Reciprocal Interactions of the SMA and Cingulate Cortex Sustain Premovement Activity for Voluntary Actions

Voluntary action is one of the core functions of the human brain, and is accompanied by the well known readiness potential or Bereitschaftspotential. A network of cortical areas is responsible for the motor preparation process, including the anterior mid-cingulate cortex (aMCC) and the SMA. However, the relationship between activity in these regions during movement preparation and the readiness potential is poorly understood. We examined this relationship by integrating simultaneously acquired EEG and fMRI through computational modeling. We first observed that global field power of premovement neural activity showed a specific correlation with BOLD responses in the aMCC. We then used dynamic causal modeling to infer premovement interactions between these regions and their relationship to the premovement neural activity underlying the readiness potential. These analyses suggest that SMA and aMCC have strong reciprocal connections that act to sustain each other's activity, and that this interaction is mediated during movement preparation according to the readiness potential amplitude, as reflected in global cortical field power. Our study suggests that the reciprocal connections between SMA and aMCC are important to maintain the sustained activity of the readiness potential before movement and lead to a weak system instability at movement onset. We suggest that the effective connectivity of this network underlies its functional role in the preparation of self-generated actions.

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

[2]  P. Haggard Human volition: towards a neuroscience of will , 2008, Nature Reviews Neuroscience.

[3]  D. Lehmann,et al.  Reference-free identification of components of checkerboard-evoked multichannel potential fields. , 1980, Electroencephalography and clinical neurophysiology.

[4]  A. Cools,et al.  Dipole source analysis suggests selective modulation of the supplementary motor area contribution to the readiness potential. , 1996, Electroencephalography and clinical neurophysiology.

[5]  Karl J. Friston,et al.  Perception and self-organized instability , 2012, Front. Comput. Neurosci..

[6]  G. Lindinger,et al.  Supplementary Motor Area Activation Preceding Voluntary Movement Is Detectable with a Whole-Scalp Magnetoencephalography System , 2000, NeuroImage.

[7]  Karl J. Friston,et al.  Nonlinear Dynamic Causal Models for Fmri Nonlinear Dynamic Causal Models for Fmri Nonlinear Dynamic Causal Models for Fmri , 2022 .

[8]  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.

[9]  Ewald Moser,et al.  The preparation and readiness for voluntary movement: a high-field event-related fMRI study of the Bereitschafts-BOLD response , 2003, NeuroImage.

[10]  Ewald Moser,et al.  Premovement activity of the pre-supplementary motor area and the readiness for action: studies of time-resolved event-related functional MRI. , 2005, Human movement science.

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

[12]  P. Fox,et al.  The role of anterior midcingulate cortex in cognitive motor control , 2014, Human brain mapping.

[13]  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.

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

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

[16]  Niall W. Duncan,et al.  Overview of potential procedural and participant-related confounds for neuroimaging of the resting state. , 2013, Journal of psychiatry & neuroscience : JPN.

[17]  Ewald Moser,et al.  The selection of intended actions and the observation of others' actions: A time-resolved fMRI study , 2006, NeuroImage.

[18]  Michael Breakspear,et al.  A Canonical Model of Multistability and Scale-Invariance in Biological Systems , 2012, PLoS Comput. Biol..

[19]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

[20]  C. Marsden,et al.  Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson's disease subjects. , 1995, Brain : a journal of neurology.

[21]  Claus Lamm,et al.  Time-resolved analysis of fMRI signal changes using Brain Activation Movies , 2008, Journal of Neuroscience Methods.

[22]  P. Brotchie,et al.  Motor function of the monkey globus pallidus. 1. Neuronal discharge and parameters of movement. , 1991, Brain : a journal of neurology.

[23]  P. Brotchie,et al.  Motor function of the monkey globus pallidus. 2. Cognitive aspects of movement and phasic neuronal activity. , 1991, Brain : a journal of neurology.

[24]  Vinh Thai Nguyen,et al.  The superior temporal sulcus and the N170 during face processing: Single trial analysis of concurrent EEG–fMRI , 2014, NeuroImage.

[25]  T. Paus Primate anterior cingulate cortex: Where motor control, drive and cognition interface , 2001, Nature Reviews Neuroscience.

[26]  J. A. Scott Kelso,et al.  Instabilities and Phase Transitions in Human Brain and Behavior , 2010, Front. Hum. Neurosci..

[27]  Keiji Tanaka,et al.  Neuronal Correlates of Goal-Based Motor Selection in the Prefrontal Cortex , 2003, Science.

