Stress response and the adolescent transition: Performance versus peer rejection stressors

Abstract Little is known about normative variation in stress response over the adolescent transition. This study examined neuroendocrine and cardiovascular responses to performance and peer rejection stressors over the adolescent transition in a normative sample. Participants were 82 healthy children (ages 7–12 years, n = 39, 22 females) and adolescents (ages 13–17, n = 43, 20 females) recruited through community postings. Following a habituation session, participants completed a performance (public speaking, mental arithmetic, mirror tracing) or peer rejection (exclusion challenges) stress session. Salivary cortisol, salivary alpha amylase (sAA), systolic and diastolic blood pressure (SBP, DBP), and heart rate were measured throughout. Adolescents showed significantly greater cortisol, sAA, SBP, and DBP stress response relative to children. Developmental differences were most pronounced in the performance stress session for cortisol and DBP and in the peer rejection session for sAA and SBP. Heightened physiological stress responses in typical adolescents may facilitate adaptation to new challenges of adolescence and adulthood. In high-risk adolescents, this normative shift may tip the balance toward stress response dysregulation associated with depression and other psychopathology. Specificity of physiological response by stressor type highlights the importance of a multisystem approach to the psychobiology of stress and may also have implications for understanding trajectories to psychopathology.

[1]  J. Long,et al.  Developmental changes in hypothalamus–pituitary–adrenal activity over the transition to adolescence: Normative changes and associations with puberty , 2009, Development and Psychopathology.

[2]  Douglas A. Granger,et al.  Salivary alpha amylase–cortisol asymmetry in maltreated youth , 2008, Hormones and Behavior.

[3]  Douglas A. Granger,et al.  Integration of salivary biomarkers into developmental and behaviorally-oriented research: Problems and solutions for collecting specimens , 2007, Physiology & Behavior.

[4]  L. Luecken,et al.  Handbook of Physiological Research Methods in Health Psychology , 2007 .

[5]  I. Goodyer,et al.  Disturbances in Morning Cortisol Secretion in Association with Maternal Postnatal Depression Predict Subsequent Depressive Symptomatology in Adolescents , 2007, Biological Psychiatry.

[6]  D. Cicchetti,et al.  Salivary biomarker levels and diurnal variation: associations with medications prescribed to control children's problem behavior. , 2007, Child development.

[7]  E. Gordis,et al.  Salivary alpha-amylase in biobehavioral research: recent developments and applications. , 2007, Annals of the New York Academy of Sciences.

[8]  Ahmad R. Hariri,et al.  Facial Expressions of Emotion Reveal Neuroendocrine and Cardiovascular Stress Responses , 2007, Biological Psychiatry.

[9]  J. Moskowitz,et al.  Positive affect and meaning-focused coping during significant psychological stress , 2007 .

[10]  E. Susman,et al.  Diurnal and Seasonal Cortisol, Testosterone, and DHEA Rhythms in Boys and Girls during Puberty , 2007, Chronobiology international.

[11]  E. Susman Psychobiology of persistent antisocial behavior: Stress, early vulnerabilities and the attenuation hypothesis , 2006, Neuroscience & Biobehavioral Reviews.

[12]  Dante Cicchetti,et al.  A Multiple‐Levels‐of‐Analysis Perspective on Resilience , 2006, Annals of the New York Academy of Sciences.

[13]  Douglas A. Granger,et al.  Asymmetry between salivary cortisol and α-amylase reactivity to stress: Relation to aggressive behavior in adolescents , 2006, Psychoneuroendocrinology.

[14]  G. Ladd,et al.  Peer rejection, aggressive or withdrawn behavior, and psychological maladjustment from ages 5 to 12: an examination of four predictive models. , 2006, Child development.

[15]  E. Adam Transactions among adolescent trait and state emotion and diurnal and momentary cortisol activity in naturalistic settings , 2006, Psychoneuroendocrinology.

[16]  Jacquelyn Mize,et al.  Integrating the measurement of salivary α-amylase into studies of child health, development, and social relationships , 2006 .

