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Thirst-associated preoptic neurons encode an aversive motivational drive.
Open accessAbstract
Water deprivation produces a drive to seek and consume water. How neural activity creates this motivation remains poorly understood. We used activity-dependent genetic labeling to characterize neurons activated by water deprivation in the hypothalamic median preoptic nucleus (MnPO). Single-cell transcriptional profiling revealed that dehydration-activated MnPO neurons consist of a single excitatory cell type. After optogenetic activation of these neurons, mice drank water and performed an operant lever-pressing task for water reward with rates that scaled with stimulation frequency. This stimulation was aversive, and instrumentally pausing stimulation could reinforce lever-pressing. Activity of these neurons gradually decreased over the course of an operant session. Thus, the activity of dehydration-activated MnPO neurons establishes a scalable, persistent, and aversive internal state that dynamically controls thirst-motivated behavior.
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“These thirst-study authors found that artificial stimulation of neurons in the hypothalamus made mice drink, but that mice would work to turn off the stimulation if given a choice, thus leading the authors to suggest that thirst is essentially aversive.”
From Evolving Concepts of Emotion and Motivation (2018) · cites this paper as Allen et al., 2017
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“To test this, future studies should combine activity - dependent labeling approaches (50–53) with targeted single cell/nucleus transcriptomics (54–56), electrophysiological characterization (45–47), and synaptic profiling (49) to define the molecular identity and functional properties of these two…”
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Chancel, A., Fort, P., Maciel, R. M., Duval, B., Malcey, J., Bellini, S., Schmidt, M. H., & Luppi, P. (2025) · SLEEP · doi:10.1093/sleep/zsaf368 · Cited by 2
Imaging Voltage Globally and in Isofrequency Lamina in Slices of Mouse Ventral Cochlear Nucleus
Ma, Y., Shu, W., Lin, L., Cao, X., Oertel, D., Smith, P. H., & Jackson, M. B. (2023) · eNeuro · doi:10.1523/eneuro.0465-22.2023 · Cited by 2
“A similar but shorter time window was adopted in another study using the TRAP approach (Allen et al., 2017).”
MethodBrain mapping, from molecules to networks
Allen, W. E. (2020) · Science · doi:10.1126/science.abf1711 · Cited by 2
Effects of maternal experience on pup-induced activation of maternal neural circuits in virgin mice
Mayer, H. S., Rosinger, Z. J., Kruithof, V. B., Mishra, S., BlackOwl Sr., A. L., & Stolzenberg, D. S. (2022) · Hormones and Behavior · doi:10.1016/j.yhbeh.2022.105129 · Cited by 2
“At least one week following TRAP induction (Allen et al., 2017), PupTRAP mice underwent a 4-day maternal experience paradigm.”
Zuk, K. E., Cansler, H. L., Wang, J., & Meeks, J. P. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0847-22.2022 · Cited by 2
“However, these and other tools that enable transient immediate-early gene-based labeling have limitations, requiring validation in a circuit and cell typespecific manner (Reijmers and Mayford, 2009; Guenthner et al., 2013; Allen et al., 2017).”
BackgroundChen, M. B., Jiang, X., Quake, S. R., & Südhof, T. C. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/784413 · Cited by 2
Xiphoid nucleus of the midline thalamus controls cold-induced food seekingPreprint
Lal, N. K., Le, P., Aggarwal, S., Zhang, A., Wang, K., Qi, T., Pang, Z., Yang, D., Nudell, V., Yeo, G. W.-M., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.16.533067 · Cited by 2
Zhao, Z., Xu, B., Loomis, C. L., Anthony, S. A., McKie, I., Srigiriraju, A., Bolton, M. M., & Stern, S. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.03.10.584229 · Cited by 2
Zhao, X., Chae, Y. C., Smith, D., Chen, V., DeFelipe, D., Sokol, J. W., Sadangi, A., & Tschida, K. (2024) · eLife · doi:10.7554/elife.94924.1 · Cited by 2
Schneider, K. N., Nota, M. H. C., Lazaro, H., Rijsketic, D. R., Jin, M., Neiswanger, C., Beck, A. I., Ressler, N., Zhang, J. J., Li, A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.03.28.646066 · Cited by 2
Cao, Z., Yung, W., & Ke, Y. (2025) · eLife · doi:10.7554/elife.101302.3 · Cited by 1
A molecularly defined brain circuit module for regulating panic-like defensive state
Zhao, M., Zhang, L., Chen, Z., Zhang, S., Cheng, X., Huang, M., Li, X., Gu, H., Guan, X., Geng, D., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-60529-3 · Cited by 2
“FosTRAP2 (Fos-2A-CreERT2) was designed to express a tamoxifen-inducible Cre recombinase in neurons that are activated during speci fi c behaviors 42 .”
