Skip to main content
SpringerLink
Log in

Sex Differences in Response to Stress and Expression of Depressive-Like Behaviours in the Rat

  • Chapter
  • First Online:
Book cover Biological Basis of Sex Differences in Psychopharmacology

Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 8))

Abstract

Women are more susceptible than men to certain stress-related psychiatric disorders, such as depression. Preclinical studies aim to understand these sex differences by studying male and female rats in stress models. In this chapter, we review sex differences in behavioural aspects, as well as neurochemical and neurobiological findings derived from acute, repeated and chronic stress models. In particular, we focus on sex differences in depressive-like symptomatology expressed in the forced swim test, the chronic mild stress (CMS) and the learned helplessness models, the Flinders Sensitive Line rats (FSL), which is a genetic model of depression and in the lipopolysaccharide (LPS)-induced sickness behaviour, a putative inflammatory model of depression. Also, sex differences in stress effects on learning and memory parameters are discussed, because cognitive alterations are often seen in sex-differentiated psychiatric disorders. The observed behavioural alterations are often linked with abnormalities in the endophenotype, such as in hormonal, neurochemical, immune and neuroplasticity indices. From these data, it is clear that all stress models have strengths and limitations that need to be recognized in order to use them effectively in the investigation of sex differences in affective disorders.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Abbreviations

8-OHDPAT:

(+)8-Hydroxy-N,N-dipropyl-2-aminotetralin hydrobromide

ACTH:

Adrenocorticotropin hormone

AVP:

Arginine vasopressin

CMS:

Chronic mild stress

FSL:

Flinders sensitive line

FST:

Forced swim test

HPA:

Hypothalamic-pituitary-adrenal

HPG:

Hypothalamus-pituitary-gonadal

LPS:

Lipopolysaccharide

LC:

Locus coeruleus

References

  • Amat J, Baratta MV, Paul E, Bland ST, Watkins LR, Maier SF (2005) Medial prefrontal cortex determines how stressor controllability affects behavior and dorsal raphe nucleus. Nat Neurosci 8:365–371

    PubMed  CAS  Google Scholar 

  • Anisman H, Matheson K (2005) Stress, depression, and anhedonia: caveats concerning animal models. Neurosci Biobehav Rev 29:525–546

    PubMed  Google Scholar 

  • Anisman H, Zacharko RM (1990) Multiple neurochemical and behavioral consequences of stressors: implications for depression. Pharmacol Ther 46:119–136

    PubMed  CAS  Google Scholar 

  • Avitsur R, Yirmiya R (1999) The immunobiology of sexual behavior: gender differences in the suppression of sexual activity during illness. Pharmacol Biochem Behav 64:787–796

    PubMed  CAS  Google Scholar 

  • Baker S, Bielajew C (2007) Influence of housing on the consequences of chronic mild stress in female rats. Stress 10:283–293

    PubMed  CAS  Google Scholar 

  • Baker SL, Kentner AC, Konkle AT, Santa-Maria Barbagallo L, Bielajew C (2006) Behavioral and physiological effects of chronic mild stress in female rats. Physiol Behav 87:314–322

    PubMed  CAS  Google Scholar 

  • Bangasser DA, Shors TJ (2007) The hippocampus is necessary for enhancements and impairments of learning following stress. Nat Neurosci 10:1401–1403

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bangasser DA, Shors TJ (2008) The bed nucleus of the stria terminalis modulates learning after stress in masculinized but not cycling females. J Neurosci 28:6383–6387

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bekris S, Antoniou K, Daskas S, Papadopoulou-Daifoti Z (2005) Behavioural and neurochemical effects induced by chronic mild stress applied to two different rat strains. Behav Brain Res 161:45–59

    PubMed  CAS  Google Scholar 

  • Beylin AV, Shors TJ (2003) Glucocorticoids are necessary for enhancing the acquisition of associative memories after acute stressful experience. Horm Behav 43:124–131

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bland ST, Schmid MJ, Greenwood BN, Watkins LR, Maier SF (2006) Behavioral control of the stressor modulates stress-induced changes in neurogenesis and fibroblast growth factor-2. Neuroreport 17:593–597

