Brain representations of affective valence and intensity in sustained pleasure and pain.

Pleasure and pain are two fundamental, intertwined aspects of human emotions. Pleasurable sensations can reduce subjective feelings of pain and vice versa, and we often perceive the termination of pain as pleasant and the absence of pleasure as unpleasant. This implies the existence of brain systems that integrate them into modality-general representations of affective experiences. Here, we examined representations of affective valence and intensity in an functional MRI (fMRI) study (n = 58) of sustained pleasure and pain. We found that the distinct subpopulations of voxels within the ventromedial and lateral prefrontal cortices, the orbitofrontal cortex, the anterior insula, and the amygdala were involved in decoding affective valence versus intensity. Affective valence and intensity predictive models showed significant decoding performance in an independent test dataset (n = 62). These models were differentially connected to distinct large-scale brain networks-the intensity model to the ventral attention network and the valence model to the limbic and default mode networks. Overall, this study identified the brain representations of affective valence and intensity across pleasure and pain, promoting a systems-level understanding of human affective experiences.

[1]  Philip A. Kragel,et al.  Common and stimulus-type-specific brain representations of negative affect , 2022, Nature Neuroscience.

[2]  H. Kober,et al.  The self in context: brain systems linking mental and physical health , 2021, Nature Reviews Neuroscience.

[3]  T. Wager,et al.  A neuroimaging biomarker for sustained experimental and clinical pain , 2021, Nature Medicine.

[4]  Christine E. Weber,et al.  A study in affect: Predicting valence from fMRI data , 2020, Neuropsychologia.

[5]  Christian Büchel,et al.  The parietal operculum preferentially encodes heat pain and not salience , 2019, bioRxiv.

[6]  K. Berridge Affective valence in the brain: modules or modes? , 2019, Nature Reviews Neuroscience.

[7]  M. Zhuo,et al.  Dual roles of anterior cingulate cortex neurons in pain and pleasure in adult mice , 2018, Molecular Brain.

[8]  T. Wager,et al.  Functional neuroanatomy of peripheral inflammatory physiology: A meta-analysis of human neuroimaging studies , 2018, Neuroscience & Biobehavioral Reviews.

[9]  Howard L Fields,et al.  How expectations influence pain. , 2018, Pain.

[10]  Yueqing Peng,et al.  The coding of valence and identity in the mammalian taste system , 2018, Nature.

[11]  Benjamin F. Grewe,et al.  An amygdalar neural ensemble that encodes the unpleasantness of pain , 2018, Science.

[12]  Patrick Dupont,et al.  Generalizable Representations of Pain, Cognitive Control, and Negative Emotion in Medial Frontal Cortex , 2017, Nature Neuroscience.

[13]  Alexander Hammers,et al.  Macroanatomy and 3D probabilistic atlas of the human insula , 2017, NeuroImage.

[14]  D. Seminowicz,et al.  The Dorsolateral Prefrontal Cortex in Acute and Chronic Pain. , 2017, The journal of pain : official journal of the American Pain Society.

[15]  Douglas H. Wedell,et al.  Representations of modality-general valence for videos and music derived from fMRI data , 2017, NeuroImage.

[16]  Luke J. Chang,et al.  Building better biomarkers: brain models in translational neuroimaging , 2017, Nature Neuroscience.

[17]  E. Rolls Functions of the anterior insula in taste, autonomic, and related functions , 2016, Brain and Cognition.

[18]  K. Davis,et al.  Cognitive behavioral training reverses the effect of pain exposure on brain network activity , 2016, Pain.

[19]  Kelvin O. Lim,et al.  Multivariate Neural Representations of Value during Reward Anticipation and Consummation in the Human Orbitofrontal Cortex , 2016, Scientific Reports.

[20]  Ajay B. Satpute,et al.  The Brain Basis of Positive and Negative Affect: Evidence from a Meta-Analysis of the Human Neuroimaging Literature. , 2016, Cerebral cortex.

[21]  Ajay B. Satpute,et al.  Involvement of Sensory Regions in Affective Experience: A Meta-Analysis , 2015, Front. Psychol..

[22]  E. Navratilova,et al.  Brain Circuits Encoding Reward from Pain Relief , 2015, Trends in Neurosciences.

[23]  Tor D. Wager,et al.  The neuroscience of placebo effects: connecting context, learning and health , 2015, Nature Reviews Neuroscience.

[24]  K. Berridge,et al.  Pleasure Systems in the Brain , 2015, Neuron.

