Large-scale functional brain connectivity during emotional engagement as revealed by beta-series correlation analysis.

It has been hypothesized that the medial prefrontal cortex (mPFC) is a hub in the network that mediates appetitive responses whereas the amygdala is thought to mediate both aversive and appetitive processing. Both structures may facilitate adaptive responses to emotional challenge by linking perception, attention, memory, and motor circuits. We provide an initial exploration of these hypotheses by recording simultaneous EEG-fMRI in eleven participants viewing affective pictures. MPFC- and amygdala-seeded functional connectivity maps were generated by applying the beta-series correlation method. The mPFC-seeded correlation map encompassed visual regions, sensorimotor areas, prefrontal cortex, and medial temporal lobe structures, exclusively for pleasant content. For the amygdala-seeded correlation map, a similar set of distributed brain areas appeared in the unpleasant-neutral contrast, with the addition of structures such as the insula and thalamus. A substantially sparser network was recruited for the pleasant-neutral contrast. Using the late positive potential (LPP) to index the intensity of emotional engagement, functional connectivity was found to be stronger in trials with larger LPP. These results demonstrate that mPFC-mediated functional interactions are engaged specifically during appetitive processing, whereas the amygdala is coupled to distinct sets of brain regions during both aversive and appetitive processing. The strength of these interactions varies as a function of the intensity of emotional engagement.

[1]  Malcolm P. Young,,et al.  Analysis of Connectivity: Neural Systems in the Cerebral Cortex , 1994, Reviews in the neurosciences.

[2]  M. Bradley,et al.  Emotion and the motivational brain , 2010, Biological Psychology.

[3]  L. Pessoa,et al.  Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance , 2010, Nature Reviews Neuroscience.

[4]  M. Bradley Natural selective attention: orienting and emotion. , 2009, Psychophysiology.

[5]  Dean Sabatinelli,et al.  Affective picture perception: gender differences in visual cortex? , 2004, Neuroreport.

[6]  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.

[7]  Francesco Versace,et al.  Emotional imagery: Assessing pleasure and arousal in the brain's reward circuitry , 2010, Human brain mapping.

[8]  G L Shulman,et al.  INAUGURAL ARTICLE by a Recently Elected Academy Member:A default mode of brain function , 2001 .

[9]  Elizabeth A. Kensinger,et al.  There are age-related changes in neural connectivity during the encoding of positive, but not negative, information , 2010, Cortex.

[10]  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.

[11]  M. Bradley,et al.  Large-scale neural correlates of affective picture processing. , 2002, Psychophysiology.

[12]  Jin Fan,et al.  Involvement of the anterior cingulate and frontoinsular cortices in rapid processing of salient facial emotional information , 2011, NeuroImage.

[13]  Kristen A. Lindquist,et al.  The brain basis of emotion: A meta-analytic review , 2012, Behavioral and Brain Sciences.

[14]  Lisa Feldman Barrett,et al.  Amygdala task‐evoked activity and task‐free connectivity independently contribute to feelings of arousal , 2014, Human brain mapping.

[15]  Gary H Glover,et al.  Estimating sample size in functional MRI (fMRI) neuroimaging studies: Statistical power analyses , 2002, Journal of Neuroscience Methods.

[16]  A. Keil,et al.  Neural Substrate of the Late Positive Potential in Emotional Processing , 2012, The Journal of Neuroscience.

[17]  Nikolai Axmacher,et al.  Interactions between Medial Temporal Lobe, Prefrontal Cortex, and Inferior Temporal Regions during Visual Working Memory: A Combined Intracranial EEG and Functional Magnetic Resonance Imaging Study , 2008, The Journal of Neuroscience.

[18]  L. Pessoa,et al.  Network Analysis Reveals Increased Integration during Emotional and Motivational Processing , 2012, The Journal of Neuroscience.

[19]  Andreas Keil,et al.  Emotional perception: Correspondence of early and late event-related potentials with cortical and subcortical functional MRI , 2013, Biological Psychology.

[20]  R. Cabeza,et al.  Role of amygdala connectivity in the persistence of emotional memories over time: an event-related FMRI investigation. , 2008, Cerebral cortex.

[21]  John J. Foxe,et al.  Integrative Neuroscience Review Article Identifying a Network of Brain Regions Involved in Aversion-related Processing: a Cross-species Translational Investigation , 2022 .

[22]  S. Bressler,et al.  Large-scale brain networks in cognition: emerging methods and principles , 2010, Trends in Cognitive Sciences.

[23]  B. Bogerts,et al.  Deep Brain Stimulation of Nucleus Accumbens Region in Alcoholism Affects Reward Processing , 2012, PloS one.

[24]  G. Hajcak,et al.  Event-Related Potentials, Emotion, and Emotion Regulation: An Integrative Review , 2010, Developmental neuropsychology.

[25]  Stephan Moratti,et al.  Prefrontal-Occipitoparietal Coupling Underlies Late Latency Human Neuronal Responses to Emotion , 2011, The Journal of Neuroscience.

