Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making

While the precise role of the anterior cingulate cortex (ACC) is still being discussed, it has been suggested that ACC activity might reflect the amount of mental effort associated with cognitive processing. So far, not much is known about the temporal dynamics of ACC activity in effort-related decision making or auditory attention, because fMRI is limited concerning its temporal resolution and electroencephalography (EEG) is limited concerning its spatial resolution. Single-trial coupling of EEG and fMRI can be used to predict the BOLD signal specifically related to amplitude variations of electrophysiological components. The striking feature of single-trial coupling is its ability to separate different aspects of the BOLD signal according to their specific relationship to a distinct neural process. In the present study we investigated 10 healthy subjects with a forced choice reaction task under both low and high effort conditions and a control condition (passive listening) using simultaneous EEG and fMRI. We detected a significant effect of mental effort only for the N1 potential, but not for the P300 potential. In the fMRI analysis, ACC activation was present only in the high effort condition. We used single-trial coupling of EEG and fMRI in order to separate information specific to N1-amplitude variations from the unrelated BOLD response. Under high effort conditions we were able to detect circumscribed BOLD activations specific to the N1 potential in the ACC (t=4.7) and the auditory cortex (t=6.1). Comparing the N1-specific BOLD activity of the high effort condition versus the control condition we found only activation of the ACC (random effects analysis, corrected for multiple comparisons, t=4.4). These findings suggest a role of early ACC activation in effort-related decision making and provide a direct link between the N1 component and its corresponding BOLD signal.

[1]  J. R. Hughes,et al.  STUDIES ON THE SUPRACALLOSAL MESIAL CORTEX OF UNANESTHETIZED, CONSCIOUS MAMMALS. II. MONKEY. D. VERTEX SHARP WAVES AND EPILEPTIFORM ACTIVITY. , 1964, Electroencephalography and clinical neurophysiology.

[2]  Jonathan D. Cohen,et al.  Conflict monitoring and anterior cingulate cortex: an update , 2004, Trends in Cognitive Sciences.

[3]  Vinod Menon,et al.  Where and When the Anterior Cingulate Cortex Modulates Attentional Response: Combined fMRI and ERP Evidence , 2006, Journal of Cognitive Neuroscience.

[4]  Y GASTAUT,et al.  [Negative points evoked on the vertex; their pathological and psychophysiological significance]. , 1953, Revue neurologique.

[5]  Christoph Mulert,et al.  The relationship between reaction time, error rate and anterior cingulate cortex activity. , 2003, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[6]  M. Roth,et al.  Single‐trial analysis of oddball event‐related potentials in simultaneous EEG‐fMRI , 2007, Human brain mapping.

[7]  S. Hillyard,et al.  Electrical Signs of Selective Attention in the Human Brain , 1973, Science.

[8]  M. Herrmann,et al.  Source localization (LORETA) of the error-related-negativity (ERN/Ne) and positivity (Pe). , 2004, Brain research. Cognitive brain research.

[9]  W. Ritter,et al.  The sources of auditory evoked responses recorded from the human scalp. , 1970, Electroencephalography and clinical neurophysiology.

[10]  Matthew F. S. Rushworth,et al.  Weighing up the benefits of work: Behavioral and neural analyses of effort-related decision making , 2006, Neural Networks.

[11]  M. Botvinick,et al.  Anterior cingulate cortex, error detection, and the online monitoring of performance. , 1998, Science.

[12]  Jonathan D. Cohen,et al.  Conflict monitoring versus selection-for-action in anterior cingulate cortex , 1999, Nature.

[13]  M. Walton,et al.  Separate neural pathways process different decision costs , 2006, Nature Neuroscience.

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

[15]  Kenneth Hugdahl,et al.  Assessing the spatiotemporal evolution of neuronal activation with single-trial event-related potentials and functional MRI. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[16]  T. Picton,et al.  The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. , 1987, Psychophysiology.

[17]  A Pfefferbaum,et al.  Event-related potentials in schizophrenics. , 1980, Electroencephalography and clinical neurophysiology.

[18]  C. Carter,et al.  The Timing of Action-Monitoring Processes in the Anterior Cingulate Cortex , 2002, Journal of Cognitive Neuroscience.

[19]  Christoph Mulert,et al.  Sound level dependence of the primary auditory cortex: Simultaneous measurement with 61-channel EEG and fMRI , 2005, NeuroImage.

[20]  Rami K. Niazy,et al.  Removal of FMRI environment artifacts from EEG data using optimal basis sets , 2005, NeuroImage.

[21]  S. Dehaene,et al.  Dynamics of prefrontal and cingulate activity during a reward-based logical deduction task. , 2006, Cerebral cortex.

[22]  Stephan Bender,et al.  Frontal lobe involvement in the processing of meaningful auditory stimuli develops during childhood and adolescence , 2006, NeuroImage.

