabn.5.2.191 · Cited by 108 · see citing works
The opposite effects of stress on dendritic spines in male vs. female rats are NMDA receptor‐dependent
Shors, T. J., Falduto, J., & Leuner, B. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.03065.x · Cited by 105 · see citing works
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Oral contraceptive usage alters the effects of cortisol on implicit fear learning
Merz, C. J., Tabbert, K., Schweckendiek, J., Klucken, T., Vaitl, D., Stark, R. M., & Wolf, O. T. (2012) · Hormones and Behavior · doi:10.1016/j.yhbeh.2012.09.001 · Cited by 101 · see citing works
Sex differences in the hypothalamic–pituitary–adrenal axis: An obstacle to antidepressant drug development?
Kokras, N., Hodes, G. E., Bangasser, D. A., & Dalla, C. (2019) · British Journal of Pharmacology · doi:10.1111/bph.14710 · Cited by 94 · see citing works
Sex differences in contextual fear conditioning are associated with differential ventral hippocampal extracellular signal-regulated kinase activation
Gresack, J. E., Schafe, G. E., Orr, P. T., & Frick, K. M. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.01.009 · Cited by 99 · see citing works
Long-term ovariectomy enhances anxiety and depressive-like behaviors in mice submitted to chronic unpredictable stress
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High levels of estrogen enhance associative memory formation in ovariectomized females
Leuner, B., Mendolia‐Loffredo, S., & Shors, T. J. (2003) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2003.08.001 · Cited by 100 · see citing works
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Biological and social influences on cognitive control processes dependent on prefrontal cortex
Diamond, A. D. (2011) · Progress in brain research · doi:10.1016/b978-0-444-53884-0.00032-4 · Cited by 96 · see citing works
Sex differences in the traumatic stress response: PTSD symptoms in women recapitulated in female rats
Pooley, A. E., Benjamin, R. C., Sreedhar, S., Eagle, A. L., Robison, A. J., Mazei‐Robison, M. S., Breedlove, S. M., & Jordan, C. L. (2018) · Biology of Sex Differences · doi:10.1186/s13293-018-0191-9 · Cited by 94 · see citing works
Sex-selective effects of neonatal isolation on fear conditioning and foot shock sensitivity
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Males and females respond differently to controllability and antidepressant treatment
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Endogenous κ Opioid Activation Mediates Stress-Induced Deficits in Learning and Memory
Carey, A. N., Lyons, A. M., Shay, C. F., Dunton, O., & McLaughlin, J. P. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.6146-08.2009 · Cited by 92 · see citing works
Sex Differences in Stress Response: Classical Mechanisms and Beyond
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Maternal care affects male and female offspring working memory and stress reactivity
Barha, C. K., Pawluski, J. L., & Galea, L. A. M. (2007) · Physiology & Behavior · doi:10.1016/j.physbeh.2007.06.022 · Cited by 91 · see citing works
Male mice exhibit better spatial working and reference memory than females in a water-escape radial arm maze task
Gresack, J. E., & Frick, K. M. (2003) · Brain Research · doi:10.1016/s0006-8993(03)03000-2 · Cited by 80 · see citing works
Behavioral training interferes with the ability of gonadal hormones to increase CA1 spine synapse density in ovariectomized female rats
Frick, K. M., Fernandez, S. M., Bennett, J. C., Prange‐Kiel, J., MacLusky, N. J., & Léránth, C. (2004) · European Journal of Neuroscience · doi:10.1111/j.0953-816x.2004.03427.x · Cited by 81 · see citing works
Testosterone in utero and at birth dictates how stressful experience will affect learning in adulthood
Shors, T. J., & Miesegaes, G. R. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.202199999 · Cited by 78 · see citing works
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Critical brain circuits at the intersection between stress and learning
Bangasser, D. A., & Shors, T. J. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.02.002 · Cited by 78 · see citing works
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The Basolateral Nucleus of the Amygdala Is Necessary to Induce the Opposing Effects of Stressful Experience on Learning in Males and Females
Waddell, J., Bangasser, D. A., & Shors, T. J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1129-08.2008 · Cited by 78 · see citing works
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Neurogenesis in the aged and neurodegenerative brain
Shruster, A., Melamed, E., & Offen, D. (2010) · APOPTOSIS · doi:10.1007/s10495-010-0491-y · Cited by 74 · see citing works
Estradiol decreases anxiety behavior and enhances inhibitory avoidance and gestational stress produces opposite effects
Walf, A. A., & Frye, C. A. (2007) · Stress · doi:10.1080/00958970701220416 · Cited by 74 · see citing works
Estradiol to aged female or male mice improves learning in inhibitory avoidance and water maze tasks
Frye, C. A., Rhodes, M. E., & Dudek, B. C. (2005) · Brain Research · doi:10.1016/j.brainres.2004.12.014 · Cited by 72 · see citing works
Sex differences in serotonergic activity in dorsal and median raphe nucleus
DOMINGUEZ, R., Cruz-Morales, S. E., de Carvalho, M. C., Xavier, M., & Brandão, M. L. (2003) · Physiology & Behavior · doi:10.1016/j.physbeh.2003.07.012 · Cited by 70 · see citing works
Progesterone to ovariectomized mice enhances cognitive performance in the spontaneous alternation, object recognition, but not placement, water maze, and contextual and cued conditioned fear tasks
Frye, C. A., & Walf, A. A. (2008) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2008.03.005 · Cited by 69 · see citing works
Stress exposure and affective modulation of aggressive behavior in men and women.
