Behavioural and Neuroendocrine Adaptations to Repeated Stress during Puberty in Male Golden Hamsters

In adult animals, the consequences of stress are often severe and long lasting. Repeated subjugation in adult male golden hamsters inhibits aggression and increases submissive and avoidant behaviours. By contrast, subjugation during puberty enhances offensive aggression. The goals of this study were to characterize behavioural and neuroendocrine responses of naïve and repeatedly subjugated juveniles to social defeat and to assess potential recovery from social stress. From the onset of puberty on postnatal day 28 (P28) to mid puberty (P42), animals were either socially subjugated or placed in a clean and empty cage for 20 min daily. The subjugated and control groups were further divided into subgroups and sacrificed under basal conditions or after social defeat on P28, P35 (early puberty), P45 (mid puberty) and P70 (early adulthood). On P35 and P45, repeatedly subjugated juveniles showed a complete inhibition of olfactory investigation (i.e. risk assessment) towards aggressive adults. Repeatedly subjugated also animals had lower postdefeat cortisol levels than controls on P45. Interestingly, basal cortisol levels increased gradually during puberty but did not differ between treatment groups at any point. Repeated subjugation was also associated with increased tyrosine hydroxylase immunoreactivity (ir‐TH) within the extended medial amygdala. After a 4‐week recovery period, none of these variables differed between subjugated and control groups. In an additional experiment, subjugated adults also had increased ir‐TH in the medial extended amygdala, suggesting that these neurones are particularly responsive to social stress. In conclusion, puberty may be a developmental period characterized by behavioural and neuroendocrine plasticity in stress responsiveness. Furthermore, peri‐pubertal changes in stress hormones may explain why juvenile hamsters are more resilient to social stress than adults.

[1]  M. Seligman,et al.  Learned helplessness in the rat. , 1975, Journal of comparative and physiological psychology.

[2]  Y. Delville,et al.  Stress and the development of agonistic behavior in golden hamsters , 2003, Hormones and Behavior.

[3]  D. Shalloway,et al.  Amygdaloid lesions and social behavior in the golden hamster. , 1970, Physiology & behavior.

[4]  R. A. Hensbroek,et al.  Muscarinic acetylcholine receptor immunoreactivity in the amygdala—II. Fear-induced plasticity , 1996, Neuroscience.

[5]  J. Herbert,et al.  Adaptation in patterns of c‐fos expression in the brain associated with exposure to either single or repeated social stress in male rats , 1998, The European journal of neuroscience.

[6]  M. Lehman,et al.  Medial nucleus of the amygdala mediates chemosensory control of male hamster sexual behavior. , 1980, Science.

[7]  C. Ferris,et al.  Neural Connections of the Anterior Hypothalamus and Agonistic Behavior in Golden Hamsters , 2000, Brain, Behavior and Evolution.

[8]  H. Albers,et al.  6 – Hormonal Basis of Social Conflict and Communication , 2002 .

[9]  B. McEwen,et al.  Tissue plasminogen activator in the amygdala is critical for stress-induced anxiety-like behavior , 2003, Nature Neuroscience.

[10]  A. Zangen,et al.  Altered gene expression for catecholamine biosynthetic enzymes and stress response in rat genetic model of depression. , 1998, Brain research. Molecular brain research.

[11]  A. Jasnow,et al.  Differential effects of two corticotropin-releasing factor antagonists on conditioned defeat in male Syrian hamsters (Mesocricetus auratus) , 1999, Brain Research.

[12]  J. A. Heyden,et al.  Characterization of stress-induced long-term behavioural changes in rats: Evidence in favor of anxiety , 1992, Physiology & Behavior.

[13]  M. Fanselow,et al.  Modality-specific retrograde amnesia of fear. , 1992, Science.

[14]  M. Lehman,et al.  Stria terminalis lesions alter the temporal pattern of copulatory behavior in the male golden hamster , 1983, Behavioural Brain Research.

[15]  S. Wiegand,et al.  Use of cryoprotectant to maintain long-term peptide immunoreactivity and tissue morphology , 1986, Peptides.

[16]  E. Nestler,et al.  Biochemical Adaptations in the Mesolimbic Dopamine System in Response to Repeated Stress , 1996, Neuropsychopharmacology.

[17]  R. Wood,et al.  Androgen receptor immunoreactivity in the male and female Syrian hamster brain. , 1999, Journal of neurobiology.

[18]  Y. Delville,et al.  Chronic social stress during puberty enhances tyrosine hydroxylase immunoreactivity within the limbic system in golden hamsters , 2002, Brain Research.

[19]  G. Griebel,et al.  Mouse defensive behaviors: pharmacological and behavioral assays for anxiety and panic , 2001, Neuroscience & Biobehavioral Reviews.

