Physiological changes in sleep that affect fMRI inference

fMRI relies on a localized cerebral blood flow (CBF) response to changes in cortical neuronal activity. An underappreciated aspect however is its sensitivity to contributions from autonomic physiology that may affect CBF through changes in vascular resistance and blood pressure. As is reviewed here, this is crucial to consider in fMRI studies of sleep, given the close linkage between the regulation of arousal state and autonomic physiology. Typical methods for separating these effects are based on the use of reference signals that may include physiological parameters such as heart rate and respiration; however, the use of time-invariant models may not be adequate due to the possibly changing relationship between reference and fMRI signals with arousal state. In addition, recent research indicates that additional physiological reference signals may be needed to accurately describe changes in systemic physiology, including sympathetic indicators such as finger skin vascular tone and blood pressure.

[1]  W. Talman,et al.  Parasympathetic tonic dilatory influences on cerebral vessels , 2009, Autonomic Neuroscience.

[2]  J. Waters,et al.  Neuromodulatory Correlates of Pupil Dilation , 2018, Front. Neural Circuits.

[3]  Ines Blockx,et al.  Cholinergic and serotonergic modulations differentially affect large-scale functional networks in the mouse brain , 2016, Brain Structure and Function.

[4]  V. Arango,et al.  Effect of chemical stimulation of the dorsal raphe nucleus on cerebral blood flow in rat , 1995, Neuroscience Letters.

[5]  M. Marcus,et al.  Effects of sympathetic nerves on cerebral vessels in dog, cat, and monkey. , 1978, The American journal of physiology.

[6]  Rafael Malach,et al.  Coupling between pupil fluctuations and resting-state fMRI uncovers a slow build-up of antagonistic responses in the human cortex , 2015, NeuroImage.

[7]  Philip N. Ainslie,et al.  Sympathetic control of the brain circulation: Appreciating the complexities to better understand the controversy , 2017, Autonomic Neuroscience.

[8]  G. E. Meadows,et al.  Hypercapnic cerebral vascular reactivity is decreased, in humans, during sleep compared with wakefulness. , 2003, Journal of applied physiology.

[9]  J. Klingelhöfer.  Cerebral blood flow velocity in sleep , 2012 .

[10]  Laura Leuchs,et al.  Spontaneous pupil dilations during the resting state are associated with activation of the salience network , 2016, NeuroImage.

[11]  Jeff H. Duyn,et al.  Contribution of systemic vascular effects to fMRI activity in white matter , 2018, NeuroImage.

[12]  Brian E. Russ,et al.  The Basal Forebrain Regulates Global Resting-State fMRI Fluctuations , 2018, Neuron.

[13]  César Caballero-Gaudes,et al.  Methods for cleaning the BOLD fMRI signal , 2016, NeuroImage.

[14]  Lino Nobili,et al.  Heart rate variability in normal and pathological sleep , 2013, Front. Physiol..

[15]  A. Braun,et al.  Decoupling of the brain's default mode network during deep sleep , 2009, Proceedings of the National Academy of Sciences.

[16]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[17]  P. Sándor,et al.  Nervous control of the cerebrovascular system: doubts and facts , 1999, Neurochemistry International.

[18]  M. Bonnet,et al.  Heart rate variability: sleep stage, time of night, and arousal influences. , 1997, Electroencephalography and clinical neurophysiology.

[19]  C. Saper,et al.  Hypothalamic regulation of sleep and circadian rhythms , 2005, Nature.

[20]  Stephen M. Smith,et al.  Using temporal ICA to selectively remove global noise while preserving global signal in functional MRI data , 2017, NeuroImage.

[21]  E. Sforza,et al.  Long-term effects of treatment with nasal continuous positive airway pressure on daytime lung function and pulmonary hemodynamics in patients with obstructive sleep apnea. , 1990, The American review of respiratory disease.

[22]  Ian M Colrain,et al.  The K-complex: a 7-decade history. , 2005, Sleep.