    PubMed  CAS  Google Scholar 

  • Bowman RE (2005) Stress-induced changes in spatial memory are sexually differentiated and vary across the lifespan. J Neuroendocrinol 17:526–535

    PubMed  CAS  Google Scholar 

  • Bowman RE, Beck KD, Luine VN (2003) Chronic stress effects on memory: sex differences in performance and monoaminergic activity. Horm Behav 43:48–59

    PubMed  CAS  Google Scholar 

  • Bowman RE, Micik R, Gautreaux C, Fernandez L, Luine VN (2009) Sex-dependent changes in anxiety, memory, and monoamines following one week of stress. Physiol Behav 97:21–29

    PubMed  CAS  Google Scholar 

  • Conrad CD, Jackson JL, Wieczorek L, Baran SE, Harman JS, Wright RL, Korol DL (2004) Acute stress impairs spatial memory in male but not female rats: influence of estrous cycle. Pharmacol Biochem Behav 78:569–579

    PubMed  CAS  Google Scholar 

  • Cryan JF, Slattery DA (2007) Animal models of mood disorders: recent developments. Curr Opin Psychiatry 20:1–7

    PubMed  Google Scholar 

  • Curtis AL, Bethea T, Valentino RJ (2006) Sexually dimorphic responses of the brain norepinephrine system to stress and corticotropin-releasing factor. Neuropsychopharmacology 31:544–554

    PubMed  CAS  Google Scholar 

  • Dalla C, Antoniou K, Drossopoulou G, Xagoraris M, Kokras N, Sfikakis A, Papadopoulou-Daifoti Z (2005) Chronic mild stress impact: are females more vulnerable? Neuroscience 135:703–714

    PubMed  CAS  Google Scholar 

  • Dalla C, Antoniou K, Kokras N, Drossopoulou G, Papathanasiou G, Bekris S, Daskas S, Papadopoulou-Daifoti Z (2008a) Sex differences in the effects of two stress paradigms on dopaminergic neurotransmission. Physiol Behav 93:595–605

    PubMed  CAS  Google Scholar 

  • Dalla C, Edgecomb C, Whetstone AS, Shors TJ (2008b) Females do not express learned helplessness like males do. Neuropsychopharmacology 33:1559–1569

    PubMed  Google Scholar 

  • Dalla C, Shors TJ (2009) Sex differences in learning processes of classical and operant conditioning. Physiol Behav 97:229–238

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dalla C, Pitychoutis PM, Kokras N, Papadopoulou-Daifoti Z (2010) Sex differences in the neurobiological substrate of depression and in antidepressant response. Basic and Clinical Pharmacology and Toxicology 106:226–233

    PubMed  CAS  Google Scholar 

  • Dalla C, Whetstone AS, Hodes GE, Shors TJ (2009) Stressful experience has opposite effects on dendritic spines in the hippocampus of cycling versus masculinized females. Neurosci Lett 449:52–56

    PubMed  CAS  PubMed Central  Google Scholar 

  • Dantzer R, O'Connor JC, Freund GG, Johnson RW, Kelley KW (2008) From inflammation to sickness and depression: when the immune system subjugates the brain. Nat Rev Neurosci 9:46–56

    PubMed  CAS  PubMed Central  Google Scholar 

  • Darmani NA (1996) Differential potentiation of L-tryptophan-induced head-twitch response in mice by cocaine and sertraline. Life Sci 59:1109–1119

    PubMed  CAS  Google Scholar 

  • DeBold CR, Sheldon WR, DeCherney GS, Jackson RV, Alexander AN, Vale W, Rivier J, Orth DN (1984) Arginine vasopressin potentiates adrenocorticotropin release induced by ovine corticotropin-releasing factor. J Clin Invest 73:533–538

    PubMed  CAS  PubMed Central  Google Scholar 

  • Deecher D, Andree TH, Sloan D, Schechter LE (2008) From menarche to menopause: exploring the underlying biology of depression in women experiencing hormonal changes. Psychoneuroendocrinology 33:3–17

    PubMed  Google Scholar 

  • Drossopoulou G, Antoniou K, Kitraki E, Papathanasiou G, Papalexi E, Dalla C, Papadopoulou-Daifoti Z (2004) Sex differences in behavioral, neurochemical and neuroendocrine effects induced by the forced swim test in rats. Neuroscience 126:849–857

