Parasympathetic arousal-related cortical activity is associated with attention during cognitive task performance

Parasympathetic arousal is associated with states of heightened attention and well-being. Arousal may affect widespread cortical and subcortical systems across the brain, however, little is known about its influence on cognitive task processing and performance. In the current study, healthy adult participants (n = 20) underwent multi-band echo-planar imaging (TR = 0.72 s) with simultaneous pulse oximetry recordings during performance of the Multi Source Interference Task (MSIT), the Oddball Task (OBT), and during rest. Processing speed on both tasks was robustly related to heart rate (HR). Participants with slower HR responded faster on both the MSIT (33% variance explained) and the OBT (25% variance explained). Within all participants, trial-to-trial fluctuations in processing speed were robustly related to the heartbeat-stimulus interval, a metric that is dependent both on the concurrent HR and the stimulus timing with respect to the heartbeat. Models examining the cardiac-BOLD response revealed that a distributed set of regions showed arousal-related activity that was distinct for different task conditions. Across these cortical regions, activity increased with slower HR. Arousal-related activity was distinct from task-evoked activity and it was robust to the inclusion of additional physiological nuisance regressors into the models. For the MSIT, such arousal-related activity occurred across visual and dorsal attention network regions. For the OBT, this activity occurred within fronto-parietal regions. For rest, arousal-related activity also occurred, but was confined to visual regions. The pulvinar nucleus of the thalamus showed arousal-related activity during all three task conditions. Widespread cortical activity, associated with increased parasympathetic arousal, may be propagated by thalamic circuits and contributes to improved attention. This activity is distinct from task-evoked activity, but affects cognitive performance and therefore should be incorporated into neurobiological models of cognition and clinical disorders.

[1]  B. Gulyás,et al.  Activation by Attention of the Human Reticular Formation and Thalamic Intralaminar Nuclei , 1996, Science.

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

[3]  Jérôme Prado,et al.  Spatial attention influences trial-by-trial relationships between response time and functional connectivity in the visual cortex , 2011, NeuroImage.

[4]  Giulio Tononi,et al.  Reduced sleep spindle activity point to a TRN-MD thalamus-PFC circuit dysfunction in schizophrenia , 2017, Schizophrenia Research.

[5]  C. Sandman,et al.  Augmentation of the auditory event related potentials of the brain during diastole. , 1984, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[6]  G. Tononi,et al.  The thalamic reticular nucleus and schizophrenia. , 2011, Schizophrenia bulletin.

[7]  Hans-Jochen Heinze,et al.  Association between heart rate variability and fluctuations in resting-state functional connectivity , 2013, NeuroImage.

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

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

[10]  D. Kimmerly,et al.  Control of Autonomic Function : Insights from Neurophysiological Studies in Conscious Animals ( Including Humans ) Association between resting-state brain functional connectivity and muscle sympathetic burst incidence , 2016 .

[11]  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.

[12]  J. Birren,et al.  Reaction Time as a Function of the Cardiac Cycle in Young Adults , 1963, Science.

[13]  J. Pekar,et al.  Decoupling of reaction time-related default mode network activity with cognitive demand , 2017, Brain Imaging and Behavior.

[14]  M. Pinsk,et al.  The Anatomical and Functional Organization of the Human Visual Pulvinar , 2015, The Journal of Neuroscience.

[15]  J. Shoemaker,et al.  Forebrain organization for autonomic cardiovascular control , 2015, Autonomic Neuroscience.

[16]  Timothy O. Laumann,et al.  Evaluation of Denoising Strategies to Address Motion-Correlated Artifacts in Resting-State Functional Magnetic Resonance Imaging Data from the Human Connectome Project , 2016, Brain Connect..

[17]  S. Jang,et al.  The ascending reticular activating system from pontine reticular formation to the hypothalamus in the human brain: A diffusion tensor imaging study , 2015, Neuroscience Letters.

[18]  B. Cohen,et al.  Eye movements induced by stimulation of the pontine reticular formation: evidence for integration in oculomotor pathways. , 1972, Experimental neurology.

[19]  M. Chee,et al.  Lapsing during Sleep Deprivation Is Associated with Distributed Changes in Brain Activation , 2008, The Journal of Neuroscience.

[20]  Catie Chang,et al.  Template-based prediction of vigilance fluctuations in resting-state fMRI , 2017, NeuroImage.

[21]  F. Crick.  Function of the thalamic reticular complex: the searchlight hypothesis. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[22]  V. Napadow,et al.  The Autonomic Brain: An Activation Likelihood Estimation Meta-Analysis for Central Processing of Autonomic Function , 2013, The Journal of Neuroscience.

[23]  Robert Desimone,et al.  Pulvinar-Cortex Interactions in Vision and Attention , 2016, Neuron.

[24]  B. Pappas,et al.  Cardiac Cycle Phase and Movement and Reaction Times , 1976, Perceptual and motor skills.