Paundralingga, O. T. K., Jia, S., Farmer, G. E., Toney, G. M., & Cunningham, J. T. (2025) · Journal of Neuroendocrinology · doi:10.1111/jne.70100 · Cited by 1
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Shu, W., & Jackson, M. B. (2025) · Hippocampus · doi:10.1002/hipo.70049 · Cited by 1
“1(iCre/ERT2)Luo , JAX, 030323) (Allen et al. 2017) with the Cre-reporter Ai35-hVoS1.”
Neural Circuits of Social and Physiological Needs
Liu, D., & Dulac, C. G. (2025) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-112723-025633 · Cited by 1
Microglial activity during postnatal development is required for infantile amnesia in mice
Stewart, E., Zielke, L. G., Guillaume, G., de Boer, A., Power, S. D., & Ryan, T. J. (2026) · PLoS Biology · doi:10.1371/journal.pbio.3003538 · Cited by 1
“We crossed a Targeted Recombination In Active Populations (TRAP2) mouse, in which the c-fos promoter drives expression of tamoxifen-inducible Cre recombinase (iCre), with an Ai32 reporter line expressing channelrhodopsin/enhance yellow fluorescent protein (Chr2-EYFP) [50,51].”
Whole-Brain Mapping of Neuronal Activity Associated with Vocal Socialization Behaviors in Adult Mice
Luo, S.-X., Chen, S.-Y., Kuo, H., & Liu, F. (2026) · eNeuro · doi:10.1523/eneuro.0400-25.2026 · Cited by 1
“In the TRAP2 line, a tamoxifen-inducible, improved Cre recombinase (iCreERT2) construct is placed under Fos promoter control (Guenthner et al., 2013; Allen et al., 2017).”
Wake-activated neuronal populations that regulate sleep drive
Joo, W. J., Diester, C. M., Bitsikas, V., Panopoulou, M., Hidalgo, A., Ντέμος, Κ., Pena, R. C. G., Imhof, F., Odstrcil, I., Donato, F., et al. (2026) · Nature · doi:10.1038/s41586-026-10928-3 · Cited by 1
Parabrachial neurons orchestrate cold-induced homeostatic responses
Jung, S., Kondaurova, A., Lee, M., Kwon, J. J., Shin, H., & Kim, S. (2026) · Nature Metabolism · doi:10.1038/s42255-026-01565-1 · Cited by 1
Architecture of the serotonergic projectome in the mouse brain
Song, J. H., Friedmann, D., Wu, Y., Moses, A., Baruni, J., Yuan, Y., Rana, I., Zhao, K., Sten, T. H., Wang, Q., et al. (2026) · Cell · doi:10.1016/j.cell.2026.08.022 · Cited by 1
Behavior of Rats in a Self-Paced Risky Decision-Making Task Based on Definite Probability
Yang, M., Fu, Q., Hu, X., Li, B., & Ma, C. (2022) · Brain Sciences · doi:10.3390/brainsci12060795 · Cited by 1
Huang, J., Crochet, S., Sandi, C., & Petersen, C. C. H. (2024) · Heliyon · doi:10.1016/j.heliyon.2024.e37831 · Cited by 1
“Neuronal activity in the median preoptic nucleus also correlates with thirst and optogenetic stimulation of these neurons also drives water-seeking behavior, apparently through inducing a negative valence state as a negative reinforcer against thirst [45,46].”
