Sex differences in anxiety and emotional behavior

Donner, Nina C.; Lowry, Christopher A.

doi:10.1007/s00424-013-1271-7

Cited by 379Neurotransmitter Receptor Influence on BehaviorStress Responses and CortisolAnxiety, Depression, Psychometrics, Treatment, Cognitive Processes

Sex differences in anxiety and emotional behavior

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Donner, Nina C., Lowry, Christopher A.·2013·Pflügers Archiv - European Journal of Physiology

DOI 10.1007/s00424-013-1271-7PMC PMC3805826

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Abstract

Research has elucidated causal links between stress exposure and the development of anxiety disorders, but due to the limited use of female or sex-comparative animal models, little is known about the mechanisms underlying sex differences in those disorders. This is despite an overwhelming wealth of evidence from the clinical literature that the prevalence of anxiety disorders is about twice as high in women compared to men, in addition to gender differences in severity and treatment efficacy. We here review human gender differences in generalized anxiety disorder, panic disorder, posttraumatic stress disorder and anxiety-relevant biological functions, discuss the limitations of classic conflict anxiety tests to measure naturally occurring sex differences in anxiety-like behaviors, describe sex-dependent manifestation of anxiety states after gestational, neonatal, or adolescent stressors, and present animal models of chronic anxiety states induced by acute or chronic stressors during adulthood. Potential mechanisms underlying sex differences in stress-related anxiety states include emerging evidence supporting the existence of two anatomically and functionally distinct serotonergic circuits that are related to the modulation of conflict anxiety and panic-like anxiety, respectively. We discuss how these serotonergic circuits may be controlled by reproductive steroid hormone-dependent modulation of crfr1 and crfr2 expression in the midbrain dorsal raphe nucleus and by estrous stage-dependent alterations of γ-aminobutyric acid (GABAergic) neurotransmission in the periaqueductal gray, ultimately leading to sex differences in emotional behavior.

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The left central amygdala is activated by stimuli and negative emotions in women, while in men it is activated by positive emotions.
“Specifically, the left central amygdala is activated by stimuli and negative emotions in women, 39 while in men, it is activated by positive emotions. 64”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
The section on anxiety-relevant physiological and psychological gender differences reports stronger left central amygdala activation with negative emotions in women and with positive emotions in men, each relative to the other sex. The citing sentence omits that comparative qualifier, and the passage does not separately establish activation by unspecified stimuli in women. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Gender socialization is, at least in part, responsible for the development of psychosocial characteristics that act as risk factors for women and protective factors for men in the onset and course of anxiety.
“The results seem to indicate that gender socialization is, at least in part, responsible for the development of the psychosocial characteristics that act as risk factors for women and protective factors for men in the onset and course of anxiety.44,54,56,59,64,70”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
The sections on the significance of gender differences and on human gender differences report higher anxiety prevalence in women and increased rumination in girls. The PTSD section also considers societal victimization as a possible contributor. The paper does not establish that gender socialization develops psychosocial risk factors for women or protective factors for men. (LLM, conf=0.78)
Experimental — accuracy not yet measured
Of the 44 documents, 31 were empirical/quantitative studies and 13 were reviews.
“Of the 44 documents, 31 were empirical/quantitative studies30–60 and 13 were reviews.61–73”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
Brain regions relevant to emotions (fear) and their regulation, such as the hippocampus, amygdala, and prefrontal cortex, are one possible explanation for differences in anxiety between sexes.
“With respect to the latter, it has been pointed out that one of the possible explanations for differences in anxiety between the sexes resides in the brain regions relevant to emotions (i.e. fear) and their regulation, such as the hippocampus, amygdala, and prefrontal cortex.63,64”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
Sex differences in anxiety disorders may be due to fluctuations of sexual hormones that affect the anxious state of women.
“(b) the fluctuations of sexual hormones that affect the anxious state of women,46,49,63,64,66,69”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]

Sex differences in anxiety disorders may be due to genetic factors.
“(c) genetic factors.30,31,52,61,64,71”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
Women generally identified themselves with expressive or feminine traits such as kindness and sweetness, while men identified themselves with instrumental or masculine traits such as competitiveness, assertiveness, and self-confidence.
