DOI: 10.1523/jneurosci.2633-06.2006. Olfactory Discrimination Learning Increases the Survival of Adult-Born Neurons in the Olfactory Bulb

Olfactory Discrimination Learning Increases the Survival of Adult-Born Neurons in the Olfactory Bulb

10.1523/jneurosci.2633-06.2006

Crossref journal-article

Society for Neuroscience

The Journal of Neuroscience (393)

Abstract

In the olfactory bulb (OB), new neurons are added throughout life, forming an integral part of the functioning circuit. Yet only some of them survive more than a month. To determine whether this turnover depends on olfactory learning, we examined the survival of adult newborn cells labeled with the cell division marker BrdU, administered before learning in an olfactory discrimination task. We report that discrimination learning increases the number of newborn neurons in the adult OB by prolonging their survival. Simple exposure to the pair of olfactory cues did not alter neurogenesis, indicating that the mere activation of sensory inputs during the learning task was insufficient to alter neurogenesis. The increase in cell survival after learning was not uniformly distributed throughout angular sectors of coronal sections of the OB. Monitoring odor activation maps using patterns of Zif268 immediate early gene expression revealed that survival was greater in regions more activated by the non-reinforced odorant. We conclude that sensory activation in a learning context not only controls the total number of newborn neurons in the adult OB, but also refines their precise location. Shaping the distribution of newborn neurons by influencing their survival could optimize the olfactory information processing required for odor discrimination.

Bibliography

Alonso, M., Viollet, C., Gabellec, M.-M., Meas-Yedid, V., Olivo-Marin, J.-C., & Lledo, P.-M. (2006). Olfactory Discrimination Learning Increases the Survival of Adult-Born Neurons in the Olfactory Bulb. The Journal of Neuroscience, 26(41), 10508â10513.

Authors 6

Mariana Alonso (first)
Cécile Viollet (additional)
Marie-Madeleine Gabellec (additional)
Vannary Meas-Yedid (additional)
Jean-Christophe Olivo-Marin (additional)
Pierre-Marie Lledo (additional)

References 32 Referenced 201

10.1152/physrev.00055.2003
10.1523/JNEUROSCI.22-03-00629.2002 / J Neurosci / Neurogenesis in adult subventricular zone by Alvarez-Buylla (2002)
10.1016/S0306-4522(02)00757-1
10.1038/nature01001
10.1523/JNEUROSCI.23-32-10411.2003 / J Neurosci / Electrophysiological differentiation of new neurons in the olfactory bulb by Belluzzi (2003)
10.1523/JNEUROSCI.22-08-03033.2002 / J Neurosci / Odorant receptor expression defines functional units in the mouse olfactory system by Bozza (2002)
10.1038/nn1048
10.1023/A:1012849801892
10.1523/JNEUROSCI.2751-04.2004
10.1073/pnas.97.4.1823
10.1523/JNEUROSCI.3512-05.2005
10.1126/science.3749894
10.1073/pnas.0508491103
10.1046/j.1460-9568.2002.01991.x
10.1016/j.conb.2004.03.001
10.1523/JNEUROSCI.22-16-06842.2002 / J Neurosci / Spontaneous versus reinforced olfactory discriminations by Linster (2002)
10.1016/j.semcdb.2006.04.011
10.1038/nrn1867
10.1523/JNEUROSCI.2250-05.2005
10.1073/pnas.0403361101
10.1146/annurev.neuro.28.051804.101459
10.1016/S0031-3203(01)00127-3
10.1523/JNEUROSCI.22-14-06106.2002 / J Neurosci / Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction by Petreanu (2002)
10.1523/JNEUROSCI.22-07-02679.2002 / J Neurosci / Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory by Rochefort (2002)
10.1093/chemse/bji055
10.1016/S0166-2236(03)00228-5
Shepherd GM Chen WR Greer CA (2004) in The synaptic organization of the brain, Olfactory bulb, ed Shepherd GM (Oxford UP, Oxford), pp 165–216. (10.1093/acprof:oso/9780195159561.003.0005)
10.1073/pnas.96.7.4040
10.1016/S0896-6273(02)00793-6
10.1016/S0166-2236(03)00076-6
10.1046/j.1460-9568.2002.02238.x
10.1073/pnas.0406082102

