PL EN


Preferencje help
Widoczny [Schowaj] Abstrakt
Liczba wyników
2020 | 80 | 3 |

Tytuł artykułu

Modulation of anxiety behavior in gonadectomized animals

Warianty tytułu

Języki publikacji

EN

Abstrakty

EN
Anxiety is a complex psychological state which happens after stressful life experiences. Many factors such as daily life events, neurotransmitter systems, and different brain areas could influence anxiety behavior in humans and animals. For example, opioids and androgens decrease anxiety behavior both in humans and animals. Furthermore, removing the testes (gonadectomy) causes higher levels of anxiety‑like behaviors, in which the administration of testosterone and opioid antagonist can reverse some of these behaviors. We review the effects of morphine and androgens on the modulation of anxiety behavior in gonadectomized animals. We begin by highlighting the effects of opioid drugs and androgens on the modulation of anxiety behavior that have been implicated in anxiety behavior. We then discuss the functional consequences of gonadectomy on anxiety behavior. Finally, we consider how the opioids and androgens may contribute to adaptive responses associated with anxiety.

Słowa kluczowe

Wydawca

-

Rocznik

Tom

80

Numer

3

Opis fizyczny

p.205-216,ref.

Twórcy

autor
  • Department of Animal Biology, Faculty of Natural Sciences, University of Tabriz, Tabriz, Iran
autor
  • Cognitive and Neuroscience Research Center, Tehran Medical Sciences, Islamic Azad University, Tehran, Iran

