434
Views
0
CrossRef citations to date
0
Altmetric
Special Issue

Low Fos expression in newly generated neurons of the main and accessory olfactory bulb following single maternal separation

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 678-687 | Received 21 Feb 2020, Accepted 20 Sep 2020, Published online: 14 Oct 2020

References

  • Arborelius, L., & Eklund, M. B. (2007). Both long and brief maternal separation produces persistent changes in tissue levels of brain monoamines in middle-aged female rats. Neuroscience, 145(2), 738–750. https://doi.org/10.1016/j.neuroscience.2006.12.007
  • Belluzzi, O., Benedusi, M., Ackman, J., & LoTurco, J. J. (2003). Electrophysiological differentiation of new neurons in the olfactory bulb. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 23(32), 10411–10418. https://doi.org/10.1523/JNEUROSCI.23-32-10411.2003
  • Belnoue, L., Grosjean, N., Abrous, D. N., & Koehl, M. (2011). A critical time window for the recruitment of bulbar newborn neurons by olfactory discrimination learning. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 31(3), 1010–1016. https://doi.org/10.1523/JNEUROSCI.3941-10.2011
  • Biagini, G., Pich, E. M., Carani, C., Marrama, P., & Agnati, L. F. (1998). Postnatal maternal separation during the stress hyporesponsive period enhances the adrenocortical response to novelty in adult rats by affecting feedback regulation in the CA1 hippocampal field. International Journal of Developmental Neuroscience, 16(3-4), 187–197. https://doi.org/10.1016/S0736-5748(98)00019-7
  • Brennan, P. A., & Zufall, F. (2006). Pheromonal communication in vertebrates. Nature, 444(7117), 308–315. https://doi.org/10.1038/nature05404
  • Breton-Provencher, V., Lemasson, M., Peralta, M. R., & Saghatelyan, A. (2009). Interneurons produced in adulthood are required for the normal functioning of the olfactory bulb network and for the execution of selected olfactory behaviors. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 29(48), 15245–15257. https://doi.org/10.1523/JNEUROSCI.3606-09.2009
  • Caldji, C., Diorio, J., & Meaney, M. J. (2000). Variations in maternal care in infancy regulate the development of stress reactivity. Biological Psychiatry, 48(12), 1164–1174. https://doi.org/10.1016/s0006-3223(00)01084-2
  • Carlen, M., Cassidy, R. M., Brismar, H., Smith, G. A., Enquist, L. W., & Frisen, J. (2002). Functional integration of adult-born neurons. Current Biology, 12(7), 606–608. https://doi.org/10.1016/s0960-9822(02)00771-6
  • Carleton, A., Petreanu, L. T., Lansford, R., Alvarez-Buylla, A., & Lledo, P. M. (2003). Becoming a new neuron in the adult olfactory bulb. Nature Neuroscience, 6(5), 507–518. https://doi.org/10.1038/nn1048
  • Carrera, O., Cerrato, M., Sanchez, A., & Gutierrez, E. (2009). Long maternal separation has protective effects in rats exposed to activity-based anorexia. Developmental Psychobiology, 51(8), 616–624. https://doi.org/10.1002/dev.20396
  • Doetsch, F., Petreanu, L., Caille, I., Garcia-Verdugo, J. M., & Alvarez-Buylla, A. (2002). EGF converts transit-amplifying neurogenic precursors in the adult brain into multipotent stem cells. Neuron, 36(6), 1021–1034. https://doi.org/10.1016/s0896-6273(02)01133-9
  • Enthoven, L., Oitzl, M. S., Koning, N., van der Mark, M., & de Kloet, E. R. (2008). Hypothalamic-pituitary-adrenal axis activity of newborn mice rapidly desensitizes to repeated maternal absence but becomes highly responsive to novelty. Endocrinology, 149(12), 6366–6377. https://doi.org/10.1210/en.2008-0238
  • Fabianová, K., Závodská, M., Raček, A., Angelidis, A., Martončíková, M., & Račeková, E. (2018). Analysis of Fos expression in the rat olfactory neurogenic region following single exposure to maternal separation during different neonatal stages. General Physiology and Biophysics, 37(3), 275–283. https://doi.org/10.4149/gpb_2017056
  • Feng, M., Sheng, G., Li, Z., Wang, J., Ren, K., Jin, X., & Jiang, K. (2014). Postnatal maternal separation enhances tonic GABA current of cortical layer 5 pyramidal neurons in juvenile rats and promotes genesis of GABAergic neurons in neocortical molecular layer and subventricular zone in adult rats. Behavioural Brain Research, 260, 74–82. https://doi.org/10.1016/j.bbr.2013.11.040
