Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making

Research output: Contribution to journalJournal articleResearchpeer-review

Standard

Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making. / Luo, Qiang; Kanen, Jonathan W.; Bari, Andrea; Skandali, Nikolina; Langley, Christelle; Knudsen, Gitte Moos; Alsiö, Johan; Phillips, Benjamin U.; Sahakian, Barbara J.; Cardinal, Rudolf N.; Robbins, Trevor W.

In: Neuropsychopharmacology, Vol. 49, No. 3, 2024, p. 600-608.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Luo, Q, Kanen, JW, Bari, A, Skandali, N, Langley, C, Knudsen, GM, Alsiö, J, Phillips, BU, Sahakian, BJ, Cardinal, RN & Robbins, TW 2024, 'Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making', Neuropsychopharmacology, vol. 49, no. 3, pp. 600-608. https://doi.org/10.1038/s41386-023-01762-6

APA

Luo, Q., Kanen, J. W., Bari, A., Skandali, N., Langley, C., Knudsen, G. M., Alsiö, J., Phillips, B. U., Sahakian, B. J., Cardinal, R. N., & Robbins, T. W. (2024). Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making. Neuropsychopharmacology, 49(3), 600-608. https://doi.org/10.1038/s41386-023-01762-6

Vancouver

Luo Q, Kanen JW, Bari A, Skandali N, Langley C, Knudsen GM et al. Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making. Neuropsychopharmacology. 2024;49(3):600-608. https://doi.org/10.1038/s41386-023-01762-6

Author

Luo, Qiang ; Kanen, Jonathan W. ; Bari, Andrea ; Skandali, Nikolina ; Langley, Christelle ; Knudsen, Gitte Moos ; Alsiö, Johan ; Phillips, Benjamin U. ; Sahakian, Barbara J. ; Cardinal, Rudolf N. ; Robbins, Trevor W. / Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making. In: Neuropsychopharmacology. 2024 ; Vol. 49, No. 3. pp. 600-608.

Bibtex

@article{1921414f2d184bbcba236936a05aaefd,
title = "Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making",
abstract = "Serotonin is critical for adapting behavior flexibly to meet changing environmental demands. Cognitive flexibility is important for successful attainment of goals, as well as for social interactions, and is frequently impaired in neuropsychiatric disorders, including obsessive–compulsive disorder. However, a unifying mechanistic framework accounting for the role of serotonin in behavioral flexibility has remained elusive. Here, we demonstrate common effects of manipulating serotonin function across two species (rats and humans) on latent processes supporting choice behavior during probabilistic reversal learning, using computational modelling. The findings support a role of serotonin in behavioral flexibility and plasticity, indicated, respectively, by increases or decreases in choice repetition ({\textquoteleft}stickiness{\textquoteright}) or reinforcement learning rates following manipulations intended to increase or decrease serotonin function. More specifically, the rate at which expected value increased following reward and decreased following punishment (reward and punishment {\textquoteleft}learning rates{\textquoteright}) was greatest after sub-chronic administration of the selective serotonin reuptake inhibitor (SSRI) citalopram (5 mg/kg for 7 days followed by 10 mg/kg twice a day for 5 days) in rats. Conversely, humans given a single dose of an SSRI (20 mg escitalopram), which can decrease post-synaptic serotonin signalling, and rats that received the neurotoxin 5,7-dihydroxytryptamine (5,7-DHT), which destroys forebrain serotonergic neurons, exhibited decreased reward learning rates. A basic perseverative tendency ({\textquoteleft}stickiness{\textquoteright}), or choice repetition irrespective of the outcome produced, was likewise increased in rats after the 12-day SSRI regimen and decreased after single dose SSRI in humans and 5,7-DHT in rats. These common effects of serotonergic manipulations on rats and humans—identified via computational modelling—suggest an evolutionarily conserved role for serotonin in plasticity and behavioral flexibility and have clinical relevance transdiagnostically for neuropsychiatric disorders.",
author = "Qiang Luo and Kanen, {Jonathan W.} and Andrea Bari and Nikolina Skandali and Christelle Langley and Knudsen, {Gitte Moos} and Johan Alsi{\"o} and Phillips, {Benjamin U.} and Sahakian, {Barbara J.} and Cardinal, {Rudolf N.} and Robbins, {Trevor W.}",
note = "Publisher Copyright: {\textcopyright} 2023, The Author(s).",
year = "2024",
doi = "10.1038/s41386-023-01762-6",
language = "English",
volume = "49",
pages = "600--608",
journal = "Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology",
issn = "0893-133X",
publisher = "Springer Nature [academic journals on nature.com]",
number = "3",

}

RIS

TY - JOUR

T1 - Comparable roles for serotonin in rats and humans for computations underlying flexible decision-making

AU - Luo, Qiang

AU - Kanen, Jonathan W.