Bibliografia

  • Aikey JL, Nyby JG, Anmuth DM, James PJ (2002) Testosterone rapidly reduces anxiety in male house mice (Mus musculus). Horm Behav 42: 448–460.
  • Ali BH, Sharif SI, Elkadi A (1995) Sex differences and the effect of gona‑dectomy on morphine‑induced antinociception and dependence in rats and mice. Clin Exp Pharmacol Physiol 22: 342–344.
  • Almeida OF, Nikolarakis KE, Herz A (1988) Neuropharmacological analysis of the control of LH secretion in gonadectomized male and female rats: altered hypothalamic responses to inhibitory neurotransmitters in long‑term castrated rats. J Endocrinol 119: 15–21.
  • Aloisi AM, Aurilio C, Bachiocco  V, Biasi G, Fiorenzani P, Pace MC, Paci  V, Pari G, Passavanti G, Ravaioli L, Sindaco G, Vellucci R, Ceccarelli I (2009) Endocrine consequences of opioid therapy. Psychoneuroendocrinology 1: S162–168.
  • Aloisi AM, Pari G, Ceccarelli I, Vecchi I, Ietta F, Lodi L, Paulesu L (2005) Gender‑related effects of chronic non‑malignant pain and opioid therapy on plasma levels of macrophage migration inhibitory factor (MIF). Pain 115: 142–151.
  • Amore M, Scarlatti F, Quarta AL, Tagariello P (2009) Partial androgen deficiency, depression and testosterone treatment in aging men. Aging Clin Exp Res 21: 1–8.
  • Areda T, Koks S, Philips MA, Vasar E, Karis A, Asser T (2005) Alterations in opioid system of the rat brain after cat odor exposure. Neurosci Lett 377: 136–139.
  • Arpels JC (1996) The female brain hypoestrogenic continuum from the premenstrual syndrome to menopause. A hypothesis and review of supporting data. J Reprod Med 41: 633–639.
  • Aubele T, Kaufman R, Montalmant F, Kritzer MF (2008) Effects of gonadectomy and hormone replacement on a spontaneous novel object recognition task in adult male rats. Horm Behav 54: 244–252.
  • Babu GN, Marco J, Bona‑Gallo A, Gallo RV (1988) Absence of steroid‑dependent, endogenous opioid peptide suppression of pulsatile luteinizing hormone release between diestrus 1 and diestrus 2 in the rat estrous cycle. Neuroendocrinology 47: 249–258.
  • Bai X, Zhang X, Li Y, Lu L, Li B, He X (2015) Sex differences in peripheral muopioid receptor mediated analgesia in rat orofacial persistent pain model. PLoS One 10: e0122924.
  • Bannerman DM, Deacon RM, Offen S, Friswell J, Grubb M, Rawlins JN (2002) Double dissociation of function within the hippocampus: spatial memory and hyponeophagia. Behav Neurosci 116: 884–901.
  • Bing O, Heilig M, Kakoulidis P, Sundblad C, Wiklund L, Eriksson E (1998) High doses of testosterone increase anticonflict behaviour in rat. Eur Neuropsychopharmacol 8: 321–323.
  • Bottcher B, Seeber B, Leyendecker G, Wildt L (2017) Impact of the opioid system on the reproductive axis. Fertil Steril 108: 207–213.
  • Buckman SG, Hodgson SR, Hofford RS, Eitan S (2009) Increased elevated plus maze open‑arm time in mice during spontaneous morphine with‑ drawal. Behav Brain Res 197: 454–456.
  • Carrier N, Kabbaj M (2012) Testosterone and imipramine have antidepressant effects in socially isolated male but not female rats. Horm Behav 61: 678–685.
  • Celec P, Ostatnikova D, Hodosy J (2015) On the effects of testosterone on brain behavioral functions. Front Neurosci 9: 12.
  • Celerier E, Yazdi MT, Castane A, Ghozland S, Nyberg F, Maldonado R (2003) Effects of nandrolone on acute morphine responses, tolerance and dependence in mice. Eur J Pharmacol 465: 69–81.
  • Chrastil J, Sampson C, Jones KB, Higgins TF (2014) Evaluating the affect and reversibility of opioid‑induced androgen deficiency in an orthopaedic animal fracture model. Clin Orthop Relat Res 472: 1964–1971.
  • Cicero TJ, Meyer ER, Schmoeker PF (1982) Development of tolerance to the effects of morphine on luteinizing hormone secretion as a function of castration in the male rat. J Pharmacol Exp Ther 223: 784–789.
