Altered tonic and phasic cortisol secretion following unilateral stroke

Evidence is accumulating that cerebral laterality appears to be an important feature in the regulation of the stress response with the right hemisphere being closely linked to stress-regulatory systems, including the hypothalamic-pituitary-adrenal (HPA) axis. Although some animal and human data support this hypothesis, studies on brain damaged patients yet failed to substantiate laterality effects on cortisol secretion. The aim of this study was to examine whether unilateral stroke differentially affects tonic and phasic response characteristics of the HPA axis, and to evaluate the impact of intrahemispheric lesion location. Basal morning cortisol levels and phasic responses towards a mentally challenging task were examined in 32 stroke patients with left-sided (LH; n=18) or right-sided (RH; n=14) infarctions and 30 healthy controls matched for age and gender. Only LH, but not RH patients displayed increased morning cortisol levels when compared to controls. In contrast, phasic reactions were blunted in the combined patient group with RH patients showing the most distinct decline. More anterior located lesions were associated with reduced phasic, but not tonic cortisol measures. This relationship appeared to be particularly pronounced in RH patients. Results support the conclusion that the central regulation of cortisol secretion is under excitatory control of the right hemisphere and can be interpreted within a framework of asymmetrical regulation of the stress response. Left- and right-sided strokes may differentially affect response patterns of the HPA axis, a stress-regulatory system that is associated with effective protection against disease and external challenges.

[1]  M. Hennerici,et al.  Pattern of Activation of the Hypothalamic‐Pituitary‐Adrenal Axis in Acute Stroke: Relation to Acute Confusional State, Extent of Brain Damage, and Clinical Outcome , 1994, Stroke.

[2]  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.

[3]  N. Kalin,et al.  Emotion, plasticity, context, and regulation: perspectives from affective neuroscience. , 2000, Psychological bulletin.

[4]  M. Kaste,et al.  Magnetic resonance imaging correlates of depression after ischemic stroke. , 2001, Archives of general psychiatry.

[5]  R. Robinson,et al.  Mood disorders in stroke patients. Importance of location of lesion. , 1984, Brain : a journal of neurology.

[6]  L. Squire,et al.  Inhibition of glucocorticoid secretion by the hippocampal formation in the primate , 1991, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  R. Sullivan,et al.  Lateralized Effects of Medial Prefrontal Cortex Lesions on Neuroendocrine and Autonomic Stress Responses in Rats , 1999, The Journal of Neuroscience.

[8]  E. Neafsey,et al.  Prefrontal cortical control of the autonomic nervous system: anatomical and physiological observations. , 1990, Progress in brain research.

[9]  Werner Wittling,et al.  Neuroendocrine hemisphere asymmetries: Salivary cortisol secretion during lateralized viewing of emotion-related and neutral films , 1990, Brain and Cognition.

[10]  D. Hellhammer,et al.  Advanced Methods in Psychobiology , 1987 .

[11]  R. Davidson,et al.  The functional neuroanatomy of emotion and affective style , 1999, Trends in Cognitive Sciences.

[12]  M. Schwarz,et al.  Die Apathy Evaluation Scale: Erste Ergebnisse zu den psychometrischen Eigenschaften einer deutschsprachigen Übersetzung der Skala , 2006 .

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

[14]  J. Doppman,et al.  Inferior petrosal sinus sampling in healthy subjects reveals a unilateral corticotropin-releasing hormone-induced arginine vasopressin release associated with ipsilateral adrenocorticotropin secretion. , 1996, The Journal of clinical investigation.

[15]  Ned H Kalin,et al.  Cerebrospinal fluid corticotropin-releasing hormone levels are elevated in monkeys with patterns of brain activity associated with fearful temperament , 2000, Biological Psychiatry.

[16]  T. Olsson,et al.  Low and high circulating cortisol levels predict mortality and cognitive dysfunction early after stroke , 2004, Journal of internal medicine.

[17]  Michael Sharpe,et al.  Depression after stroke and lesion location: a systematic review , 2000, The Lancet.

