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

doi:10.1016/j.celrep.2024.115162

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

Cell Rep. 2025 Jan 7;44(1):115162. doi: 10.1016/j.celrep.2024.115162. Online ahead of print.

Authors

Seth R Batten¹, Alec E Hartle², Leonardo S Barbosa³, Beniamino Hadj-Amar⁴, Dan Bang⁵, Natalie Melville³, Tom Twomey³, Jason P White³, Alexis Torres⁶, Xavier Celaya⁶, Samuel M McClure⁶, Gene A Brewer⁶, Terry Lohrenz³, Kenneth T Kishida⁷, Robert W Bina⁸, Mark R Witcher⁹, Marina Vannucci⁴, Brooks Casas¹⁰, Pearl Chiu¹⁰, Pendleton R Montague¹¹, William M Howe¹²

Affiliations

¹ Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA. Electronic address: [email protected].
² School of Neuroscience, Virginia Tech, Blacksburg, VA 24060, USA.
³ Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA.
⁴ Department of Statistics, Rice University, Houston, TX 77005, USA.
⁵ 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.
⁶ Department of Psychology, Arizona State University, Tempe, AZ 85281, USA.
⁷ 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.
⁸ Department of Neurosurgery, Banner University Medical Center, Phoenix, AZ 85281, USA.
⁹ 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.
¹⁰ Fralin Biomedical Research Institute at VTC, Virginia Tech, Roanoke, VA 24016, USA; Department of Psychology, Virginia Tech, Blacksburg, VA 24060, USA.
¹¹ 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. Electronic address: [email protected].
¹² School of Neuroscience, Virginia Tech, Blacksburg, VA 24060, USA. Electronic address: [email protected].

PMID: 39786997
DOI: 10.1016/j.celrep.2024.115162

Abstract

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.

Keywords: CP: Neuroscience; anterior cingulate cortex; cortex; dopamine; electrochemistry; emotional valence; human brain; norepinephrine; serotonin; thalamus; word valence.