Associations among parenting experiences during childhood and adolescence, hypothalamus‐pituitary‐adrenal axis hypoactivity, and hippocampal gray matter volume reduction in young adults

Recent human studies have indicated that adverse parenting experiences during childhood and adolescence are associated with adulthood hypothalamus‐pituitary‐adrenal (HPA) axis hypoactivity. Chronic HPA axis hypoactivity inhibits hippocampal gray matter (GM) development, as shown by animal studies. However, associations among adverse parenting experiences during childhood and adolescence, HPA axis activity, and brain development, particularly hippocampal development, are insufficiently investigated in humans. In this voxel‐based structural magnetic resonance imaging study, using a cross‐sectional design, we examined the associations among the scores of parental bonding instrument (PBI; a self‐report scale to rate the attitudes of parents during the first 16 years), cortisol response determined by the dexamethasone/corticotropin‐releasing hormone test, and regional or total hippocampal GM volume in forty healthy young adults with the following features: aged between 18 and 35 years, no cortisol hypersecretion in response to the dexamethasone test, no history of traumatic events, or no past or current conditions of significant medical illness or neuropsychiatric disorders. As a result, parental overprotection scores significantly negatively correlated with cortisol response. Additionally, a significant positive association was found between cortisol response and total or regional hippocampal GM volume. No significant association was observed between PBI scores and total or regional hippocampal GM volume. In conclusion, statistical associations were found between parental overprotection during childhood and adolescence and adulthood HPA axis hypoactivity, and between HPA axis hypoactivity and hippocampal GM volume reduction in healthy young adults, but no significant relationship was observed between any PBI scores and adulthood hippocampal GM volume. Hum Brain Mapp 33:2211–2223, 2012. © 2011 Wiley Periodicals, Inc.

[1]  A. Dagher,et al.  Perceived early-life maternal care and the cortisol response to repeated psychosocial stress. , 2010, Journal of psychiatry & neuroscience : JPN.

[2]  K. Dedovic,et al.  Investigating the Association Between Early Life Parental Care and Stress Responsivity in Adulthood , 2010, Developmental neuropsychology.

[3]  Jean-Luc Anton,et al.  Region of interest analysis using an SPM toolbox , 2010 .

[4]  L. Price,et al.  Interaction of Childhood Maltreatment with the Corticotropin-Releasing Hormone Receptor Gene: Effects on Hypothalamic-Pituitary-Adrenal Axis Reactivity , 2009, Biological Psychiatry.

[5]  L. Price,et al.  Effect of Childhood Emotional Abuse and Age on Cortisol Responsivity in Adulthood , 2009, Biological Psychiatry.

[6]  Nuno Sousa,et al.  Effects of altered corticosteroid milieu on rat hippocampal neurochemistry and structure--an in vivo magnetic resonance spectroscopy and imaging study. , 2008, Journal of psychiatric research.

[7]  D. Hedges,et al.  Hippocampal and amygdala volumes in children and adults with childhood maltreatment‐related posttraumatic stress disorder: A meta‐analysis , 2008, Hippocampus.

[8]  C. Nemeroff,et al.  The Dexamethasone/Corticotropin-Releasing Factor Test in Men with Major Depression: Role of Childhood Trauma , 2008, Biological Psychiatry.

[9]  C. Conrad.  Chronic Stress-induced Hippocampal Vulnerability: The Glucocorticoid Vulnerability Hypothesis , 2008, Reviews in the neurosciences.

[10]  M. Fukuda,et al.  HPA axis dysfunction in unmedicated major depressive disorder and its normalization by pharmacotherapy correlates with alteration of neural activity in prefrontal cortex and limbic/paralimbic regions , 2007, Psychiatry Research: Neuroimaging.

[11]  G. Miller,et al.  If it goes up, must it come down? Chronic stress and the hypothalamic-pituitary-adrenocortical axis in humans. , 2007, Psychological bulletin.

[12]  K. Kasai,et al.  Estimation of premorbid IQ in individuals with Alzheimer’s disease using Japanese ideographic script (Kanji) compound words: Japanese version of National Adult Reading Test , 2006, Psychiatry and clinical neurosciences.

[13]  S. Kanba,et al.  Assessment of the Dexamethasone/CRH Test as a State-Dependent Marker for Hypothalamic-Pituitary-Adrenal (HPA) Axis Abnormalities in Major Depressive Episode: A Multicenter Study , 2006, Neuropsychopharmacology.

[14]  J. Feldon,et al.  Long-term effects of early-life environmental manipulations in rodents and primates: Potential animal models in depression research , 2005, Neuroscience & Biobehavioral Reviews.

[15]  D. Hellhammer,et al.  A new view on hypocortisolism , 2005, Psychoneuroendocrinology.

[16]  Karl J. Friston,et al.  Structural Covariance in the Human Cortex , 2005, The Journal of Neuroscience.

[17]  K. Dedovic,et al.  The Montreal Imaging Stress Task: using functional imaging to investigate the effects of perceiving and processing psychosocial stress in the human brain. , 2005, Journal of psychiatry & neuroscience : JPN.