  • Cooper SE, Wood RI (2014) Androgens and opiates: testosterone interaction with morphine self‑administration in male rats. Neuroreport 25: 521–526.
  • Craft RM, Mogil JS, Aloisi AM (2004) Sex differences in pain and analgesia: the role of gonadal hormones. Eur J Pain 8: 397–411.
  • Domonkos E, Borbelyova  V, Csongova  M, Bosy  M, Kacmarova  M, Ostatnikova D, Hodosy J, Celec P (2017) Sex differences and sex hormones in anxiety‑like behavior of aging rats. Horm Behav 93: 159–165.
  • Domonkos E, Hodosy J, Ostatnikova D, Celec P (2018) On the role of testosterone in anxiety‑like behavior across life in experimental rodents. Front Endocrinol 9: 441.
  • Dossat AM, Jourdi H, Wright KN, Strong CE, Sarkar A, Kabbaj M (2017) Viral‑mediated Zif268 expression in the prefrontal cortex protects against gonadectomy‑induced working memory, long‑term memory, and social interaction deficits in male rats. Neuroscience 340: 243–257.
  • Edinger KL, Frye CA (2004) Testosterone’s analgesic, anxiolytic, and cognitive‑enhancing effects may be due in part to actions of its 5al‑ phareduced metabolites in the hippocampus. Behav Neurosci 118: 1352–1364.
  • Edinger KL, Frye CA (2005) Testosterone’s anti‑anxiety and analgesic effects may be due in part to actions of its 5alpha‑reduced metabolites in the hippocampus. Psychoneuroendocrinology 30: 418–430.
  • Edinger KL, Frye CA (2007a) Androgens’ effects to enhance learning may be mediated in part through actions at estrogen receptor‑beta in the hippocampus. Neurobiol Learn Mem 87: 78–85. Edinger KL, Frye CA (2007b) Sexual experience of male rats influences anxiety‑like behavior and androgen levels. Physiol Behav 92: 443–453.
  • Erbs E, Faget L, Scherrer G, Kessler P, Hentsch D, Vonesch JL, Matifas A, Kieffer BL, Massotte D (2012) Distribution of delta opioid receptor‑expressing neurons in the mouse hippocampus. Neuroscience 221: 203–213.
  • Eskelinen SI, Vahlberg TJ, Isoaho RE, Kivela SL, Irjala KM (2007) Associations of sex hormone concentrations with health and life satisfaction in elder‑ ly men. Endocr Pract 13: 743–749.
  • Eslimi D, Oryan S, Nasehi M, Zarrindast MR (2011) Effects of opioidergic systems upon anxiolytic‑like behaviors induced in cholestatic rats. Eur J Pharmacol 670: 180–185. Fernandez‑Guasti A, Martinez‑Mota L (2003) Orchidectomy sensitizes male rats to the action of diazepam on burying behavior latency: role of testosterone. Pharmacol Biochem Behav 75: 473–479.
  • Fernandez‑Guasti A, Martinez‑Mota L (2005) Anxiolytic‑like actions of testosterone in the burying behavior test: role of androgen and GABA‑benzodiazepine receptors. Psychoneuroendocrinology 30: 762–770.
  • Frye CA, Edinger K, Sumida K (2008) Androgen administration to aged male mice increases anti‑anxiety behavior and enhances cognitive performance. Neuropsychopharmacology 33: 1049–1061.
  • Frye CA, Edinger KL (2004) Testosterone’s metabolism in the hippocampus may mediate its anti‑anxiety effects in male rats. Pharmacol Biochem Behav 78: 473–481.
  • Frye CA, Edinger KL, Seliga AM, Wawrzycki JM (2004) 5alpha‑reduced androgens may have actions in the hippocampus to enhance cognitive performance of male rats. Psychoneuroendocrinology 29: 1019–1027.
  • Frye CA, Seliga AM (2001) Testosterone increases analgesia, anxiolysis, and cognitive performance of male rats. Cogn Affect Behav Neurosci 1: 371–381.
  • Gartner U HW, Brauer K, Bruckner G, Arendt T (2001) Immunofluorescence and immunoelectron microscopic evidence for differences in myelination of GABAergic and cholinergic septohippocampal fibres. Int J Dev Neurosci 19: 347–352.