BackgroundChemogenetic Modulation of Preoptic Gabre Neurons Decreases Body Temperature and Heart Rate
Wang, Z., Li, L., Li, M., Lu, Z., Qin, L., Naumann, R. K., & Wang, H. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms252313061 · Cited by 2
Redefining Neuropsychiatric Disorder Treatment: Innovations in Drug Design and Targeted Therapy
Kadiri, S. K., Rout, S. K., & Tiwari, P. K. (2025) · Drug Delivery Letters · doi:10.2174/0122103031375761250801075431 · Cited by 1
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“The signals from CVOs converge in the hypothalamic median preoptic nucleus (MnPO) to trigger water seeking/taking behavior through a distributed neural network 7,10 .”
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Using Viral Vectors to Visualize Pain-Related Neural Circuits in Mice
Chen, B., Takatoh, J., & Wang, F. (2022) · Neuromethods · doi:10.1007/978-1-0716-2039-7_12 · Cited by 1
Temporal Association Cortex - A Cortical Hub for Processing Infant VocalizationsPreprint
Tasaka, G., Feigin, L., Maor, I., Groysman, M., DeNardo, L. A., Schiavo, J. K., Froemke, R. C., Luo, L., & Mizrahi, A. (2019) · SSRN Electronic Journal · doi:10.2139/ssrn.3385122 · Cited by 1
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Neural Mechanism of Hunger-gated Food-seeking and EvaluatingPreprint
Lee, Y. H., Kim, Y., Kim, K. S., Song, H. Y., Jang, M., Ha, D.-S., Park, J. S., Jung, S.-H., Lee, J., Kim, K. M., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.23.352187 · Cited by 1
“swallowing behaviour, we defined food-swallowing based on two criteria: (1) presence of both front paws inside the food zone in the bottom view and (2) snout facing toward the centre of the food.”
Metadata
- Authors
- Allen, W. E., DeNardo, L. A., Chen, M. Z., Liu, C. D., Loh, K. M., Fenno, L. E., Ramakrishnan, C., Deisseroth, K., & Luo, L.
- Affiliations
- Stanford University (US)
- Howard Hughes Medical Institute (US)
- Institute for Stem Cell Biology and Regenerative Medicine (US)
- Stanford Medicine (US)
- Corresponding author
- Allen, William E.
- DeNardo, Laura A.
- Chen, Michael Z.
- Deisseroth, Karl
- Luo, Liqun
- ORCID
- Venue
- Science
- Published
- 2017-09-15
- Volume
- 357
- Issue
- 6356
- Pages
- 1149-1155
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC5723384
- OpenAlex
- W2754841759
- Cited by
- 390
- References
- 52
- Citations by year
- 2026: 41 · 2025: 67 · 2024: 67 · 2023: 39 · 2022: 32 · 2021: 38 · 2020: 43 · 2019: 35 · 2018: 23 · 2017: 3
- FWCI
- 17.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Science Foundation (award315464, 1546612)
- National Institutes of Health (award315463, TR01-MH099642, award340292, R01-NS50835)
- Howard Hughes Medical Institute (Hughes Collaborative Innovation Award, award315462)
- Topics
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Regulation of Appetite and Obesity
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
- Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Neuroscience of respiration and sleep
- Keywords
- thirst, water deprivation, median preoptic nucleus, hypothalamus, aversive motivation, optogenetic stimulation, internal state
- MeSH terms
- Animals, Cell Line, Dehydration, Drinking Behavior, Motivation, Neurons, Preoptic Area, Thirst, Gene Expression Profiling, TNF Receptor-Associated Factor 2, Mice, Single-Cell Analysis, Optogenetics
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