Elsevier

NeuroImage

Volume 152, 15 May 2017, Pages 381-389
NeuroImage

Interactions between the anterior cingulate-insula network and the fronto-parietal network during perceptual decision-making

https://doi.org/10.1016/j.neuroimage.2017.03.014Get rights and content

Abstract

Information processing in the human brain during cognitively demanding goal-directed tasks is thought to involve several large-scale brain networks, including the anterior cingulate-insula network (aCIN) and the fronto-parietal network (FPN). Recent functional MRI (fMRI) studies have provided clues that the aCIN initiates activity changes in the FPN. However, when and how often these networks interact remains largely unknown to date. Here, we systematically examined the oscillatory interactions between the aCIN and the FPN by using the spectral Granger causality analysis of reconstructed brain source signals from the scalp electroencephalography (EEG) recorded from human participants performing a face-house perceptual categorization task. We investigated how the aCIN and the FPN interact, what the temporal sequence of events in these nodes is, and what frequency bands of information flow bind these nodes in networks. We found that beta band (13–30 Hz) and gamma (30–100 Hz) bands of interactions are involved between the aCIN and the FPN during decision-making tasks. In gamma band, the aCIN initiated the Granger causal control over the FPN in 25–225 ms timeframe. In beta band, the FPN achieved a control over the aCIN in 225–425 ms timeframe. These band-specific time-dependent Granger causal controls of the aCIN and the FPN were retained for behaviorally harder decision-making tasks. These findings of times and frequencies of oscillatory interactions in the aCIN and FPN provide us new insights into the general neural mechanisms for sensory information-guided, goal-directed behaviors, including perceptual decision-making processes.

Introduction

Previous neuroimaging investigations have described large-scale, intrinsically organized brain networks underlying a broad range of brain functions, from sensory to motor and to higher-level cognitive functions (Deco et al., 2011, Power et al., 2011, Seeley et al., 2007). The anterior cingulate-insula network (aCIN) and the fronto-parietal network (FPN) are known to be central for cognitive functions (Chen et al., 2013, Uddin, 2015). Functional magnetic resonance imaging (fMRI) studies (Goulden et al., 2014, Sridharan et al., 2008) have demonstrated that the aCIN sends a dominant information flow to the FPN in goal-directed tasks. However, what remains poorly understood is how these networks interact in the time-scales of human cognitive processes.

The individual functional roles of the brain areas in the aCIN have not been precisely resolved. The dorsal anterior cingulate cortex (DACC) of aCIN is known to monitor performance, to signal the need for behavioral adaptation (Ridderinkhof et al., 2004), and in concert with the lateral prefrontal cortex to signal enhanced cognitive control and implement behavioral changes (Egner, 2009, Ridderinkhof et al., 2004). The anterior insula (AI), especially the right AI (R AI), is known as cortical outflow hub of the aCIN to coordinate a change in activity across multiple brain networks, including the FPN (Bonnelle et al., 2012, Menon and Uddin, 2010, Sridharan et al., 2008). Here, we seek to examine the interactions between the aCIN and the FPN in millisecond time-scale. Since multiple frequency bands of neural oscillations have important implications for cognitive processes (Diener et al., 2012, Hipp et al., 2011, Siegel et al., 2012), we also seek to examine the spectra of information flow between the aCIN and the FPN during perceptual decision-making.

We performed electroencephalography (EEG) experiments by using clear and degraded face-house images in perceptual categorization task. We reconstructed waveforms of EEG sources associated with perceptual decisions and applied spectral Granger causality methods (Dhamala et al., 2008a, Dhamala et al., 2008b) to examine at the frequency-specific network interactions between the aCIN and the FPN. We hypothesized that the FPN would be under Granger causal control from the aCIN, this causal influence would change during a course of a perceptual decision, and this casual influence would be retained by the task difficulty.

Section snippets

Participants

In this study, 26 human volunteers (21 males, 5 females) of age ranged from 22 to 38 years (mean: 26.3 years, standard deviation: 4.7 years) participated. Each participant reported that he or she is not currently on medication for mental illness or had a prior history of mental illness affecting decision-making abilities. Out of 26 participants, 4 participants reported that they are left-handed. We collected a written informed consent from each participant prior to the data collection. The

Behavioral results

The overall accuracy percent is defined as the ratio of the number of correctly responded trials to the total number of presented trials multiplied by hundred. The accuracy percent was significantly higher for 0% noise compared with that of 40% and 55% noises. The average response times for 0%, 40%, and 55% noisy stimuli were 434.02 ms, 484.28 ms, and 565.70 ms, respectively. We limited our analysis (electrophysiological results below) within 425 ms to exclude the possibility of finger movement

Discussion

Our analyses demonstrated that beta (~22 Hz) and gamma (~80 Hz) bands of neural activity involve between the aCIN and the FPN interactions for both easier and harder decisions. In behaviorally easier task, our gamma Granger causal outflow calculations in 25–225 ms indicated that the aCIN played a Granger causal control to the FPN consistent with previous fMRI studies (Goulden et al., 2014, Sridharan et al., 2008). In contrast, beta Granger causal outflow calculations further uncovered that the FPN

Acknowledgements

This work was financially supported by a National Science Foundation CAREER award to MD (BCS 0955037).