[23]  Michael A. Cohen,et al.  Sympathetic Control of the Cerebral Vasculature in Humans , 2010, Stroke.

[24]  D. Cechetto,et al.  Cortical control of the autonomic nervous system , 2014, Experimental physiology.

[25]  Kevin Murphy,et al.  fMRI in the presence of task-correlated breathing variations , 2009, NeuroImage.

[26]  T. Moreira,et al.  New advances in the neural control of breathing , 2015, The Journal of physiology.

[27]  B. Jones.  Arousal and sleep circuits , 2019, Neuropsychopharmacology.

[28]  Vivek Jain,et al.  Respiratory rate variability in sleeping adults without obstructive sleep apnea , 2016, Physiological reports.

[29]  J. Shaw,et al.  The form voltage distribution and physiological significance of the K-complex. , 1956, Electroencephalography and clinical neurophysiology.

[30]  Juan Zhou,et al.  Spontaneous eyelid closures link vigilance fluctuation with fMRI dynamic connectivity states , 2016, Proceedings of the National Academy of Sciences.

[31]  R. Dampney.  Central neural control of the cardiovascular system: current perspectives. , 2016, Advances in physiology education.

[32]  D. Picchioni,et al.  Sympathetic activity contributes to the fMRI signal , 2019, Communications Biology.

[33]  K. Shelley.  Photoplethysmography: Beyond the Calculation of Arterial Oxygen Saturation and Heart Rate , 2007, Anesthesia and analgesia.

[34]  E. Hamel.  Perivascular nerves and the regulation of cerebrovascular tone. , 2006, Journal of applied physiology.

[35]  S. Foote,et al.  Development of the noradrenergic, serotonergic, and dopaminergic innervation of neocortex. , 1987, Current topics in developmental biology.

[36]  E. Benarroch.  Control of the cardiovascular and respiratory systems during sleep , 2019, Autonomic Neuroscience.

[37]  M. Schölvinck,et al.  Tracking brain arousal fluctuations with fMRI , 2016, Proceedings of the National Academy of Sciences.

[38]  J. Skatrud,et al.  Cerebrovascular response to arousal from NREM and REM sleep. , 2008, Sleep.

[39]  Jeff H. Duyn,et al.  Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal , 2007, NeuroImage.

[40]  C. Iadecola.  The Neurovascular Unit Coming of Age: A Journey through Neurovascular Coupling in Health and Disease , 2017, Neuron.

[41]  M. P. van den Heuvel,et al.  Exploring the brain network: a review on resting-state fMRI functional connectivity. , 2010, European neuropsychopharmacology : the journal of the European College of Neuropsychopharmacology.

[42]  B. Levine,et al.  Autonomic Neural Control of Dynamic Cerebral Autoregulation in Humans , 2002, Circulation.

[43]  Helmut Laufs,et al.  Where the BOLD signal goes when alpha EEG leaves , 2006, NeuroImage.

[44]  H. L. Stone,et al.  The Role of the Peripheral Sympathetic Nervous System in Cerebral Blood Flow Autoregulation , 1975, Stroke.

[45]  G. Pampiglione,et al.  The effects of repeated stimuli upon EEG and vasomotor activity during sleep in man. , 1958, Brain : a journal of neurology.

[46]  Manuel Schabus,et al.  Spontaneous neural activity during human slow wave sleep , 2008, Proceedings of the National Academy of Sciences.

[47]  Helmut Laufs,et al.  To wake or not to wake? The two-sided nature of the human K-complex , 2012, NeuroImage.

[48]  D Kurtz,et al.  Breathing during sleep in normal middle-aged subjects. , 1990, Sleep.

[49]  R. Dampney,et al.  Bidirectional interactions between the baroreceptor reflex and arousal: an update. , 2015, Sleep medicine.

[50]  John R. Huguenard,et al.  Breathing control center neurons that promote arousal in mice , 2017, Science.

