Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex
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
Affiliations
Seth R. Batten
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Corresponding author
Alec E. Hartle
School of Neuroscience, Virginia Tech, Blacksburg, VA 24060, USA
Leonardo S. Barbosa
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA
Beniamino Hadj-Amar
Department of Statistics, Rice University, Houston, TX 77005, USA
Dan Bang
Fralin 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, UK
Natalie Melville
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA
Tom Twomey
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA
Jason P. White
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA
Alexis Torres
Department of Psychology, Arizona State University, Tempe, AZ 85281, USA
Xavier Celaya
Department of Psychology, Arizona State University, Tempe, AZ 85281, USA
Samuel M. McClure
Department of Psychology, Arizona State University, Tempe, AZ 85281, USA
Gene A. Brewer
Department of Psychology, Arizona State University, Tempe, AZ 85281, USA
Terry Lohrenz
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA
Kenneth T. Kishida
Department 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, USA
Robert W. Bina
Department of Neurosurgery, Banner University Medical Center, Phoenix, AZ 85281, USA
Mark R. Witcher
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Division of Neurosurgery, Virginia Tech Carilion School of Medicine, Roanoke, VA 24014, USA
Marina Vannucci
Department of Statistics, Rice University, Houston, TX 77005, USA
Brooks Casas
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Department of Psychology, Virginia Tech, Blacksburg, VA 24060, USA
Pearl Chiu
Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Department of Psychology, Virginia Tech, Blacksburg, VA 24060, USA
Pendleton R. Montague
Fralin 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 author
William M. Howe
School of Neuroscience, Virginia Tech, Blacksburg, VA 24060, USA; Corresponding author
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.
