Vulnerability to simple faints is predicted by regional differences in brain anatomy

Neurocardiogenic syncope (NCS, simple fainting) is a common and typically benign familial condition, which rarely may result in traumatic injury or hypoxic convulsions. NCS is associated with emotional triggers, anxiety states and stress. However, the etiology of NCS, as a psychophysiological process, is poorly understood. We therefore investigated the relationship between NCS and brain anatomy. We studied a non-clinical sample of eighteen individuals with histories characteristic of NCS, and nineteen matched controls who had never fainted. We recorded fainting frequency, resting heart rate variability measures and anxiety levels. Structural T1-weighted magnetic resonance images (MRI) were acquired at 1.5 T. Associations between brain morphometry (regional gray and white matter volumes) and NCS, resting physiology and anxiety were tested using voxel-based morphometry (VBM). Compared to controls, NCS participants had lower regional brain volume within medulla and midbrain (a priori regions of interest). Moreover, across NCS individuals, lower gray matter volume in contiguous regions of left caudate nucleus predicted enhanced parasympathetic cardiac tone, fainting frequency and anxiety levels. Our findings provide preliminary evidence for a hierarchical anatomical basis to NCS. First, differences in the volume of brainstem centers supporting cardiovascular homeostasis may relate to constitutional predisposition to NCS. Second, differences in the structural organization of the caudate nucleus in NCS individuals may relate to fainting frequency via interactions between emotional state and parasympathetic control of the heart. These observations highlight the application of VBM to the identification of neurovisceral mechanisms relevant to psychosomatic medicine and the neuroscience of emotion.

[1]  F. Golla The Central Nervous System , 1960, Nature.

[2]  Christine Baker,et al.  The role of psychological factors in response to treatment in neurocardiogenic (vasovagal) syncope. , 2006, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[3]  W. Kapoor,et al.  Guidelines on management (diagnosis and treatment) of syncope. , 2001, European heart journal.

[4]  G. Moody,et al.  Spectral characteristics of heart rate variability before and during postural tilt. Relations to aging and risk of syncope. , 1990, Circulation.

[5]  P. Thorén,et al.  Increased activity in left ventricular receptors during hemorrhage or occlusion of caval veins in the cat. A possible cause of the vaso-vagal reaction. , 1972, Acta physiologica Scandinavica.

[6]  Martin Skalej,et al.  Visualization and quantification of disease progression in multiple system atrophy , 2006, Movement disorders : official journal of the Movement Disorder Society.

[7]  Rose Anne Kenny,et al.  Guidelines on management (diagnosis and treatment) of syncope--update 2004. , 2004, Europace : European pacing, arrhythmias, and cardiac electrophysiology : journal of the working groups on cardiac pacing, arrhythmias, and cardiac cellular electrophysiology of the European Society of Cardiology.

[8]  Kazushi Deguchi,et al.  Frequency of family history in vasovagal syncope , 1998, The Lancet.

[9]  B. Grubb,et al.  Cerebral Vasoconstriction During Head‐Upright Tilt‐Induced Vasovagal Syncope: A Paradoxic and Unexpected Response , 1991, Circulation.

[10]  G. Piccirillo,et al.  Heart rate and blood pressure variability in subjects with vasovagal syncope. , 2004, Clinical science.

[11]  H Ikram,et al.  Autonomic control of vasovagal syncope. , 1998, The American journal of physiology.

[12]  David Araújo,et al.  Regional gray matter abnormalities in panic disorder: A voxel-based morphometry study , 2008, Psychiatry Research: Neuroimaging.

[13]  B. Grubb,et al.  Clinical practice. Neurocardiogenic syncope. , 2005, The New England journal of medicine.

[14]  R. Sutton,et al.  Proposed classification for tilt induced vasovagal syncope , 1992 .

[15]  A Steptoe,et al.  Emotional fainting and the psychophysiologic response to blood and injury: autonomic mechanisms and coping strategies. , 1988, Psychosomatic medicine.

[16]  A. Mark The Bezold-Jarisch reflex revisited: clinical implications of inhibitory reflexes originating in the heart. , 1983, Journal of the American College of Cardiology.