    PubMed  CAS  Google Scholar 

  • Duncko R, Kiss A, Skultetyova I, Rusnak M, Jezova D (2001) 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. Psychoneuroendocrinology 26:77–89

    PubMed  CAS  Google Scholar 

  • Duncko R, Schwendt M, Jezova D (2003) Altered glutamate receptor and corticoliberin gene expression in brain regions related to hedonic behavior in rats. Pharmacol Biochem Behav 76:9–16

    PubMed  CAS  Google Scholar 

  • Engeland CG, Kavaliers M, Ossenkopp KP (2006) Influence of the estrous cycle on tolerance development to LPS-induced sickness behaviors in rats. Psychoneuroendocrinology 31:510–525

    PubMed  CAS  Google Scholar 

  • Franklin TB, Perrot-Sinal TS (2006) Sex and ovarian steroids modulate brain-derived neurotrophic factor (BDNF) protein levels in rat hippocampus under stressful and non-stressful conditions. Psychoneuroendocrinology 31:38–48

    PubMed  CAS  Google Scholar 

  • Frederic F, Oliver C, Wollman E, Delhaye-Bouchaud N, Mariani J (1993) IL-1 and LPS induce a sexually dimorphic response of the hypothalamo-pituitary-adrenal axis in several mouse strains. Eur Cytokine Netw 4:321–329

    PubMed  CAS  Google Scholar 

  • Galea LA, McEwen BS, Tanapat P, Deak T, Spencer RL, Dhabhar FS (1997) Sex differences in dendritic atrophy of CA3 pyramidal neurons in response to chronic restraint stress. Neuroscience 81:689–697

    PubMed  CAS  Google Scholar 

  • Garrett JE, Wellman CL (2009) Chronic stress effects on dendritic morphology in medial prefrontal cortex: sex differences and estrogen dependence. Neuroscience 162:195–207

    PubMed  CAS  PubMed Central  Google Scholar 

  • Grippo AJ, Sullivan NR, Damjanoska KJ, Crane JW, Carrasco GA, Shi J, Chen Z, Garcia F, Muma NA, Van de Kar LD (2005) Chronic mild stress induces behavioral and physiological changes, and may alter serotonin 1A receptor function, in male and cycling female rats. Psychopharmacology (Berl) 179:769–780

    CAS  Google Scholar 

  • Handa RJ, Nunley KM, Lorens SA, Louie JP, McGivern RF, Bollnow MR (1994) Androgen regulation of adrenocorticotropin and corticosterone secretion in the male rat following novelty and foot shock stressors. Physiol Behav 55:117–124

    PubMed  CAS  Google Scholar 

  • Heinrichs SC, Koob GF (2004) Corticotropin-releasing factor in brain: a role in activation, arousal, and affect regulation. J Pharmacol Exp Ther 311:427–440

    PubMed  CAS  Google Scholar 

  • Heinsbroek RP, van Haaren F, Feenstra MG, van Galen H, Boer G, van de Poll NE (1990) Sex differences in the effects of inescapable footshock on central catecholaminergic and serotonergic activity. Pharmacol Biochem Behav 37:539–550

    PubMed  CAS  Google Scholar 

  • Heinsbroek RP, van Haaren F, Feenstra MG, Boon P, van de Poll NE (1991) Controllable and uncontrollable footshock and monoaminergic activity in the frontal cortex of male and female rats. Brain Res 551:247–255

    PubMed  CAS  Google Scholar 

  • Holden C (2005) Sex and the suffering brain. Science 308:1574

    PubMed  CAS  Google Scholar 

  • Holsboer F (2000) The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23:477–501

    PubMed  CAS  Google Scholar 

  • Holsboer F (2001) Stress, hypercortisolism and corticosteroid receptors in depression: implications for therapy. J Affect Disord 62:77–91

    PubMed  CAS  Google Scholar 

  • Kamper EF, Chatzigeorgiou A, Tsimpoukidi O, Kamper M, Dalla C, Pitychoutis PM, Papadopoulou-Daifoti Z (2009) Sex differences in oxidant/antioxidant balance under a chronic mild stress regime. Physiol Behav 98:215–222