[25]  Christian Frings,et al.  Cardiac cycle time effects on selection efficiency in vision. , 2016, Psychophysiology.

[26]  Philip A. Kragel,et al.  Deconstructing arousal into wakeful, autonomic and affective varieties , 2018, Neuroscience Letters.

[27]  Katrin Amunts,et al.  Stereotaxic probabilistic maps of the magnocellular cell groups in human basal forebrain , 2008, NeuroImage.

[28]  Andrew H. Song,et al.  Pharmacological Modulation of Noradrenergic Arousal Circuitry Disrupts Functional Connectivity of the Locus Ceruleus in Humans , 2017, The Journal of Neuroscience.

[29]  David L. Sparks,et al.  Coordination of eye and head components of movements evoked by stimulation of the paramedian pontine reticular formation , 2008, Experimental Brain Research.

[30]  S. Jang,et al.  The direct pathway from the brainstem reticular formation to the cerebral cortex in the ascending reticular activating system: A diffusion tensor imaging study , 2015, Neuroscience Letters.

[31]  M. Schölvinck,et al.  Subcortical evidence for a contribution of arousal to fMRI studies of brain activity , 2018, Nature Communications.

[32]  S. Porges.  Cardiac vagal tone: A physiological index of stress , 1995, Neuroscience & Biobehavioral Reviews.

[33]  Catie Chang,et al.  Influence of heart rate on the BOLD signal: The cardiac response function , 2009, NeuroImage.

[34]  V. Macefield,et al.  Resting regional brain activity and connectivity vary with resting blood pressure but not muscle sympathetic nerve activity in normotensive humans: An exploratory study , 2018, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[35]  G. Dai,et al.  Neuroanatomic Connectivity of the Human Ascending Arousal System Critical to Consciousness and Its Disorders , 2012, Journal of neuropathology and experimental neurology.

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

[37]  Lisa Y. M. Chuah,et al.  Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition , 2008, Current opinion in neurology.

[38]  Jeff H. Duyn,et al.  Early anti-correlated BOLD signal changes of physiologic origin , 2014, NeuroImage.

[39]  Catie Chang,et al.  Effects of model-based physiological noise correction on default mode network anti-correlations and correlations , 2009, NeuroImage.

[40]  Justin L. Vincent,et al.  Spontaneous neuronal activity distinguishes human dorsal and ventral attention systems. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[41]  S. Porges,et al.  Vagal tone and the physiological regulation of emotion. , 1994, Monographs of the Society for Research in Child Development.

[42]  Miho Nakajima,et al.  Thalamic control of functional cortical connectivity , 2017, Current Opinion in Neurobiology.

[43]  J. Thayer,et al.  Heart Rate Variability, Prefrontal Neural Function, and Cognitive Performance: The Neurovisceral Integration Perspective on Self-regulation, Adaptation, and Health , 2009, Annals of behavioral medicine : a publication of the Society of Behavioral Medicine.

[44]  S. Porges.  The polyvagal perspective , 2007, Biological Psychology.

[45]  Justin L. Vincent,et al.  Evidence for a frontoparietal control system revealed by intrinsic functional connectivity. , 2008, Journal of neurophysiology.

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

[47]  G. J. Horst,et al.  Projections from the rostral parvocellular reticular formation to pontine and medullary nuclei in the rat: Involvement in autonomic regulation and orofacial motor control , 1991, Neuroscience.

[48]  S. Jang,et al.  The Ascending Reticular Activating System from Pontine Reticular Formation to the Thalamus in the Human Brain , 2013, Front. Hum. Neurosci..

[49]  Andreas Schulze-Bonhage,et al.  Heart cycle-related effects on event-related potentials, spectral power changes, and connectivity patterns in the human ECoG , 2013, NeuroImage.

[50]  Hugo D. Critchley,et al.  Psychophysiology of neural, cognitive and affective integration: fMRI and autonomic indicants , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[51]  David McIntyre,et al.  Psychomotor speed in hypertension: effects of reaction time components, stimulus modality, and phase of the cardiac cycle. , 2007, Psychophysiology.

[52]  Frank Seifert,et al.  Activation of central sympathetic networks during innocuous and noxious somatosensory stimulation , 2011, NeuroImage.

[53]  Mary Beth Nebel,et al.  Reduction of motion-related artifacts in resting state fMRI using aCompCor , 2014, NeuroImage.

[54]  Wolfgang Klimesch,et al.  Heartbeat-related EEG amplitude and phase modulations from wakefulness to deep sleep: Interactions with sleep spindles and slow oscillations. , 2015, Psychophysiology.

[55]  M. W. Molen,et al.  Phasic heart rate responses and cardiac cycle time in auditory choice reaction time , 1983, Biological Psychology.