[28]  Christian Seifert,et al.  Single-trial coupling of EEG and fMRI reveals the involvement of early anterior cingulate cortex activation in effortful decision making , 2008, NeuroImage.

[29]  B. Feige,et al.  The Role of Higher-Order Motor Areas in Voluntary Movement as Revealed by High-Resolution EEG and fMRI , 1999, NeuroImage.

[30]  Karl J. Friston,et al.  Interhemispheric Integration of Visual Processing during Task-Driven Lateralization , 2007, The Journal of Neuroscience.

[31]  Takashi Hanakawa,et al.  Generators of Movement-Related Cortical Potentials: fMRI-Constrained EEG Dipole Source Analysis , 2002, NeuroImage.

[32]  Simon B. Eickhoff,et al.  Dynamic intra- and interhemispheric interactions during unilateral and bilateral hand movements assessed with fMRI and DCM , 2008, NeuroImage.

[33]  Kenneth Hugdahl,et al.  Realignment parameter-informed artefact correction for simultaneous EEG–fMRI recordings , 2009, NeuroImage.

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

[35]  K. Zilles,et al.  The "what" and "when" of self-initiated movements. , 2013, Cerebral cortex.

[36]  Rupert Lanzenberger,et al.  The suppressive influence of SMA on M1 in motor imagery revealed by fMRI and dynamic causal modeling , 2008, NeuroImage.

[37]  M. Breakspear Nonlinear phase desynchronization in human electroencephalographic data , 2002, Human brain mapping.

[38]  G. Baselli,et al.  Single sweep analysis of visual evoked potentials through a model of parametric identification , 1987, Biological Cybernetics.

[39]  R. Passingham,et al.  Self-initiated versus externally triggered movements. II. The effect of movement predictability on regional cerebral blood flow. , 2000, Brain : a journal of neurology.

[40]  Alan C. Evans,et al.  Role of the human anterior cingulate cortex in the control of oculomotor, manual, and speech responses: a positron emission tomography study. , 1993, Journal of neurophysiology.

[41]  Simon B. Eickhoff,et al.  Network dynamics engaged in the modulation of motor behavior in healthy subjects , 2013, NeuroImage.

[42]  M. Hallett,et al.  What is the Bereitschaftspotential? , 2006, Clinical Neurophysiology.

[43]  Michael Breakspear,et al.  Fusing concurrent EEG–fMRI with dynamic causal modeling: Application to effective connectivity during face perception , 2014, NeuroImage.

[44]  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.

[45]  A. Roskies,et al.  How does neuroscience affect our conception of volition? , 2010, Annual review of neuroscience.

[46]  J. Tanji,et al.  Role for cingulate motor area cells in voluntary movement selection based on reward. , 1998, Science.

[47]  William D. Penny,et al.  Comparing Dynamic Causal Models using AIC, BIC and Free Energy , 2012, NeuroImage.

[48]  O. Sporns,et al.  Rich-Club Organization of the Human Connectome , 2011, The Journal of Neuroscience.

[49]  Elizabeth B. Liddle,et al.  Motion-related artefacts in EEG predict neuronally plausible patterns of activation in fMRI data , 2012, NeuroImage.

[50]  Michael Breakspear,et al.  Critical Fluctuations in Cortical Models Near Instability , 2012, Front. Physio..

[51]  P. Strick,et al.  Motor areas of the medial wall: a review of their location and functional activation. , 1996, Cerebral cortex.

[52]  R. Iansek,et al.  Movement-related potentials in Parkinson's disease. Presence and predictability of temporal and spatial cues. , 1995, Brain : a journal of neurology.

[53]  Karl J. Friston The free-energy principle: a unified brain theory? , 2010, Nature Reviews Neuroscience.

[54]  R. Iansek,et al.  Movement-related potentials in Parkinson's disease. Motor imagery and movement preparation. , 1997, Brain : a journal of neurology.

[55]  T. Mima,et al.  Human presupplementary motor area is active before voluntary movement: subdural recording of Bereitschaftspotential from medial frontal cortex , 2000, Experimental Brain Research.

[56]  H. C Lau,et al.  Willed action and attention to the selection of action , 2004, NeuroImage.

[57]  L. Deecke,et al.  The Preparation and Execution of Self-Initiated and Externally-Triggered Movement: A Study of Event-Related fMRI , 2002, NeuroImage.

[58]  N. Logothetis,et al.  Neurophysiological investigation of the basis of the fMRI signal , 2001, Nature.

[59]  Karl J. Friston,et al.  Modulation of excitatory synaptic coupling facilitates synchronization and complex dynamics in a biophysical model of neuronal dynamics , 2003, Network.