    PubMed  CAS  Google Scholar 

  • Karandrea D, Kittas C, Kitraki E (2000) Contribution of sex and cellular context in the regulation of brain corticosteroid receptors following restraint stress. Neuroendocrinology 71:343–353

    PubMed  CAS  Google Scholar 

  • Karandrea D, Kittas C, Kitraki E (2002) Forced swimming differentially affects male and female brain corticosteroid receptors. Neuroendocrinology 75:217–226

    PubMed  CAS  Google Scholar 

  • Kendler KS, Thornton LM, Prescott CA (2001) Gender differences in the rates of exposure to stressful life events and sensitivity to their depressogenic effects. Am J Psychiatry 158:587–593

    PubMed  CAS  Google Scholar 

  • Khurana RC, Devaud LL (2007) Sex differences in neurotransmission parameters in response to repeated mild restraint stress exposures in intact male, female and ovariectomised female rats. J Neuroendocrinol 19:511–520

    PubMed  CAS  Google Scholar 

  • Kioukia N, Bekris S, Antoniou K, Papadopoulou-Daifoti Z, Christofidis I (2000) Effects of chronic mild stress (CMS) on thyroid hormone function in two rat strains. Psychoneuroendocrinology 25:247–257

    PubMed  CAS  Google Scholar 

  • Kioukia-Fougia N, Antoniou K, Bekris S, Liapi C, Christofidis I, Papadopoulou-Daifoti Z (2002) The effects of stress exposure on the hypothalamic-pituitary-adrenal axis, thymus, thyroid hormones and glucose levels. Prog Neuropsychopharmacol Biol Psychiatry 26:823–830

    PubMed  CAS  Google Scholar 

  • Kitay JI (1961) Sex differences in adrenal cortical secretion in the rat. Endocrinology 68:818–824

    PubMed  CAS  Google Scholar 

  • Kitraki E, Kremmyda O, Youlatos D, Alexis MN, Kittas C (2004) Gender-dependent alterations in corticosteroid receptor status and spatial performance following 21 days of restraint stress. Neuroscience 125:47–55

    PubMed  CAS  Google Scholar 

  • Klein LC, Corwin EJ (2002) Seeing the unexpected: how sex differences in stress responses may provide a new perspective on the manifestation of psychiatric disorders. Curr Psychiatry Rep 4:441–448

    PubMed  Google Scholar 

  • Kokras N, Antoniou K, Dalla C, Bekris S, Xagoraris M, Ovestreet D, Papadopoulou-Daifoti Z (2009a) Sex-related differential response to clomipramine treatment in a rat model of depression. J Psychopharmacol 23:945–956

    PubMed  CAS  Google Scholar 

  • Kokras N, Antoniou K, Polissidis A, Papadopoulou-Daifoti Z (2009b) Antidepressants induce regionally discrete, sex-dependent changes in brain’s glutamate content. Neurosci Lett 464:98–102

    PubMed  CAS  Google Scholar 

  • Konkle AT, Baker SL, Kentner AC, Barbagallo LS, Merali Z, Bielajew C (2003) Evaluation of the effects of chronic mild stressors on hedonic and physiological responses: sex and strain compared. Brain Res 992:227–238

    PubMed  CAS  Google Scholar 

  • Leuner B, Mendolia-Loffredo S, Shors TJ (2004) Males and females respond differently to controllability and antidepressant treatment. Biol Psychiatry 56:964–970

    PubMed  CAS  PubMed Central  Google Scholar 

  • Luine V (2002) Sex differences in chronic stress effects on memory in rats. Stress 5:205–216

    PubMed  CAS  Google Scholar 

  • Lupien SJ, McEwen BS, Gunnar MR, Heim C (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10:434–445

    PubMed  CAS  Google Scholar 

  • Maciejewski PK, Prigerson HG, Mazure CM (2001) Sex differences in event-related risk for major depression. Psychol Med 31:593–604

    PubMed  CAS  Google Scholar 

  • Maier SF (1984) Learned helplessness and animal models of depression. Prog Neuropsychopharmacol Biol Psychiatry 8:435–446

