Regional cerebral blood flow correlates with heart period and high-frequency heart period variability during working-memory tasks: Implications for the cortical and subcortical regulation of cardiac autonomic activity.

The aim of the present study was to characterize the functional relationships between behaviorally evoked regional brain activation and cardiac autonomic activity in humans. Concurrent estimates of regional cerebral blood flow (rCBF; obtained by positron emission tomography), heart period, and high-frequency heart period variability (HF-HPV; an indicator of cardiac parasympathetic activity) were examined in 93 adults (aged 50-70 years) who performed a series of increasingly difficult working-memory tasks. Increased task difficulty resulted in decreased heart period (indicating cardioacceleration) and decreased HF-HPV (indicating decreased cardiac parasympathetic activity). Task-induced decreases in heart period and HF-HPV were associated with concurrent increases and decreases in rCBF to cortical and subcortical brain regions that are speculated to regulate cardiac autonomic activity during behavioral processes: the medial-prefrontal, insular, and anterior cingulate cortices, the amygdala-hippocampal complex, and the cerebellum. These findings replicate and extend a small number of functional neuroimaging studies that suggest an important role for both cortical and subcortical brain systems in human cardiac autonomic regulation.

[1]  N. Alpert,et al.  Strategy for the Measurement of Regional Cerebral Blood Flow Using Short-Lived Tracers and Emission Tomography , 1984, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[2]  J. Strackee,et al.  Comparing Spectra of a Series of Point Events Particularly for Heart Rate Variability Data , 1984, IEEE Transactions on Biomedical Engineering.

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

[4]  P. Grossman,et al.  Cardiac autonomic mechanisms associated with borderline hypertension under varying behavioral demands: evidence for attenuated parasympathetic tone but not for enhanced beta-adrenergic activity. , 2007 .

[5]  M. W. van der Molen,et al.  A nonstationarity test for the spectral analysis of physiological time series with an application to respiratory sinus arrhythmia. , 1992, Psychophysiology.

[6]  Alan C. Evans,et al.  A Three-Dimensional Statistical Analysis for CBF Activation Studies in Human Brain , 1992, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[7]  P. Grossman.  Breathing rhythms of the heart in a world of no steady state: a comment on Weber, Molenaar, and van der Molen. , 1992, Psychophysiology.

[8]  J. Mazziotta,et al.  Rapid Automated Algorithm for Aligning and Reslicing PET Images , 1992, Journal of computer assisted tomography.

[9]  J. Girvin,et al.  Cardiovascular effects of human insular cortex stimulation , 1992, Neurology.

[10]  D. Powell,et al.  Cingulothalamic and Prefrontal Control of Autonomic Function , 1993 .

[11]  G. K. Røste,et al.  Hypothalamocerebellar and cerebellohypothalamic projections--circuits for regulating nonsomatic cerebellar activity? , 1994, Histology and histopathology.

[12]  N Birbaumer,et al.  Central effects of baroreceptor activation in humans: attenuation of skeletal reflexes and pain perception. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[13]  Bert N. Uchino,et al.  Autonomic cardiac control. III. Psychological stress and cardiac response in autonomic space as revealed by pharmacological blockades. , 1994, Psychophysiology.

[14]  H. Rüddel,et al.  Reduced parasympathetic cardiac control in patients with hypertension at rest and under mental stress. , 1994, American heart journal.

[15]  D. Cechetto,et al.  Identification of a cortical site for stress-induced cardiovascular dysfunction , 1994, Integrative physiological and behavioral science : the official journal of the Pavlovian Society.

[16]  J. Cacioppo,et al.  Individual differences in the autonomic origins of heart rate reactivity: the psychometrics of respiratory sinus arrhythmia and preejection period. , 1994, Psychophysiology.

[17]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .

[18]  S. Porges.  Orienting in a defensive world: mammalian modifications of our evolutionary heritage. A Polyvagal Theory. , 1995, Psychophysiology.

[19]  Scott T. Grafton,et al.  Vagus nerve stimulation activates central nervous system structures in epileptic patients during PET H2(15)O blood flow imaging. , 1996, Neurosurgery.

[20]  J. Jonides,et al.  Dissociating verbal and spatial working memory using PET. , 1996, Cerebral cortex.

[21]  Eraldo Paulesu,et al.  Silent Ischemia as a Central Problem: Regional Brain Activation Compared in Silent and Painful Myocardial Ischemia , 1996, Annals of Internal Medicine.

[22]  H. Nagaraja,et al.  Heart rate variability: origins, methods, and interpretive caveats. , 1997, Psychophysiology.

[23]  P. Goldman-Rakic,et al.  Cerebral cortical hyperactivation in response to mental stress in patients with coronary artery disease. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[24]  A. Verberne,et al.  Cortical Modulation of theCardiovascular System , 1998, Progress in Neurobiology.

[25]  Martin Sarter,et al.  Anxiety and cardiovascular reactivity: the basal forebrain cholinergic link , 1998, Behavioural Brain Research.

[26]  A. Oto,et al.  Effects of stroke localization on cardiac autonomic balance and sudden death. , 1999, Stroke.

[27]  P A Shapiro,et al.  Cerebral activation, hostility, and cardiovascular control during mental stress. , 2000, Journal of psychosomatic research.

[28]  H. Critchley,et al.  Cerebral correlates of autonomic cardiovascular arousal: a functional neuroimaging investigation in humans , 2000, The Journal of physiology.

[29]  H. Groenewegen,et al.  The prefrontal cortex and the integration of sensory, limbic and autonomic information. , 2000, Progress in brain research.

[30]  N. Schneiderman,et al.  Afferents to the central nucleus of the amygdala and functional subdivisions of the periaqueductal gray: neuroanatomical substrates for affective behavior , 2000, Brain Research.

[31]  Joseph E LeDoux.  Emotion Circuits in the Brain , 2000 .

[32]  R. Lane,et al.  A model of neurovisceral integration in emotion regulation and dysregulation. , 2000, Journal of affective disorders.

[33]  M. Weinand,et al.  Heart Rate and Heart Rate Variability Changes in the Intracarotid Sodium Amobarbital Test , 2001, Epilepsia.

[34]  Julian F. Thayer,et al.  21. Activity in medial prefrontal cortex correlates with vagal component of heart rate variability during emotion , 2001 .

[35]  R. Watts,et al.  Cerebral Activation during Vagus Nerve Stimulation: A Functional MR Study , 2002, Epilepsia.

[36]  H. Diener,et al.  Fear conditioned changes of heart rate in patients with medial cerebellar lesions , 2002, Journal of neurology, neurosurgery, and psychiatry.

[37]  W. Lovallo,et al.  Psychophysiological Reactivity: Mechanisms and Pathways to Cardiovascular Disease , 2003, Psychosomatic medicine.

[38]  Patrizia Baraldi,et al.  Functional activity mapping of the mesial hemispheric wall during anticipation of pain , 2003, NeuroImage.

[39]  J. Jennings,et al.  Autoregulation of Blood Pressure and Thought: Preliminary Results of an Application of Brain Imaging to Psychosomatic Medicine , 2003, Psychosomatic medicine.