  • Giltay EJ, Enter D, Zitman FG, Penninx BW, van Pelt J, Spinhoven P, Roelofs K (2012) Salivary testosterone: associations with depression, anxiety disorders, and antidepressant use in a large cohort study. J Psychosom Res 72: 205–213.
  • Granger DA, Shirtcliff EA, Zahn‑Waxler C, Usher B, Klimes‑Dougan B, Hastings P (2003) Salivary testosterone diurnal variation and psycho‑ pathology in adolescent males and females: individual differences and developmental effects. Dev Psychopathol 15: 431–449.
  • Hajszan T, MacLusky NJ, Leranth C (2004) Dehydroepiandrosterone increases hippocampal spine synapse density in ovariectomized female rats. Endocrinology 145: 1042–1045.
  • Hermans EJ, Putman P, Baas JM, Koppeschaar HP, van Honk J (2006) A single administration of testosterone reduces fear‑potentiated startle in humans. Biol Psychiatry 59: 872–874.
  • Hodosy J, Zelmanova D, Majzunova M, Filova B, Malinova M, Ostatnikova D, Celec P (2012) The anxiolytic effect of testosterone in the rat is mediated via the androgen receptor. Pharmacol Biochem Behav 102: 191–195.
  • Hofford RS, Wellman PJ, Eitan S (2010) Social influences on plasma testosterone levels in morphine withdrawn adolescent mice and their drug‑naive cage‑mates. Psychoneuroendocrinology 36: 728–736.
  • Justel N, Ruetti E, Bentosela M, Mustaca AE, Papini MR (2012a) Effects of testosterone administration and gonadectomy on incentive downshift and open field activity in rats. Physiol Behav 106: 657–663.
  • Justel N, Ruetti E, Mustaca AE, Papini MR (2012b) Effects of pretraining treatment with testosterone on successive and anticipatory negative contrast. Physiol Behav 105: 933–937.
  • Kahveci N, Gulec G, Ozluk K (2006) Effects of intracerebroventricularly‑in‑ jected morphine on anxiety, memory retrieval and locomotor activity in rats: involvement of vasopressinergic system and nitric oxide pathway. Pharmacol Biochem Behav 85: 859–867.
  • Kaminetsky JC (2005) Benefits of a new testosterone gel formulation for hypogonadal men. Clin Cornerstone 4: S8–12.
  • Katz N, Mazer NA (2009) The impact of opioids on the endocrine system. Clin J Pain 25: 170–175.
  • Kepler KL, Kest B, Kiefel JM, Cooper ML, Bodnar RJ (1989) Roles of gender, gonadectomy and estrous phase in the analgesic effects of intra‑ cerebroventricular morphine in rats. Pharmacol Biochem Behav 34: 119–127.
  • Kepler KL, Standifer KM, Paul D, Kest B, Pasternak GW, Bodnar RJ (1991) Gender effects and central opioid analgesia. Pain 45: 87–94.
  • Kesmati  M, Mard‑Soltani  M, Khajehpour  L (2014) Anxiogenic effects of acute injection of sesame oil may be mediated by beta‑1 adrenoceptors in the basolateral amygdala. Adv Pharm Bull 4: 35–42.
  • Kessler RC, Brandenburg N, Lane  M, Roy‑Byrne P, Stang PD, Stein DJ, Wittchen HU (2005) Rethinking the duration requirement for generalized anxiety disorder: evidence from the National Comorbidity Survey Replication. Psychol Med 35: 1073–1082.
  • Kest B, Sarton E, Dahan A (2000) Gender differences in opioid‑mediated analgesia: animal and human studies. Anesthesiology 93: 539–547.
  • Kest B, Wilson SG, Mogil JS (1999) Sex differences in supraspinal morphine analgesia are dependent on genotype. J  Pharmacol Exp Ther 289: 1370–1375.
  • Khakpai F (2014) The effect of opiodergic system and testosterone on anxiety behavior in gonadectomized rats. Behav Brain Res 263: 9–15.
  • Khera M (2013) Patients with testosterone deficit syndrome and depression. Arch Esp Urol 66: 729–736.
  • Kim DH, Kim NJ, Zhao RJ, Yang CH, Kim HY, Gwak YS, Jang EY, Kim JS, Lee YK, Lee HJ, Lim SC, Lee BH (2018) Effects of acupuncture on the anxiety‑like behavior induced by withdrawal from chronic morphine use. Neurosci Lett 664: 38–42.
  • Kim EU, Spear LP (2016) Sex‑dependent consequences of pre‑pubertal gonadectomy: Social behavior, stress and ethanol responsivity. Behav Brain Res 296: 260–269.
