Adult-born neurons boost odor-reward association
Open accessAbstract
Olfaction is an important sensory modality driving fundamental behaviors. During odor-dependent learning, a positive value is commonly assigned to an odorant, and multiple forms of plasticity are involved when such odor-reward associations are formed. In rodents, one of the mechanisms underlying plasticity in the olfactory bulb consists in recruiting new neurons daily throughout life. However, it is still unknown whether adult-born neurons might participate in encoding odor value. Here, we demonstrate that exposure to reward-associated odors specifically increases activity of adult-born neurons but not preexisting neurons. Remarkably, adult-born neuron activation during rewarded odor presentation heightens discrimination learning and enhances the ability to update the odor value during reversal association. Moreover, in some cases, activation of this interneuron population can trigger olfactory learning without sensory stimulation. Taken together, our results show a specific involvement of adult-born neurons in facilitating odor-reward association during adaptive learning.
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Adult-born granule cells support flexible olfactory behaviors in adulthood.
“while adult-born GCs are well-known to support flexible olfactory behaviors in adulthood [19,50–52]”
From Positive early-life olfactory memory is rooted in the olfactory bulb and triggers large-scale changes beyond the olfactory system (2026) · cites this paper as [50]
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Cites
Roles of continuous neurogenesis in the structural and functional integrity of the adult forebrain
Imayoshi, I., Sakamoto, M., Ohtsuka, T., Takao, K., Miyakawa, T., Yamaguchi, M., Mori, K., Ikeda, T., Itohara, S., & Kageyama, R. (2008) · Nature Neuroscience · doi:10.1038/nn.2185 · Cited by 1,054 · see citing works
Schultz, W. (2007) · Trends in Neurosciences · doi:10.1016/j.tins.2007.03.007 · Cited by 1,028 · see citing works
Becoming a new neuron in the adult olfactory bulb
Carleton, A., Petreanu, L., Lansford, R. D., Álvarez-Buylla, A., & Lledo, P. (2003) · Nature Neuroscience · doi:10.1038/nn1048 · Cited by 808 · see citing works
Self-citationRochefort, C., Gheusi, G., Vincent, J., & Lledo, P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-07-02679.2002 · Cited by 678 · see citing works
Self-citationEnwere, E. K., Shingo, T., Gregg, C., Fujikawa, H., Ohta, S., & Weiss, S. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.2751-04.2004 · Cited by 549 · see citing works
Silencing Neurons: Tools, Applications, and Experimental Constraints
Wiegert, J. S., Mahn, M., Prigge, M., Printz, Y., & Yizhar, O. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.050 · Cited by 306 · see citing works
Cortical Feedback Control of Olfactory Bulb Circuits
Boyd, A. M., Sturgill, J. F., Poo, C., & Isaacson, J. S. (2012) · Neuron · doi:10.1016/j.neuron.2012.10.020 · Cited by 290 · see citing works
Is adult neurogenesis essential for olfaction?