“The results from other studies also showed that women generally identified themselves with expressive or feminine traits such as kindness and sweetness, while men identified themselves with instrumental or masculine traits such as competitiveness, assertiveness, and self-confidence.59,64”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
The section on anxiety-relevant physiological and psychological gender differences discusses stress responses and emotional distress, not how women or men describe their own traits (page unavailable). Searches for expressive and instrumental traits, the named examples, and gendered self-identification found no passage addressing the claim. (LLM, conf=0.73)
Experimental — accuracy not yet measured
Women who scored higher on instrumentality reported lower subjective anxiety and less fear.
“Importantly, women who scored higher on instrumentality reported lower subjective anxiety and less fear. 64”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
The Generalized anxiety disorder and Panic disorder sections discuss women’s anxiety and subjective fear, but neither links them to instrumentality scores. Searches for instrumentality, instrumental gender-role traits, and lower subjective anxiety and fear found no passage addressing the claimed association. Page numbers were unavailable in our copy. (LLM, conf=0.72)
Experimental — accuracy not yet measured
Evidence on the relationship between femininity and anxiety is contradictory.
“With respect to femininity, the results showed contradictory information. While there are studies that have not found a relationship between femininity and anxiety, 64 other studies revealed that femininity accompanied by low self-esteem favored the development of anxiety.49,70”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
The section on human gender differences in anxiety reports differences between women and men, not findings about femininity as a trait. Searches for femininity, low self-esteem, and their relationship to anxiety found no passage addressing the claimed contradictory evidence. No page number was available in our copy. (LLM, conf=0.74)
Experimental — accuracy not yet measured
Instrumentality mediates between anxiety and gender, not biological sex.
“Therefore, instrumentality mediates between anxiety and gender, not biological sex.”
From Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review (2022) · cites this paper as [64]
The Conclusions discuss biological sex and gender identity in relation to anxiety, but do not address instrumentality or mediation. Searches for instrumentality and masculine traits found no passage supporting the claimed distinction between gender and biological sex. (LLM, conf=0.76)
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“particular relevance because acute, repeated, or chronic stress exposures are common triggers for these psychiatric disorders [273, 286], because women may have an inherently increased stress vulnerability, and because key symptoms of these disorders have been successfully modeled in animals.”
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Corticotropin-releasing hormone mRNA levels in response to chronic mild stress rise in male but not in female rats while tyrosine hydroxylase mRNA levels decrease in both sexes
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Behavioral Validation of the Elevated T-Maze, a New Animal Model of Anxiety
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Opioids suppress spontaneous and NMDA-induced inhibitory postsynaptic currents in the dorsal raphe nucleus of the rat in vitro
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A Longitudinal Study of Childhood Depression and Anxiety in Relation to Weight Gain
Rofey, D. L., Kolko, R. P., Iosif, A., Silk, J. S., Bost, J. E., Feng, W., Szigethy, E., Noll, R. B., Ryan, N. D., & Dahl, R. E. (2009) · Child Psychiatry & Human Development · doi:10.1007/s10578-009-0141-1 · Cited by 170 · see citing works
Early life experience alters behavior during social defeat: Focus on serotonergic systems
Gardner, K. L., Thrivikraman, K. V., Lightman, S. L., Plotsky, P. M., & Lowry, C. A. (2005) · Neuroscience · doi:10.1016/j.neuroscience.2005.07.042 · Cited by 169 · see citing works
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Maternal high-fat diet in mice programs emotional behavior in adulthood
Peleg-Raibstein, D., Luca, E., & Wolfrum, C. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.05.027 · Cited by 167 · see citing works
Morphometry of the dorsal raphe nucleus serotonergic neurons in suicide victims
Underwood, M. D., Khaibulina, A. A., Ellis, S. P., Moran, A., Rice, P. M., Mann, J. J., & Arango, V. (1999) · Biological Psychiatry · doi:10.1016/s0006-3223(99)00043-8 · Cited by 165 · see citing works
Minireview: Sex Chromosomes and Brain Sexual Differentiation
Arnold, A. P., Xu, J., Grisham, W., Chen, X., Kim, Y., & Itoh, Y. (2003) · Endocrinology · doi:10.1210/en.2003-1491 · Cited by 164 · see citing works
Smaller amygdala is associated with anxiety in patients with panic disorder
Hayano, F., Nakamura, M., Asami, T., Uehara, K., Yoshida, T., Roppongi, T., Otsuka, T., Inoue, T., & Hirayasu, Y. (2009) · Psychiatry and Clinical Neurosciences · doi:10.1111/j.1440-1819.2009.01960.x · Cited by 163 · see citing works
Estrogen Selectively Increases Tryptophan Hydroxylase-2 mRNA Expression in Distinct Subregions of Rat Midbrain Raphe Nucleus: Association between Gene Expression and Anxiety Behavior in the Open Field
Hiroi, R., McDevitt, R. A., & Neumaier, J. F. (2006) · Biological Psychiatry · doi:10.1016/j.biopsych.2005.10.019 · Cited by 161 · see citing works
Women and Depression
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Behavioural and Neurochemical Consequences of Early Weaning in Rodents
Kikusui, T., & Mori, Y. (2009) · Journal of Neuroendocrinology · doi:10.1111/j.1365-2826.2009.01837.x · Cited by 158 · see citing works
SSRIs act as selective brain steroidogenic stimulants (SBSSs) at low doses that are inactive on 5-HT reuptake
Pinna, G., Costa, E., & Guidotti, A. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2008.12.006 · Cited by 156 · see citing works
Maternal care, isolation-induced infant ultrasonic calling, and their relations to adult anxiety-related behavior in the rat.