    PubMed  CAS  Google Scholar 

  • Maier SF, Watkins LR (2005) Stressor controllability and learned helplessness: the roles of the dorsal raphe nucleus, serotonin, and corticotropin-releasing factor. Neurosci Biobehav Rev 29:829–841

    PubMed  CAS  Google Scholar 

  • Malberg JE, Duman RS (2003) Cell proliferation in adult hippocampus is decreased by inescapable stress: reversal by fluoxetine treatment. Neuropsychopharmacology 28:1562–1571

    PubMed  CAS  Google Scholar 

  • Marcus SM, Young EA, Kerber KB, Kornstein S, Farabaugh AH, Mitchell J, Wisniewski SR, Balasubramani GK, Trivedi MH, Rush AJ (2005) Gender differences in depression: findings from the STAR*D study. J Affect Disord 87:141–150

    PubMed  Google Scholar 

  • Marriott I, Bost KL, Huet-Hudson YM (2006) Sexual dimorphism in expression of receptors for bacterial lipopolysaccharides in murine macrophages: a possible mechanism for gender-based differences in endotoxic shock susceptibility. J Reprod Immunol 71:12–27

    PubMed  CAS  Google Scholar 

  • Matuszewich L, Yamamoto BK (2003) Long-lasting effects of chronic stress on DOI-induced hyperthermia in male rats. Psychopharmacology (Berl) 169:169–175

    CAS  Google Scholar 

  • McEwen BS (2002) Sex, stress and the hippocampus: allostasis, allostatic load and the aging process. Neurobiol Aging 23:921–939

    PubMed  CAS  Google Scholar 

  • Merali Z, Brennan K, Brau P, Anisman H (2003) Dissociating anorexia and anhedonia elicited by interleukin-1beta: antidepressant and gender effects on responding for “free chow” and “earned” sucrose intake. Psychopharmacology (Berl) 165:413–418

    CAS  Google Scholar 

  • Miller WR, Seligman ME (1975) Depression and learned helplessness in man. J Abnorm Psychol 84:228–238

    PubMed  CAS  Google Scholar 

  • Mitsushima D, Yamada K, Takase K, Funabashi T, Kimura F (2006) Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur J Neurosci 24:3245–3254

    PubMed  Google Scholar 

  • Moore SA (2009) Cognitive abnormalities in posttraumatic stress disorder. Curr Opin Psychiatry 22:19–24

    PubMed  Google Scholar 

  • Nemeroff CB, Bremner JD, Foa EB, Mayberg HS, North CS, Stein MB (2006) Posttraumatic stress disorder: a state-of-the-science review. J Psychiatr Res 40:1–21

    PubMed  Google Scholar 

  • Nielsen CK, Arnt J, Sanchez C (2000) Intracranial self-stimulation and sucrose intake differ as hedonic measures following chronic mild stress: interstrain and interindividual differences. Behav Brain Res 107:21–33

    PubMed  CAS  Google Scholar 

  • Overstreet DH, Friedman E, Mathe AA, Yadid G (2005) The Flinders Sensitive Line rat: a selectively bred putative animal model of depression. Neurosci Biobehav Rev 29:739–759

    PubMed  CAS  Google Scholar 

  • Padilla E, Barrett D, Shumake J, Gonzalez-Lima F (2009) Strain, sex, and open-field behavior: factors underlying the genetic susceptibility to helplessness. Behav Brain Res 201:257–264

    PubMed  PubMed Central  Google Scholar 

  • Palanza P (2001) Animal models of anxiety and depression: how are females different? Neurosci Biobehav Rev 25:219–233

    PubMed  CAS  Google Scholar 

  • Papp M, Klimek V, Willner P (1994) Effects of imipramine on serotonergic and beta-adrenergic receptor binding in a realistic animal model of depression. Psychopharmacology (Berl) 114:309–314

    CAS  Google Scholar 

  • Pinos H, Collado P, Rodriguez-Zafra M, Rodriguez C, Segovia S, Guillamon A (2001) The development of sex differences in the locus coeruleus of the rat. Brain Res Bull 56:73–78