[23]  T. Braver,et al.  Anterior cingulate cortex and response conflict: effects of response modality and processing domain. , 2001, Cerebral Cortex.

[24]  E. Schröger,et al.  The development of involuntary and voluntary attention from childhood to adulthood: A combined behavioral and event-related potential study , 2006, Clinical Neurophysiology.

[25]  D. Pandya,et al.  Efferent connections of the cingulate gyrus in the rhesus monkey , 1981, Experimental Brain Research.

[26]  A. Engel,et al.  Trial-by-Trial Coupling of Concurrent Electroencephalogram and Functional Magnetic Resonance Imaging Identifies the Dynamics of Performance Monitoring , 2005, The Journal of Neuroscience.

[27]  Clay B. Holroyd,et al.  Sensitivity of electrophysiological activity from medial frontal cortex to utilitarian and performance feedback. , 2004, Cerebral cortex.

[28]  I D Wilkinson,et al.  Neural activity in speech-sensitive auditory cortex during silence. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[29]  Kenneth M. Heilman,et al.  Neuropsychology of human emotion , 1983 .

[30]  M. Scherg,et al.  Two bilateral sources of the late AEP as identified by a spatio-temporal dipole model. , 1985, Electroencephalography and clinical neurophysiology.

[31]  J. Hohnsbein,et al.  Event-related potential correlates of errors in reaction tasks. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

[32]  K. A. Hadland,et al.  The anterior cingulate and reward-guided selection of actions. , 2003, Journal of neurophysiology.

[33]  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.

[34]  A. Engel,et al.  Opinion TRENDS in Cognitive Sciences Vol.10 No.12 Single-trial EEG–fMRI reveals the dynamics of cognitive function , 2022 .

[35]  Stanislas Dehaene,et al.  Effortless control: executive attention and conscious feeling of mental effort are dissociable , 2005, Neuropsychologia.

[36]  Daniel Senkowski,et al.  Frontal and Temporal Dysfunction of Auditory Stimulus Processing in Schizophrenia , 2002, NeuroImage.

[37]  M G Coles,et al.  A brain potential manifestation of error-related processing. , 1995, Electroencephalography and clinical neurophysiology. Supplement.

[38]  D. Pandya,et al.  Cingulate cortex of the rhesus monkey: II. Cortical afferents , 1987, The Journal of comparative neurology.

[39]  P. Schlattmann,et al.  Reduced Event-Related Current Density in the Anterior Cingulate Cortex in Schizophrenia , 2001, NeuroImage.

[40]  Robert Schmitt,et al.  Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection , 2004, NeuroImage.

[41]  D. Kahneman.  Attention and Effort , 1973 .

[42]  Gregor Leicht,et al.  Auditory cortex and anterior cingulate cortex sources of the early evoked gamma-band response: Relationship to task difficulty and mental effort , 2007, Neuropsychologia.

[43]  A. Dale,et al.  Dorsal anterior cingulate cortex: A role in reward-based decision making , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[44]  T. Braver,et al.  Anterior Cingulate Cortex and Response Conflict : Effects of Response Modality and Processing Domain , 2022 .

[45]  R. Wilkinson,et al.  Auditory evoked response and reaction time. , 1967, Electroencephalography and clinical neurophysiology.

[46]  C. Elger,et al.  Subdural recordings of the mismatch negativity (MMN) in patients with focal epilepsy. , 2005, Brain : a journal of neurology.

[47]  M. Walton,et al.  The Role of Rat Medial Frontal Cortex in Effort-Based Decision Making , 2002, The Journal of Neuroscience.

[48]  F. Vidal,et al.  Is the ‘error negativity’ specific to errors? , 2000, Biological Psychology.

[49]  R T Wilkinson,et al.  Evoked response and reaction time. , 1967, Acta psychologica.

[50]  Jeffrey L. Cummings,et al.  Contemporary behavioral neurology , 1997 .

[51]  F. Perrin,et al.  Dissociation of temporal and frontal components in the human auditory N1 wave: a scalp current density and dipole model analysis. , 1994, Electroencephalography and clinical neurophysiology.

[52]  W. Gehring,et al.  More attention must be paid: The neurobiology of attentional effort , 2006, Brain Research Reviews.

[53]  J. Voogd,et al.  The human central nervous system , 1978 .

[54]  K. R. Ridderinkhof,et al.  Selective attention to spatial and non-spatial visual stimuli is affected differentially by age: effects on event-related brain potentials and performance data. , 2006, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[55]  Adrian R. Willoughby,et al.  The Medial Frontal Cortex and the Rapid Processing of Monetary Gains and Losses , 2002, Science.

[56]  Gregor Leicht,et al.  Evidence for a close relationship between conscious effort and anterior cingulate cortex activity. , 2005, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[57]  T. Paus,et al.  Regional differences in the effects of task difficulty and motor output on blood flow response in the human anterior cingulate cortex: a review of 107 PET activation studies , 1998, Neuroreport.