Wöhr, M., & Schwarting, R. K. W. (2008) · Behavioral Neuroscience · doi:10.1037/0735-7044.122.2.310 · Cited by 156 · see citing works
It is not all hormones: Alternative explanations for sexual differentiation of the brain
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Development of Disturbing Dreams During Adolescence and Their Relation to Anxiety Symptoms
Nielsen, T., Laberge, L., Paquet, J., Tremblay, R. E., Vitaro, F., & Montplaisir, J. Y. (2000) · SLEEP · doi:10.1093/sleep/23.6.1 · Cited by 155 · see citing works
Elevated expression of tryptophan hydroxylase-2 mRNA at the neuronal level in the dorsal and median raphe nuclei of depressed suicides
Bach-Mizrachi, H., Underwood, M. D., Tin, A., Ellis, S. P., Mann, J. J., & Arango, V (2008) · Molecular Psychiatry · doi:10.1038/sj.mp.4002143 · Cited by 153 · see citing works
Maternal nurturing is dependent on her innate anxiety: The behavioral roles of brain oxytocin and vasopressin
Bosch, O. J. (2010) · Hormones and Behavior · doi:10.1016/j.yhbeh.2010.11.012 · Cited by 153 · see citing works
Neonatal lipopolysaccharide and adult stress exposure predisposes rats to anxiety-like behaviour and blunted corticosterone responses: Implications for the double-hit hypothesis
Walker, A. K., Nakamura, T., Byrne, R. J., Naicker, S., Tynan, R. J., Hunter, M., & Hodgson, D. M. (2009) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2009.05.010 · Cited by 150 · see citing works
Chronic Stress Induces Sex-Specific Alterations in Methylation and Expression of Corticotropin-Releasing Factor Gene in the Rat
Sterrenburg, L., Gaszner, B., Boerrigter, J., Santbergen, L., Bramini, M., Elliott, E., Chen, A., Peeters, B. W. M. M., Roubos, E. W., & Kozicz, T. (2011) · PLoS ONE · doi:10.1371/journal.pone.0028128 · Cited by 149 · see citing works
Sex chromosome complement regulates habit formation
Quinn, J. J., Hitchcott, P. K., Umeda, E. A., Arnold, A. P., & Taylor, J. R. (2007) · Nature Neuroscience · doi:10.1038/nn1994 · Cited by 148 · see citing works
Adaptive modulation of behavioural profiles by social stress during early phases of life and adolescence
Sachser, N., Hennessy, M. B., & Kaiser, S. (2010) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2010.09.002 · Cited by 147 · see citing works
Lasting anxiogenic effects of feline predator stress in mice: sex differences in vulnerability to stress and predicting severity of anxiogenic response from the stress experience
Adamec, R., Head, D., Blundell, J., Burton, P., & Berton, O. (2006) · Physiology & Behavior · doi:10.1016/j.physbeh.2006.03.005 · Cited by 145 · see citing works
Gender differences in sympathoadrenal activity in rats at rest and in response to footshock stress
Weinstock, M., Razin, M., Schorer-Apelbaum, D., Men, D., & McCarty, R. C. (1998) · International Journal of Developmental Neuroscience · doi:10.1016/s0736-5748(98)00021-5 · Cited by 144 · see citing works