References (76)

  • N. Goulden et al.

    The salience network is responsible for switching between the default mode network and the central executive network: replication from DCM

    Neuroimage

    (2014)
  • J.F. Hipp et al.

    Oscillatory synchronization in large-scale cortical networks predicts perception

    Neuron

    (2011)
  • O. Jensen et al.

    Human gamma-frequency oscillations associated with attention and memory

    Trends Neurosci.

    (2007)
  • E. Koechlin et al.

    An information theoretical approach to prefrontal executive function

    Trends Cogn. Sci.

    (2007)
  • V. Menon

    Large-scale brain networks and psychopathology: a unifying triple network model

    Trends Cogn. Sci.

    (2011)
  • C.M. Michel et al.

    EEG source imaging

    Clin. Neurophysiol.

    (2004)
  • N.G. Muller et al.

    The functional neuroanatomy of working memory: contributions of human brain lesion studies

    Neuroscience

    (2006)
  • V.T. Nguyen et al.

    Fusing concurrent EEG-fMRI with dynamic causal modeling: application to effective connectivity during face perception

    Neuroimage

    (2014)
  • R.D. Pascual-Marqui et al.

    Low resolution electromagnetic tomography: a new method for localizing electrical activity in the brain

    Int. J. Psychophysiol.

    (1994)
  • J.D. Power et al.

    Functional network organization of the human brain

    Neuron

    (2011)
  • C.N. Riddle et al.

    Digit displacement, not object compliance, underlies task dependent modulations in human corticomuscular coherence

    Neuroimage

    (2006)
  • D. Senkowski et al.

    Crossmodal binding through neural coherence: implications for multisensory processing

    Trends Neurosci.

    (2008)
  • L.Q. Uddin et al.

    The anterior insula in autism: under-connected and under-examined

    Neurosci. Biobehav. Rev.

    (2009)
  • S. Velikova et al.

    Dysfunctional brain circuitry in obsessive-compulsive disorder: source and coherence analysis of EEG rhythms

    Neuroimage

    (2010)
  • K.K. Watson et al.

    Dendritic architecture of the von Economo neurons

    Neuroscience

    (2006)
  • S. Bajaj et al.

    Bridging the gap: dynamic causal modeling and Granger causality analysis of resting state fMRI

    Brain Connect

    (2016)
  • Y. Benjamini et al.

    Controlling the false discovery rate: a practical and powerful approach to multiple testing

    J R. Stat. Soc. B (Methodol.)

    (1995)
  • V. Bonnelle et al.

    Salience network integrity predicts default mode network function after traumatic brain injury

    Proc. Natl. Acad. Sci. USA

    (2012)
  • G. Buzsaki et al.

    Mechanisms of gamma oscillations

    Annu. Rev. Neurosci.

    (2012)
  • V. Chakarov et al.

    Beta-range EEG-EMG coherence with isometric compensation for increasing modulated low-level forces

    J. Neurophysiol.

    (2009)
  • G.B. Chand et al.

    Interactions among the brain default-mode, salience, and central-executive networks during perceptual decision-making of moving dots

    Brain Connect

    (2016)
  • G.B. Chand et al.

    Face or house image perception: beta and gamma bands of oscillations in brain networks carry out decision-making

    Brain Connect

    (2016)
  • A.C. Chen et al.

    Causal interactions between fronto-parietal central executive and default-mode networks in humans

    Proc. Natl. Acad. Sci. USA

    (2013)
  • H.D. Critchley et al.

    Neural systems supporting interoceptive awareness

    Nat. Neurosci.

    (2004)
  • S. Crottaz-Herbette et al.

    Where and when the anterior cingulate cortex modulates attentional response: combined fMRI and ERP evidence

    J. Cogn. Neurosci.

    (2006)
  • A.M. Dale et al.

    Improved localization of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach

    J. Cogn. Neurosci.

    (1993)
  • N.J. Davis et al.

    The role of beta-frequency neural oscillations in motor control

    J. Neurosci.

    (2012)
  • S. Debener et al.

    Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring

    J. Neurosci.

    (2005)
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