Coupling of the HPA and HPG axes in the context of early life adversity in incarcerated male adolescents.

The effects of early life adversity can be observed across the lifespan, and the hypothalamic-pituitary-adrenal (HPA) and hypothalamic-pituitary-gonadal (HPG) axes could be mechanistic intermediaries underlying this phenomenon. The current study examined 50 adolescent males aged 12-18 in a maximum-security correctional and treatment setting. Saliva samples were collected five times a day for 2 days and assayed for cortisol, testosterone, and DHEA. Youth completed semi-structured life stress interviews and self-reports of child maltreatment to index adversity. When youth had higher testosterone levels, they had higher cortisol and DHEA levels, indicating positive "coupling" of the HPA-HPG axes. In addition, children experiencing greater life adversity had tighter coupling of the HPA-HPG axes. Additional analyses hint that coupling may be driven largely by HPG axis functioning. Results indicate that positive coupling of the HPA-HPG axis is observed within incarcerated adolescents, especially for those with the greatest life stress.

[1]  A. Hupbach,et al.  Beyond the Stress Concept: Allostatic Load—A Developmental Biological and Cognitive Perspective , 2015 .

[2]  C. Zahn-Waxler,et al.  Within-person coupling of changes in cortisol, testosterone, and DHEA across the day in adolescents. , 2015, Developmental psychobiology.

[3]  E. Shirtcliff,et al.  Neuroendocrine coupling across adolescence and the longitudinal influence of early life stress. , 2015, Developmental psychobiology.

[4]  E. Shirtcliff,et al.  Psychopathy's influence on the coupling between hypothalamic-pituitary-adrenal and -gonadal axes among incarcerated adolescents. , 2014, Developmental psychobiology.

[5]  Dan J Stein,et al.  Testosterone administration in women increases amygdala responses to fearful and happy faces , 2013, Psychoneuroendocrinology.

[6]  Pranjal H. Mehta,et al.  Endogenous testosterone and cortisol jointly influence reactive aggression in women , 2013, Psychoneuroendocrinology.

[7]  K. Marceau,et al.  Stress and puberty-related hormone reactivity, negative emotionality, and parent–adolescent relationships , 2012, Psychoneuroendocrinology.

[8]  N. Kalin,et al.  Longitudinal stability and developmental properties of salivary cortisol levels and circadian rhythms from childhood to adolescence. , 2012, Developmental psychobiology.

[9]  Ned H Kalin,et al.  Influence of early life stress on later hypothalamic–pituitary–adrenal axis functioning and its covariation with mental health symptoms: A study of the allostatic process from childhood into adolescence , 2011, Development and Psychopathology.

[10]  G. Fernández,et al.  Gonadal hormone regulation of the emotion circuitry in humans , 2011, Neuroscience.

[11]  C. Kuzawa,et al.  Cortisol and testosterone in Filipino young adult men: Evidence for co‐regulation of both hormones by fatherhood and relationship status , 2011, American journal of human biology : the official journal of the Human Biology Council.

[12]  Andrea L Glenn,et al.  Increased testosterone-to-cortisol ratio in psychopathy. , 2011, Journal of abnormal psychology.

[13]  K. Harkness,et al.  Cortisol reactivity to social stress in adolescents: Role of depression severity and child maltreatment , 2011, Psychoneuroendocrinology.

[14]  D. Schteingart Glucocorticoids in the prefrontal cortex enhance memory consolidation and impair working memory by a common neural mechanism , 2011 .

[15]  Pranjal H. Mehta,et al.  Testosterone and cortisol jointly regulate dominance: Evidence for a dual-hormone hypothesis , 2010, Hormones and Behavior.

[16]  R. Kahn,et al.  HPG-axis hormones during puberty: A study on the association with hypothalamic and pituitary volumes , 2010, Psychoneuroendocrinology.

[17]  Steven J. Stanton,et al.  Dominance, Politics, and Physiology: Voters' Testosterone Changes on the Night of the 2008 United States Presidential Election , 2009, PloS one.

[18]  S. Pollak,et al.  Hormonal reactivity to MRI scanning in adolescents , 2009, Psychoneuroendocrinology.

[19]  Ewald Moser,et al.  Amygdala activity to fear and anger in healthy young males is associated with testosterone , 2009, Psychoneuroendocrinology.

[20]  Steven J. Stanton,et al.  Endogenous testosterone levels are associated with amygdala and ventromedial prefrontal cortex responses to anger faces in men but not women , 2009, Biological Psychology.

[21]  S. Chiavegatto,et al.  Anabolic‐androgenic steroid treatment induces behavioral disinhibition and downregulation of serotonin receptor messenger RNA in the prefrontal cortex and amygdala of male mice , 2009, Genes, brain, and behavior.

[22]  J. Buitelaar,et al.  Testosterone Increases Amygdala Reactivity in Middle-Aged Women to a Young Adulthood Level , 2008, Neuropsychopharmacology.

[23]  J. Buitelaar,et al.  Testosterone Increases Amygdala Reactivity in Middle-Aged Women to a Young Adulthood Level , 2009, Neuropsychopharmacology.