[17]  Karl J. Friston,et al.  A Voxel-Based Morphometric Study of Ageing in 465 Normal Adult Human Brains , 2001, NeuroImage.

[18]  Eugene V. Golanov,et al.  Neurons of nucleus of the solitary tract synchronize the EEG and elevate cerebral blood flow via a novel medullary area , 2001, Brain Research.

[19]  M. Giannelli,et al.  Brain structural damage in Friedreich’s ataxia , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[20]  D Lacroix,et al.  Inadequate sympathovagal balance in response to orthostatism in patients with unexplained syncope and a positive head up tilt test , 1999, Heart.

[21]  M Akhtar,et al.  Echocardiographic demonstration of decreased left ventricular dimensions and vigorous myocardial contraction during syncope induced by head-up tilt. , 1991, Journal of the American College of Cardiology.

[22]  J. Ashburner,et al.  Voxel-by-Voxel Comparison of Automatically Segmented Cerebral Gray Matter—A Rater-Independent Comparison of Structural MRI in Patients with Epilepsy , 1999, NeuroImage.

[23]  Sung-Cheng Huang,et al.  Cerebral metabolism in major depression and obsessive-compulsive disorder occurring separately and concurrently , 2001, Biological Psychiatry.

[24]  R. Bandler,et al.  Hypovolemic shock: Critical involvement of a projection from the ventrolateral periaqueductal gray to the caudal midline medulla , 2008, Neuroscience.

[25]  Kazushi Deguchi,et al.  Observations on recurrent syncope and presyncope in 641 patients , 2001, The Lancet.

[26]  Rose Anne Kenny,et al.  Guidelines on management (diagnosis and treatment) of syncope-update 2004. Executive Summary. , 2005, European heart journal.

[27]  Hugo D. Critchley,et al.  Following One's Heart: Cardiac Rhythms Gate Central Initiation of Sympathetic Reflexes , 2009, The Journal of Neuroscience.

[28]  R Furlan,et al.  Neurally mediated syncope: pathophysiology and implications for treatment. , 1999, The American journal of the medical sciences.

[29]  Michael A Yassa,et al.  A quantitative evaluation of cross-participant registration techniques for MRI studies of the medial temporal lobe , 2009, NeuroImage.

[30]  Lars-Göran Öst,et al.  Physiological responses in blood phobics. , 1984, Behaviour research and therapy.

[31]  Robert S Sheldon,et al.  Vasovagal syncope in medical students and their first-degree relatives. , 2006, European heart journal.

[32]  Julian F. Thayer,et al.  Autonomic characteristics of nonclinical panic and blood phobia , 1993, Biological Psychiatry.

[33]  Roger Hainsworth,et al.  Pathophysiology of syncope , 2004, Clinical Autonomic Research.

[34]  Paul M. Pilowsky,et al.  Retrograde projections to a discrete apneic site in the midline medulla oblongata of the rat , 2008, Brain Research.

[35]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

[36]  R Furlan,et al.  Sympathetic and baroreceptor reflex function in neurally mediated syncope evoked by tilt. , 1997, The Journal of clinical investigation.

[37]  R Bandler,et al.  Caudal midline medulla mediates behaviourally-coupled but not baroreceptor-mediated vasodepression , 2000, Neuroscience.

[38]  P. Vardas,et al.  Spectral analysis of heart rate variability during tilt-table testing in patients with vasovagal syncope. , 1998, International journal of cardiology.

[39]  Dominique Lacroix,et al.  Prevalence and prognostic significance of psychiatric disorders in patients evaluated for recurrent unexplained syncope. , 2002, The American journal of cardiology.

[40]  D L Eckberg,et al.  Vagal and sympathetic mechanisms in patients with orthostatic vasovagal syncope. , 1997, Circulation.

[41]  P. Vardas,et al.  Autonomic Nervous System Activity During Tilt Testing in Syncopal Patients, Estimated by Power Spectral Analysis of Heart Rate Variability , 1997, Pacing and clinical electrophysiology : PACE.