Sexual dimorphism in locus coeruleus dendritic morphology: A structural basis for sex differences in emotional arousal
Bangasser, D. A., Zhang, X., Garachh, V., Hanhauser, E., & Valentino, R. J. (2011) · Physiology & Behavior · doi:10.1016/j.physbeh.2011.02.037 · Cited by 144 · see citing works
Neuroactive steroids: focus on human brain
Melcangi, R. C., Panzica, G., & García‐Segura, L. M. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.024 · Cited by 143 · see citing works
Chronic Glucocorticoids Increase Hippocampal Vulnerability to Neurotoxicity under Conditions That Produce CA3 Dendritic Retraction But Fail to Impair Spatial Recognition Memory
Conrad, C. D., McLaughlin, K. J., Harman, J. S., Foltz, C. H., Wieczorek, L., Lightner, E. N., & Wright, R. L. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2121-07.2007 · Cited by 143 · see citing works
Handbook of Anxiety and Fear
Blanchard, R. J. (2008) · Handbook of behavioral neuroscience · doi:10.1016/s1569-7339(07)x0001-8 · Cited by 142 · see citing works
Chronic social instability stress in female rats: A potential animal model for female depression
Herzog, C., Czéh, B., Corbach‐Söhle, S., Wuttke, W., Schulte‐Herbrüggen, O., Hellweg, R., Flügge, G., & Fuchs, E. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.01.059 · Cited by 142 · see citing works
IGF-I Treatment Reduces Hyperphagia, Obesity, and Hypertension in Metabolic Disorders Induced by Fetal Programming
Vickers, M. H., Ikenasio, B. A., & Breier, B. H. (2001) · Endocrinology · doi:10.1210/endo.142.9.8390 · Cited by 142 · see citing works
Neuroactive steroids in affective disorders: target for novel antidepressant or anxiolytic drugs?
Schüle, C., Eser, D., Baghai, T. C., Nothdurfter, C., Kessler, J. S., & Rupprecht, R. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.03.025 · Cited by 141 · see citing works
Neurogenesis and Helplessness Are Mediated by Controllability in Males But Not in Females
Shors, T. J., Mathew, J., Sisti, H. M., Edgecomb, C., Beckoff, S., & Dalla, C. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.10.033 · Cited by 140 · see citing works
Recent progress in the genetics of common obesity
Loos, R. J. F. (2009) · British Journal of Clinical Pharmacology · doi:10.1111/j.1365-2125.2009.03523.x · Cited by 139 · see citing works
Disentangling prenatal and inherited influences in humans with an experimental design
Rice, F. J., Harold, G. T., Boivin, J., Hay, D. F., van den Bree, M. B. M., & Thapar, A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0808798106 · Cited by 134 · see citing works
Rumination and Depression in Adolescence: Investigating Symptom Specificity in a Multiwave Prospective Study
Hankin, B. L. (2008) · Journal of Clinical Child & Adolescent Psychology · doi:10.1080/15374410802359627 · Cited by 133 · see citing works
Chemical Lesion of the Bed Nucleus of the Stria Terminalis Blocks the Behavioral Consequences of Uncontrollable Stress.