[51]  W. Talman,et al.  Parasympathetic stimulation elicits cerebral vasodilatation in rat , 2007, Autonomic Neuroscience.

[52]  Catie Chang,et al.  Relationship between respiration, end-tidal CO2, and BOLD signals in resting-state fMRI , 2009, NeuroImage.

[53]  D. Velis,et al.  Correction for pulse height variability reduces physiological noise in functional MRI when studying spontaneous brain activity , 2009, Human brain mapping.

[54]  M. Schölvinck,et al.  Neural basis of global resting-state fMRI activity , 2010, Proceedings of the National Academy of Sciences.

[55]  Thoralf M. Sundt,et al.  The effect of carbon dioxide on the diameter of brain capillaries , 1990, Brain Research.

[56]  N. Kleitman,et al.  Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. , 1953, Science.

[57]  P. Bandettini,et al.  The effect of respiration variations on independent component analysis results of resting state functional connectivity , 2008, Human brain mapping.

[58]  H. Hotta.  Neurogenic control of parenchymal arterioles in the cerebral cortex. , 2016, Progress in brain research.

[59]  L. Johnson,et al.  The orienting reflex during waking and sleeping. , 1967, Electroencephalography and clinical neurophysiology.

[60]  E. Benarroch.  Brainstem integration of arousal, sleep, cardiovascular, and respiratory control , 2018, Neurology.

[61]  Han Yuan,et al.  Correlated slow fluctuations in respiration, EEG, and BOLD fMRI , 2013, NeuroImage.

[62]  Thomas T. Liu,et al.  Noise contributions to the fMRI signal: An overview , 2016, NeuroImage.

[63]  P. Ainslie,et al.  Hypoxemia, oxygen content, and the regulation of cerebral blood flow. , 2016, American journal of physiology. Regulatory, integrative and comparative physiology.

[64]  Cheree James,et al.  Real-time imaging of cortical areas involved in the generation of increases in skin sympathetic nerve activity when viewing emotionally charged images , 2012, NeuroImage.

[65]  E. Poole.  Nervous Activity in Relation to the Respiratory Cycle , 1961, Nature.

[66]  P. Halász.  Arousals without awakening—Dynamic aspect of sleep , 1993, Physiology & Behavior.

[67]  K. Shivkumar,et al.  Cardiac autonomic control in health and disease , 2016, The Journal of physiology.

[68]  D. Bayliss,et al.  Neural Control of Breathing and CO2 Homeostasis , 2015, Neuron.

[69]  T. Similowski,et al.  REM sleep respiratory behaviours match mental content in narcoleptic lucid dreamers , 2018, Scientific Reports.

[70]  E. Hamel,et al.  Neuronal networks and mediators of cortical neurovascular coupling responses in normal and altered brain states , 2016, Philosophical Transactions of the Royal Society B: Biological Sciences.

[71]  G. Pampiglione,et al.  SOME RELATIONSHIPS BETWEEN PERIPHERAL VASOMOTOR AND E.E.G. CHANGES , 1957, Journal of neurology, neurosurgery, and psychiatry.

[72]  A. Absalom,et al.  Sympathetic regulation of cerebral blood flow in humans: a review. , 2013, British journal of anaesthesia.

[73]  Alessandro Silvani,et al.  Brain–heart interactions: physiology and clinical implications , 2016, Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences.

[74]  Yang Li,et al.  Cerebrovascular reactivity mapping without gas challenges , 2017, NeuroImage.

[75]  Jin Fan,et al.  Spontaneous Brain Activity Relates to Autonomic Arousal , 2012, The Journal of Neuroscience.

[76]  Jessica A. Cardin,et al.  Waking State: Rapid Variations Modulate Neural and Behavioral Responses , 2015, Neuron.

[77]  G. Kranz,et al.  Differential modulation of the default mode network via serotonin-1A receptors , 2012, Proceedings of the National Academy of Sciences.