The norepinephrine system and its relevance for multi-component behavior

Abstract The ability to execute several actions in a specific temporal order to achieve an overarching goal, a process often termed action cascading or multi‐component behavior, is essential for everyday life requirements. We are only at the beginning to understand the neurobiological mechanisms important for these cognitive processes. However, it is likely that the locus coeruleus‐norepinephrine (LC‐NE) system may be of importance. In the current study we examine the relevance of the LC‐NE system for action cascading processes using a system neurophysiological approach combining high‐density EEG recordings and source localization to analyze event‐related potentials (ERPs) with recordings of pupil diameter as a proximate of LC‐NE system activity. N=25 healthy participants performed an action cascading stop‐change paradigm. Integrating ERPs and pupil diameter using Pearson correlations, the results show that the LC‐NE system is important for processes related to multi‐component behavior. However, the LC‐NE system does not seem to be important during the time period of response selection processes during multi‐component behavior (reflected in the P3) as well as during perceptual and attentional selection (P1 and N1 ERPs). Rather, it seems that the neurophysiological processes in the fore period of a possibly upcoming imperative stimulus to initiate multi‐component behavior are correlated with the LC‐NE system. It seems that the LC‐NE system facilitates responses to task‐relevant processes and supports task‐related decision and response selection processes by preparing cognitive control processes in case these are required during multi‐component behavior rather than modulating these processes once they are operating. HighlightsThe role of the norepinephrine system for multi‐component behavior is examined.Pupil diameter and ERP data are integrated and related to the functional neuroanatomy.The NE‐system predicts attentional gating and response selection processes.NE system prepares cognitive control processes for multi‐component behavior.

[1]  C. Beste,et al.  Psychophysiological mechanisms of interindividual differences in goal activation modes during action cascading. , 2014, Cerebral cortex.

[2]  Christian Beste,et al.  DRD1 and DRD2 Genotypes Modulate Processing Modes of Goal Activation Processes during Action Cascading , 2014, The Journal of Neuroscience.

[3]  P L Nunez,et al.  The Spline‐Laplacian in Clinical Neurophysiology: A Method to Improve EEG Spatial Resolution , 1991, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[4]  Kensuke Sekihara,et al.  Localization bias and spatial resolution of adaptive and non-adaptive spatial filters for MEG source reconstruction , 2005, NeuroImage.

[5]  R. Knight,et al.  Mechanisms of human attention: event-related potentials and oscillations , 2001, Neuroscience & Biobehavioral Reviews.

[6]  T. Ziemssen,et al.  The norepinephrine system affects specific neurophysiological subprocesses in the modulation of inhibitory control by working memory demands , 2017, Human brain mapping.

[7]  Clay B. Holroyd,et al.  What can topology changes in the oddball N2 reveal about underlying processes? , 2011, Neuroreport.

[8]  Josep Marco-Pallarés,et al.  Combined ICA-LORETA analysis of mismatch negativity , 2005, NeuroImage.

[9]  M. Posner,et al.  The attention system of the human brain. , 1990, Annual review of neuroscience.

[10]  Rolf Verleger,et al.  Testing the S–R link hypothesis of P3b: The oddball effect on S1-evoked P3 gets reduced by increased task relevance of S2 , 2015, Biological Psychology.

[11]  Christian Beste,et al.  Questioning the role of the frontopolar cortex in multi-component behavior – a TMS/EEG study , 2016, Scientific Reports.

[12]  R D Pascual-Marqui,et al.  Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. , 2002, Methods and findings in experimental and clinical pharmacology.

[13]  Arnaud Delorme,et al.  EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis , 2004, Journal of Neuroscience Methods.

[14]  John J. Foxe,et al.  Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. , 2002, Brain research. Cognitive brain research.

[15]  C. Bradshaw,et al.  Does modafinil activate the locus coeruleus in man? Comparison of modafinil and clonidine on arousal and autonomic functions in human volunteers , 2005, Psychopharmacology.

[16]  Jonathan D. Cohen,et al.  An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. , 2005, Annual review of neuroscience.

[17]  Marco Zorzi,et al.  Pupil dilation reveals top–down attentional load during spatial monitoring , 2015, Biological Psychology.

[18]  C. M. Bradshaw,et al.  Comparison of the effects of clonidine and yohimbine on spontaneous pupillary fluctuations in healthy human volunteers , 2000, Psychopharmacology.

[19]  Angie A. Kehagia,et al.  Learning and cognitive flexibility: frontostriatal function and monoaminergic modulation , 2010, Current Opinion in Neurobiology.

[20]  Clay B. Holroyd,et al.  The Impact of Deliberative Strategy Dissociates ERP Components Related to Conflict Processing vs. Reinforcement Learning , 2012, Front. Neurosci..