Hammack, S. E., Richey, K. J., Watkins, L. R., & Maier, S. F. (2004) · Behavioral Neuroscience · doi:10.1037/0735-7044.118.2.443 · Cited by 130 · see citing works
Steroid withdrawal in the mouse results in anxiogenic effects of 3α,5β-THP: a possible model of premenstrual dysphoric disorder
Smith, S. S., Ruderman, Y., Frye, C. A., Homanics, G. E., & Yuan, M. (2005) · Psychopharmacology · doi:10.1007/s00213-005-0168-3 · Cited by 130 · see citing works
A friendly version of the Trier Social Stress Test does not activate the HPA axis in healthy men and women
Wiemers, U. S., Schoofs, D., & Wolf, O. T. (2012) · Stress · doi:10.3109/10253890.2012.714427 · Cited by 130 · see citing works
Sex differences and phase of light cycle modify chronic stress effects on anxiety and depressive-like behavior
Huynh, T. N., Krigbaum, A. M., Hanna, J. J., & Conrad, C. D. (2011) · Behavioural Brain Research · doi:10.1016/j.bbr.2011.03.038 · Cited by 129 · see citing works
Chromatin of the Barr body: histone and non-histone proteins associated with or excluded from the inactive X chromosome
Chadwick, B. P. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg229 · Cited by 128 · see citing works
Corticotropin-releasing factor 1 and 2 receptors in the dorsal raphé differentially affect serotonin release in the nucleus accumbens
Lukkes, J. L., Forster, G. L., Renner, K. J., & Summers, C. H. (2007) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2007.09.024 · Cited by 126 · see citing works

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Sex differences in anxiety and depression: circuits and mechanisms
Bangasser, D. A., & Cuarenta, A. (2021) · Nature Reviews Neuroscience · doi:10.1038/s41583-021-00513-0 · Cited by 479 · see citing works
Sex differences in animal models of psychiatric disorders
Kokras, N., & Dalla, C. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12710 · Cited by 418 · see citing works
Factors associated with gender and sex differences in anxiety prevalence and comorbidity: A systematic review
Farhane-Medina, N. Z., Luque, B., Tabernero, C., & Castillo-Mayén, R. (2022) · Science Progress · doi:10.1177/00368504221135469 · Cited by 409 · see citing works
“Finally, some studies suggest that women’s hormonal fluctuations (progesterone, estrogens, and oxytocin) may be the cause of sexual differences in anxiety.(30,49,64,69) According to Murphy et al.”
BackgroundResultInfluential
The Role of Early Growth Response 1 (EGR1) in Brain Plasticity and Neuropsychiatric Disorders
Duclot, F., & Kabbaj, M. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00035 · Cited by 359 · see citing works
Sex hormone fluctuation and increased female risk for depression and anxiety disorders: From clinical evidence to molecular mechanisms
Kundaković, M., & Rocks, D. (2022) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2022.101010 · Cited by 333 · see citing works
Virtual Reality Is Sexist: But It Does Not Have to Be
Stanney, K. M., Fidopiastis, C., & Foster, L. (2020) · Frontiers in Robotics and AI · doi:10.3389/frobt.2020.00004 · Cited by 318 · see citing works
Sex differences in anxiety-like behaviors in rats
Scholl, J. L., Afzal, A., Fox, L. C., Watt, M. J., & Forster, G. L. (2019) · Physiology & Behavior · doi:10.1016/j.physbeh.2019.112670 · Cited by 216 · see citing works
You’ve got male: Sex and the microbiota-gut-brain axis across the lifespan
Jaggar, M., Rea, K., Spichak, S., Dinan, T. G., & Cryan, J. F. (2020) · Frontiers in Neuroendocrinology · doi:10.1016/j.yfrne.2019.100815 · Cited by 200 · see citing works
The Relationships Between Stress, Mental Disorders, and Epigenetic Regulation of BDNF
Miao, Z., Wang, Y., & Sun, Z. S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041375 · Cited by 178 · see citing works
COVID-19 misinformation: Mere harmless delusions or much more? A knowledge and attitude cross-sectional study among the general public residing in Jordan
Sallam, M., Dababseh, D., Yaseen, A. I. B., Al-Haidar, A., Taim, D., Eid, H., Ababneh, N. A., Bakri, F. G., & Mahafzah, A. M. (2020) · PLoS ONE · doi:10.1371/journal.pone.0243264 · Cited by 178 · see citing works