Lazarini, F., & Lledo, P. (2010) · Trends in Neurosciences · doi:10.1016/j.tins.2010.09.006 · Cited by 285 · see citing works
Self-citationThe participation of cortical amygdala in innate, odour-driven behaviour
Root, C. M., Denny, C. A., Hen, R., & Axel, R. (2014) · Nature · doi:10.1038/nature13897 · Cited by 281 · see citing works
The auditory cortex mediates the perceptual effects of acoustic temporal expectation
Jaramillo, S., & Zador, A. M. (2010) · Nature Neuroscience · doi:10.1038/nn.2688 · Cited by 267 · see citing works
Olfactory perceptual learning requires adult neurogenesis
Moreno, M., Linster, C., Escanilla, O., Sacquet, J., Didier, A., & Mandairon, N. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0907063106 · Cited by 265 · see citing works
Breton‐Provencher, V., Lemasson, M., Peralta, M. R., & Saghatelyan, A. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.3606-09.2009 · Cited by 263 · see citing works
Adult neurogenesis promotes synaptic plasticity in the olfactory bulb
Nissant, A., Bardy, C., Katagiri, H., Murray, K., & Lledo, P. (2009) · Nature Neuroscience · doi:10.1038/nn.2298 · Cited by 252 · see citing works
Self-citationFunctional Properties of Cortical Feedback Projections to the Olfactory Bulb
Markopoulos, F., Rokni, D., Gire, D. H., & Murthy, V. N. (2012) · Neuron · doi:10.1016/j.neuron.2012.10.028 · Cited by 220 · see citing works
Lemasson, M., Saghatelyan, A., Olivo-Marin, J.-C., & Lledo, P.-M. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1114-05.2005 · Cited by 218 · see citing works
Self-citationMagavi, S. S. P., Mitchell, B. D., Szentirmai, O., Carter, B. S., & Macklis, J. D. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2250-05.2005 · Cited by 215 · see citing works
Activation of adult-born neurons facilitates learning and memory
Alonso, M., Lepousez, G., Wagner, S., Bardy, C., Gabellec, M., Torquet, N., & Lledo, P. (2012) · Nature Neuroscience · doi:10.1038/nn.3108 · Cited by 215 · see citing works
Self-citationCellular and Behavioral Effects of Cranial Irradiation of the Subventricular Zone in Adult Mice
Lazarini, F., Mouthon, M., Gheusi, G., de Chaumont, F., Olivo‐Marín, J., Lamarque, S., Abrous, D. N., Boussin, F. D., & Lledo, P. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007017 · Cited by 204 · see citing works
Self-citationAversion and Attraction through Olfaction
Li, Q., & Liberles, S. D. (2015) · Current Biology · doi:10.1016/j.cub.2014.11.044 · Cited by 200 · see citing works
Neuronal pattern separation in the olfactory bulb improves odor discrimination learning
Gschwend, O., Abraham, N. M., Lagier, S., Begnaud, F., Rodríguez, I., & Carleton, A. (2015) · Nature Neuroscience · doi:10.1038/nn.4089 · Cited by 198 · see citing works
Continuous neurogenesis in the adult forebrain is required for innate olfactory responses
Sakamoto, M., Imayoshi, I., Ohtsuka, T., Yamaguchi, M., Mori, K., & Kageyama, R. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1018782108 · Cited by 198 · see citing works
The Impact of Adult Neurogenesis on Olfactory Bulb Circuits and Computations
Lepousez, G., Valley, M. T., & Lledo, P. (2012) · Annual Review of Physiology · doi:10.1146/annurev-physiol-030212-183731 · Cited by 168 · see citing works
Self-citationAssociative Cortex Features in the First Olfactory Brain Relay Station
Doucette, W. T., Gire, D. H., Whitesell, J. D., Carmean, V., Lucero, M. T., & Restrepo, D. (2011) · Neuron · doi:10.1016/j.neuron.2011.02.024 · Cited by 167 · see citing works
Learning‐dependent neurogenesis in the olfactory bulb determines long‐term olfactory memory
Sultan, S., Mandairon, N., Kermen, F., Garcia, S., Sacquet, J., & Didier, A. (2010) · The FASEB Journal · doi:10.1096/fj.09-151456 · Cited by 159 · see citing works
Effects of Cue-Triggered Expectation on Cortical Processing of Taste