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

[57]  M. Fukunaga,et al.  Negative BOLD-fMRI Signals in Large Cerebral Veins , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[58]  G. Moruzzi,et al.  Brain stem reticular formation and activation of the EEG. , 1949, Electroencephalography and clinical neurophysiology.

[59]  Michael M. Halassa,et al.  State-Dependent Architecture of Thalamic Reticular Subnetworks , 2014, Cell.

[60]  J. Pekar,et al.  Reaction time-related activity reflecting periodic, task-specific cognitive control , 2016, Behavioural Brain Research.

[61]  Martin Sarter,et al.  Ascending visceral regulation of cortical affective information processing , 2003, The European journal of neuroscience.

[62]  Alan C. Evans,et al.  Applications of random field theory to functional connectivity , 1998, Human brain mapping.

[63]  H. Critchley,et al.  What the heart forgets: Cardiac timing influences memory for words and is modulated by metacognition and interoceptive sensitivity. , 2013, Psychophysiology.

[64]  K. Worsley,et al.  Unified univariate and multivariate random field theory , 2004, NeuroImage.

[65]  C. Saper.  The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. , 2002, Annual review of neuroscience.

[66]  S. Porges,et al.  Cardiac vagal tone and sustained attention in school-age children. , 1994, Psychophysiology.

[67]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[68]  M. Fukunaga,et al.  Sources of functional magnetic resonance imaging signal fluctuations in the human brain at rest: a 7 T study. , 2009, Magnetic resonance imaging.

[69]  Vivien A. Casagrande,et al.  Gating and control of primary visual cortex by pulvinar , 2012, Nature Neuroscience.

[70]  S. Porges.  The Polyvagal Theory: phylogenetic contributions to social behavior , 2003, Physiology & Behavior.

[71]  J. Jennings,et al.  Test-retest reliability of an fMRI paradigm for studies of cardiovascular reactivity. , 2012, Psychophysiology.

[72]  Timothy O. Laumann,et al.  Sources and implications of whole-brain fMRI signals in humans , 2017, NeuroImage.

[73]  Essa Yacoub,et al.  The WU-Minn Human Connectome Project: An overview , 2013, NeuroImage.

[74]  D. Mcintyre,et al.  Simple reaction time as a function of the phase of the cardiac cycle in young adults at risk for hypertension. , 2008, Psychophysiology.

[75]  J. Thayer,et al.  Vagal influence on working memory and attention. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[76]  Vaughan G. Macefield,et al.  Identification of the human sympathetic connectome involved in blood pressure regulation , 2019, NeuroImage.

[77]  J. Thayer,et al.  The relationship of autonomic imbalance, heart rate variability and cardiovascular disease risk factors. , 2010, International journal of cardiology.

[78]  Mark A. Eckert,et al.  Histologic validation of locus coeruleus MRI contrast in post-mortem tissue , 2015, NeuroImage.

[79]  Peter A. Bandettini,et al.  Task-Independent Functional Brain Activity Correlation with Skin Conductance Changes: An fMRI Study , 2002, NeuroImage.

[80]  Michael M. Halassa,et al.  Thalamic Circuit Mechanisms Link Sensory Processing in Sleep and Attention , 2016, Front. Neural Circuits.

[81]  S. Ogoh,et al.  Gravity, intracranial pressure, and cerebral autoregulation , 2019, Physiological reports.

[82]  M. Corbetta,et al.  Neural Systems for Visual Orienting and Their Relationships to Spatial Working Memory , 2002, Journal of Cognitive Neuroscience.

[83]  S. Porges.  The polyvagal theory: New insights into adaptive reactions of the autonomic nervous system , 2009, Cleveland Clinic Journal of Medicine.

[84]  Christos Davatzikos,et al.  Benchmarking of participant-level confound regression strategies for the control of motion artifact in studies of functional connectivity , 2017, NeuroImage.

[85]  Hans Knutsson,et al.  Cluster failure revisited: Impact of first level design and physiological noise on cluster false positive rates , 2018, Human brain mapping.

[86]  J. Thayer,et al.  Neurovisceral integration in cardiac and emotional regulation , 2002, IEEE Engineering in Medicine and Biology Magazine.

[87]  S Shipp,et al.  The functional logic of cortico-pulvinar connections. , 2003, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[88]  Ralf D. Wimmer,et al.  Thalamic amplification of cortical connectivity sustains attentional control , 2017, Nature.

[89]  Xiao-Jing Wang,et al.  Engagement of Pulvino-cortical Feedforward and Feedback Pathways in Cognitive Computations , 2018, Neuron.

[90]  Y. Saalmann,et al.  The Pulvinar Regulates Information Transmission Between Cortical Areas Based on Attention Demands , 2012, Science.

[91]  Timothy Edward John Behrens,et al.  Functional-anatomical validation and individual variation of diffusion tractography-based segmentation of the human thalamus. , 2005, Cerebral cortex.