[20]  A. Kincaid,et al.  A species-specific population of tyrosine hydroxylase-immunoreactive neurons in the medial amygdaloid nucleus of the Syrian hamster , 1992, Brain Research.

[21]  F. Petty,et al.  Previous stress increases in vivo biogenic amine response to swim stress , 1994, Neurochemical Research.

[22]  M. Elmlinger,et al.  Reference Ranges for Serum Concentrations of Lutropin (LH), Follitropin (FSH), Estradiol (E2), Prolactin, Progesterone, Sex Hormone-Binding Globulin (SHBG), Dehydroepiandrosterone Sulfate (DHEAS), Cortisol and Ferritin in Neonates, Children and Young Adults , 2002, Clinical chemistry and laboratory medicine.

[23]  K. Miczek A new test for aggression in rats without aversive stimulation: Differential effects of d-amphetamine and cocaine , 1979, Psychopharmacology.

[24]  K. Huhman,et al.  Hormonal responses to fighting in hamsters: Separation of physical and psychological causes , 1992, Physiology & Behavior.

[25]  J. Weinberg,et al.  Adrenocortical responsiveness to novelty in the hamster , 1986, Physiology & Behavior.

[26]  G. S. Greenwald,et al.  The development of gonadotropin and steroid hormone patterns in male and female hamsters from birth to puberty. , 1979, Endocrinology.

[27]  Y. Delville,et al.  Repeated exposure to social stress alters the development of agonistic behavior in male golden hamsters , 2003, Hormones and Behavior.

[28]  C. McKittrick,et al.  13 – Effects of Social Stress on Hormones, Brain, and Behavior , 2002 .

[29]  Y. Delville,et al.  Repeated social stress and the development of agonistic behavior: individual differences in coping responses in male golden hamsters , 2003, Physiology & Behavior.

[30]  R. Wood,et al.  Androgen and estrogen concentrating neurons in chemosensory pathways of the male Syrian hamster brain , 1992, Brain Research.

[31]  S. Newman,et al.  Tyrosine hydroxylase neurons in the male hamster chemosensory pathway contain androgen receptors and are influenced by gonadal hormones , 1993, The Journal of comparative neurology.

[32]  L. P. Morin,et al.  stereotaxic atlas of the golden hamster brain , 2001 .

[33]  C. Sisk,et al.  Pubertal and seasonal plasticity in the amygdala , 2001, Brain Research.

[34]  H. Houshyar,et al.  Marked regulatory shifts in gonadal, adrenal, and metabolic system responses to repeated restraint stress occur within a 3-week period in pubertal male rats. , 2002, Endocrinology.

[35]  M. Potegal,et al.  Conditioned defeat in the Syrian golden hamster (Mesocricetus auratus). , 1993, Behavioral and neural biology.

[36]  Akil,et al.  Differential Expression of c‐fos mRNA Within Neurocircuits of Male Hamsters Exposed to Acute or Chronic Defeat , 1999, Journal of neuroendocrinology.

[37]  C. Ferris,et al.  Behavioral and Neurobiological Consequences of Social Subjugation during Puberty in Golden Hamsters , 1998, The Journal of Neuroscience.

[38]  S. Bhatnagar,et al.  Facilitation of hypothalamic–pituitary–adrenal responses to novel stress following repeated social stress using the resident/intruder paradigm , 2003, Hormones and Behavior.

[39]  W. Kiess,et al.  Salivary Cortisol Levels throughout Childhood and Adolescence: Relation with Age, Pubertal Stage, and Weight , 1995, Pediatric Research.

[40]  B. McEwen,et al.  Isolation stress increases tyrosine hydroxylase mRNA in the locus coeruleus and midbrain and decreases proenkephalin mRNA in the striatum and nucleus accumbens. , 1991, Brain Research. Molecular Brain Research.

[41]  L. Jonetz-Mentzel,et al.  Establishment of Reference Ranges for Cortisol in Neonates, Infants, Children and Adolescents , 1993, European journal of clinical chemistry and clinical biochemistry : journal of the Forum of European Clinical Chemistry Societies.

[42]  A. Jasnow,et al.  Conditioned defeat in male and female syrian hamsters , 2003, Hormones and Behavior.

[43]  C. Ferris,et al.  Acute and repeated exposure to social conflict in male golden hamsters: Increases in plasma POMC-peptides and cortisol and decreases in plasma testosterone , 1991, Hormones and Behavior.

[44]  M. Potegal,et al.  Brief, high-frequency stimulation of the corticomedial amygdala induces a delayed and prolonged increase of aggressiveness in male Syrian golden hamsters. , 1996, Behavioral neuroscience.

[45]  G. J. Vries,et al.  Estrogen-receptor immunoreactivity in hamster brain: preoptic area, hypothalamus and amygdala , 1993, Brain Research.