    PubMed  CAS  Google Scholar 

  • Pitychoutis PM, Griva E, Ioannou K, Tsitsilonis OE, Papadopoulou-Daifoti Z (2009a) Chronic antidepressant treatment exerts sexually dimorphic immunomodulatory effects in an experimental model of major depression: do females lack an advantage? Int J Neuropsychopharmacol 12:1–7

    Google Scholar 

  • Pitychoutis PM, Nakamura K, Tsonis PA, Papadopoulou-Daifoti Z (2009b) Neurochemical and behavioral alterations in an inflammatory model of depression: sex differences exposed. Neuroscience 159:1216–1232

    PubMed  CAS  Google Scholar 

  • Pitychoutis PM, Papadopoulou-Daifoti Z (2010) Of Depression and Immunity: Does Sex matter? Int J Neuropsychopharmacol 13:675–689

    PubMed  CAS  Google Scholar 

  • Pitychoutis PM, Tsitsilonis OE, Papadopoulou-Daifoti Z (2010) Antidepressant Pharmacotherapy: Focus on Sex Differences in Neuroimmunopharmacological Crossroads. Future Neurology 5:581–596

    Google Scholar 

  • Seale JV, Wood SA, Atkinson HC, Bate E, Lightman SL, Ingram CD, Jessop DS, Harbuz MS (2004a) Gonadectomy reverses the sexually diergic patterns of circadian and stress-induced hypothalamic-pituitary-adrenal axis activity in male and female rats. J Neuroendocrinol 16:516–524

    PubMed  CAS  Google Scholar 

  • Seale JV, Wood SA, Atkinson HC, Harbuz MS, Lightman SL (2004b) Gonadal steroid replacement reverses gonadectomy-induced changes in the corticosterone pulse profile and stress-induced hypothalamic-pituitary-adrenal axis activity of male and female rats. J Neuroendocrinol 16:989–998

    PubMed  CAS  Google Scholar 

  • Sherrill JT, Anderson B, Frank E, Reynolds CF III, Tu XM, Patterson D, Ritenour A, Kupfer DJ (1997) Is life stress more likely to provoke depressive episodes in women than in men? Depress Anxiety 6:95–105

    PubMed  CAS  Google Scholar 

  • Shors TJ (1998) Stress and sex effects on associative learning: for better or for worse. Neuroscientist 4:353–364

    Google Scholar 

  • Shors TJ (2006) Stressful experience and learning across the lifespan. Annu Rev Psychol 57:55–85

    PubMed  PubMed Central  Google Scholar 

  • Shors TJ, Seib TB, Levine S, Thompson RF (1989) Inescapable versus escapable shock modulates long-term potentiation in the rat hippocampus. Science 244:224–226

    PubMed  CAS  Google Scholar 

  • Shors TJ, Lewczyk C, Pacynski M, Mathew PR, Pickett J (1998) Stages of estrous mediate the stress-induced impairment of associative learning in the female rat. Neuroreport 9:419–423

    PubMed  CAS  Google Scholar 

  • Shors TJ, Chua C, Falduto J (2001) Sex differences and opposite effects of stress on dendritic spine density in the male versus female hippocampus. J Neurosci 21:6292–6297

    PubMed  CAS  Google Scholar 

  • Shors TJ, Falduto J, Leuner B (2004) The opposite effects of stress on dendritic spines in male vs. female rats are NMDA receptor-dependent. Eur J Neurosci 19:145–150

    PubMed  CAS  PubMed Central  Google Scholar 

  • Shors TJ, Mathew J, Sisti HM, Edgecomb C, Beckoff S, Dalla C (2007) Neurogenesis and helplessness are mediated by controllability in males but not in females. Biol Psychiatry 62:487–495

    PubMed  PubMed Central  Google Scholar 

  • Sotiropoulos I, Cerqueira JJ, Catania C, Takashima A, Sousa N, Almeida OF (2008) Stress and glucocorticoid footprints in the brain-the path from depression to Alzheimer’s disease. Neurosci Biobehav Rev 32:1161–1173

    PubMed  CAS  Google Scholar 

  • Spinedi E, Salas M, Chisari A, Perone M, Carino M, Gaillard RC (1994) Sex differences in the hypothalamo-pituitary-adrenal axis response to inflammatory and neuroendocrine stressors. Evidence for a pituitary defect in the autoimmune disease-susceptible female Lewis rat. Neuroendocrinology 60:609–617