Microbiota influence the development of the brain and behaviors in C57BL/6J mice
Lu, J., Synowiec, S., Lu, L., Yu, Y., Bretherick, T., Takada, S., Yarnykh, V., Caplan, J., Caplan, M., Claud, E. C., et al. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201829 · Cited by 159 · see citing works
Antidepressant-Like and Anxiolytic-Like Effects of Cannabidiol: A Chemical Compound of Cannabis sativa
Schier, A. R. D. M., Ribeiro, N. D. C. R., Coutinho, D. C. O., Machado, S. E. D. C., Arias-Carrión, Ó., Crippa, J. A. S., Zuardi, A. W., Nardi, A. E., & Silva, A. R. (2014) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527313666140612114838 · Cited by 154 · see citing works
The Stage of the Estrus Cycle Is Critical for Interpretation of Female Mouse Social Interaction Behavior
Chari, T., Griswold, S., Andrews, N. A., & Fagiolini, M. (2020) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2020.00113 · Cited by 141 · see citing works
Sex and gender influences on pharmacological response: an overview
Franconi, F., & Campesi, I. (2014) · Expert Review of Clinical Pharmacology · doi:10.1586/17512433.2014.922866 · Cited by 132 · see citing works
Androgens increase excitatory neurogenic potential in human brain organoids
Kelava, I., Chiaradia, I., Pellegrini, L., Kalinka, A. T., & Lancaster, M. A. (2022) · Nature · doi:10.1038/s41586-021-04330-4 · Cited by 123 · see citing works
Knowledge, Attitudes, Practices and Information Needs During the COVID-19 Pandemic in Indonesia
Sulistyawati, S., Rokhmayanti, R., Aji, B., Wijayanti, S. P. M., Hastuti, S. K. W., Sukesi, T. W., & Mulasari, S. A. (2021) · Risk Management and Healthcare Policy · doi:10.2147/rmhp.s288579 · Cited by 120 · see citing works
Default mode network alterations in individuals with high-trait-anxiety: An EEG functional connectivity study
Imperatori, C., Farina, B., Adenzato, M., Valenti, E. M., Murgia, C., Marca, G. D., Brunetti, R., Fontana, E., & Ardito, R. B. (2018) · Journal of Affective Disorders · doi:10.1016/j.jad.2018.12.071 · Cited by 119 · see citing works
The intersection of gender and resilience
Hirani, S. A. A., Lasiuk, G. C., & Hegadoren, K. (2016) · Journal of Psychiatric and Mental Health Nursing · doi:10.1111/jpm.12313 · Cited by 118 · see citing works
The neurobiological basis of sex differences in learned fear and its inhibition
Day, H. L. L., & Stevenson, C. W. (2020) · European Journal of Neuroscience · doi:10.1111/ejn.14602 · Cited by 114 · see citing works
Association between anxiety and aggression in adolescents: a cross-sectional study
Chung, J. E., Song, G., Kim, K., Yee, J., Kim, J. H., Lee, K. E., & Gwak, H. S. (2019) · BMC Pediatrics · doi:10.1186/s12887-019-1479-6 · Cited by 109 · see citing works
Symptoms of depression and anxiety in Indonesian medical students: association with coping strategy and resilience
Ramadianto, A. S., Kusumadewi, I., Agiananda, F., & Raharjanti, N. W. (2022) · BMC Psychiatry · doi:10.1186/s12888-022-03745-1 · Cited by 107 · see citing works
Neuropsychiatric Symptom Modeling in Male and Female C57BL/6J Mice after Experimental Traumatic Brain Injury
Tucker, L. B., Burke, J. F., Fu, A. H., & McCabe, J. T. (2016) · Journal of Neurotrauma · doi:10.1089/neu.2016.4508 · Cited by 106 · see citing works
Sexually dimorphic effects of prenatal exposure to lipopolysaccharide, and prenatal and postnatal exposure to propionic acid, on acoustic startle response and prepulse inhibition in adolescent rats: Relevance to autism spectrum disorders
Foley, K. A., MacFabe, D. F., Kavaliers, M., & Ossenkopp, K. (2014) · Behavioural Brain Research · doi:10.1016/j.bbr.2014.09.032 · Cited by 96 · see citing works
From Systemic Inflammation to Neuroinflammation: The Case of Neurolupus
Bendorius, M., Po, C., Muller, S., & Jeltsch‐David, H. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19113588 · Cited by 96 · see citing works
The estrous cycle surpasses sex differences in regulating the transcriptome in the rat medial prefrontal cortex and reveals an underlying role of early growth response 1