[24]  Pranjal H. Mehta,et al.  The social endocrinology of dominance: basal testosterone predicts cortisol changes and behavior following victory and defeat. , 2008, Journal of personality and social psychology.

[25]  R. Steiner,et al.  The role of kisspeptins and GPR54 in the neuroendocrine regulation of reproduction. , 2008, Annual review of physiology.

[26]  Erno J. Hermans,et al.  Exogenous Testosterone Enhances Responsiveness to Social Threat in the Neural Circuitry of Social Aggression in Humans , 2008, Biological Psychiatry.

[27]  C. Zahn-Waxler,et al.  Salivary dehydroepiandrosterone responsiveness to social challenge in adolescents with internalizing problems. , 2007, Journal of child psychology and psychiatry, and allied disciplines.

[28]  L. Kriegsfeld,et al.  Environmental control of kisspeptin: implications for seasonal reproduction. , 2007, Endocrinology.

[29]  Desmond K. Runyan,et al.  Effect of early childhood adversity on child health. , 2006, Archives of pediatrics & adolescent medicine.

[30]  Jonathan B. Kotch,et al.  Child Maltreatment in the United States: Prevalence, Risk Factors, and Adolescent Health Consequences , 2006, Pediatrics.

[31]  Peter Kirsch,et al.  Influence of the stress hormone cortisol on fear conditioning in humans: Evidence for sex differences in the response of the prefrontal cortex , 2006, NeuroImage.

[32]  E. Gordon,et al.  Early Life Stress and Morphometry of the Adult Anterior Cingulate Cortex and Caudate Nuclei , 2006, Biological Psychiatry.

[33]  Karen J. Ferguson,et al.  Smaller left anterior cingulate cortex volumes are associated with impaired hypothalamic-pituitary-adrenal axis regulation in healthy elderly men. , 2006, The Journal of clinical endocrinology and metabolism.

[34]  J. Detre,et al.  Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[35]  James P. Herman,et al.  Limbic system mechanisms of stress regulation: Hypothalamo-pituitary-adrenocortical axis , 2005, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[36]  M. Weinstock The potential influence of maternal stress hormones on development and mental health of the offspring , 2005, Brain, Behavior, and Immunity.

[37]  Derek A. Hamilton,et al.  Virtual navigation in humans: the impact of age, sex, and hormones on place learning , 2005, Hormones and Behavior.

[38]  B. Dubrovsky Steroids, neuroactive steroids and neurosteroids in psychopathology , 2005, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[39]  B. Ellis Timing of pubertal maturation in girls: an integrated life history approach. , 2004, Psychological bulletin.

[40]  D. Hellhammer,et al.  Autobiographic memory impairment following acute cortisol administration , 2004, Psychoneuroendocrinology.

[41]  C. Mazure,et al.  Childhood maltreatment as a risk factor for adult cardiovascular disease and depression. , 2004, The Journal of clinical psychiatry.

[42]  Dennis C. Choi,et al.  Central mechanisms of stress integration: hierarchical circuitry controlling hypothalamo–pituitary–adrenocortical responsiveness , 2003, Frontiers in Neuroendocrinology.

[43]  V. Viau,et al.  Functional Cross‐Talk Between the Hypothalamic‐Pituitary‐Gonadal and ‐Adrenal Axes , 2002, Journal of neuroendocrinology.

[44]  Alan Booth,et al.  Testosterone, cortisol, and women's competition. , 2002 .

[45]  M. Wilson,et al.  Sex differences in hippocampal slice excitability: role of testosterone , 2002, Neuroscience.

[46]  D. Cicchetti,et al.  Diverse patterns of neuroendocrine activity in maltreated children , 2001, Development and Psychopathology.

[47]  M. Gunnar,et al.  Low cortisol and a flattening of expected daytime rhythm: Potential indices of risk in human development , 2001, Development and Psychopathology.

[48]  D. Charney,et al.  Effects of early stress on brain structure and function: Implications for understanding the relationship between child maltreatment and depression , 2001, Development and Psychopathology.

[49]  C. Kirschbaum,et al.  Genetic factors, perceived chronic stress, and the free cortisol response to awakening , 2000, Psychoneuroendocrinology.

[50]  R. Davidson,et al.  Dysfunction in the neural circuitry of emotion regulation--a possible prelude to violence. , 2000, Science.

[51]  I. Clarke,et al.  Effects of stress on reproduction in non-rodent mammals: the role of glucocorticoids and sex differences. , 2000, Reviews of reproduction.

[52]  J. Garber,et al.  Psychosocial antecedents of variation in girls' pubertal timing: maternal depression, stepfather presence, and marital and family stress. , 2000, Child development.

[53]  R. Sapolsky,et al.  How do glucocorticoids influence stress responses? Integrating permissive, suppressive, stimulatory, and preparative actions. , 2000, Endocrine reviews.

[54]  J. Douglas Bremner,et al.  Does stress damage the brain? , 1999, Biological Psychiatry.