[25]  Daphna Shohamy,et al.  Representation of aversive prediction errors in the human periaqueductal gray , 2014, Nature Neuroscience.

[26]  Jing Wang,et al.  Representations of modality‐specific affective processing for visual and auditory stimuli derived from functional magnetic resonance imaging data , 2014, Human brain mapping.

[27]  Adam K. Anderson,et al.  Population coding of affect across stimuli, modalities and individuals , 2014, Nature Neuroscience.

[28]  John-Dylan Haynes,et al.  Disentangling neural representations of value and salience in the human brain , 2014, Proceedings of the National Academy of Sciences.

[29]  David Borsook,et al.  The human amygdala and pain: Evidence from neuroimaging , 2014, Human brain mapping.

[30]  A. Milton,et al.  The amygdala: securing pleasure and avoiding pain , 2013, Front. Behav. Neurosci..

[31]  J. Wessberg,et al.  Placebo improves pleasure and pain through opposite modulation of sensory processing , 2013, Proceedings of the National Academy of Sciences.

[32]  Joseph W. Kable,et al.  The valuation system: A coordinate-based meta-analysis of BOLD fMRI experiments examining neural correlates of subjective value , 2013, NeuroImage.

[33]  Lisa Feldman Barrett,et al.  Neural Evidence That Human Emotions Share Core Affective Properties , 2013, Psychological science.

[34]  I. Tracey,et al.  The importance of context: When relative relief renders pain pleasant , 2013, PAIN®.

[35]  Daniel C. McNamee,et al.  Category-dependent and category-independent goal-value codes in human ventromedial prefrontal cortex , 2013, Nature Neuroscience.

[36]  Marisa O. Hollinshead,et al.  The organization of the human cerebral cortex estimated by intrinsic functional connectivity. , 2011, Journal of neurophysiology.

[37]  J. Andersson,et al.  Relief as a Reward: Hedonic and Neural Responses to Safety from Pain , 2011, PloS one.

[38]  Lief E. Fenno,et al.  Amygdala circuitry mediating reversible and bidirectional control of anxiety , 2011, Nature.

[39]  F. Grabenhorst,et al.  Value, pleasure and choice in the ventral prefrontal cortex , 2011, Trends in Cognitive Sciences.

[40]  V. Menon,et al.  Saliency, switching, attention and control: a network model of insula function , 2010, Brain Structure and Function.

[41]  Patricia H. Janak,et al.  Substantial similarity in amygdala neuronal activity during conditioned appetitive and aversive emotional arousal , 2009, Proceedings of the National Academy of Sciences.

[42]  M. Corbetta,et al.  The Reorienting System of the Human Brain: From Environment to Theory of Mind , 2008, Neuron.

[43]  I. Tracey,et al.  A common neurobiology for pain and pleasure , 2008, Nature Reviews Neuroscience.

[44]  Rainer Goebel,et al.  Information-based functional brain mapping. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[45]  Joseph J. Paton,et al.  The primate amygdala represents the positive and negative value of visual stimuli during learning , 2006, Nature.

[46]  L. Marks,et al.  Valid across-group comparisons with labeled scales: the gLMS versus magnitude matching , 2004, Physiology & Behavior.

[47]  J. Russell,et al.  Core affect, prototypical emotional episodes, and other things called emotion: dissecting the elephant. , 1999, Journal of personality and social psychology.

[48]  M. Bradley,et al.  Emotion and motivation: measuring affective perception. , 1998, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[49]  R. F. Ling,et al.  Some cautionary notes on the use of principal components regression , 1998 .

[50]  M. Bradley,et al.  Lateralized startle probes in the study of emotion. , 1996, Psychophysiology.

[51]  Lawrence E. Marks,et al.  Magnitude-matching: the measurement of taste and smell , 1988 .

[52]  J. Singer,et al.  Cognitive, social, and physiological determinants of emotional state. , 1962, Psychological review.

[53]  C. Saper The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. , 2002, Annual review of neuroscience.

[54]  Y. Benjamini,et al.  Controlling the false discovery rate: a practical and powerful approach to multiple testing , 1995 .

[55]  Yi Wang,et al.  Neuroscience and Biobehavioral Reviews The role of hedonics in the Human A ff ectome , 2022 .

[56]  Ethan Kross,et al.  Discriminating Neural Representations of Physical and Social Pains: How Multivariate Statistics Challenge the 'shared Representation' Theory of Pain Rogachov a Hanna Jr, and Wager Td. Separate Neural Representations for Physical Pain and Social Rejection , 2022 .