Developmentally defined forebrain circuits regulate appetitive and aversive olfactory learning
Open accessAbstract
Postnatal and adult neurogenesis are region- and modality-specific, but the significance of developmentally distinct neuronal populations remains unclear. We demonstrate that chemogenetic inactivation of a subset of forebrain and olfactory neurons generated at birth disrupts responses to an aversive odor. In contrast, novel appetitive odor learning is sensitive to inactivation of adult-born neurons, revealing that developmentally defined sets of neurons may differentially participate in hedonic aspects of sensory learning.
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Neonatal-born granule cells have been primarily associated with innate olfactory responses.
“neonatal-born GCs have been primarily associated with innate olfactory responses [14,20,21,53,54].”
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 [53]
The paper reports that inhibiting neurons targeted at birth disrupted freezing responses to the aversive odor TMT (section labeled Abstract; page unavailable). But it does not isolate neonatal-born granule cells: targeted cells occupied several olfactory-bulb layers and forebrain regions, and the paper links the observed effect to periglomerular and mitral layers as well. It therefore supports an association for birth-targeted olfactory circuits, not the claim that neonatal-born granule cells were primarily associated with innate responses. (LLM, conf=0.86)
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Cites
Neurodegenerative Disorders: Parkinson's Disease and Huntington's Disease
Hague, S., Klaffke, S., & Bandmann, O. (2006) · IMPERIAL COLLEGE PRESS eBooks · doi:10.1142/9781860948961_0007 · Cited by 2,767 · see citing works
Optogenetics in neural systems
Yizhar, O., Fenno, L. E., Davidson, T. J., Mogri, M., & Deisseroth, K. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.004 · Cited by 1,881 · see citing works
Urban, D. J., & Roth, B. L. (2014) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev-pharmtox-010814-124803 · Cited by 660 · see citing works
Innate versus learned odour processing in the mouse olfactory bulb
Kobayakawa, K., Kobayakawa, R., Matsumoto, H., Oka, Y., Imai, T., Ikawa, M., Okabe, M., Ikeda, T., Itohara, S., Kikusui, T., et al. (2007) · Nature · doi:10.1038/nature06281 · Cited by 659 · see citing works
Origin and function of olfactory bulb interneuron diversity
Lledo, P., Merkle, F. T., & Álvarez-Buylla, A. (2008) · Trends in Neurosciences · doi:10.1016/j.tins.2008.05.006 · Cited by 422 · see citing works
A directional strategy for monitoring Cre-mediated recombination at the cellular level in the mouse
Schnütgen, F., Doerflinger, N., Calleja, C., Wendling, O., Chambon, P., & Ghyselinck, N. B. (2003) · Nature Biotechnology · doi:10.1038/nbt811 · Cited by 401 · see citing works
Male pheromone–stimulated neurogenesis in the adult female brain: possible role in mating behavior.
Mak, G. K., Enwere, E. K., Gregg, C., Pakarainen, T., POUTANEN, M. H., Huhtaniemi, I. T., & Weiss, S. (2007) · Nature Neuroscience · doi:10.1038/nn1928 · Cited by 314 · see citing works
Non-redundant coding of aversive odours in the main olfactory pathway
Dewan, A., Pacifico, R., Zhan, R., Rinberg, D. A., & Bozza, T. C. (2013) · Nature · doi:10.1038/nature12114 · Cited by 219 · see citing works
Magavi, 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
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
Cooperative subnetworks of molecularly similar interneurons in mouse neocortex
Karnani, M. M., Jackson, J., Ayzenshtat, I., Tucciarone, J., Manoocheri, K., Snider, W. G., & Yuste, R. (2016) · Neuron · doi:10.1016/j.neuron.2016.02.037 · Cited by 196 · see citing works
Adult neural stem cells stake their ground
Lim, D. A., & Álvarez-Buylla, A. (2014) · Trends in Neurosciences · doi:10.1016/j.tins.2014.08.006 · Cited by 179 · 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
Kügler, S., Lingor, P., Schöll, U., Zolotukhin, S., & Bähr, M. (2003) · Virology · doi:10.1016/s0042-6822(03)00162-4 · Cited by 153 · see citing works
Sakamoto, M., Ieki, N., Miyoshi, G., Mochimaru, D., Miyachi, H., Imura, T., Yamaguchi, M., Fishell, G., Mori, K., Kageyama, R., et al. (2014) · The Journal of Neuroscience · doi:10.1523/jneurosci.0674-14.2014 · Cited by 131 · see citing works
