Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex

Summary: Words represent a uniquely human information channel—humans use words to express thoughts and feelings and to assign emotional valence to experience. Work from model organisms suggests that valence assignments are carried out in part by the neuromodulators dopamine, serotonin, and norepinep...

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Main Authors: Seth R. Batten, Alec E. Hartle, Leonardo S. Barbosa, Beniamino Hadj-Amar, Dan Bang, Natalie Melville, Tom Twomey, Jason P. White, Alexis Torres, Xavier Celaya, Samuel M. McClure, Gene A. Brewer, Terry Lohrenz, Kenneth T. Kishida, Robert W. Bina, Mark R. Witcher, Marina Vannucci, Brooks Casas, Pearl Chiu, Pendleton R. Montague, William M. Howe
Format: Article
Language:English
Published: Elsevier 2025-01-01
Series:Cell Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2211124724015134
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author Seth R. Batten
Alec E. Hartle
Leonardo S. Barbosa
Beniamino Hadj-Amar
Dan Bang
Natalie Melville
Tom Twomey
Jason P. White
Alexis Torres
Xavier Celaya
Samuel M. McClure
Gene A. Brewer
Terry Lohrenz
Kenneth T. Kishida
Robert W. Bina
Mark R. Witcher
Marina Vannucci
Brooks Casas
Pearl Chiu
Pendleton R. Montague
William M. Howe
author_facet Seth R. Batten
Alec E. Hartle
Leonardo S. Barbosa
Beniamino Hadj-Amar
Dan Bang
Natalie Melville
Tom Twomey
Jason P. White
Alexis Torres
Xavier Celaya
Samuel M. McClure
Gene A. Brewer
Terry Lohrenz
Kenneth T. Kishida
Robert W. Bina
Mark R. Witcher
Marina Vannucci
Brooks Casas
Pearl Chiu
Pendleton R. Montague
William M. Howe
author_sort Seth R. Batten
collection DOAJ
description Summary: Words represent a uniquely human information channel—humans use words to express thoughts and feelings and to assign emotional valence to experience. Work from model organisms suggests that valence assignments are carried out in part by the neuromodulators dopamine, serotonin, and norepinephrine. Here, we ask whether valence signaling by these neuromodulators extends to word semantics in humans by measuring sub-second neuromodulator dynamics in the thalamus (N = 13) and anterior cingulate cortex (N = 6) of individuals evaluating positive, negative, and neutrally valenced words. Our combined results suggest that valenced words modulate neuromodulator release in both the thalamus and cortex, but with region- and valence-specific response patterns, as well as hemispheric dependence for dopamine release in the anterior cingulate. Overall, these experiments provide evidence that neuromodulator-dependent valence signaling extends to word semantics in humans, but not in a simple one-valence-per-transmitter fashion.
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spelling doaj-art-13bd41aa01b24de0bd811b300ab4ce6d2025-01-09T06:13:49ZengElsevierCell Reports2211-12472025-01-01441115162Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortexSeth R. Batten0Alec E. Hartle1Leonardo S. Barbosa2Beniamino Hadj-Amar3Dan Bang4Natalie Melville5Tom Twomey6Jason P. White7Alexis Torres8Xavier Celaya9Samuel M. McClure10Gene A. Brewer11Terry Lohrenz12Kenneth T. Kishida13Robert W. Bina14Mark R. Witcher15Marina Vannucci16Brooks Casas17Pearl Chiu18Pendleton R. Montague19William M. Howe20Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Corresponding authorSchool of Neuroscience, Virginia Tech, Blacksburg, VA 24060, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USADepartment of Statistics, Rice University, Houston, TX 77005, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Center of Functionally Integrative Neuroscience, Aarhus University, 8000 Aarhus, Denmark; Wellcome Centre for Human Neuroimaging, University College London, London WC1N 3BG, UK; Department of Experimental Psychology, University of Oxford, Oxford OX2 6GG, UKFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USADepartment of Psychology, Arizona State University, Tempe, AZ 85281, USADepartment of Psychology, Arizona State University, Tempe, AZ 85281, USADepartment of Psychology, Arizona State University, Tempe, AZ 85281, USADepartment of Psychology, Arizona State University, Tempe, AZ 85281, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USADepartment of Physiology and Pharmacology, Wake Forest School of Medicine, Winston-Salem, NC 27101, USA; Department of Neurosurgery, Wake Forest School of Medicine, Winston-Salem, NC 27101, USADepartment of Neurosurgery, Banner University Medical Center, Phoenix, AZ 85281, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Division of Neurosurgery, Virginia Tech Carilion School of Medicine, Roanoke, VA 24014, USADepartment of Statistics, Rice University, Houston, TX 77005, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Department of Psychology, Virginia Tech, Blacksburg, VA 24060, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Department of Psychology, Virginia Tech, Blacksburg, VA 24060, USAFralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Wellcome Centre for Human Neuroimaging, University College London, London WC1N 3BG, UK; Department of Physics, Virginia Tech, Blacksburg, VA 24061, USA; Corresponding authorSchool of Neuroscience, Virginia Tech, Blacksburg, VA 24060, USA; Corresponding authorSummary: Words represent a uniquely human information channel—humans use words to express thoughts and feelings and to assign emotional valence to experience. Work from model organisms suggests that valence assignments are carried out in part by the neuromodulators dopamine, serotonin, and norepinephrine. Here, we ask whether valence signaling by these neuromodulators extends to word semantics in humans by measuring sub-second neuromodulator dynamics in the thalamus (N = 13) and anterior cingulate cortex (N = 6) of individuals evaluating positive, negative, and neutrally valenced words. Our combined results suggest that valenced words modulate neuromodulator release in both the thalamus and cortex, but with region- and valence-specific response patterns, as well as hemispheric dependence for dopamine release in the anterior cingulate. Overall, these experiments provide evidence that neuromodulator-dependent valence signaling extends to word semantics in humans, but not in a simple one-valence-per-transmitter fashion.http://www.sciencedirect.com/science/article/pii/S2211124724015134CP: Neuroscience
spellingShingle Seth R. Batten
Alec E. Hartle
Leonardo S. Barbosa
Beniamino Hadj-Amar
Dan Bang
Natalie Melville
Tom Twomey
Jason P. White
Alexis Torres
Xavier Celaya
Samuel M. McClure
Gene A. Brewer
Terry Lohrenz
Kenneth T. Kishida
Robert W. Bina
Mark R. Witcher
Marina Vannucci
Brooks Casas
Pearl Chiu
Pendleton R. Montague
William M. Howe
Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex
Cell Reports
CP: Neuroscience
title Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex
title_full Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex
title_fullStr Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex
title_full_unstemmed Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex
title_short Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex
title_sort emotional words evoke region and valence specific patterns of concurrent neuromodulator release in human thalamus and cortex
topic CP: Neuroscience
url http://www.sciencedirect.com/science/article/pii/S2211124724015134
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