Samuelsen, C. L., Gardner, M., & Fontanini, A. (2012) · Neuron · doi:10.1016/j.neuron.2012.02.031 · Cited by 156 · see citing works
Roesch, M. R., Stalnaker, T. A., & Schoenbaum, G. M. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhk009 · Cited by 130 · see citing works
Adult Neurogenesis and the Future of the Rejuvenating Brain Circuits
Lepousez, G., Nissant, A., & Lledo, P. (2015) · Neuron · doi:10.1016/j.neuron.2015.01.002 · Cited by 129 · see citing works
Self-citationThe Olfactory Tubercle Encodes Odor Valence in Behaving Mice
Gadziola, M. A., Tylicki, K. A., Christian, D. L., & Wesson, D. W. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4750-14.2015 · Cited by 128 · see citing works
Associative Encoding in Posterior Piriform Cortex during Odor Discrimination and Reversal Learning
Calu, D. J., Roesch, M. R., Stalnaker, T. A., & Schoenbaum, G. M. (2006) · Cerebral Cortex · doi:10.1093/cercor/bhl045 · Cited by 125 · see citing works
Ablation of mouse adult neurogenesis alters olfactory bulb structure and olfactory fear conditioning
Valley, M. T. (2009) · Frontiers in Neuroscience · doi:10.3389/neuro.22.003.2009 · Cited by 92 · see citing works
Olfactory learning promotes input-specific synaptic plasticity in adult-born neurons
Lepousez, G., Nissant, A., Bryant, A. K., Gheusi, G., Greer, C. A., & Lledo, P. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1404991111 · Cited by 92 · see citing works
Self-citationInformation for decision-making and stimulus identification is multiplexed in sensory cortex
Gire, D. H., Whitesell, J. D., Doucette, W. T., & Restrepo, D. (2013) · Nature Neuroscience · doi:10.1038/nn.3432 · Cited by 85 · see citing works
Functional imaging of cortical feedback projections to the olfactory bulb
Rothermel, M., & Wachowiak, M. (2014) · Frontiers in Neural Circuits · doi:10.3389/fncir.2014.00073 · Cited by 83 · see citing works
Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice
Cazakoff, B. N., Lau, B. Y. B., Crump, K. L., Demmer, H. S., & Shea, S. D. (2014) · Nature Neuroscience · doi:10.1038/nn.3669 · Cited by 81 · see citing works
Experience-dependent plasticity of mature adult-born neurons
Livneh, Y., & Mizrahi, A. (2011) · Nature Neuroscience · doi:10.1038/nn.2980 · Cited by 80 · see citing works
Persistent Structural Plasticity Optimizes Sensory Information Processing in the Olfactory Bulb
Sailor, K. A., Valley, M. T., Wiechert, M. T., Riecke, H., Sun, G. J., Adams, W., Dennis, J. C., Sharafi, S., Ming, G., Song, H., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.06.004 · Cited by 77 · see citing works
Self-citationIGF1-Dependent Synaptic Plasticity of Mitral Cells in Olfactory Memory during Social Learning
Liu, Z., Chen, Z., Shang, C., Yan, F., Shi, Y., Zhang, J., Qu, B., Han, H., Wang, Y., Li, D., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.06.015 · Cited by 69 · see citing works
Role of centrifugal projections to the olfactory bulb in olfactory processingPreprint
Kiselycznyk, C., Zhang, S., & Linster, C. (2006) · Learning & Memory · doi:10.1101/lm.285706 · Cited by 67 · see citing works
Adult neurogenesis beyond the niche: its potential for driving brain plasticity
Sailor, K. A., Schinder, A. F., & Lledo, P. (2016) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2016.12.001 · Cited by 67 · see citing works
Self-citationHow, When, and Where New Inhibitory Neurons Release Neurotransmitters in the Adult Olfactory Bulb
Bardy, C., Alonso, M., Bouthour, W., & Lledo, P. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4543-10.2010 · Cited by 64 · see citing works
Self-citationGlomerulus-Specific, Long-Latency Activity in the Olfactory Bulb Granule Cell Network
Kapoor, V., & Urban, N. N. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3371-06.2006 · Cited by 60 · see citing works
Principal cell activity induces spine relocation of adult-born interneurons in the olfactory bulb