[18]  D. Swaab,et al.  The stress system in the human brain in depression and neurodegeneration , 2005, Ageing Research Reviews.

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

[20]  Joseph A Maldjian,et al.  Precentral gyrus discrepancy in electronic versions of the Talairach atlas , 2004, NeuroImage.

[21]  S. Claes.  Corticotropin‐releasing hormone (CRH) in psychiatry: from stress to psychopathology , 2004, Annals of medicine.

[22]  G. Parker,et al.  The parental bonding instrument , 1979, Social Psychiatry and Psychiatric Epidemiology.

[23]  Paul J. Laurienti,et al.  An automated method for neuroanatomic and cytoarchitectonic atlas-based interrogation of fMRI data sets , 2003, NeuroImage.

[24]  S. Southwick,et al.  MRI and PET study of deficits in hippocampal structure and function in women with childhood sexual abuse and posttraumatic stress disorder. , 2003, The American journal of psychiatry.

[25]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[26]  R. Bonsall,et al.  Altered pituitary-adrenal axis responses to provocative challenge tests in adult survivors of childhood abuse. , 2003, The American journal of psychiatry.

[27]  M. Massagli,et al.  Longitudinal study of psychiatric symptoms, disability, mortality, and emigration among Bosnian refugees. , 2001, JAMA.

[28]  Carmine M Pariante,et al.  Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment , 2001, Biological Psychiatry.

[29]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

[30]  D. Hellhammer,et al.  The potential role of hypocortisolism in the pathophysiology of stress-related bodily disorders , 2000, Psychoneuroendocrinology.

[31]  H. Matsunaga,et al.  [Low-dose (0.5 mg) DST in manic and major depressive episodes: in relation to the severity of symptoms]. , 2000, Seishin shinkeigaku zasshi = Psychiatria et neurologia Japonica.

[32]  R. Sapolsky,et al.  Glucocorticoids, stress, and their adverse neurological effects: relevance to aging , 1999, Experimental Gerontology.

[33]  A. Convit,et al.  Cortisol levels during human aging predict hippocampal atrophy and memory deficits , 1998, Nature Neuroscience.

[34]  M. Stein,et al.  Hippocampal volume in women victimized by childhood sexual abuse , 1997, Psychological Medicine.

[35]  C. Brewin,et al.  The assessment of parenting using the Parental Bonding Instrument: two or three factors? , 1997, Psychological Medicine.

[36]  M. First,et al.  Structured clinical interview for DSM-IV axis II personality disorders : SCID-II , 1997 .

[37]  J T O'Brien,et al.  Clinical and Magnetic Resonance Imaging Correlates of Hypothalamic–Pituitary–Adrenal Axis Function in Depression and Alzheimer's Disease , 1996, British Journal of Psychiatry.

[38]  F. Holsboer,et al.  Altered hypothalamic-pituitary-adrenocortical regulation in healthy subjects at high familial risk for affective disorders. , 1995, Neuroendocrinology.

[39]  G. Migliorati,et al.  Neuroendocrine correlates of the aging brain in humans. , 1995, Neuroendocrinology.

[40]  E. Seifritz,et al.  Hypothalamic-pituitary-adrenal system function in patients with alzheimer's disease , 1995, Neurobiology of Aging.

[41]  S. Shelton,et al.  Neurotoxicity of Glucocorticoids in the Primate Brain , 1994, Hormones and Behavior.

[42]  I. Heuser,et al.  The combined dexamethasone/CRH test: a refined laboratory test for psychiatric disorders. , 1994, Journal of psychiatric research.

[43]  J. Schulkin,et al.  Corticosterone effects on corticotropin-releasing hormone mRNA in the central nucleus of the amygdala and the parvocellular region of the paraventricular nucleus of the hypothalamus , 1994, Brain Research.

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

[45]  J W Mason,et al.  Enhanced suppression of cortisol following dexamethasone administration in posttraumatic stress disorder. , 1993, The American journal of psychiatry.

[46]  D. Leibfritz,et al.  Multinuclear NMR studies on the energy metabolism of glial and neuronal cells. , 1993, Developmental neuroscience.

[47]  D. Hadzi-Pavlovic,et al.  Parental representations of melancholic and non-melancholic depressives: examining for specificity to depressive type and for evidence of additive effects , 1992, Psychological Medicine.

[48]  S. Southwick,et al.  Lymphocyte glucocorticoid receptor number in posttraumatic stress disorder. , 1991, The American journal of psychiatry.

[49]  S. Gullans,et al.  Characterization of the major brain osmolytes that accumulate in salt-loaded rats. , 1989, The American journal of physiology.

[50]  R. Hauger,et al.  Corticotropin-releasing factor receptors and pituitary adrenal responses during immobilization stress. , 1988, Endocrinology.

[51]  R. C. Oldfield.  The assessment and analysis of handedness: the Edinburgh inventory. , 1971, Neuropsychologia.

[52]  W. Zung.  A SELF-RATING DEPRESSION SCALE. , 1965, Archives of general psychiatry.

[53]  August B. Hollingshead,et al.  Two Factor Index of Social Position , 1957 .