Activation of dorsal raphe serotonin neurons is necessary for waiting for delayed rewards
Open accessAbstract
The forebrain serotonergic system is a crucial component in the control of impulsive behaviors. We previously reported that the activity of serotonin neurons in the midbrain dorsal raphe nucleus increased when rats performed a task that required them to wait for delayed rewards. However, the causal relationship between serotonin neural activity and the tolerance for the delayed reward remained unclear. Here, we test whether the inhibition of serotonin neural activity by the local application of the 5-HT(1A) receptor agonist 8-hydroxy-2-(di-n-propylamino) tetralin in the dorsal raphe nucleus impairs rats' tolerance for delayed rewards. Rats performed a sequential food-water navigation task that required them to visit food and water sites alternately via a tone site to get rewards at both sites after delays. During the short (2 s) delayed reward condition, the inhibition of serotonin neural activity did not significantly influence the numbers of reward choice errors (nosepoke at an incorrect reward site following a conditioned reinforcer tone), reward wait errors (failure to wait for the delayed rewards), or total trials (sum of reward choice errors, reward wait errors, and acquired rewards). By contrast, during the long (7-11 s) delayed reward condition, the number of wait errors significantly increased while the numbers of total trials and choice errors did not significantly change. These results indicate that the activation of dorsal raphe serotonin neurons is necessary for waiting for long delayed rewards and suggest that elevated serotonin activity facilitates waiting behavior when there is the prospect of forthcoming rewards.
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Serotonergic neurons are active while rats wait for delayed rewards and blocking serotonin neuron activity results in premature responses.
“Serotonergic neurons are active while rats wait for delayed rewards and blocking serotonin neuron activity results in premature responses [67].”
From Linking ADHD to the Neural Circuitry of Attention (2017) · cites this paper as [67]
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Cites
The rat brain in stereotaxic coordinates
Palkovits, M. (1983) · Neuropeptides · doi:10.1016/0143-4179(83)90049-5 · Cited by 28,959 · see citing works
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Evenden, J. L. (1999) · Psychopharmacology · doi:10.1007/pl00005481 · Cited by 2,044 · see citing works
Reconciling the role of central serotonin neurons in human and animal behavior
Soubrié, P. (1986) · Behavioral and Brain Sciences · doi:10.1017/s0140525x00022871 · Cited by 993 · see citing works
Opponent interactions between serotonin and dopamine
Daw, N. D., Kakade, S., & Dayan, P. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00052-7 · Cited by 844 · see citing works
Metalearning and neuromodulation
Doya, K. (2002) · Neural Networks · doi:10.1016/s0893-6080(02)00044-8 · Cited by 704 · see citing works
Self-citationOptogenetic interrogation of neural circuits: technology for probing mammalian brain structures
Zhang, F., Gradinaru, V., Adamantidis, A. R., Durand, R., Airan, R. D., de Lecea, L., & Deisseroth, K. (2010) · Nature Protocols · doi:10.1038/nprot.2009.226 · Cited by 692 · see citing works
Artigas, F., Romero, L. I., de Montigny, C., & Blier, P. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10037-0 · Cited by 655 · see citing works
Evenden, J. L., & Ryan, C. N. (1996) · Psychopharmacology · doi:10.1007/s002130050121 · Cited by 636 · see citing works
Serotonin and dopamine: unifying affective, activational, and decision functions.
