Brain Networks Involved in Early versus Late Response Anticipation and Their Relation to Conflict Processing

Previous electrophysiological studies have clearly identified separable neural events underlying early and late components of response anticipation. Functional neuroimaging studies, however, have so far failed to account for this separation. Here, we performed functional magnetic resonance imaging (fMRI) of an anticipation paradigm in 12 healthy adult subjects that reliably produced early and late expectancy waves in the electroencephalogram. We furthermore compared fMRI activations elicited during early and late anticipation to those associated with response conflict. Our results demonstrate the existence of distinct cortical and subcortical brain regions underlying early and late anticipation. Although late anticipatory behavior was associated with activations in dorsal ACC, frontal cortex, and thalamus, brain responses linked to the early expectancy wave were localized mainly in motor and premotor cortical areas as well as the caudate nucleus. Additionally, late anticipation was associated with increased activity in midbrain dopaminergic nuclei, very likely corresponding to the substantia nigra. Furthermore, whereas regions involved in late anticipation proved to be very similar to activations elicited by response conflict, this was not the case for early anticipation. The current study supports a distinction between early and late anticipatory processes, in line with a plethora of neurophysiological work, and for the first time describes the brain structures differentially involved in these processes.

[1]  Jens Frahm,et al.  Lateralized anterior cingulate function during error processing and conflict monitoring as revealed by high-resolution fMRI. , 2008, Cerebral cortex.

[2]  Yoshiharu Tamakawa,et al.  The substantia nigra in Parkinson disease: proton density-weighted spin-echo and fast short inversion time inversion-recovery MR findings. , 2002, AJNR. American journal of neuroradiology.

[3]  C. F. Beckmann,et al.  Tensorial extensions of independent component analysis for multisubject FMRI analysis , 2005, NeuroImage.

[4]  J. Tecce Contingent negative variation (CNV) and psychological processes in man. , 1972, Psychological bulletin.

[5]  C. Eriksen,et al.  Effects of noise letters upon the identification of a target letter in a nonsearch task , 1974 .

[6]  A. Cools,et al.  tion in Time course and distribution of movement-rela ted potentials in a movement precueing task , 1996 .

[7]  Aapo Hyvärinen,et al.  Fast and robust fixed-point algorithms for independent component analysis , 1999, IEEE Trans. Neural Networks.

[8]  M. Corbetta,et al.  Control of goal-directed and stimulus-driven attention in the brain , 2002, Nature Reviews Neuroscience.

[9]  T. Banaschewski,et al.  Bedeutung funktioneller psychophysiologischer Methoden in der Kinder- und Jugendpsychiatrie , 2010 .

[10]  S. Carlson,et al.  Distribution of cortical activation during visuospatial n-back tasks as revealed by functional magnetic resonance imaging. , 1998, Cerebral cortex.

[11]  Michael J. Martinez,et al.  Bias between MNI and Talairach coordinates analyzed using the ICBM‐152 brain template , 2007, Human brain mapping.

[12]  Stephan Bender,et al.  Specific task anticipation versus unspecific orienting reaction during early contingent negative variation , 2004, Clinical Neurophysiology.

[13]  Raymond J. Dolan,et al.  Anterior cingulate activity during error and autonomic response , 2005, NeuroImage.

[14]  C. Brunia,et al.  Motor and non-motor aspects of slow brain potentials , 1994, Biological Psychology.

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

[16]  Soichiro Nomura,et al.  Autonomic arousal in cognitive conflict resolution , 2007, Autonomic Neuroscience.

[17]  Aribert Rothenberger,et al.  Training of slow cortical potentials in attention-deficit/hyperactivity disorder: evidence for positive behavioral and neurophysiological effects , 2004, Biological Psychiatry.

[18]  A. Schleicher,et al.  Two different areas within the primary motor cortex of man , 1996, Nature.

[19]  Michael Brady,et al.  Improved Optimization for the Robust and Accurate Linear Registration and Motion Correction of Brain Images , 2002, NeuroImage.

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

[21]  Aapo Hyv Fast and Robust Fixed-Point Algorithms for Independent Component Analysis , 1999 .

[22]  A. Sanford,et al.  Effects of age on the contingent negative variation and preparatory set in a reaction-time task. , 1974, Journal of gerontology.

[23]  F. Wilcoxon Individual Comparisons by Ranking Methods , 1945 .

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

[25]  Daniel Brandeis,et al.  Differences in Neurophysiological Markers of Inhibitory and Temporal Processing Deficits in Children and Adults with ADHD , 2009 .

[26]  M. Honda,et al.  Dissociation between contingent negative variation (CNV) and Bereitschaftspotential (BP) in patients with parkinsonism. , 1997, Electroencephalography and clinical neurophysiology.