    PubMed  CAS  Google Scholar 

  • Sun MK, Alkon DL (2006) Differential gender-related vulnerability to depression induction and converging antidepressant responses in rats. J Pharmacol Exp Ther 316:926–932

    PubMed  CAS  Google Scholar 

  • Tanapat P, Hastings NB, Reeves AJ, Gould E (1999) Estrogen stimulates a transient increase in the number of new neurons in the dentate gyrus of the adult female rat. J Neurosci 19:5792–5801

    PubMed  CAS  Google Scholar 

  • Tonelli LH, Holmes A, Postolache TT (2008) Intranasal immune challenge induces sex-dependent depressive-like behavior and cytokine expression in the brain. Neuropsychopharmacology 33:1038–1048

    PubMed  CAS  PubMed Central  Google Scholar 

  • Trentani A, Kuipers SD, te Meerman GJ, Beekman J, ter Horst GJ, den Boer JA (2003) Immunohistochemical changes induced by repeated footshock stress: revelations of gender-based differences. Neurobiol Dis 14:602–618

    PubMed  CAS  Google Scholar 

  • Willner P (1997) Validity, reliability and utility of the chronic mild stress model of depression: a 10-year review and evaluation. Psychopharmacology (Berl) 134:319–329

    CAS  Google Scholar 

  • Willner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52:90–110

    PubMed  CAS  Google Scholar 

  • Willner P, Towell A, Sampson D, Sophokleous S, Muscat R (1987) Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berl) 93:358–364

    CAS  Google Scholar 

  • Wood GE, Shors TJ (1998) Stress facilitates classical conditioning in males, but impairs classical conditioning in females through activational effects of ovarian hormones. Proc Natl Acad Sci U S A 95:4066–4071

    PubMed  CAS  PubMed Central  Google Scholar 

  • Yadid G, Nakash R, Deri I, Tamar G, Kinor N, Gispan I, Zangen A (2000) Elucidation of the neurobiology of depression: insights from a novel genetic animal model. Prog Neurobiol 62:353–378

    PubMed  CAS  Google Scholar 

  • Zampeli E, Pitychoutis PM, Papadopoulou-Daifoti Z, Tiligada E (2009) Systemic challenge with lipopolysaccharide increases histamine levels in the conjunctiva and cartilage, but not hypothalamus of Sprague Dawley rats. Inflamm Res 58(Suppl 1):49–50

    PubMed  Google Scholar 

Download references

Acknowledgements

Dr. Christina Dalla was a Marie Curie International Fellow, funded from the European Commission within the 6th European Community Framework Programme. This work has been supported by the Greek General Secretariat of Research and Technology and by Research Grants from the Special Account for Research Grants of the University of Athens (Greece).

Author information

Authors and Affiliations

  1. Department of Pharmacology, Medical School, University of Athens, Mikras Asias 75, Goudi, 11527, Athens, Greece

    Christina Dalla, Pothitos M. Pitychoutis, Nikolaos Kokras & Zeta Papadopoulou-Daifoti

Authors
  1. Christina Dalla
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Pothitos M. Pitychoutis
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nikolaos Kokras
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zeta Papadopoulou-Daifoti
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Bradford School of Pharmacy, University Bradford, Bradford, W.Yorkshire, BD7 1DP, United Kingdom

    Jo C. Neill

  2. Monash Alfred Psychiatry Research Centre, Commercial Rd., Melbourne, 3004, Australia

    Jayashri Kulkarni

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Dalla, C., Pitychoutis, P.M., Kokras, N., Papadopoulou-Daifoti, Z. (2010). Sex Differences in Response to Stress and Expression of Depressive-Like Behaviours in the Rat. In: Neill, J., Kulkarni, J. (eds) Biological Basis of Sex Differences in Psychopharmacology. Current Topics in Behavioral Neurosciences, vol 8. Springer, Berlin, Heidelberg. https://doi.org/10.1007/7854_2010_94

Download citation

Publish with us

Policies and ethics

Search

Navigation