AU - Bari, Andrea

AU - Skandali, Nikolina

AU - Langley, Christelle

AU - Knudsen, Gitte Moos

AU - Alsiö, Johan

AU - Phillips, Benjamin U.

AU - Sahakian, Barbara J.

AU - Cardinal, Rudolf N.

AU - Robbins, Trevor W.

N1 - Publisher Copyright: © 2023, The Author(s).

PY - 2024

Y1 - 2024

N2 - Serotonin is critical for adapting behavior flexibly to meet changing environmental demands. Cognitive flexibility is important for successful attainment of goals, as well as for social interactions, and is frequently impaired in neuropsychiatric disorders, including obsessive–compulsive disorder. However, a unifying mechanistic framework accounting for the role of serotonin in behavioral flexibility has remained elusive. Here, we demonstrate common effects of manipulating serotonin function across two species (rats and humans) on latent processes supporting choice behavior during probabilistic reversal learning, using computational modelling. The findings support a role of serotonin in behavioral flexibility and plasticity, indicated, respectively, by increases or decreases in choice repetition (‘stickiness’) or reinforcement learning rates following manipulations intended to increase or decrease serotonin function. More specifically, the rate at which expected value increased following reward and decreased following punishment (reward and punishment ‘learning rates’) was greatest after sub-chronic administration of the selective serotonin reuptake inhibitor (SSRI) citalopram (5 mg/kg for 7 days followed by 10 mg/kg twice a day for 5 days) in rats. Conversely, humans given a single dose of an SSRI (20 mg escitalopram), which can decrease post-synaptic serotonin signalling, and rats that received the neurotoxin 5,7-dihydroxytryptamine (5,7-DHT), which destroys forebrain serotonergic neurons, exhibited decreased reward learning rates. A basic perseverative tendency (‘stickiness’), or choice repetition irrespective of the outcome produced, was likewise increased in rats after the 12-day SSRI regimen and decreased after single dose SSRI in humans and 5,7-DHT in rats. These common effects of serotonergic manipulations on rats and humans—identified via computational modelling—suggest an evolutionarily conserved role for serotonin in plasticity and behavioral flexibility and have clinical relevance transdiagnostically for neuropsychiatric disorders.

AB - Serotonin is critical for adapting behavior flexibly to meet changing environmental demands. Cognitive flexibility is important for successful attainment of goals, as well as for social interactions, and is frequently impaired in neuropsychiatric disorders, including obsessive–compulsive disorder. However, a unifying mechanistic framework accounting for the role of serotonin in behavioral flexibility has remained elusive. Here, we demonstrate common effects of manipulating serotonin function across two species (rats and humans) on latent processes supporting choice behavior during probabilistic reversal learning, using computational modelling. The findings support a role of serotonin in behavioral flexibility and plasticity, indicated, respectively, by increases or decreases in choice repetition (‘stickiness’) or reinforcement learning rates following manipulations intended to increase or decrease serotonin function. More specifically, the rate at which expected value increased following reward and decreased following punishment (reward and punishment ‘learning rates’) was greatest after sub-chronic administration of the selective serotonin reuptake inhibitor (SSRI) citalopram (5 mg/kg for 7 days followed by 10 mg/kg twice a day for 5 days) in rats. Conversely, humans given a single dose of an SSRI (20 mg escitalopram), which can decrease post-synaptic serotonin signalling, and rats that received the neurotoxin 5,7-dihydroxytryptamine (5,7-DHT), which destroys forebrain serotonergic neurons, exhibited decreased reward learning rates. A basic perseverative tendency (‘stickiness’), or choice repetition irrespective of the outcome produced, was likewise increased in rats after the 12-day SSRI regimen and decreased after single dose SSRI in humans and 5,7-DHT in rats. These common effects of serotonergic manipulations on rats and humans—identified via computational modelling—suggest an evolutionarily conserved role for serotonin in plasticity and behavioral flexibility and have clinical relevance transdiagnostically for neuropsychiatric disorders.

U2 - 10.1038/s41386-023-01762-6

DO - 10.1038/s41386-023-01762-6

M3 - Journal article

C2 - 37914893

AN - SCOPUS:85175379955

VL - 49

SP - 600

EP - 608

JO - Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

JF - Neuropsychopharmacology : official publication of the American College of Neuropsychopharmacology

SN - 0893-133X

IS - 3

ER -

ID: 380213527