  • King JA, De Oliveira WL, Patel N (2005) Deficits in testosterone facilitate enhanced fear response. Psychoneuroendocrinology 30: 333–340.
  • Kudryavtseva NN, Gerrits MA, Avgustinovich DF, Tenditnik MV, Van Ree JM (2004) Modulation of anxiety‑related behaviors by mu‑ and kappa‑opioid receptor agonists depends on the social status of mice. Peptides 25: 1355–1363.
  • Lacreuse A, King HM, Kurdziel LB, Partan SR, Caldwell KM, Chiavetta MR, Millette MM, Meyer JS, Grow DR (2010) Testosterone may increase selective attention to threat in young male macaques. Horm Behav 58: 854–863.
  • Lambert GM, Erskine MS, Baum MJ (1990) Effect of naloxone on the pulsatile secretion of luteinizing hormone in gonadectomized male and female ferrets before and after oestradiol replacement. J Neuroendo‑ crinol 2: 701–705.
  • Le Merrer J, Cagniard B, Cazala P (2006) Modulation of anxiety by mu‑opioid receptors of the lateral septal region in mice. Pharmacol Biochem Behav 83: 465–479.
  • Leuner B, Shors TJ (2012) Stress, anxiety, and dendritic spines: What are the connections? Neuroscience 251: 108–119.
  • Liang Y, Li J, Jin T, Gu T, Zhu Q, Hu Y, Yang Y, Wu D, Jiang K, Xu X (2018) Bisphenol‑A inhibits improvement of testosterone in anxiety‑ and depression‑like behaviors in gonadectomied male mice. Horm Behav 102: 129–138.
  • Loyd DR, Wang X, Murphy AZ (2008) Sex differences in micro‑opioid receptor expression in the rat midbrain periaqueductal gray are essential for eliciting sex differences in morphine analgesia. J  Neurosci 28: 14007–14017.
  • Lund TD, Rovis T, Chung WC, Handa RJ (2005) Novel actions of estrogen receptor‑beta on anxiety‑related behaviors. Endocrinology 146: 797–807.
  • Masotto C, Negro‑Vilar A (1988) Gonadectomy influences the inhibitory effect of the endogenous opiate system on pulsatile gonadotropin secretion. Endocrinology 123: 747–752.
  • Mateo AR, Hijazi  M, Hammer RP Jr. (1992) Dynamic patterns of medial preoptic muopiate receptor regulation by gonadal steroid hormones. Neuroendocrinology 55: 51–58.
  • McDermott CM, Liu D, Schrader LA (2012) Role of gonadal hormones in anxiety and fear memory formation and inhibition in male mice. Physiol Behav 105: 1168–1174.
  • McHenry J, Carrier N, Hull E, Kabbaj M (2014) Sex differences in anxiety and depression: role of testosterone. Front Neuroendocrinol 35: 42–57.
  • McHugh RK, Votaw VR, Barlow DH, Fitzmaurice GM, Greenfield SF, Weiss RD (2017) Development of an integrated cognitive behavioral therapy for anxiety and opioid use disorder: Study protocol and methods. Contemp Clin Trials 60: 105–112.
  • Meyers B, D’Agostino A, Walker J, Kritzer MF (2010) Gonadectomy and hor‑ mone replacement exert region‑ and enzyme isoform‑specific effects on monoamine oxidase and catechol‑O‑methyltransferase activity in prefrontal cortex and neostriatum of adult male rats. Neuroscience 165: 850–862.
  • Miladi‑Gorji H, Rashidy‑Pour A, Fathollahi Y (2012) Anxiety profile in morphine‑dependent and withdrawn rats: effect of voluntary exercise. Physiol Behav 105: 195–202.
  • Miller KK, Perlis RH, Papakostas GI, Mischoulon D, Losifescu DV, Brick DJ, Fava M (2009) Low‑dose transdermal testosterone augmentation therapy improves depression severity in women. CNS Spectr 14: 688–694.
  • Moghadami S, Jahanshahi  M, Sepehri H, Amini H (2016) Gonadectomy reduces the density of androgen receptor‑immunoreactive neurons in male rat’s hippocampus: testosterone replacement compensates it. Be‑ hav Brain Funct 12: 5.
  • Morales A, Bebb RA, Manjoo P, Assimakopoulos P, Axler J, Collier C, Elliott S, Goldenberg L, Gottesman I, Grober ED, Guyatt GH, Holmes DT, Lee JC (2015) Diagnosis and management of testosterone deficiency syndrome in men: clinical practice guideline. CMAJ 187: 1369–1377.