[17]  R. L. Marca,et al.  Stress-induced changes in human salivary alpha-amylase activity—associations with adrenergic activity , 2006, Psychoneuroendocrinology.

[18]  Nicolas Rohleder,et al.  Salivary alpha amylase as marker for adrenergic activity during stress: Effect of betablockade , 2006, Psychoneuroendocrinology.

[19]  Charissa S. L. Cheah,et al.  Adolescent girls' interpersonal vulnerability to depressive symptoms: a longitudinal examination of reassurance-seeking and peer relationships. , 2005, Journal of abnormal psychology.

[20]  R. Dahl,et al.  Neural systems of positive affect: Relevance to understanding child and adolescent depression? , 2005, Development and Psychopathology.

[21]  S. Matthews,et al.  Depressive Symptoms Are Associated With Increased Systemic Vascular Resistance to Stress , 2005, Psychosomatic medicine.

[22]  B. McEwen,et al.  Differential Stress Reactivity in Intact and Ovariectomized Prepubertal and Adult Female Rats , 2005, Neuroendocrinology.

[23]  H. MacMillan,et al.  Child maltreatment and HPA axis dysregulation: relationship to major depressive disorder and post traumatic stress disorder in females , 2005, Psychoneuroendocrinology.

[24]  E. Leibenluft,et al.  The social re-orientation of adolescence: a neuroscience perspective on the process and its relation to psychopathology , 2005, Psychological Medicine.

[25]  R. Dahl Adolescent Development and the Regulation of Behavior and Emotion: Introduction to Part VIII , 2004, Annals of the New York Academy of Sciences.

[26]  R. Dahl,et al.  Sex Differences in the Effects of Pubertal Development on Responses to a Corticotropin‐Releasing Hormone Challenge: The Pittsburgh Psychobiologic Studies , 2004, Annals of the New York Academy of Sciences.

[27]  S. Dickerson,et al.  Acute stressors and cortisol responses: a theoretical integration and synthesis of laboratory research. , 2004, Psychological bulletin.

[28]  I. Goodyer,et al.  Salivary cortisol and dehydroepiandrosterone in relation to puberty and gender , 2004, Psychoneuroendocrinology.

[29]  M. Gunnar,et al.  Integrating Neuroscience and Psychological Approaches in the Study of Early Experiences , 2003, Annals of the New York Academy of Sciences.

[30]  Carol Porth,et al.  Essentials of Pathophysiology: Concepts of Altered Health States , 2003 .

[31]  김지혜,et al.  아동 발현 불안 척도(Revised Children`s Manifest Anxiety Scale)의 요인구조 분석 , 2003 .

[32]  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.

[33]  Peter Salovey,et al.  Sex differences in stress responses: social rejection versus achievement stress , 2002, Biological Psychiatry.

[34]  W. Boyce,et al.  Associations Between Physiological Reactivity and Children’s Behavior: Advantages of a Multisystem Approach , 2002, Journal of developmental and behavioral pediatrics : JDBP.

[35]  P. Fechner Gender differences in puberty. , 2002, The Journal of adolescent health : official publication of the Society for Adolescent Medicine.

[36]  C. Zahn-Waxler,et al.  Adrenocortical activity in at-risk and normally developing adolescents: Individual differences in salivary cortisol basal levels, diurnal variation, and responses to social challenges , 2001, Development and Psychopathology.

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

[38]  E. Walker,et al.  Developmental changes in cortisol secretion in normal and at-risk youth , 2001, Development and Psychopathology.

[39]  B. McEwen,et al.  Can poverty get under your skin? Basal cortisol levels and cognitive function in children from low and high socioeconomic status , 2001, Development and Psychopathology.

[40]  Florian Holsboer,et al.  The Corticosteroid Receptor Hypothesis of Depression , 2000, Neuropsychopharmacology.

[41]  P. Salovey,et al.  The Yale Interpersonal Stressor (YIPS): Affective, physiological, and behavioral responses to a novel interpersonal rejection paradigm , 2000, Annals of behavioral medicine : a publication of the Society of Behavioral Medicine.

[42]  L. Spear The adolescent brain and age-related behavioral manifestations , 2000, Neuroscience & Biobehavioral Reviews.