Feierstein, C. E., Lazarini, F., Wagner, S., Gabellec, M., de Chaumont, F., Olivo‐Marín, J., Boussin, F. D., Lledo, P., & Gheusi, G. (2010) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2010.00176 · Cited by 112 · see citing works
The functional significance of newly born neurons integrated into olfactory bulb circuits
Sakamoto, M., Kageyama, R., & Imayoshi, I. (2014) · Frontiers in Neuroscience · doi:10.3389/fnins.2014.00121 · Cited by 87 · see citing works
Jacquet, B. V., Muthusamy, N., Sommerville, L. J., Xiao, G., Liang, H., Zhang, Y., Holtzman, M. J., & Ghashghaei, H. T. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0171-11.2011 · Cited by 58 · see citing works
Self-citationHammad, M. A., Schmidt, S. L., Zhang, X., Bray, R., Frӧhlich, F., & Ghashghaei, H. T. (2014) · Cerebral Cortex · doi:10.1093/cercor/bhu094 · Cited by 43 · see citing works
Self-citationGarcia, I., Bhullar, P. K., Tepe, B., Ortiz‐Guzman, J., Huang, L., Herman, A. M., Chaboub, L. S., Deneen, B., Justice, N. J., & Arenkiel, B. R. (2014) · Brain Structure and Function · doi:10.1007/s00429-014-0888-4 · Cited by 42 · see citing works
Voltage-dependent intrinsic bursting in olfactory bulb Golgi cellsPreprint
Pressler, R. T., Rozman, P. A., & Strowbridge, B. W. (2013) · Learning & Memory · doi:10.1101/lm.031856.113 · Cited by 17 · see citing works
Identification of neuronal loci involved with displays of affective aggression in NC900 mice
Nehrenberg, D. L., Sheikh, A., & Ghashghaei, H. T. (2012) · Brain Structure and Function · doi:10.1007/s00429-012-0445-y · Cited by 11 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Adult-born neurons boost odor-reward association
Grelat, A., Benoit, L., Wagner, S., Moigneu, C., Lledo, P.-M., & Alonso, M. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1716400115 · Cited by 72 · see citing works
Synaptic pruning of murine adult-born neurons by microglia depends on phosphatidylserine
Kurematsu, C., Sawada, M., Ohmuraya, M., Tanaka, M., Kuboyama, K., Ogino, T., Matsumoto, M., Oishi, H., Inada, H., Ishido, Y., et al. (2022) · Journal of Experimental Medicine · doi:10.1084/jem.20202304 · Cited by 60 · see citing works
Chen, F., Liu, W., Liu, P., Wang, Z., Zhou, Y., Liu, X., & Li, A. (2021) · npj Parkinson s Disease · doi:10.1038/s41531-021-00259-7 · Cited by 54 · see citing works
Abrous, D., Koehl, M., & Lemoine, M. (2021) · Molecular Psychiatry · doi:10.1038/s41380-021-01172-4 · Cited by 41 · see citing works
Green, W. W., Uytingco, C. R., Ukhanov, K., Kolb, Z., Moretta, J. C., McIntyre, J. C., & Martens, J. R. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.0084-18.2018 · Cited by 36 · see citing works
Forest, J., Chalençon, L., Midroit, M., Terrier, C., Caillé, I., Sacquet, J., Benetollo, C., Martin, K., Richard, M., Didier, A., et al. (2019) · Cerebral Cortex · doi:10.1093/cercor/bhz105 · Cited by 27 · see citing works
Different forms of structural plasticity in the adult olfactory bulb
Hardy, D., & Saghatelyan, A. (2017) · Neurogenesis · doi:10.1080/23262133.2017.1301850 · Cited by 25 · see citing works
Wu, J., Liu, P., Chen, F., Ge, L., Lu, Y., & Li, A. (2020) · Genes · doi:10.3390/genes11040433 · Cited by 21 · see citing works
Postnatal neuronal migration in health and disease
Nakajima, C., Sawada, M., & Sawamoto, K. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.06.001 · Cited by 21 · see citing works
Odor hedonics coding in the vertebrate olfactory bulb
Kermen, F., Mandairon, N., & Chalençon, L. (2021) · Cell and Tissue Research · doi:10.1007/s00441-020-03372-w · Cited by 13 · see citing works
Zhang, X., Xiao, G., Johnson, C. A., Cai, Y., Horowitz, Z. K., Mennicke, C. V., Coffey, R. J., Haider, M. A., Threadgill, D. W., Eliscu, R., et al. (2022) · iScience · doi:10.1016/j.isci.2023.106242 · Cited by 14 · see citing works
Self-citationLipp, H. (2017) · Frontiers in Neuroscience · doi:10.3389/fnins.2017.00420 · Cited by 13 · see citing works
Advances in inutero electroporation
Kittock, C. M., & Pilaz, L. (2023) · Developmental Neurobiology · doi:10.1002/dneu.22910 · Cited by 10 · see citing works
Chemogenetic manipulation of astrocyte activity at the synapse— a gateway to manage brain disease
Pereira, M. J., Ayana, R., Holt, M. G., & Arckens, L. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1193130 · Cited by 10 · see citing works
Distinct Developmental Features of Olfactory Bulb Interneurons.
