Simultaneous EEG and fMRI Reveals a Causally Connected Subcortical-Cortical Network during Reward Anticipation

Electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) have been used to study the neural correlates of reward anticipation, but the interrelation of EEG and fMRI measures remains unknown. The goal of the present study was to investigate this relationship in response to a well established reward anticipation paradigm using simultaneous EEG-fMRI recording in healthy human subjects. Analysis of causal interactions between the thalamus (THAL), ventral-striatum (VS), and supplementary motor area (SMA), using both mediator analysis and dynamic causal modeling, revealed that (1) THAL fMRI blood oxygenation level-dependent (BOLD) activity is mediating intermodal correlations between the EEG contingent negative variation (CNV) signal and the fMRI BOLD signal in SMA and VS, (2) the underlying causal connectivity network consists of top-down regulation from SMA to VS and SMA to THAL along with an excitatory information flow through a THAL→VS→SMA route during reward anticipation, and (3) the EEG CNV signal is best predicted by a combination of THAL fMRI BOLD response and strength of top-down regulation from SMA to VS and SMA to THAL. Collectively, these findings represent a likely neurobiological mechanism mapping a primarily subcortical process, i.e., reward anticipation, onto a cortical signature.

[1]  D. A. Kenny,et al.  The moderator-mediator variable distinction in social psychological research: conceptual, strategic, and statistical considerations. , 1986, Journal of personality and social psychology.

[2]  M. Kimura,et al.  Monitoring and switching of cortico-basal ganglia loop functions by the thalamo-striatal system , 2004, Neuroscience Research.

[3]  B. Abler,et al.  Neural reward processing under dopamine agonists: Imaging , 2011, Journal of the Neurological Sciences.

[4]  W. Walter,et al.  Contingent Negative Variation : An Electric Sign of Sensori-Motor Association and Expectancy in the Human Brain , 1964, Nature.

[5]  A. Hayes.  PROCESS : A Versatile Computational Tool for Observed Variable Mediation , Moderation , and Conditional Process Modeling 1 , 2012 .

[6]  Robert Turner,et al.  A Method for Removing Imaging Artifact from Continuous EEG Recorded during Functional MRI , 2000, NeuroImage.

[7]  Matthijs Vink,et al.  Top–down‐directed synchrony from medial frontal cortex to nucleus accumbens during reward anticipation , 2012, Human brain mapping.

[8]  Brian Knutson,et al.  Dissociation of reward anticipation and outcome with event-related fMRI , 2001, Neuroreport.

[9]  Peter Kirsch,et al.  Anticipation of reward in a nonaversive differential conditioning paradigm and the brain reward system: an event-related fMRI study , 2003, NeuroImage.

[10]  E. H. Boyd,et al.  Observations on the M-wave and the CNV in the squirrel monkey. , 1979, Electroencephalography and clinical neurophysiology.

[11]  E. Sonuga-Barke,et al.  Electrophysiological markers of the motivational salience of delay imposition and escape , 2012, Neuropsychologia.

[12]  N. Ramsey,et al.  Involvement of the endocannabinoid system in reward processing in the human brain , 2011, Psychopharmacology.

[13]  J. Kaas,et al.  The thalamic connections of motor, premotor, and prefrontal areas of cortex in a prosimian primate (Otolemur garnetti) , 2006, Neuroscience.

[14]  M. Reuter,et al.  Imaging gene–substance interactions: The effect of the DRD2 TaqIA polymorphism and the dopamine agonist bromocriptine on the brain activation during the anticipation of reward , 2006, Neuroscience Letters.

[15]  Michael X. Cohen,et al.  Neuroelectric Signatures of Reward Learning and Decision-Making in the Human Nucleus Accumbens , 2009, Neuropsychopharmacology.

[16]  Jeffrey C. Cooper,et al.  Functional magnetic resonance imaging of reward prediction , 2005, Current opinion in neurology.

[17]  Brian Knutson,et al.  Anticipation of Increasing Monetary Reward Selectively Recruits Nucleus Accumbens , 2001, The Journal of Neuroscience.

[18]  Karl J. Friston,et al.  Dynamic causal models of neural system dynamics: current state and future extensions , 2007, Journal of Biosciences.

[19]  B. Rockstroh,et al.  Slow potentials of the cerebral cortex and behavior. , 1990, Physiological reviews.