[55]  M. Gunnar,et al.  Assessing salivary cortisol in studies of child development. , 1998, Child development.

[56]  Desmond K. Runyan,et al.  Identification of child maltreatment with the Parent-Child Conflict Tactics Scales: development and psychometric data for a national sample of American parents. , 1998, Child abuse & neglect.

[57]  S. Schanberg,et al.  Neuroendocrine, Cardiovascular, and Emotional Responses of Hostile Men: The Role of Interpersonal Challenge , 1998, Psychosomatic medicine.

[58]  J. M. Dabbs,et al.  Age, Testosterone, and Behavior Among Female Prison Inmates , 1997, Psychosomatic medicine.

[59]  D. Bernstein,et al.  Validity of the Childhood Trauma Questionnaire in an adolescent psychiatric population. , 1997, Journal of the American Academy of Child and Adolescent Psychiatry.

[60]  J. Herman,et al.  Neurocircuitry of stress: central control of the hypothalamo–pituitary–adrenocortical axis , 1997, Trends in Neurosciences.

[61]  C. Ferris,et al.  Testosterone facilitates aggression by modulating vasopressin receptors in the hypothalamus , 1996, Physiology & Behavior.

[62]  T. Kupers Trauma and its sequelae in male prisoners: effects of confinement, overcrowding, and diminished services. , 1996, The American journal of orthopsychiatry.

[63]  Jasmin K. Riad,et al.  Testosterone, crime, and misbehavior among 692 male prison inmates , 1995 .

[64]  P. Giancola EVidence for dorsolateral and orbital prefrontal cortical involvement in the expression of aggressive behavior , 1995 .

[65]  S. Feldman,et al.  Differential effect of amygdaloid lesions on CRF-41, ACTH and corticosterone responses following neural stimuli , 1994, Brain Research.

[66]  T. Gray,et al.  Amygdaloid CRF Pathways: Role in Autonomic, Neuroendocrine, and Behavioral Responses to Stress , 1993, Annals of the New York Academy of Sciences.

[67]  M. Meaney,et al.  The role of the medial prefrontal cortex (cingulate gyrus) in the regulation of hypothalamic-pituitary-adrenal responses to stress , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[68]  C. Hammen,et al.  Stress exposure and stress generation in children of depressed mothers. , 1993, Journal of consulting and clinical psychology.

[69]  T. Tabira,et al.  Stress induces neuronal death in the hippocampus of castrated rats , 1992, Neuroscience Letters.

[70]  Michael Davis,et al.  The role of the amygdala in fear and anxiety. , 1992, Annual review of neuroscience.

[71]  S. Rivest,et al.  Effect of stress on the activity of the hypothalamic-pituitary-gonadal axis: peripheral and central mechanisms. , 1991, Biology of reproduction.

[72]  G. Jurkovic,et al.  Salivary testosterone and cortisol among late adolescent male offenders , 1991, Journal of abnormal child psychology.

[73]  R. Sapolsky,et al.  The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. , 1991, Endocrine reviews.

[74]  R. Ahima,et al.  Charting of Type II glucocorticoid receptor-like immunoreactivity in the rat central nervous system , 1990, Neuroscience.

[75]  S. Gauthier,et al.  Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[76]  R. L. Frady,et al.  Changes in Saliva Testosterone Levels During a 90-Day Shock Incarceration Program , 1990 .

[77]  D. Lincoln,et al.  Plasma cortisol is increased during the inhibition of LH secretion by central LHRH in the ewe. , 1990, Neuroendocrinology.

[78]  K. Fuxe,et al.  Localization of glucocorticoid receptor mRNA in the male rat brain by in situ hybridization. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[79]  A. Petersen,et al.  A self-report measure of pubertal status: Reliability, validity, and initial norms , 1988, Journal of youth and adolescence.

[80]  C. Léránth,et al.  Immunocytochemical evidence for direct synaptic connections between corticotrophin-releasing factor (CRF) and gonadotrophin-releasing hormone (GnRH)- containing neurons in the preoptic area of the rat , 1988, Brain Research.

[81]  J. Koolhaas,et al.  Medial amygdala lesions in male rats reduce aggressive behavior: interference with experience , 1987, Physiology & Behavior.

[82]  R. Sapolsky Stress-induced elevation of testosterone concentration in high ranking baboons: role of catecholamines. , 1986, Endocrinology.

[83]  B. McEwen,et al.  Glucocorticoid-sensitive hippocampal neurons are involved in terminating the adrenocortical stress response. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[84]  J. Allen,et al.  Role of the amygdaloid complexes in the stress-induced release of ACTH in the rat. , 1974, Neuroendocrinology.

[85]  M. Chhetri Plasma cortisol. , 1972, Journal of the Indian Medical Association.

[86]  G K Matheson,et al.  Effects of amygdaloid stimulation on pituitary-adrenal activity in conscious cats. , 1971, Brain research.

[87]  G. Popa A Portal Circulation from the Pituitary to the Hypothalamic Region. , 1930, Journal of anatomy.