[27]  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.

[28]  Stephen M Smith,et al.  Fast robust automated brain extraction , 2002, Human brain mapping.

[29]  N Birbaumer,et al.  P3 and contingent negative variation in Parkinson's disease. , 1996, Electroencephalography and clinical neurophysiology.

[30]  A. Cools,et al.  Movement preparation in Parkinson's disease. Time course and distribution of movement-related potentials in a movement precueing task. , 1996, Brain : a journal of neurology.

[31]  E Donchin,et al.  A new method for off-line removal of ocular artifact. , 1983, Electroencephalography and clinical neurophysiology.

[32]  T. Robbins,et al.  Differential Responses in Human Striatum and Prefrontal Cortex to Changes in Object and Rule Relevance , 2004, The Journal of Neuroscience.

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

[34]  Andreas Kleinschmidt,et al.  Recent advances in recording electrophysiological data simultaneously with magnetic resonance imaging , 2008, NeuroImage.

[35]  Paul A. Pope,et al.  Slow brain potential and oscillatory EEG manifestations of impaired temporal preparation in Parkinson's disease. , 2007, Journal of neurophysiology.

[36]  M. D’Esposito,et al.  The Variability of Human, BOLD Hemodynamic Responses , 1998, NeuroImage.

[37]  P. Hjemdahl,et al.  Cardiovascular and sympathoadrenal responses to mental stress: influence of beta-blockade. , 1988, The American journal of physiology.

[38]  C. Kennard,et al.  Human Medial Frontal Cortex Mediates Unconscious Inhibition of Voluntary Action , 2007, Neuron.

[39]  M. Walton,et al.  Action sets and decisions in the medial frontal cortex , 2004, Trends in Cognitive Sciences.

[40]  C. Kennard,et al.  The role of the pre-supplementary motor area in the control of action , 2007, NeuroImage.

[41]  M. Friedman The Use of Ranks to Avoid the Assumption of Normality Implicit in the Analysis of Variance , 1937 .

[42]  Timothy E. J. Behrens,et al.  Functional organization of the medial frontal cortex , 2007, Current Opinion in Neurobiology.

[43]  Stephen M. Smith,et al.  General multilevel linear modeling for group analysis in FMRI , 2003, NeuroImage.

[44]  Stephen M. Smith,et al.  Probabilistic independent component analysis for functional magnetic resonance imaging , 2004, IEEE Transactions on Medical Imaging.

[45]  T. Robbins,et al.  Striatal contributions to working memory: a functional magnetic resonance imaging study in humans , 2004, The European journal of neuroscience.

[46]  Stephen M. Smith,et al.  Temporal Autocorrelation in Univariate Linear Modeling of FMRI Data , 2001, NeuroImage.

[47]  Simon B. Eickhoff,et al.  A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data , 2005, NeuroImage.

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

[49]  P. Lang,et al.  Cortical slow-wave and cardiac rate responses in stimulus orientation and reaction time conditions. , 1969, Journal of experimental psychology.

[50]  E. Vaadia,et al.  Coincident but Distinct Messages of Midbrain Dopamine and Striatal Tonically Active Neurons , 2004, Neuron.

[51]  W. Gehring,et al.  Medial Frontal Cortex Activity and Loss-Related Responses to Errors , 2006, The Journal of Neuroscience.

[52]  Bruce D. McCandliss,et al.  Response Anticipation and Response Conflict: An Event-Related Potential and Functional Magnetic Resonance Imaging Study , 2007, The Journal of Neuroscience.

[53]  P. Morgane,et al.  A review of systems and networks of the limbic forebrain/limbic midbrain , 2005, Progress in Neurobiology.

[54]  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.

[55]  P. Fenwick,et al.  Activation sequence of discrete brain areas during cognitive processes: results from magnetic field tomography. , 1994, Electroencephalography and clinical neurophysiology.

[56]  T. Shallice,et al.  Human cingulate cortex and autonomic control: converging neuroimaging and clinical evidence. , 2003, Brain : a journal of neurology.

[57]  G. Lohmann,et al.  Color-Word Matching Stroop Task: Separating Interference and Response Conflict , 2001, NeuroImage.

[58]  Mark W. Woolrich,et al.  Multilevel linear modelling for FMRI group analysis using Bayesian inference , 2004, NeuroImage.

[59]  Roland E. Suri,et al.  Temporal Difference Model Reproduces Anticipatory Neural Activity , 2001, Neural Computation.

[60]  G E Stelmach,et al.  Movement preparation in Parkinson's disease. The use of advance information. , 1986, Brain : a journal of neurology.