Continuous postnatal neurogenesis contributes to formation of the olfactory bulb neural circuits and flexible olfactory associative learning
Open accessAbstract
The olfactory bulb (OB) is one of the two major loci in the mammalian brain where newborn neurons are constantly integrated into the neural circuit during postnatal life. Newborn neurons are generated from neural stem cells in the subventricular zone (SVZ) of the lateral ventricle and migrate to the OB through the rostral migratory stream. The majority of these newborn neurons differentiate into inhibitory interneurons, such as granule cells and periglomerular cells. It has been reported that prolonged supply of newborn neurons leads to continuous addition/turnover of the interneuronal populations and contributes to functional integrity of the OB circuit. However, it is not still clear how and to what extent postnatal-born neurons contribute to OB neural circuit formation, and the functional role of postnatal neurogenesis in odor-related behaviors remains elusive. To address this question, here by using genetic strategies, we first determined the unique integration mode of newly born interneurons during postnatal development of the mouse OB. We then manipulated these interneuron populations and found that continuous postnatal neurogenesis in the SVZ-OB plays pivotal roles in flexible olfactory associative learning and memory.
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P1-born granule cells are required for some olfactory learning in adulthood.
“The production of GCs born at P1 can be modulated by early-life olfactory experience [14,18], and these cells are required for some olfactory learning in adulthood [19–21].”
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 [21]
The section ‘Postnatal-born OB interneurons are essential for flexible olfactory associative learning’ (page unavailable) reports impaired reversal learning in 3-month-old mice when postnatal-born olfactory-bulb interneurons were silenced. But the paper does not isolate GCs born specifically at P1 as necessary: its P1 treatment labels stem cells and their subsequent progeny, while the learning experiments target broader postnatal-born populations. (LLM, conf=0.87)
Experimental — accuracy not yet measuredMost transduced GCs present in the adult olfactory bulb originate from the early postnatal period.
“we argue that in our experimental conditions, most of the transduced GCs present in the adult OB originate from the early postnatal period, as this stage is concerned by a proliferation 3-fold larger than in adulthood, and producing GCs with very low cell death if any [14,20,21,55].”
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 [21]
The Results report that most adult olfactory-bulb GCs are postnatally born and propose that newborn neurons build the circuit before P35. They do not establish that most transduced GCs in the citing authors’ experimental conditions originated in the early postnatal period, or support the stated threefold proliferation and very-low-cell-death rationale; the Results instead propose ongoing GC replacement after P35. (LLM, conf=0.85)
Experimental — accuracy not yet measuredNeonatal-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 [21]
The Discussion (page unavailable) links postnatal-born interneurons to flexible olfactory associative learning and says embryonically born interneurons suffice for simple odor discrimination and initial memory acquisition. The behavioral-results section reports preserved spontaneous odor exploration in mice with impaired postnatal neurogenesis. Neither passage identifies neonatal-born granule cells as primarily associated with innate olfactory responses; searches for neonatal-born cells and innate responses found no such statement. (LLM, conf=0.73)
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“However, OB neurogenesis is necessary for olfactory learning and memory (Breton-Provencher et al., 2009; Arruda-Carvalho et al., 2014; Sakamoto et al., 2014) and mating behavior (Feierstein et al.”
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“…(i.e., P1), we argue that in our experimental conditions, most of the transduced GCs present in the adult OB originate from the early postnatal period, as this stage is concerned by a proliferation 3-fold larger than in adulthood, and producing GCs with very low cell death if any [14,20,21,55].”
- Authors
- Sakamoto, M., Ieki, N., Miyoshi, G., Mochimaru, D., Miyachi, H., Imura, T., Yamaguchi, M., Fishell, G., Mori, K., Kageyama, R., & Imayoshi, I.
- Affiliations
- Fukushima Medical University (JP)
- The University of Tokyo (JP)
- New York University (US)
- Kyoto University (JP)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2014-04-23
- Volume
- 34
- Issue
- 17
- Pages
- 5788-5799
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6608281
- OpenAlex
- W2093502142
- Cited by
- 131
- References
- 60
- Citations by year
- 2026: 2 · 2025: 7 · 2024: 8 · 2023: 15 · 2022: 12 · 2021: 9 · 2020: 10 · 2019: 15 · 2018: 11 · 2017: 10 · 2016: 18 · 2015: 8 · 2014: 6
- FWCI
- 4.87
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Mitsubishi Foundation
- Japan Society for the Promotion of Science (24680035, 24300118, 23240046)
- Japan Science and Technology Agency
- Precursory Research for Embryonic Science and Technology
- Topics
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- postnatal neurogenesis, olfactory bulb, subventricular zone, rostral migratory stream, granule cells, periglomerular cells, olfactory associative learning, olfactory memory, neural stem cells
- MeSH terms
- Animals, Association Learning, Cerebral Ventricles, Interneurons, Male, Mice, Transgenic, Nerve Net, Neurons, Odorants, Olfactory Bulb, Dentate Gyrus, Mice, Neurogenesis, Olfactory Perception, Neural Stem Cells
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