  • Morris RW, Fung SJ, Rothmond DA, Richards B, Ward S, Noble PL, Woodward RA, Weickert CS, Winslow JT (2010) The effect of gonadec‑ tomy on prepulse inhibition and fear‑potentiated startle in adolescent rhesus macaques. Psychoneuroendocrinology 35: 896–905.
  • Perrine SA, Hoshaw BA, Unterwald EM (2006) Delta opioid receptor ligands modulate anxiety‑like behaviors in the rat. Br J Pharmacol 147: 864–872.
  • Peters KD, Wood RI (2005) Androgen dependence in hamsters: overdose, tolerance, and potential opioidergic mechanisms. Neuroscience 130: 971–981.
  • Philipova T, Ivanova T, Pavlova E, Kasakov  L, Vlaskovska  M (2003) Nan-drolone modulates the non‑opioid and opioid analgesia and tolerance/ dependence: role of sexual dimorphism. Arch Physiol Biochem 111: 429–436.
  • Pooriamehr A, Sabahi P, Miladi‑Gorji H (2017) Effects of environmental enrichment during abstinence in morphine dependent parents on anxiety, depressive‑like behaviors and voluntary morphine consumption in rat offspring. Neurosci Lett 656: 37–42.
  • Prut L, Belzung C (2003) The open field as a paradigm to measure the effects of drugs on anxiety‑like behaviors: a review. Eur J Pharmacol 463: 3–33.
  • Rezayof A, Hosseini SS, Zarrindast MR (2009) Effects of morphine on rat behaviour in the elevated plus maze: the role of central amygdala dopamine receptors. Behav Brain Res 202: 171–178.
  • Rhodes ME, Frye CA (2004) Androgens in the hippocampus can alter, and be altered by, ictal activity. Pharmacol Biochem Behav 78: 483–493.
  • Roeska K, Doods H, Arndt K, Treede RD, Ceci A (2008) Anxiety‑like behaviour in rats with mononeuropathy is reduced by the analgesic drugs morphine and gabapentin. Pain 139: 349–357.
  • Ruka KA, Burger LL, Moenter SM (2016) Both estrogen and androgen modify the response to activation of neurokinin‑3 and kappa‑opioid rece tors in arcuate kisspeptin neurons from male mice. Endocrinology 157: 752–763.
  • Seidman SN, Orr G, Raviv G, Levi R, Roose SP, Kravitz E, Amiaz R, Weiser M (2009) Effects of testosterone replacement in middle‑aged men with dysthymia: a randomized, placebo‑controlled clinical trial. J Clin Psycho‑ pharmacol 29: 216–221.
  • Shin IC, Kim HC, Swanson J, Hong JT, Oh  KW (2003) Anxiolytic effects of acute morphine can be modulated by nitric oxide systems. Pharmacol‑ ogy 68: 183–189.
  • Siepmann M, Joraschky P (2007) Modelling anxiety in humans for drug development. Curr Neuropharmacol 5: 65–72.
  • Solati J (2011) Dorsal hippocampal N‑methyl‑D‑aspartate glutamatergic and delta‑opioidergic systems modulate anxiety behaviors in rats in a noninteractive manner. Kaohsiung J Med Sci 27: 485–493.
  • Solati J, Zarrindast MR, Salari AA (2010) Dorsal hippocampal opioidergic system modulates anxiety‑like behaviors in adult male Wistar rats. Psy‑ chiatry Clin Neurosci 64: 634–641.
  • Svensson AI, Soderpalm B, Engel JA (2000) Gonadectomy enhances shock‑induced behavioral inhibition in adult male rats: implications for impulsive behavior. Pharmacol Biochem Behav 65: 731–736.
  • Terburg D, Syal S, Rosenberger LA, Heany SJ, Stein DJ, Honk J (2016) Testos‑ terone abolishes implicit subordination in social anxiety. Psychoneuroendocrinology 72: 205–211.
  • Terner JM, Barrett AC, Grossell E, Picker MJ (2002) Influence of gonadec‑ tomy on the antinociceptive effects of opioids in male and female rats. Psychopharmacology 163: 183–193.
  • Toufexis D, Davis C, Hammond A, Davis  M (2005) Sex differences in hormonal modulation of anxiety measured with light‑enhanced startle: possible role for arginine vasopressin in the male. J Neurosci 25: 9010–9016.