[43]  J. Arnett Adolescent storm and stress, reconsidered. , 1999, The American psychologist.

[44]  D. D. Weinstein,et al.  Minor physical anomalies, dermatoglyphic asymmetries, and cortisol levels in adolescents with schizotypal personality disorder. , 1999, The American journal of psychiatry.

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

[46]  D. Vázquez STRESS AND THE DEVELOPING LIMBIC–HYPOTHALAMIC–PITUITARY–ADRENAL AXIS , 1998, Psychoneuroendocrinology.

[47]  G. Chrousos,et al.  Interactions between the Hypothalamic-Pituitary-Adrenal Axis and the Female Reproductive System: Clinical Implications , 1998, Annals of Internal Medicine.

[48]  C. Nemeroff,et al.  Psychoneuroendocrinology of depression. Hypothalamic-pituitary-adrenal axis. , 1998, The Psychiatric clinics of North America.

[49]  J. Schulkin,et al.  From normal fear to pathological anxiety. , 1998, Psychological review.

[50]  R. S. Jorgensen,et al.  Sociotropic cognition moderates blood pressure response to interpersonal stress in high-risk adolescent girls. , 1998, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[51]  B. McEwen Protective and damaging effects of stress mediators. , 1998, The New England journal of medicine.

[52]  G. Breakwell Transitions through adolescence: Interpersonal domains and context - Graber,JA, BrooksGunn,J, Petersen,AC , 1997 .

[53]  Wolfgang Rauh,et al.  Attenuated Free Cortisol Response to Psychosocial Stress in Children with Atopic Dermatitis , 1997, Psychosomatic medicine.

[54]  N. Schmidt,et al.  Salivary cortisol testing in children. , 1997, Issues in comprehensive pediatric nursing.

[55]  K. Matthews,et al.  Hemodynamic responses to laboratory stressors in children and adolescents: the influences of age, race, and gender. , 1997, Psychophysiology.

[56]  S Rosberg,et al.  Journal of Clinical Endocrinology and Metabolism Printed in U.S.A. Copyright © 1997 by The Endocrine Society Circadian Cortisol Rhythms in Healthy Boys and Girls: Relationship with Age, Growth, Body Composition, and , 2022 .

[57]  C. Kellogg,et al.  Adolescent development influences functional responsiveness of noradrenergic projections to the hypothalamus in male rats. , 1996, Brain research. Developmental brain research.

[58]  A. Armario,et al.  Comparison of the behavioural and endocrine response to forced swimming stress in five inbred strains of rats , 1995, Psychoneuroendocrinology.

[59]  D. Cardinali,et al.  Cardiovascular tests of autonomic function and sympathetic skin responses in patients with major depression. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[60]  C. Walker,et al.  Dissociation Between Behavioral and Hormonal Responses to the Forced Swim Stress in Lactating Rats , 1995, Journal of neuroendocrinology.

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

[62]  C. Kirschbaum,et al.  Salivary cortisol in psychoneuroendocrine research: Recent developments and applications , 1994, Psychoneuroendocrinology.

[63]  B. Campbell,et al.  Paradoxical autonomic responses to aversive stimuli in the developing rat. , 1994, Behavioral neuroscience.

[64]  G. Gensini,et al.  Changes in Blood Pressure Reactivity and 24-Hour Blood Pressure Profile Occurring at Puberty , 1994, Angiology.

[65]  C. Labrid Changes in blood pressure reactivity and 24-hour blood pressure profile occurring at puberty. , 1994 .

[66]  C. Kirschbaum,et al.  The 'Trier Social Stress Test'--a tool for investigating psychobiological stress responses in a laboratory setting. , 1993, Neuropsychobiology.

[67]  J P Henry,et al.  Biological basis of the stress response. , 1993, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[68]  M. Gunnar Reactivity of the hypothalamic-pituitary-adrenocortical system to stressors in normal infants and children. , 1992, Pediatrics.

[69]  R. Dahl,et al.  The Dexamethasone Suppression Test in children and adolescents: A review and a controlled study , 1992, Biological Psychiatry.

