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

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^*

^*Corresponding author for this work

Department of Clinical Medicine - Center of Functionally Integrative Neuroscience

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

1 Citation (Scopus)

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.

Original language	English
Article number	115162
Journal	Cell Reports
Volume	44
Issue	1
ISSN	2639-1856
DOIs	https://doi.org/10.1016/j.celrep.2024.115162
Publication status	Published - 28 Jan 2025

Keywords

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

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10.1016/j.celrep.2024.115162

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Batten, S. R., Hartle, A. E., Barbosa, L. S., Hadj-Amar, B., Bang, D., Melville, N., Twomey, T., White, J. P., Torres, A., Celaya, X., McClure, S. M., Brewer, G. A., Lohrenz, T., Kishida, K. T., Bina, R. W., Witcher, M. R., Vannucci, M., Casas, B., Chiu, P., ... Howe, W. M. (2025). Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex. Cell Reports, 44(1), Article 115162. https://doi.org/10.1016/j.celrep.2024.115162

@article{6eb6dc5028db44ffb3d28ceffee26fa6,

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

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 = "anterior cingulate cortex, cortex, CP: Neuroscience, dopamine, electrochemistry, emotional valence, human brain, norepinephrine, serotonin, thalamus, word valence",

author = "Batten, {Seth R.} and Hartle, {Alec E.} and Barbosa, {Leonardo S.} and Beniamino Hadj-Amar and Dan Bang and Natalie Melville and Tom Twomey and White, {Jason P.} and Alexis Torres and Xavier Celaya and McClure, {Samuel M.} and Brewer, {Gene A.} and Terry Lohrenz and Kishida, {Kenneth T.} and Bina, {Robert W.} and Witcher, {Mark R.} and Marina Vannucci and Brooks Casas and Pearl Chiu and Montague, {Pendleton R.} and Howe, {William M.}",

note = "Publisher Copyright: {\textcopyright} 2024 The Author(s)",

year = "2025",

month = jan,

day = "28",

doi = "10.1016/j.celrep.2024.115162",

language = "English",

volume = "44",

journal = "Cell Reports",

issn = "2639-1856",

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number = "1",

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Batten, SR, Hartle, AE, Barbosa, LS, Hadj-Amar, B, Bang, D, Melville, N, Twomey, T, White, JP, Torres, A, Celaya, X, McClure, SM, Brewer, GA, Lohrenz, T, Kishida, KT, Bina, RW, Witcher, MR, Vannucci, M, Casas, B, Chiu, P, Montague, PR & Howe, WM 2025, 'Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex', Cell Reports, vol. 44, no. 1, 115162. https://doi.org/10.1016/j.celrep.2024.115162

Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex. / Batten, Seth R.; Hartle, Alec E.; Barbosa, Leonardo S. et al.
In: Cell Reports, Vol. 44, No. 1, 115162, 28.01.2025.

Research output: Contribution to journal/Conference contribution in journal/Contribution to newspaper › Journal article › Research › peer-review

TY - JOUR

T1 - Emotional words evoke region- and valence-specific patterns of concurrent neuromodulator release in human thalamus and cortex

AU - Batten, Seth R.

AU - Hartle, Alec E.

AU - Barbosa, Leonardo S.

AU - Hadj-Amar, Beniamino

AU - Bang, Dan

AU - Melville, Natalie

AU - Twomey, Tom

AU - White, Jason P.

AU - Torres, Alexis

AU - Celaya, Xavier

AU - McClure, Samuel M.

AU - Brewer, Gene A.

AU - Lohrenz, Terry

AU - Kishida, Kenneth T.

AU - Bina, Robert W.

AU - Witcher, Mark R.

AU - Vannucci, Marina

AU - Casas, Brooks

AU - Chiu, Pearl

AU - Montague, Pendleton R.

AU - Howe, William M.

PY - 2025/1/28

Y1 - 2025/1/28

N2 - 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.

AB - 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.

KW - anterior cingulate cortex

KW - cortex

KW - CP: Neuroscience

KW - dopamine

KW - electrochemistry

KW - emotional valence

KW - human brain

KW - norepinephrine

KW - serotonin

KW - thalamus

KW - word valence

UR - http://www.scopus.com/inward/record.url?scp=85214349372&partnerID=8YFLogxK

U2 - 10.1016/j.celrep.2024.115162

DO - 10.1016/j.celrep.2024.115162

M3 - Journal article

C2 - 39786997

AN - SCOPUS:85214349372

SN - 2639-1856

VL - 44

JO - Cell Reports

JF - Cell Reports

IS - 1

M1 - 115162

ER -

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

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Keywords

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