Duclot, F., & Kabbaj, M. (2015) · Genome biology · doi:10.1186/s13059-015-0815-x · Cited by 95 · see citing works
The anxiolytic effect of essential oil of Cananga odorata exposure on mice and determination of its major active constituents
Zhang, N., Zhang, L. J., Feng, L., & Yao, L. (2016) · Phytomedicine · doi:10.1016/j.phymed.2016.10.017 · Cited by 92 · see citing works
GPR30 activation decreases anxiety in the open field test but not in the elevated plus maze test in female mice
Anchan, M., Clark, S. M., Pollard, K. J., & Vasudevan, N. (2013) · Brain and Behavior · doi:10.1002/brb3.197 · Cited by 92 · see citing works
Amygdala subnuclei resting-state functional connectivity sex and estrogen differences
Engman, J., Linnman, C., Van Dijk, K. R. A., & Milad, M. R. (2016) · Psychoneuroendocrinology · doi:10.1016/j.psyneuen.2015.09.012 · Cited by 89 · see citing works
Predicting Facebook addiction and state anxiety without Facebook by gender, trait anxiety, Facebook intensity, and different Facebook activities
Xie, W., & Karan, K. (2019) · Journal of Behavioral Addictions · doi:10.1556/2006.8.2019.09 · Cited by 89 · see citing works
Prospective Associations between Sport Participation and Indices of Mental Health across Adolescence
Graupensperger, S. A., Sutcliffe, J., & Vella, S. A. (2021) · Journal of Youth and Adolescence · doi:10.1007/s10964-021-01416-0 · Cited by 89 · see citing works
Recent Perspectives on Sex Differences in Compulsion-Like and Binge Alcohol Drinking
Radke, A. K., Sneddon, E. A., Frasier, R. M., & Hopf, F. W. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22073788 · Cited by 88 · see citing works
Sex differences in developmental patterns of neocortical astroglia: A mouse translatome database
Rurak, G. M., Simard, S., Andrade, M. F., Lacoste, B., Charih, F., Geel, A. V., Stead, J. D. H., Woodside, B. C., Green, J. R., Coppola, G., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110310 · Cited by 87 · see citing works
Use of Cannabidiol for the Treatment of Anxiety: A Short Synthesis of Pre-Clinical and Clinical Evidence
Wright, M., Ciano, P. D., & Brands, B. (2020) · Cannabis and Cannabinoid Research · doi:10.1089/can.2019.0052 · Cited by 85 · see citing works
Endocannabinoids, cannabinoids and the regulation of anxiety
Petrie, G. N., Nastase, A. S., Aukema, R. J., & Hill, M. N. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108626 · Cited by 85 · see citing works
Patient-reported Outcomes and Quality of Life After Treatment of Choroidal Melanoma: A Comparison of Enucleation Versus Radiotherapy in 1596 Patients
Damato, B. E., Hope‐Stone, L., Cooper, B. A., Brown, S. L., Salmon, P., Heimann, H., & Dunn, L. B. (2018) · American Journal of Ophthalmology · doi:10.1016/j.ajo.2018.03.015 · Cited by 83 · see citing works
Prefrontal modulation of anxiety through a lens of noradrenergic signaling
Bouras, N. N., Mack, N. R., & Gao, W. (2023) · Frontiers in Systems Neuroscience · doi:10.3389/fnsys.2023.1173326 · Cited by 81 · see citing works
Gender Differences of B Cell Signature in Healthy Subjects Underlie Disparities in Incidence and Course of SLE Related to Estrogen
Fan, H., Dong, G., Zhao, G., Liu, F., Yao, G., Zhu, Y., & Hou, Y. (2014) · Journal of Immunology Research · doi:10.1155/2014/814598 · Cited by 80 · see citing works
Assessing the effects of stress on feeding behaviors in laboratory mice
Francois, M., Delgado, I. C., Shargorodsky, N., Leu, C.-S., & Zeltser, L. M. (2021) · eLife · doi:10.7554/elife.70271 · Cited by 77 · see citing works
Generalized fear after acute stress is caused by change in neuronal cotransmitter identity
Li, H.-Q., Jiang, W., Ling, L., Gupta, V., Chen, C., Gupta, V., Godavarthi, S. K., & Spitzer, N. C. (2024) · Science · doi:10.1126/science.adj5996 · Cited by 73 · see citing works
NMDA 2A receptors in parvalbumin cells mediate sex-specific rapid ketamine response on cortical activity
Picard, N., Takesian, A. E., Fagiolini, M., & Hensch, T. K. (2019) · Molecular Psychiatry · doi:10.1038/s41380-018-0341-9 · Cited by 71 · see citing works
Anxiety and depression in patients with advanced cancer during the COVID-19 pandemic