Dates

Type	When
Created	18 years, 10 months ago (Oct. 11, 2006, 1:30 p.m.)
Deposited	2 years, 4 months ago (April 13, 2023, 1:40 p.m.)
Indexed	2 months, 2 weeks ago (June 2, 2025, 12:27 p.m.)
Issued	18 years, 10 months ago (Oct. 11, 2006)
Published	18 years, 10 months ago (Oct. 11, 2006)
Published Online	18 years, 10 months ago (Oct. 11, 2006)
Published Print	18 years, 10 months ago (Oct. 11, 2006)

Funders 0

None

BibTeX

@article{Alonso_2006, title={Olfactory Discrimination Learning Increases the Survival of Adult-Born Neurons in the Olfactory Bulb}, volume={26}, ISSN={1529-2401}, url={http://dx.doi.org/10.1523/jneurosci.2633-06.2006}, DOI={10.1523/jneurosci.2633-06.2006}, number={41}, journal={The Journal of Neuroscience}, publisher={Society for Neuroscience}, author={Alonso, Mariana and Viollet, Cécile and Gabellec, Marie-Madeleine and Meas-Yedid, Vannary and Olivo-Marin, Jean-Christophe and Lledo, Pierre-Marie}, year={2006}, month=oct, pages={10508–10513} }