[26]  M. Bradley,et al.  Brain potentials in affective picture processing: covariation with autonomic arousal and affective report , 2000, Biological Psychology.

[27]  Peter Lang,et al.  Brain processes in emotional perception: Motivated attention , 2004 .

[28]  L. Pessoa Understanding brain networks and brain organization. , 2014, Physics of life reviews.

[29]  G. Glover,et al.  Dissociable Intrinsic Connectivity Networks for Salience Processing and Executive Control , 2007, The Journal of Neuroscience.

[30]  Florin Dolcos,et al.  Effects of aging on functional connectivity of the amygdala during negative evaluation: A network analysis of fMRI data , 2010, Neurobiology of Aging.

[31]  Adam Gazzaley,et al.  Measuring functional connectivity during distinct stages of a cognitive task , 2004, NeuroImage.

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

[33]  M. Bradley,et al.  Emotional perception: correlation of functional MRI and event-related potentials. , 2006, Cerebral cortex.

[34]  Jian Li,et al.  ASEO: A Method for the Simultaneous Estimation of Single-Trial Event-Related Potentials and Ongoing Brain Activities , 2009, IEEE Transactions on Biomedical Engineering.

[35]  Joseph J Paton,et al.  Flexible Neural Representations of Value in the Primate Brain , 2007, Annals of the New York Academy of Sciences.

[36]  A. Bechara,et al.  The insula and drug addiction: an interoceptive view of pleasure, urges, and decision-making , 2010, Brain Structure and Function.

[37]  K. Luan Phan,et al.  Functional Neuroanatomy of Emotion: A Meta-Analysis of Emotion Activation Studies in PET and fMRI , 2002, NeuroImage.

[38]  E. Kensinger,et al.  Age-related differences in functional connectivity during cognitive emotion regulation. , 2014, The journals of gerontology. Series B, Psychological sciences and social sciences.

[39]  Jasna Martinovic,et al.  Electrocortical amplification for emotionally arousing natural scenes: The contribution of luminance and chromatic visual channels , 2015, Biological Psychology.

[40]  J. Price Prefrontal Cortical Networks Related to Visceral Function and Mood , 1999, Annals of the New York Academy of Sciences.

[41]  Tim P. Moran,et al.  The psychometric properties of the late positive potential during emotion processing and regulation , 2013, Brain Research.

[42]  Joseph E LeDoux Rethinking the Emotional Brain , 2012, Neuron.

[43]  P. Lang,et al.  Re‐entrant projections modulate visual cortex in affective perception: Evidence from Granger causality analysis , 2009, Human brain mapping.

[44]  J. Mumford A power calculation guide for fMRI studies. , 2012, Social cognitive and affective neuroscience.

[45]  Vincent D Costa,et al.  Tagging cortical networks in emotion: A topographical analysis , 2012, Human brain mapping.

[46]  Alexandru D. Iordan,et al.  Brain Activity and Network Interactions Linked to Valence‐Related Differences in the Impact of Emotional Distraction , 2015, Cerebral cortex.

[47]  Adam Gazzaley,et al.  Differential coupling of visual cortex with default network or frontal-parietal network based on goals , 2011, Nature Neuroscience.

[48]  W. Singer Cortical dynamics revisited , 2013, Trends in Cognitive Sciences.

[49]  Vera Ferrari,et al.  Repetitive exposure: brain and reflex measures of emotion and attention. , 2011, Psychophysiology.

[50]  Andreas Keil,et al.  The Timing of Emotional Discrimination in Human Amygdala and Ventral Visual Cortex , 2009, The Journal of Neuroscience.

[51]  Vera Ferrari,et al.  Repetitive picture processing: Autonomic and cortical correlates , 2006, Brain Research.

[52]  R. Dolan,et al.  The neurobiology of punishment , 2007, Nature Reviews Neuroscience.

[53]  L. Swanson Cerebral hemisphere regulation of motivated behavior 1 1 Published on the World Wide Web on 2 November 2000. , 2000, Brain Research.

[54]  Qingyang Li,et al.  Emotional perception: Meta-analyses of face and natural scene processing , 2011, NeuroImage.

[55]  Vincent D Costa,et al.  Imaging distributed and massed repetitions of natural scenes: Spontaneous retrieval and maintenance , 2014, Human brain mapping.

[56]  Andreas Keil,et al.  Cross-modal attention capture by affective stimuli: Evidence from event-related potentials , 2007, Cognitive, affective & behavioral neuroscience.

[57]  Adam Gazzaley,et al.  Dynamic adjustments in prefrontal, hippocampal, and inferior temporal interactions with increasing visual working memory load. , 2008, Cerebral cortex.

[58]  M. Bradley,et al.  Measuring emotion: the Self-Assessment Manikin and the Semantic Differential. , 1994, Journal of behavior therapy and experimental psychiatry.

[59]  Francesco Versace,et al.  Pleasure rather than salience activates human nucleus accumbens and medial prefrontal cortex. , 2007, Journal of neurophysiology.