[70]  M. Colten,et al.  Adolescent stress: Causes and consequences , 1992 .

[71]  N. Schneiderman,et al.  The reliability and specificity of delta versus residualized change as measures of cardiovascular reactivity to behavioral challenges. , 1991, Psychophysiology.

[72]  R. Dahl,et al.  24-Hour cortisol measures in adolescents with major depression: A controlled study , 1991, Biological Psychiatry.

[73]  T. Achenbach Integrative Guide for the 1991 CBCL/4-18, Ysr, and Trf Profiles , 1991 .

[74]  M. Gunnar Studies of the human infant's adrenocortical response to potentially stressful events. , 1989, New directions for child development.

[75]  C. Kellogg,et al.  Pubertal-related changes influence the development of environment-related social interaction in the male rat. , 1989, Developmental Psychobiology.

[76]  C. Kirschbaum,et al.  Salivary cortisol in psychobiological research: an overview. , 1989, Neuropsychobiology.

[77]  B. Alpert,et al.  Race and cardiovascular reactivity. A replication. , 1988, Hypertension.

[78]  J. Thayer,et al.  The continuing problem of false positives in repeated measures ANOVA in psychophysiology: a multivariate solution. , 1987, Psychophysiology.

[79]  R. Sapolsky,et al.  Maturation of the adrenocortical stress response: Neuroendocrine control mechanisms and the stress hyporesponsive period , 1986, Brain Research Reviews.

[80]  M. Frankenhaeuser Challenge-control interaction as reflected in sympathetic-adrenal and pituitary-adrenal activity: comparison between the sexes. , 1982, Scandinavian journal of psychology.

[81]  J M Tanner,et al.  Variations in the Pattern of Pubertal Changes in Boys , 1970, Archives of disease in childhood.

[82]  J M Tanner,et al.  Variations in pattern of pubertal changes in girls. , 1969, Archives of disease in childhood.

[83]  F. Heald,et al.  Cortisol production rate in adolescent males in different stages of sexual maturation. , 1966, The Journal of clinical endocrinology and metabolism.

[84]  R. Liebelt,et al.  Sex difference in resting pituitary-adrenal function in the rat. , 1963, The American journal of physiology.

[85]  E. Gordis,et al.  Assessment of salivary a-amylase in biobehavioral research , 2008 .

[86]  G. Harold,et al.  The evidence for a neurobiological model of childhood antisocial behavior. , 2007, Psychological bulletin.

[87]  V. Viau,et al.  Gender and puberty interact on the stress-induced activation of parvocellular neurosecretory neurons and corticotropin-releasing hormone messenger ribonucleic acid expression in the rat. , 2005, Endocrinology.

[88]  Evangelia Charmandari,et al.  Endocrinology of the stress response. , 2005, Annual review of physiology.

[89]  R. S. Jorgensen,et al.  Agonistic interpersonal striving: social-cognitive mechanism of cardiovascular risk in youth? , 2004, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[90]  T. Lloyd,et al.  Urinary free cortisol increases in adolescent caucasian females during perimenarche. , 2003, The Journal of clinical endocrinology and metabolism.

[91]  C. Ferris,et al.  Roots of mental illness in children. , 2003 .

[92]  K. Matthews,et al.  Cardiovascular reactivity during social and nonsocial stressors: do children's personal goals and expressive skills matter? , 2002, Health psychology : official journal of the Division of Health Psychology, American Psychological Association.

[93]  D. Cicchetti,et al.  A developmental psychopathology perspective on adolescence. , 2002, Journal of consulting and clinical psychology.

[94]  T. Achenbach Manual for ASEBA School-Age Forms & Profiles , 2001 .

[95]  C. Gerhardt,et al.  Adolescent development: pathways and processes of risk and resilience. , 1995, Annual review of psychology.

[96]  G. Pons,et al.  Estudio psicométrico del State-Trait Anxiety Inventory for Children (STAIC) , 1994 .

[97]  C. Midgley,et al.  Development during adolescence. The impact of stage-environment fit on young adolescents' experiences in schools and in families. , 1993, The American psychologist.

[98]  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.