Obispo, B., Cruz‐Castellanos, P., Jiménez‐Fonseca, P., Rogado, J., Hernández, R., Trujillo, O. A. C., Asensio-Martínez, E., González-Moya, M., Carmona‐Bayonas, A., & Calderón, C. (2022) · Supportive Care in Cancer · doi:10.1007/s00520-021-06789-3 · Cited by 71 · see citing works
IL-10 normalizes aberrant amygdala GABA transmission and reverses anxiety-like behavior and dependence-induced escalation of alcohol intake
Patel, R. R., Wolfe, S. A., Bajo, M., Abeynaike, S. A., Pahng, A. R., Borgonetti, V., D’Ambrosio, S. R., Nikzad, R., Edwards, S., Paust, S., et al. (2020) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2020.101952 · Cited by 70 · see citing works
Comparison of memory, affective behavior, and neuropathology in APPNLGF knock-in mice to 5xFAD and APP/PS1 mice
Locci, A., Orellana, H., Rodríguez, G., Gottliebson, M., McClarty, B. M., Dominguez, S., Keszycki, R. M., & Dong, H. (2021) · Behavioural Brain Research · doi:10.1016/j.bbr.2021.113192 · Cited by 68 · see citing works
Anxiety-like behaviors in adulthood are altered in male but not female rats exposed to low dosages of polychlorinated biphenyls in utero
Gillette, R., Reilly, M. P., Topper, V. Y., Thompson, L. M., Crews, D. P., & Gore, A. C. (2016) · Hormones and Behavior · doi:10.1016/j.yhbeh.2016.10.011 · Cited by 66 · see citing works
Early-life risk factors for panic and separation anxiety disorder: Insights and outstanding questions arising from human and animal studies of CO2 sensitivity
Battaglia, M., Ogliari, A., D’Amato, F., & Kinkead, R. (2014) · Neuroscience & Biobehavioral Reviews · doi:10.1016/j.neubiorev.2014.04.005 · Cited by 66 · see citing works
The Wistar-Kyoto rat model of endogenous depression: a tool for exploring treatment resistance with an urgent need to focus on sex differences
Millard, S. J., Weston-Green, K., & Newell, K. A. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109908 · Cited by 62 · see citing works
Stress, sex, and addiction
Bisagno, V., & Cadet, J. L. (2014) · Behavioural Pharmacology · doi:10.1097/fbp.0000000000000049 · Cited by 60 · see citing works
Bidirectional Regulation of Cognitive and Anxiety-like Behaviors by Dentate Gyrus Mossy Cells in Male and Female Mice
Botterill, J. J., Vinod, K. Y., Gerencer, K. J., Teixeira, C. M., LaFrancois, J. J., & Scharfman, H. E. (2021) · Journal of Neuroscience · doi:10.1523/jneurosci.1724-20.2021 · Cited by 59 · see citing works
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Authors: Donner, N. C., & Lowry, C. A.
Affiliations: University of Colorado Boulder (US)
Corresponding author: Donner, Nina C.
ORCID: Donner, Nina C.
Lowry, Christopher A.
Venue: Pflügers Archiv - European Journal of Physiology
Publisher: Springer Science and Business Media LLC
Published: 2013-04-16
Volume: 465
Issue: 5
Pages: 601-626
ISSN: 0031-6768 (ISSN-L)
1432-2013
DOI: 10.1007/s00424-013-1271-7
PMC: PMC3805826
OpenAlex: W2008301991
Cited by: 379
References: 404
Citations by year: 2026: 16 · 2025: 33 · 2024: 39 · 2023: 39 · 2022: 45 · 2021: 47 · 2020: 37 · 2019: 32 · 2018: 28 · 2017: 13 · 2016: 16 · 2015: 12 · 2014: 18 · 2013: 3
FWCI: 1.66
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Pflügers Archiv - European Journal of Physiology (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Funders: National Institutes of Health (UL1TR001108)
National Institute of Mental Health (F32MH084463, R01MH086539, R01MH065702)
National Center for Advancing Translational Sciences
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Social Sciences › Psychology › Experimental and Cognitive Psychology › Anxiety, Depression, Psychometrics, Treatment, Cognitive Processes
Keywords: sex differences, anxiety disorders, generalized anxiety disorder, panic disorder, post-traumatic stress disorder, dorsal raphe nucleus, CRF1 receptor, CRF receptor 2, estrous cycle, GABAergic neurotransmission, periaqueductal gray, stress exposure, animal models of anxiety, emotional behavior
MeSH terms: Animals, Anxiety, Female, Humans, Male, Rodentia, Sex Characteristics, Stress Disorders, Post-Traumatic, Panic Disorder

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