Cools, R., Nakamura, K., & Daw, N. D. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.121 · Cited by 464 · see citing works
Opponency revisited: competition and cooperation between dopamine and serotonin
Boureau, Y.-L., & Dayan, P. (2011) · Neuropsychopharmacology · doi:10.1038/npp.2010.151 · Cited by 456 · see citing works
Harrison, A. A., Everitt, B. J., & Robbins, T. W. (1997) · Psychopharmacology · doi:10.1007/s002130050410 · Cited by 452 · see citing works
Serotonin in Affective Control
Dayan, P., & Huys, Q. J. M. (2009) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.051508.135607 · Cited by 381 · see citing works
Bari, A., Theobald, D. E., Caprioli, D., Mar, A. C., Aidoo-Micah, A., Dalley, J. W., & Robbins, T. W. (2010) · Neuropsychopharmacology · doi:10.1038/npp.2009.233 · Cited by 325 · see citing works
Neural systems implicated in delayed and probabilistic reinforcement
Cardinal, R. N. (2006) · Neural Networks · doi:10.1016/j.neunet.2006.03.004 · Cited by 318 · see citing works
Invernizzi, R. W., Belli, S., & SAMANIN, R. (1992) · Brain Research · doi:10.1016/0006-8993(92)90914-u · Cited by 275 · see citing works
Activation of Dorsal Raphe Serotonin Neurons Underlies Waiting for Delayed Rewards
Miyazaki, K., Miyazaki, K. W., & Doya, K. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3714-10.2011 · Cited by 257 · see citing works
Self-citationSerotonin and tolerance to delay of reward in rats
Bizot, J., Bihan, C. L., Puech, A. J., Hamon, M., & Thiébot, M.-H. (1999) · Psychopharmacology · doi:10.1007/pl00005485 · Cited by 252 · see citing works
Important messages in the ‘post’: recent discoveries in 5-HT neurone feedback control
Sharp, T., Boothman, L. J., Raley, J., & Quérée, P. (2007) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2007.10.009 · Cited by 190 · see citing works
Control of Breathing by Raphe Obscurus Serotonergic Neurons in Mice
DePuy, S. D., Kanbar, R., Coates, M. B., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4639-10.2011 · Cited by 176 · see citing works
The role of serotonin in the regulation of patience and impulsivity
Miyazaki, K., Miyazaki, K. W., & Doya, K. (2012) · Molecular Neurobiology · doi:10.1007/s12035-012-8232-6 · Cited by 162 · see citing works
Self-citationHarrison, A. A., Everitt, B. J., & Robbins, T. W. (1999) · Behavioural Brain Research · doi:10.1016/s0166-4328(98)00117-x · Cited by 152 · see citing works
Adell, A., Carceller, A., & Artigas, F. (1993) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1993.tb13390.x · Cited by 137 · see citing works
Newman‐Tancredi, A., Martel, J.-C., Assié, M. B., Buritova, J., Lauressergues, E., Cosi, C., Heusler, P., Slot, L. A. B., Colpaert, F. C., Vacher, B., et al. (2009) · British Journal of Pharmacology · doi:10.1111/j.1476-5381.2008.00001.x · Cited by 128 · see citing works
Carli, M., & SAMANIN, R. (2000) · Psychopharmacology · doi:10.1007/s002139900368 · Cited by 124 · see citing works
Haj�s, M., Gartside, S. E., & Sharp, T. (1995) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/bf00170162 · Cited by 117 · see citing works
Assié, M., Bardin, L., Auclair, A. L., Carilla-Durand, E., Depoortère, R., Koek, W., Kleven, M. S., Colpaert, F. C., Vacher, B., & Newman‐Tancredi, A. (2010) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145709991222 · Cited by 106 · see citing works
Bizot, J., Thiébot, M.-H., Bihan, C. L., Soubrié, P., & Simon, P. (1988) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1016/s0022-3565(25)22218-2 · Cited by 99 · see citing works
A microdialysis study of the in vivo release of 5‐HT in the median raphe nucleus of the rat
Adell, A., & Artigas, F. (1998) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0702206 · Cited by 65 · see citing works
Activation of the central serotonergic system in response to delayed but not omitted rewards
Miyazaki, K. W., Miyazaki, K., & Doya, K. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07480.x · Cited by 59 · see citing works