Verona, E., & Kilmer, A. (2007) · Journal of Abnormal Psychology · doi:10.1037/0021-843x.116.2.410 · Cited by 68 · see citing works
Social instability is an effective chronic stress paradigm for both male and female mice
Yohn, C. N., Ashamalla, S. A., Bokka, L., Gergues, M. M., Garino, A., & Samuels, B. A. (2019) · Neuropharmacology · doi:10.1016/j.neuropharm.2019.107780 · Cited by 67 · see citing works
Estrogen has mnemonic-enhancing effects in the inhibitory avoidance task
Rhodes, M. E., & Frye, C. A. (2004) · Pharmacology Biochemistry and Behavior · doi:10.1016/j.pbb.2004.03.025 · Cited by 66 · see citing works
Stereological estimation of Purkinje neuron number in C57BL/6 mice and its relation to associative learning
Woodruff‐Pak, D. S. (2006) · Neuroscience · doi:10.1016/j.neuroscience.2006.03.070 · Cited by 66 · see citing works
The Bed Nucleus of the Stria Terminalis Modulates Learning after Stress in Masculinized But Not Cycling Females
Bangasser, D. A., & Shors, T. J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0831-08.2008 · Cited by 64 · see citing works
Self-citation
The Prefrontal Cortex Communicates with the Amygdala to Impair Learning after Acute Stress in Females but Not in Males
Maeng, L. Y., Waddell, J., & Shors, T. J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.2265-10.2010 · Cited by 63 · see citing works
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Age-related dendritic hypertrophy and sexual dimorphism in rat basolateral amygdala
Rubinow, M. J., Drogos, L. L., & Juraska, J. M. (2007) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2007.05.006 · Cited by 61 · see citing works
A trip down memory lane about sex differences in the brain
Shors, T. J. (2016) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0124 · Cited by 58 · see citing works
Self-citation
Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females
Dalla, C., Whetstone, A. S., Hodes, G. E., & Shors, T. J. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2008.10.051 · Cited by 56 · see citing works
Self-citation
Sex differences in aversive memory in rats: Possible role of extinction and reactive emotional factors
Ribeiro, A. M., Barbosa, F. F., Godinho, M., Fernandes, V. S., Munguba, H., Melo, T. G., Barbosa, M. T., Eufrásio, R., Cabral, A., Izídio, G. S., et al. (2010) · Brain and Cognition · doi:10.1016/j.bandc.2010.07.012 · Cited by 56 · see citing works
A stress-induced anxious state in male rats: Corticotropin-releasing hormone induces persistent changes in associative learning and startle reactivity
Servatius, R. J., Beck, K. D., Moldow, R. L., Salameh, G., Tumminello, T., & Short, K. R. (2005) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.01.015 · Cited by 56 · see citing works
Estradiol and GPER Activation Differentially Affect Cell Proliferation but Not GPER Expression in the Hippocampus of Adult Female Rats
Duarte‐Guterman, P., Lieblich, S. E., Chow, C., & Galea, L. A. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0129880 · Cited by 54 · see citing works
HPA-axis stress reactivity in youth depression: evidence of impaired regulatory processes in depressed boys
Lopez‐Duran, N. L., McGinnis, E. W., Kuhlman, K. R., Geiss, E. G., Vargas, I., & Mayer, S. E. (2015) · Stress · doi:10.3109/10253890.2015.1053455 · Cited by 52 · see citing works
Estrogen, cognitive functions and emotion: an overview on humans, non-human primates and rodents in reproductive years
Gasbarri, A., Tavares, M. C. H., Rodrigues, R. C., Tomaz, C. A. B., & Pompili, A. (2012) · Reviews in the Neurosciences · doi:10.1515/revneuro-2012-0051 · Cited by 49 · see citing works
Effect of the Estrous Cycle on Water Maze Acquisition Depends on the Temperature of the Water.
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Influence of housing on the consequences of chronic mild stress in female rats
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Authors: Wood, G. E., Beylin, A. V., & Shors, T. J.
Affiliations: Rockefeller University (US)
ORCID: Wood, Gwendolyn E.
Shors, Tracey J.
Venue: Behavioral Neuroscience
Publisher: American Psychological Association (APA)
Published: 2001
Volume: 115
Issue: 1
Pages: 175-187
ISSN: 0735-7044 (ISSN-L)
1939-0084
DOI: 10.1037/0735-7044.115.1.175
OpenAlex: W2039652271
Cited by: 198
References: 97
Citations by year: 2026: 2 · 2025: 2 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 1 · 2020: 1 · 2019: 4 · 2018: 5 · 2017: 4 · 2016: 4 · 2015: 6 · 2014: 9 · 2013: 5 · 2012: 7
FWCI: 6.11
Type: journal article
Language: en
Open access: closed
Locations: Behavioral Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: National Institute of Mental Health (R01MH059740, MH-59970, MH-59740, R01MH059970)
Topics: Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords: stress, trace conditioning, sex differences, hippocampus-dependent learning, corticosterone, adrenalectomy, estrous cycle, reproductive hormones, adrenal hormones, classical conditioning, rats
MeSH terms: Adrenalectomy, Animals, Conditioning, Psychological, Corticosterone, Estrogens, Female, Hippocampus, Male, Progesterone, Sex Factors, Stress, Psychological, Rats, Sprague-Dawley, Rats

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The contribution of adrenal and reproductive hormones to the opposing effects of stress on trace conditioning males versus females.

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