[18]  R. Sullivan,et al.  Prefrontal cortical regulation of hypothalamic–pituitary–adrenal function in the rat and implications for psychopathology: side matters , 2002, Psychoneuroendocrinology.

[19]  C. Granger,et al.  The functional independence measure: a new tool for rehabilitation. , 1987, Advances in clinical rehabilitation.

[20]  A. Damasio,et al.  Lesion analysis in neuropsychology , 1989 .

[21]  N. Herrmann,et al.  The Importance of Lesion Location in Poststroke Depression: A Critical Review , 1998, Canadian journal of psychiatry. Revue canadienne de psychiatrie.

[22]  G. Gainotti.  Emotional behavior and hemispheric side of the lesion. , 1972, Cortex; a journal devoted to the study of the nervous system and behavior.

[23]  Huikuri Heikki,et al.  Neurohormonal activation in ischemic stroke: effects of acute phase disturbances on long-term mortality. , 2007, Current neurovascular research.

[24]  S. Schwab,et al.  Neuroendocrine changes in patients with acute space occupying ischaemic stroke , 2003, Journal of neurology, neurosurgery, and psychiatry.

[25]  S. Shelton,et al.  Asymmetric frontal brain activity, cortisol, and behavior associated with fearful temperament in rhesus monkeys. , 1998, Behavioral neuroscience.

[26]  M. Schwarz,et al.  [Psychometric properties of a German version of the Apathy Evaluation Scale]. , 2006, Fortschritte der Neurologie-Psychiatrie.

[27]  R. Joynt,et al.  Prognostic value of the stress response following stroke. , 1977, JAMA.

[28]  A. Craig.  Forebrain emotional asymmetry: a neuroanatomical basis? , 2005, Trends in Cognitive Sciences.

[29]  R G Robinson,et al.  Comparison of cortical and subcortical lesions in the production of poststroke mood disorders. , 1987, Brain : a journal of neurology.

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

[31]  R. Fogelholm,et al.  Serum cortisol and outcome of ischemic brain infarction , 1993, Journal of the Neurological Sciences.

[32]  C. Kirschbaum,et al.  Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change , 2003, Psychoneuroendocrinology.

[33]  J. Stroop.  Studies of interference in serial verbal reactions. , 1992 .

[34]  R. Robinson,et al.  Mood changes in stroke patients: relationship to lesion location. , 1983, Comprehensive psychiatry.

[35]  Y. Gustafson,et al.  Abnormalities at Different Levels of the Hypothalamic‐Pituitary‐Adrenocortical Axis Early After Stroke , 1992, Stroke.

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

[37]  J. Price,et al.  The organization of networks within the orbital and medial prefrontal cortex of rats, monkeys and humans. , 2000, Cerebral cortex.

[38]  Dr.T. Olsson.  Urinary free Cortisol excretion shortly after ischaemic stroke , 1990, Journal of internal medicine.

[39]  Johannes Hewig,et al.  Associations of the cortisol awakening response (CAR) with cortical activation asymmetry during the course of an exam stress period , 2008, Psychoneuroendocrinology.

[40]  C. Kirschbaum,et al.  Synthesis of a cortisol-biotin conjugate and evaluation as a tracer in an immunoassay for salivary cortisol measurement , 1992, The Journal of Steroid Biochemistry and Molecular Biology.

[41]  N. Holbrook,et al.  Physiological functions of glucocorticoids in stress and their relation to pharmacological actions. , 1984, Endocrine reviews.

[42]  Right frontal brain activity, cortisol, and withdrawal behavior in 6-month-old infants. , 2003, Behavioral neuroscience.

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

[44]  T. Olsson,et al.  Hypercortisolism revealed by the dexamethasone suppression test in patients [corrected] with acute ischemic stroke. , 1989, Stroke.

[45]  Sonia J. Lupien,et al.  Impact of a unilateral brain lesion on cortisol secretion and emotional state: anterior/posterior dissociation in humans , 2003, Psychoneuroendocrinology.