Self-citationWaterhouse, B. D., Devilbiss, D. M., Seiple, S., & Markowitz, R. S. (2004) · Brain Research · doi:10.1016/j.brainres.2003.11.030 · Cited by 56 · see citing works
Hajós, M., Hoffmann, W. E., Tetko, I. V., et al. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(01)01751-7 · Cited by 53 · see citing works
Casanovas, J. M., Berton, O., Celada, P., & Artigas, F. (2000) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s002100000291 · Cited by 38 · see citing works
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Ullsperger, M., Danielmeier, C., & Jocham, G. (2014) · Physiological Reviews · doi:10.1152/physrev.00041.2012 · Cited by 634 · see citing works
Anatomically defined and functionally distinct dorsal raphe serotonin sub-systems
Ren, J., Friedmann, D., Xiong, J., Liu, C. D., Ferguson, B. R., Weerakkody, T., DeLoach, K. E., Ran, C., Pun, A., Sun, Y., et al. (2018) · Cell · doi:10.1016/j.cell.2018.07.043 · Cited by 498 · see citing works
Dorsal raphe neurons signal reward through 5-HT and glutamate
Liu, Z., Zhou, J., Li, Y., Hu, F., Lu, Y., Ma, M., Feng, Q., Zhang, J.-E., Wang, D., Zeng, J., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.02.010 · Cited by 469 · see citing works
Overlapping neural systems represent cognitive effort and reward anticipation
Vassena, E., Silvetti, M., Boehler, C. N., Achten, E., Fias, W., & Verguts, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091008 · Cited by 200 · see citing works
Linking ADHD to the Neural Circuitry of Attention
Mueller, A., Hong, D. S., Shepard, S., & Moore, T. (2017) · Trends in Cognitive Sciences · doi:10.1016/j.tics.2017.03.009 · Cited by 158 · see citing works
Serotonin regulation of behavior via large-scale neuromodulation of serotonin receptor networks
Salvan, P., Fonseca, M., Winkler, A. M., Beauchamp, A., Lerch, J. P., & Johansen-Berg, H. (2023) · Nature Neuroscience · doi:10.1038/s41593-022-01213-3 · Cited by 101 · see citing works
Yu, C., Garcia-Olivares, J., Candler, S., Schwabe, S., & Maletic, V. (2020) · Journal of Experimental Pharmacology · doi:10.2147/jep.s256586 · Cited by 96 · see citing works
Fischer, A. G., Endrass, T., Reuter, M., Kubisch, C., & Ullsperger, M. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.5124-14.2015 · Cited by 29 · see citing works
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Desrochers, S. S., Spring, M. G., & Nautiyal, K. M. (2022) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2022.791749 · Cited by 29 · see citing works
- Authors
- Miyazaki, K. W., Miyazaki, K., & Doya, K.
- Affiliations
- Okinawa Institute of Science and Technology Graduate University (JP)
- ORCID
- Doya, K.
- Venue
- Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2012-08-01
- Volume
- 32
- Issue
- 31
- Pages
- 10451-10457
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6621383
- OpenAlex
- W1978699011
- Cited by
- 106
- References
- 34
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 9 · 2023: 8 · 2022: 6 · 2021: 3 · 2020: 10 · 2019: 5 · 2018: 5 · 2017: 5 · 2016: 15 · 2015: 10 · 2014: 11 · 2013: 10 · 2012: 1
- FWCI
- 4.22
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Journal of Neuroscience (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministry of Education, Culture, Sports, Science and Technology (23120007)
- Japan Society for the Promotion of Science (24730643, 23120007)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- dorsal raphe nucleus, serotonergic neurons, 5-HT1A receptor agonist, 8-OH-DPAT, impulsive behavior
- MeSH terms
- Action Potentials, Analysis of Variance, Animals, Choice Behavior, Conditioning, Operant, Male, Raphe Nuclei, Reward, Serotonin, Time Factors, Serotonin Receptor Agonists, 8-Hydroxy-2-(di-n-propylamino)tetralin, Microdialysis, Rats, Long-Evans, Rats, Serotonergic Neurons
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