Kim, J. Y., & Choe, J. (2020) · Europe PMC (PubMed Central) · doi:10.14348/molcells.2020.0033 · Cited by 7 · see citing works
Dejou, J., Mandairon, N., & Didier, A. (2024) · Frontiers in Neural Circuits · doi:10.3389/fncir.2024.1467203 · Cited by 4 · see citing works
Uncovering novel regulators of memory using C. elegans genetic and genomic analysis
Brandel-Ankrapp, K. L., & Arey, R. N. (2023) · Biochemical Society Transactions · doi:10.1042/bst20220455 · Cited by 5 · see citing works
Timely Inhibitory Circuit Formation Controlled by Abl1 Regulates Innate Olfactory Behaviors in Mouse
Kim, J. Y., Cho, B., & Moon, C. (2020) · Cell Reports · doi:10.1016/j.celrep.2019.12.004 · Cited by 5 · see citing works
Neuronal migration in the postnatal brain
Sawada, M., & Sawamoto, K. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-814407-7.00021-3 · Cited by 3 · see citing works
Synaptogenesis in the adult CNS—olfactory system
Mizrahi, A., & Vinograd, A. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-823672-7.00011-9 · Cited by 2 · 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].”
Spence, N. J., Martín-López, E., Han, K., Lefèvre, M., Lange, N. W., Brennan, B., & Greer, C. A. (2024) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2025.104007 · Cited by 2 · see citing works
Sawada, M., Hamaguchi, A., Mano, N., Yoshida, Y., Uemura, A., & Sawamoto, K. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1143130 · Cited by 1 · see citing works
Zhang, X., Xiao, G., Johnson, C. A., Cai, Y., Mennicke, C. V., Coffey, R. J., Haider, M. A., Threadgill, D. W., Eliscu, R., Oldham, M. C., et al. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4141622 · Cited by 1 · see citing works
Self-citationLewis, S. (2017) · Nature reviews. Neuroscience · doi:10.1038/nrn.2017.2
Spence, N. J., Martín-López, E., Han, K., Lefèvre, M., Lange, N. W., Brennan, B., & Greer, C. A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.11.25.625264
Heyward, F. D., Pan, H., & Dreyfuss, J. M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.06.680592
Rôle et connectivité des néo-neurones formés à l’âge adulte dans le bulbe olfactif
Grelat, A. (2018) · theses.fr (ABES) · doi:10.70675/c01c4ec0zba51z466aza2f1z09fdd6310b8f
Olfactory learning potentiates long-range cortical GABAergic inputs onto adult-born neuronsPreprint
Peroni, E., Badts, C.-H. D., Lepousez, G., Hiridjee, A., Renvoise, J., Lafosse, I., Wagner, S., Jacquemet, E., Lledo, P., Alonso, M., et al. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.05.29.728424
- Authors
- Muthusamy, N., Zhang, X., Johnson, C. A., Yadav, P. N., & Ghashghaei, H. T.
- Affiliations
- North Carolina State University (US)
- Central Drug Research Institute (IN)
- Corresponding author
- Ghashghaei, H Troy
- Venue
- Nature Neuroscience
- Published
- 2016-12-05
- Volume
- 20
- Issue
- 1
- Pages
- 20-23
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC5191939
- OpenAlex
- W2560698288
- Cited by
- 29
- References
- 23
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 2 · 2023: 5 · 2022: 2 · 2021: 3 · 2020: 6 · 2019: 1 · 2018: 3 · 2017: 3
- FWCI
- 1.19
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- North Carolina State University
- National Institute of Neurological Disorders and Stroke (R01NS089795, R01NS098370)
- 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
- olfactory learning, adult neurogenesis, postnatal neurogenesis, chemogenetic inactivation, odor aversion, neuronal development, olfactory behavior
- MeSH terms
- Animals, Appetitive Behavior, Avoidance Learning, Behavior, Animal, Conditioning, Classical, Male, Neurons, Smell, Mice, Neurogenesis, Olfactory Cortex
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