[42]  M. Nakai,et al.  Effects of microinjection of N-methyl-D-aspartic acid into the nucleus tractus solitarii on cerebral blood flow in anesthetized rats. , 1994, Journal of the autonomic nervous system.

[43]  R. Bandler,et al.  Haemodynamic response to haemorrhage: distinct contributions of midbrain and forebrain structures , 2003, Autonomic Neuroscience.

[44]  J. Rapoport,et al.  Cerebral glucose metabolism in childhood-onset obsessive-compulsive disorder. , 1989, Archives of general psychiatry.

[45]  G O Barnett,et al.  Patients with syncope admitted to medical intensive care units. , 1982, JAMA.

[46]  Christian Lovis,et al.  Prospective evaluation of patients with syncope: a population-based study. , 2001, The American journal of medicine.

[47]  R Bandler,et al.  Haemorrhage-evoked compensation and decompensation are mediated by distinct caudal midline medullary regions in the urethane-anaesthetised rat , 2002, Neuroscience.

[48]  Douglas L. Jones,et al.  Time and frequency domain analyses of heart rate variability during orthostatic stress in patients with neurally mediated syncope. , 1994, The American journal of cardiology.

[49]  J Ludbrook,et al.  Hemodynamic and neurohumoral responses to acute hypovolemia in conscious mammals. , 1991, The American journal of physiology.

[50]  Karsten Specht,et al.  Voxel-based morphometry and voxel-based relaxometry in multiple system atrophy—A comparison between clinical subtypes and correlations with clinical parameters , 2007, NeuroImage.

[51]  A. Ginestroni,et al.  Brain structural damage in spinocerebellar ataxia type 1 , 2008, Journal of Neurology.

[52]  S. Su,et al.  Excessive myocardial contraction in vasovagal syncope demonstrated by echocardiography during head‐up tilt test , 1996, Clinical cardiology.

[53]  A. Canavan,et al.  Associative learning in degenerative neostriatal disorders: Contrasts in explicit and implicit remembering between Parkinson's and huntington's diseases , 1995, Movement disorders : official journal of the Movement Disorder Society.

[54]  R. Rubin,et al.  Regional xenon 133 cerebral blood flow and cerebral technetium 99m HMPAO uptake in unmedicated patients with obsessive-compulsive disorder and matched normal control subjects. Determination by high-resolution single-photon emission computed tomography. , 1992, Archives of general psychiatry.

[55]  C. Morillo,et al.  Neural Monitoring of Vasovagal Syncope , 1997, Pacing and clinical electrophysiology : PACE.

[56]  S Cerutti,et al.  Cardiac autonomic patterns preceding occasional vasovagal reactions in healthy humans. , 1998, Circulation.

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

[58]  Marie Chupin,et al.  Can voxel based morphometry, manual segmentation and automated segmentation equally detect hippocampal volume differences in acute depression? , 2009, NeuroImage.

[59]  John Ashburner,et al.  A fast diffeomorphic image registration algorithm , 2007, NeuroImage.

[60]  W R Millington,et al.  Evidence that hemorrhagic hypotension is mediated by the ventrolateral periaqueductal gray region. , 2001, American journal of physiology. Regulatory, integrative and comparative physiology.

[61]  Richard Tressider The Surgical aid Society and its Methods , 1899 .

[62]  W. Quan,et al.  An Association Between Anxiety and Neurocardiogenic Syncope During Head‐Up Tilt Table Testing , 2000, Pacing and clinical electrophysiology : PACE.

[63]  P Pietrini,et al.  Cerebral glucose metabolism in childhood-onset obsessive-compulsive disorder. Revisualization during pharmacotherapy. , 1992, Archives of general psychiatry.

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

[65]  Pietro Cortelli,et al.  Arousal elicits exaggerated inhibition of sympathetic nerve activity in phobic syncope patients. , 2007, Brain : a journal of neurology.

[66]  M Ashtari,et al.  Reduced caudate nucleus volume in obsessive-compulsive disorder. , 1995, Archives of general psychiatry.