JSON

{
  "indexed": {
    "date-parts": [
      [
        2025,
        6,
        2
      ]
    ],
    "date-time": "2025-06-02T16:27:22Z",
    "timestamp": 1748881642635
  },
  "reference-count": 32,
  "publisher": "Society for Neuroscience",
  "issue": "41",
  "license": [
    {
      "start": {
        "date-parts": [
          [
            2007,
            4,
            11
          ]
        ],
        "date-time": "2007-04-11T00:00:00Z",
        "timestamp": 1176249600000
      },
      "content-version": "vor",
      "delay-in-days": 182,
      "URL": "https://creativecommons.org/licenses/by-nc-sa/4.0/"
    }
  ],
  "content-domain": {
    "domain": [],
    "crossmark-restriction": false
  },
  "published-print": {
    "date-parts": [
      [
        2006,
        10,
        11
      ]
    ]
  },
  "abstract": "<jats:p>In the olfactory bulb (OB), new neurons are added throughout life, forming an integral part of the functioning circuit. Yet only some of them survive more than a month. To determine whether this turnover depends on olfactory learning, we examined the survival of adult newborn cells labeled with the cell division marker BrdU, administered before learning in an olfactory discrimination task. We report that discrimination learning increases the number of newborn neurons in the adult OB by prolonging their survival. Simple exposure to the pair of olfactory cues did not alter neurogenesis, indicating that the mere activation of sensory inputs during the learning task was insufficient to alter neurogenesis. The increase in cell survival after learning was not uniformly distributed throughout angular sectors of coronal sections of the OB. Monitoring odor activation maps using patterns of Zif268 immediate early gene expression revealed that survival was greater in regions more activated by the non-reinforced odorant. We conclude that sensory activation in a learning context not only controls the total number of newborn neurons in the adult OB, but also refines their precise location. Shaping the distribution of newborn neurons by influencing their survival could optimize the olfactory information processing required for odor discrimination.</jats:p>",
  "DOI": "10.1523/jneurosci.2633-06.2006",
  "type": "journal-article",
  "created": {
    "date-parts": [
      [
        2006,
        10,
        11
      ]
    ],
    "date-time": "2006-10-11T17:30:03Z",
    "timestamp": 1160587803000
  },
  "page": "10508-10513",
  "source": "Crossref",
  "is-referenced-by-count": 201,
  "title": "Olfactory Discrimination Learning Increases the Survival of Adult-Born Neurons in the Olfactory Bulb",
  "prefix": "10.1523",
  "volume": "26",
  "author": [
    {
      "given": "Mariana",
      "family": "Alonso",
      "sequence": "first",
      "affiliation": []
    },
    {
      "given": "C\u00e9cile",
      "family": "Viollet",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Marie-Madeleine",
      "family": "Gabellec",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Vannary",
      "family": "Meas-Yedid",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Jean-Christophe",
      "family": "Olivo-Marin",
      "sequence": "additional",
      "affiliation": []
    },
    {
      "given": "Pierre-Marie",
      "family": "Lledo",
      "sequence": "additional",
      "affiliation": []
    }
  ],
  "member": "393",
  "published-online": {
    "date-parts": [
      [
        2006,
        10,
        11
      ]
    ]
  },
  "reference": [
    {
      "key": "2023041303212224000_26.41.10508.1",
      "doi-asserted-by": "publisher",
      "DOI": "10.1152/physrev.00055.2003"
    },
    {
      "key": "2023041303212224000_26.41.10508.2",
      "doi-asserted-by": "crossref",
      "first-page": "629",
      "DOI": "10.1523/JNEUROSCI.22-03-00629.2002",
      "article-title": "Neurogenesis in adult subventricular zone",
      "volume": "22",
      "author": "Alvarez-Buylla",
      "year": "2002",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303212224000_26.41.10508.3",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0306-4522(02)00757-1"
    },
    {
      "key": "2023041303212224000_26.41.10508.4",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nature01001"
    },
    {
      "key": "2023041303212224000_26.41.10508.5",
      "doi-asserted-by": "crossref",
      "first-page": "10411",
      "DOI": "10.1523/JNEUROSCI.23-32-10411.2003",
      "article-title": "Electrophysiological differentiation of new neurons in the olfactory bulb",
      "volume": "23",
      "author": "Belluzzi",
      "year": "2003",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303212224000_26.41.10508.6",
      "doi-asserted-by": "crossref",
      "first-page": "3033",
      "DOI": "10.1523/JNEUROSCI.22-08-03033.2002",
      "article-title": "Odorant receptor expression defines functional units in the mouse olfactory system",
      "volume": "22",
      "author": "Bozza",
      "year": "2002",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303212224000_26.41.10508.7",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nn1048"
    },
    {
      "key": "2023041303212224000_26.41.10508.8",
      "doi-asserted-by": "publisher",
      "DOI": "10.1023/A:1012849801892"
    },
    {
      "key": "2023041303212224000_26.41.10508.9",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.2751-04.2004"
    },
    {
      "key": "2023041303212224000_26.41.10508.10",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.97.4.1823"