[20]  S. Haber,et al.  The cortico-basal ganglia integrative network: The role of the thalamus , 2009, Brain Research Bulletin.

[21]  S. Debener,et al.  Trial-by-Trial Fluctuations in the Event-Related Electroencephalogram Reflect Dynamic Changes in the Degree of Surprise , 2008, The Journal of Neuroscience.

[22]  Michael J. Frank,et al.  Single dose of a dopamine agonist impairs reinforcement learning in humans: Evidence from event‐related potentials and computational modeling of striatal‐cortical function , 2009, Human brain mapping.

[23]  Y. Smith,et al.  The thalamostriatal system: a highly specific network of the basal ganglia circuitry , 2004, Trends in Neurosciences.

[24]  P. Falkai,et al.  The role of the human ventral striatum and the medial orbitofrontal cortex in the representation of reward magnitude – An activation likelihood estimation meta-analysis of neuroimaging studies of passive reward expectancy and outcome processing , 2012, Neuropsychologia.

[25]  Karl J. Friston,et al.  Bayesian model selection for group studies , 2009, NeuroImage.

[26]  N Lesevre,et al.  Electrophysiological changes elicited by auditory stimuli given a positive or negative value: a study comparing anhedonic with hedonic subjects. , 1987, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[27]  Felix Breuer,et al.  Neural response to reward anticipation is modulated by Gray's impulsivity , 2009, NeuroImage.

[28]  Heleen A Slagter,et al.  Event‐related potential activity in the basal ganglia differentiates rewards from nonrewards: Temporospatial principal components analysis and source localization of the feedback negativity: Commentary , 2011, Human brain mapping.

[29]  K. Lesch,et al.  Neural Hyporesponsiveness and Hyperresponsiveness During Immediate and Delayed Reward Processing in Adult Attention-Deficit/Hyperactivity Disorder , 2009, Biological Psychiatry.

[30]  Justin L. Vincent,et al.  Intrinsic Fluctuations within Cortical Systems Account for Intertrial Variability in Human Behavior , 2007, Neuron.

[31]  H. Groenewegen,et al.  The specificity of the ‘nonspecific’ midline and intralaminar thalamic nuclei , 1994, Trends in Neurosciences.

[32]  A. Graybiel,et al.  Neurons in the thalamic CM-Pf complex supply striatal neurons with information about behaviorally significant sensory events. , 2001, Journal of neurophysiology.

[33]  Brian Knutson,et al.  Ventral Striatal Hyporesponsiveness During Reward Anticipation in Attention-Deficit/Hyperactivity Disorder , 2007, Biological Psychiatry.

[34]  W. Sommer,et al.  Effects of Parametrical and Trial-to-Trial Variation in Prior Probability Processing Revealed by Simultaneous Electroencephalogram/Functional Magnetic Resonance Imaging , 2010, The Journal of Neuroscience.

[35]  A. Engel,et al.  Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2006, Trends in Cognitive Sciences.

[36]  Brian Knutson,et al.  Spatial smoothing systematically biases the localization of reward-related brain activity , 2013, NeuroImage.

[37]  Peter Kirsch,et al.  Test–retest reliability of evoked BOLD signals from a cognitive–emotive fMRI test battery , 2012, NeuroImage.

[38]  R. Davidson,et al.  Anterior brain electrical asymmetries in response to reward and punishment. , 1992, Electroencephalography and clinical neurophysiology.

[39]  C. Brunia,et al.  Changes in heart rate and slow brain potentials related to motor preparation and stimulus anticipation in a time estimation task. , 1987, Psychophysiology.

[40]  J. Dreher,et al.  Long-lasting effects of performance-contingent unconscious and conscious reward incentives during cued task-switching , 2013, Cortex.

[41]  Samantha J. Broyd,et al.  An electrophysiological monetary incentive delay (e-MID) task: A way to decompose the different components of neural response to positive and negative monetary reinforcement , 2012, Journal of Neuroscience Methods.

[42]  Louis Lemieux,et al.  Identification of EEG Events in the MR Scanner: The Problem of Pulse Artifact and a Method for Its Subtraction , 1998, NeuroImage.

[43]  Anna Weinberg,et al.  Event‐related potential activity in the basal ganglia differentiates rewards from nonrewards: Temporospatial principal components analysis and source localization of the feedback negativity , 2011, Human brain mapping.