[21]  G. Logan,et al.  Models of response inhibition in the stop-signal and stop-change paradigms , 2009, Neuroscience & Biobehavioral Reviews.

[22]  Roberta Sellaro,et al.  Transcutaneous Vagal Nerve Stimulation (tVNS): a new neuromodulation tool in healthy humans? , 2015, Front. Psychol..

[23]  A. Hahne,et al.  Improvements of sensorimotor processes during action cascading associated with changes in sensory processing architecture–insights from sensory deprivation , 2016, Scientific Reports.

[24]  A. Jacobs,et al.  Coregistration of eye movements and EEG in natural reading: analyses and review. , 2011, Journal of experimental psychology. General.

[25]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[26]  J. Leon Kenemans,et al.  The effect of noradrenergic attenuation by clonidine on inhibition in the stop signal task , 2013, Pharmacology Biochemistry and Behavior.

[27]  Paul Sajda,et al.  Your Eyes Give You Away: Prestimulus Changes in Pupil Diameter Correlate with Poststimulus Task-Related EEG Dynamics , 2014, PloS one.

[28]  L. Colzato,et al.  Transcutaneous vagus nerve stimulation (tVNS) enhances response selection during action cascading processes , 2015, European Neuropsychopharmacology.

[29]  C. Beste,et al.  A causal role of the right inferior frontal cortex in implementing strategies for multi-component behaviour , 2015, Nature Communications.

[30]  F. Perrin,et al.  Spherical splines for scalp potential and current density mapping. , 1989, Electroencephalography and clinical neurophysiology.

[31]  Antoni Rodríguez-Fornells,et al.  Noradrenergic Stimulation Enhances Human Action Monitoring , 2005, The Journal of Neuroscience.

[32]  R. Raedt,et al.  Increased hippocampal noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model , 2011, Journal of neurochemistry.

[33]  R. O’Connell,et al.  Pupillometry and P3 index the locus coeruleus-noradrenergic arousal function in humans. , 2011, Psychophysiology.

[34]  John J. Foxe,et al.  Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. , 2005, Cerebral cortex.

[35]  Christina F. Lavallee,et al.  Electroencephalography of response inhibition tasks: functional networks and cognitive contributions. , 2013, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[36]  R. Geva,et al.  Alerting, orienting or executive attention networks: differential patters of pupil dilations , 2013, Front. Behav. Neurosci..

[37]  M. Posner,et al.  The attention system of the human brain: 20 years after. , 2012, Annual review of neuroscience.

[38]  Mark S. Gilzenrat,et al.  Pupil diameter tracks changes in control state predicted by the adaptive gain theory of locus coeruleus function , 2010, Cognitive, affective & behavioral neuroscience.

[39]  Christian Beste,et al.  On the relevance of the NPY2-receptor variation for modes of action cascading processes , 2014, NeuroImage.

[40]  S. Kelly,et al.  The classic P300 encodes a build‐to‐threshold decision variable , 2015, The European journal of neuroscience.

[41]  J. Duncan.  The multiple-demand (MD) system of the primate brain: mental programs for intelligent behaviour , 2010, Trends in Cognitive Sciences.

[42]  Frederick Verbruggen,et al.  How to Stop and Change a Response: the Role of Goal Activation in Multitasking , 2022 .

[43]  C. Beste,et al.  The importance of sensory integration processes for action cascading , 2015, Scientific Reports.

[44]  G. Logan.  On the ability to inhibit thought and action , 1984 .

[45]  J. Gold,et al.  Relationships between Pupil Diameter and Neuronal Activity in the Locus Coeruleus, Colliculi, and Cingulate Cortex , 2016, Neuron.

[46]  R. Edden,et al.  Feeling safe in the plane: Neural mechanisms underlying superior action control in airplane pilot trainees—A combined EEG/MRS study , 2014, Human brain mapping.

[47]  Sander Nieuwenhuis,et al.  Pupil Diameter Predicts Changes in the Exploration–Exploitation Trade-off: Evidence for the Adaptive Gain Theory , 2011, Journal of Cognitive Neuroscience.

[48]  M. Fuchs,et al.  A standardized boundary element method volume conductor model , 2002, Clinical Neurophysiology.

[49]  Christian Beste,et al.  Age-related differences in task goal processing strategies during action cascading , 2015, Brain Structure and Function.

[50]  Christian Beste,et al.  Different strategies, but indifferent strategy adaptation during action cascading , 2015, Scientific reports.

[51]  Jonathan D. Cohen,et al.  Decision making, the P3, and the locus coeruleus-norepinephrine system. , 2005, Psychological bulletin.