  • Toufexis DJ, Myers KM, Davis M (2006) The effect of gonadal hormones and gender on anxiety and emotional learning. Horm Behav 50: 539–549.
  • Turvin JC, Messer WS Jr., Kritzer MF (2007) On again, off again effects of gonadectomy on the acoustic startle reflex in adult male rats. Physiol Behav 90: 473–482.
  • van Honk J, Peper JS, Schutter DJ (2005) Testosterone reduces unconscious fear but not consciously experienced anxiety: implications for the disorders of fear and anxiety. Biol Psychiatry 58: 218–225.
  • Walf AA, Frye CA (2005a) Antianxiety and antidepressive behavior produced by physiological estradiol regimen may be modulated by hypothalamic‑pituitary‑adrenal axis activity. Neuropsychopharmacology 30: 1288–1301.
  • Walf AA, Frye CA (2005b) ERbeta‑selective estrogen receptor modulators produce antianxiety behavior when administered systemically to ovariectomized rats. Neuropsychopharmacology 30: 1598–1609.
  • Wang J, Zhu G, Huang L, Nie T, Tao K, Li Y, Gao G (2017) Morphine administration induces change in anxiety‑related behavior via Wnt/beta‑catenin signaling. Neurosci Lett 639: 199–206.
  • Whisnant CS, Goodman RL (1988) Effects of an opioid antagonist on pulsatile luteinizing hormone secretion in the ewe vary with changes in steroid negative feedback. Biol Reprod 39: 1032–1038.
  • Yan W, Kang J, Zhang G, Li S, Kang Y, Wang L, Shi G (2015) The effects of gonadectomy and binge‑like ethanol exposure during adolescence on open field behaviour in adult male rats. Neurosci Lett 604: 52–57.
  • Yazici K, Pata O, Yazici A, Aktas A, Tot S, Kanik A (2003) The effects of hormone replacement therapy in menopause on symptoms of anxiety and depression (in Turkish). Turk Psikiyatri Derg 14: 101–105.
  • Zarrindast MR, Babapoor‑Farrokhran S, Rezayof A (2008) Involvement of opioidergic system of the ventral hippocampus, the nucleus accumbens or the central amygdala in anxiety‑related behavior. Life Sci 82: 1175–1181.
  • Zarrindast MR, Khodarahmi P, Rezayof A, Oryan S (2010) Withdrawal from repeated administration of morphine alters histamine‑induced anxiogenic effects produced by intraventral hippocampal microinjection. J Psychopharmacol 24: 881–889.
  • Zarrindast MR, Rostami P, Zarei M, Roohbakhsh A (2005) Intracerebroven‑ tricular effects of histaminergic agents on morphine‑induced anxioly‑ sis in the elevated plus‑maze in rats. Basic Clin Pharmacol Toxicol 97: 276–281.
  • Zarrindast MR, Sarahroodi S, Arzi A, Khodayar MJ, Taheri‑Shalmani S, Rezayof A (2008) Cannabinoid CB1 receptors of the rat central amygdala mediate anxiety‑like behavior: interaction with the opioid system. Behav Pharmacol 19: 716–723.
  • Zarrouf FA, Artz S, Griffith J, Sirbu C, Kommor M (2009) Testosterone and depression: systematic review and meta‑analysis. J Psychiatr Pract 15: 289–305.
  • Zhang G, Shi G, Tan H, Kang Y, Cui H (2011) Intranasal administration of testosterone increased immobile‑sniffing, exploratory behavior, motor behavior and grooming behavior in rats. Horm Behav 59: 477–483.
  • Zuloaga DG, Morris JA, Jordan CL, Breedlove SM (2008) Mice with the testicular feminization mutation demonstrate a role for androgen receptors in the regulation of anxiety‑related behaviors and the hypothalamic‑pituitary‑adrenal axis. Horm Behav 54: 758–766.
  • Zuloaga DG, Poort JE, Jordan CL, Breedlove SM (2011) Male rats with the testicular feminization mutation of the androgen receptor display elevated anxiety‑related behavior and corticosterone response to mild stress. Horm Behav 60: 380–388.

Typ dokumentu

Bibliografia

Identyfikatory

Identyfikator YADDA

bwmeta1.element.agro-1bfd61cc-f8e7-455e-b70e-1616a0496bf7
JavaScript jest wyłączony w Twojej przeglądarce internetowej. Włącz go, a następnie odśwież stronę, aby móc w pełni z niej korzystać.