[44]  D. Smith,et al.  Exploiting Trial-to-Trial Variability in Multimodal Experiments , 2011, Frontiers in Human Neuroscience.

[45]  A. Hariri,et al.  Genetic variation in components of dopamine neurotransmission impacts ventral striatal reactivity associated with impulsivity , 2009, Molecular Psychiatry.

[46]  B. Abler,et al.  Human reward system activation is modulated by a single dose of olanzapine in healthy subjects in an event-related, double-blind, placebo-controlled fMRI study , 2007, Psychopharmacology.

[47]  R. D. Pascual-Marqui,et al.  The continuous performance test revisited with neuroelectric mapping: impaired orienting in children with attention deficits , 1998, Behavioural Brain Research.

[48]  D B Lindsley,et al.  Brain wave components of the contingent negative variation in humans. , 1976, Science.

[49]  S. Hyman,et al.  Acute Effects of Cocaine on Human Brain Activity and Emotion , 1997, Neuron.

[50]  S. Haber.  Neuroanatomy of Reward: A View from the Ventral Striatum , 2011 .

[51]  D L Jewett,et al.  Human Auditory Evoked Potentials: Possible Brain Stem Components Detected on the Scalp , 1970, Science.

[52]  Hugo D. Critchley,et al.  Brain activity relating to the contingent negative variation: an fMRI investigation , 2004, NeuroImage.

[53]  K. R. Ridderinkhof,et al.  Dose dependent dopaminergic modulation of reward-based learning in Parkinson's disease , 2012, Neuropsychologia.

[54]  K. Suda,et al.  Effect of positive and negative emotion on stimulus-preceding negativity prior to feedback stimuli. , 2001, Psychophysiology.

[55]  Brian Knutson,et al.  Amphetamine Modulates Human Incentive Processing , 2004, Neuron.

[56]  Ashley R. Smith,et al.  The effect of intravenous alcohol on the neural correlates of risky decision making in healthy social drinkers , 2012, Addiction biology.

[57]  H. Heinrich,et al.  Differential effects of methylphenidate and atomoxetine on attentional processes in children with ADHD: An event-related potential study using the Attention Network Test , 2012, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[58]  R. Dahl,et al.  Reward-related brain function as a predictor of treatment response in adolescents with major depressive disorder , 2010, Cognitive, affective & behavioral neuroscience.

[59]  Jeffrey L. Birk,et al.  Childhood Adversity Is Associated with Left Basal Ganglia Dysfunction During Reward Anticipation in Adulthood , 2009, Biological Psychiatry.

[60]  S. Debener,et al.  Properties of the ballistocardiogram artefact as revealed by EEG recordings at 1.5, 3 and 7 T static magnetic field strength. , 2008, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

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

[62]  Jin Fan,et al.  Common and distinct networks underlying reward valence and processing stages: A meta-analysis of functional neuroimaging studies , 2011, Neuroscience & Biobehavioral Reviews.

[63]  Brian Knutson,et al.  Ventral Striatal Activation during Reward Processing in Subjects with Ultra-High Risk for Schizophrenia , 2012, Neuropsychobiology.

[64]  Kristopher J Preacher,et al.  SPSS and SAS procedures for estimating indirect effects in simple mediation models , 2004, Behavior research methods, instruments, & computers : a journal of the Psychonomic Society, Inc.

[65]  C. M Gómez,et al.  Preparatory visuo-motor cortical network of the contingent negative variation estimated by current density , 2003, NeuroImage.

[66]  Sebastian Heinzel,et al.  Association between reward‐related activation in the ventral striatum and trait reward sensitivity is moderated by dopamine transporter genotype , 2011, Human brain mapping.

[67]  T. Münte,et al.  Dopamine Agonist Increases Risk Taking but Blunts Reward-Related Brain Activity , 2008, PloS one.

[68]  Karl J. Friston,et al.  Ten simple rules for dynamic causal modeling , 2010, NeuroImage.

[69]  Karl J. Friston,et al.  Dynamic causal modelling , 2003, NeuroImage.

[70]  Thomas Wichmann,et al.  The thalamostriatal systems: Anatomical and functional organization in normal and parkinsonian states , 2009, Brain Research Bulletin.