Breton-Provencher, V., Bakhshetyan, K., Hardy, D., Bammann, R. R., Cavarretta, F., Snapyan, M., Côté, D., Migliore, M., & Saghatelyan, A. (2016) · Nature Communications · doi:10.1038/ncomms12659 · Cited by 60 · see citing works
Topographical representation of odor hedonics in the olfactory bulb
Kermen, F., Midroit, M., Kuczewski, N., Forest, J., Thévenet, M., Sacquet, J., Benetollo, C., Richard, M., Didier, A., & Mandairon, N. (2016) · Nature Neuroscience · doi:10.1038/nn.4317 · Cited by 55 · see citing works
Garrett, L., Zhang, J., Zimprich, A., Niedermeier, K. M., Fuchs, H., Gailus-Durner, V., Hrabě de Angelis, M., Vogt Weisenhorn, D., Wurst, W., & Hölter, S. M. (2015) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2015.00302 · Cited by 37 · see citing works
Posttraining Ablation of Adult-Generated Olfactory Granule Cells Degrades Odor–Reward Memories
Arruda-Carvalho, M., Akers, K. G., Guskjolen, A. J., Sakaguchi, M., Josselyn, S. A., & Frankland, P. W. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.2336-13.2014 · Cited by 36 · see citing works
Reward Activates Stimulus-Specific and Task-Dependent Representations in Visual Association Cortices
Schiffer, A., Müller, T., Yeung, N., & Waszak, F. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.1640-14.2014 · Cited by 33 · see citing works
Developmentally defined forebrain circuits regulate appetitive and aversive olfactory learning
Muthusamy, N., Zhang, X., Johnson, C. A., Yadav, P. N., & Ghashghaei, H. T. (2017) · Nature Neuroscience · doi:10.1038/nn.4452 · Cited by 29 · see citing works
Adult Neurogenesis Produces Neurons with Unique GABAergic Synapses in the Olfactory Bulb
Valley, M. T., Henderson, L. G., Inverso, S. A., & Lledo, P. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.2845-13.2013 · Cited by 28 · see citing works
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Neural stem cells: origin, heterogeneity and regulation in the adult mammalian brain
Obernier, K., & Alvarez-Buylla, A. (2019) · Development · doi:10.1242/dev.156059 · Cited by 578 · see citing works
Short-term availability of adult-born neurons for memory encoding
Forest, J., Moreno, M., Cavelius, M., Chalençon, L., Ziessel, A., Sacquet, J., Richard, M., Didier, A., & Mandairon, N. (2019) · Nature Communications · doi:10.1038/s41467-019-13521-7 · Cited by 24 · see citing works
Dejou, J., Athanassi, A., Brunel, T., Thevenet, M., Didier, A., & Mandairon, N. (2026) · PLOS Biology · doi:10.1371/journal.pbio.3003845 · Cited by 1 · see citing works
“At the neuronal level, while adult-born GCs are well-known to support flexible olfactory behaviors in adulthood [19,50–52], neonatal-born GCs have been primarily associated with innate olfactory responses [14,20,21,53,54].”
- Authors
- Grelat, A., Benoit, L., Wagner, S., Moigneu, C., Lledo, P.-M., & Alonso, M.
- Affiliations
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Lledo, Pierre-Marie
- Alonso, Mariana
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2018-02-21
- Volume
- 115
- Issue
- 10
- Pages
- 2514-2519
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5877928
- OpenAlex
- W2791493345
- Cited by
- 72
- References
- 48
- Citations by year
- 2026: 4 · 2025: 10 · 2024: 6 · 2023: 7 · 2022: 10 · 2021: 8 · 2020: 12 · 2019: 8 · 2018: 7
- FWCI
- 3.22
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- Funders
- Agence Nationale de la Recherche (ANR-15-CE37-0004-01, ANR-15-NEUC-0004-02, ANR-10-LABX-73)
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- adult neurogenesis, adult-born neurons, olfactory bulb, olfactory learning, reversal learning, interneurons
- MeSH terms
- Animals, Discrimination Learning, Female, Male, Models, Neurological, Odorants, Olfactory Bulb, Reward, Smell, Olfactory Receptor Neurons, Rats
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