    },
    {
      "key": "2023041303212224000_26.41.10508.11",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.3512-05.2005"
    },
    {
      "key": "2023041303212224000_26.41.10508.12",
      "doi-asserted-by": "publisher",
      "DOI": "10.1126/science.3749894"
    },
    {
      "key": "2023041303212224000_26.41.10508.13",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0508491103"
    },
    {
      "key": "2023041303212224000_26.41.10508.14",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1460-9568.2002.01991.x"
    },
    {
      "key": "2023041303212224000_26.41.10508.15",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.conb.2004.03.001"
    },
    {
      "key": "2023041303212224000_26.41.10508.16",
      "doi-asserted-by": "crossref",
      "first-page": "6842",
      "DOI": "10.1523/JNEUROSCI.22-16-06842.2002",
      "article-title": "Spontaneous versus reinforced olfactory discriminations",
      "volume": "22",
      "author": "Linster",
      "year": "2002",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303212224000_26.41.10508.17",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/j.semcdb.2006.04.011"
    },
    {
      "key": "2023041303212224000_26.41.10508.18",
      "doi-asserted-by": "publisher",
      "DOI": "10.1038/nrn1867"
    },
    {
      "key": "2023041303212224000_26.41.10508.19",
      "doi-asserted-by": "publisher",
      "DOI": "10.1523/JNEUROSCI.2250-05.2005"
    },
    {
      "key": "2023041303212224000_26.41.10508.20",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0403361101"
    },
    {
      "key": "2023041303212224000_26.41.10508.21",
      "doi-asserted-by": "publisher",
      "DOI": "10.1146/annurev.neuro.28.051804.101459"
    },
    {
      "key": "2023041303212224000_26.41.10508.22",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0031-3203(01)00127-3"
    },
    {
      "key": "2023041303212224000_26.41.10508.23",
      "doi-asserted-by": "crossref",
      "first-page": "6106",
      "DOI": "10.1523/JNEUROSCI.22-14-06106.2002",
      "article-title": "Maturation and death of adult-born olfactory bulb granule neurons: role of olfaction",
      "volume": "22",
      "author": "Petreanu",
      "year": "2002",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303212224000_26.41.10508.24",
      "doi-asserted-by": "crossref",
      "first-page": "2679",
      "DOI": "10.1523/JNEUROSCI.22-07-02679.2002",
      "article-title": "Enriched odor exposure increases the number of newborn neurons in the adult olfactory bulb and improves odor memory",
      "volume": "22",
      "author": "Rochefort",
      "year": "2002",
      "journal-title": "J Neurosci"
    },
    {
      "key": "2023041303212224000_26.41.10508.25",
      "doi-asserted-by": "publisher",
      "DOI": "10.1093/chemse/bji055"
    },
    {
      "key": "2023041303212224000_26.41.10508.26",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0166-2236(03)00228-5"
    },
    {
      "key": "2023041303212224000_26.41.10508.27",
      "doi-asserted-by": "crossref",
      "unstructured": "Shepherd GM Chen WR Greer CA (2004) in The synaptic organization of the brain, Olfactory bulb, ed Shepherd GM (Oxford UP, Oxford), pp 165\u2013216.",
      "DOI": "10.1093/acprof:oso/9780195159561.003.0005"
    },
    {
      "key": "2023041303212224000_26.41.10508.28",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.96.7.4040"
    },
    {
      "key": "2023041303212224000_26.41.10508.29",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0896-6273(02)00793-6"
    },
    {
      "key": "2023041303212224000_26.41.10508.30",
      "doi-asserted-by": "publisher",
      "DOI": "10.1016/S0166-2236(03)00076-6"
    },
    {
      "key": "2023041303212224000_26.41.10508.31",
      "doi-asserted-by": "publisher",
      "DOI": "10.1046/j.1460-9568.2002.02238.x"
    },
    {
      "key": "2023041303212224000_26.41.10508.32",
      "doi-asserted-by": "publisher",
      "DOI": "10.1073/pnas.0406082102"
    }
  ],
  "container-title": "The Journal of Neuroscience",
  "original-title": [],
  "language": "en",
  "link": [
    {
      "URL": "https://syndication.highwire.org/content/doi/10.1523/JNEUROSCI.2633-06.2006",
      "content-type": "unspecified",
      "content-version": "vor",
      "intended-application": "similarity-checking"
    }
  ],
  "deposited": {
    "date-parts": [
      [
        2023,
        4,
        13
      ]
    ],
    "date-time": "2023-04-13T17:40:50Z",
    "timestamp": 1681407650000
  },
  "score": 1,
  "resource": {
    "primary": {
      "URL": "https://www.jneurosci.org/lookup/doi/10.1523/JNEUROSCI.2633-06.2006"
    }
  },
  "subtitle": [],
  "short-title": [],
  "issued": {
    "date-parts": [
      [
        2006,
        10,
        11
      ]
    ]
  },
  "references-count": 32,
  "journal-issue": {
    "issue": "41",
    "published-online": {
      "date-parts": [
        [
          2006,
          10,
          11
        ]
      ]
    },
    "published-print": {
      "date-parts": [
        [
          2006,
          10,
          11
        ]
      ]
    }
  },
  "alternative-id": [
    "10.1523/JNEUROSCI.2633-06.2006"
  ],
  "URL": "http://dx.doi.org/10.1523/JNEUROSCI.2633-06.2006",
  "relation": {},
  "ISSN": [
    "0270-6474",
    "1529-2401"
  ],
  "subject": [],
  "container-title-short": "J. Neurosci.",
  "published": {
    "date-parts": [
      [
        2006,
        10,
        11
      ]
    ]
  }
}