  • Guthrie, K. M., & Gall, C. M. (1995). Functional mapping of odor-activated neurons in the olfactory bulb. Chemical Senses, 20(2), 271–282. https://doi.org/10.1093/chemse/20.2.271
  • Hofer, M. A. (1975). Studies on how early maternal separation produces behavioral change in young rats. Psychosomatic Medicine, 37(3), 245–264. https://doi.org/10.1097/00006842-197505000-00003
  • Horii-Hayashi, N., Sasagawa, T., Matsunaga, W., Matsusue, Y., Azuma, C., & Nishi, M. (2013). Developmental changes in desensitisation of c-Fos expression induced by repeated maternal separation in pre-weaned mice. Journal of Neuroendocrinology, 25(2), 158–167. https://doi.org/10.1111/j.1365-2826.2012.02377.x
  • Huang, L., & Bittman, E. L. (2002). Olfactory bulb cells generated in adult male golden hamsters are specifically activated by exposure to estrous females. Hormones and Behavior, 41(3), 343–350. https://doi.org/10.1006/hbeh.2002.1767
  • Illig, K. R. (2005). Projections from orbitofrontal cortex to anterior piriform cortex in the rat suggest a role in olfactory information processing. The Journal of Comparative Neurology, 488(2), 224–231. https://doi.org/10.1002/cne.20595
  • Kay, L. M. (2011). Olfactory coding: Random scents make sense. Current Biology, 21, 928–929. https://doi.org/10.1016/j.cub.2011.10.008
  • Klintsova, A. Y., Philpot, B. D., & Brunjes, P. C. (1995). Fos protein immunoreactivity in the developing olfactory bulbs of normal and naris-occluded rats. Brain Research Developmental Brain Research, 86(1–2), 114–122. https://doi.org/10.1016/0165-3806(95)00015-6
  • Kondoh, K., Lu, Z., Ye, X., Olson, D. P., Lowell, B. B., & Buck, L. B. (2016). A specific area of the olfactory cortex involved in stress hormone responses to predator odors. Nature, 532(7597), 103–106. https://doi.org/10.1038/nature17156
  • Larsen, C. M., Kokay, I. C., & Grattan, D. R. (2008). Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice. Hormones and Behavior, 53(4), 509–517. https://doi.org/10.1016/j.yhbeh.2007.11.020
  • Lievajova, K., Blasko, J., Martoncikova, M., Cigankova, V., & Racekova, E. (2011). Delayed maturation and altered proliferation within the rat rostral migratory stream following maternal deprivation. European Journal of Histochemistry, 55(4), e33. https://doi.org/10.4081/ejh.2011.e33
  • Livneh, Y., Adam, Y., & Mizrahi, A. (2014). Odor processing by adult-born neurons. Neuron, 81(5), 1097–1110. https://doi.org/10.1016/j.neuron.2014.01.007
  • Lledo, P. M., & Saghatelyan, A. (2005). Integrating new neurons into the adult olfactory bulb: Joining the network, life-death decisions, and the effects of sensory experience. Trends in Neurosciences, 28(5), 248–254. https://doi.org/10.1016/j.tins.2005.03.005
  • Lois, C., & Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science, 264(5162), 1145–1148. https://doi.org/10.1126/science.8178174
  • Luskin, M. B. (1993). Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron, 11(1), 173–189. https://doi.org/10.1016/0896-6273(93)90281-u
  • Magavi, S. S., Mitchell, B. D., Szentirmai, O., Carter, B. S., & Macklis, J. D. (2005). Adult-born and preexisting olfactory granule neurons undergo distinct experience-dependent modifications of their olfactory responses in vivo. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 25(46), 10729–10739. https://doi.org/10.1523/JNEUROSCI.2250-05.2005
  • Marais, L., van Rensburg, S. J., van Zyl, J. M., Stein, D. J., & Daniels, W. M. (2008). Maternal separation of rat pups increases the risk of developing depressive like behavior after subsequent chronic stress by altering corticosterone and neurotrophin levels in the hippocampus. Neuroscience Research, 61(1), 106–112. https://doi.org/10.1016/j.neures.2008.01.011
  • Matsuoka, M., Yokosuka, M., Mori, Y., & Ichikawa, M. (1999). Specific expression pattern of Fos in the accessory olfactory bulb of male mice after exposure to soiled bedding of females. Neuroscience Research, 35(3), 189–195. https://doi.org/10.1016/s0168-0102(99)00082-6
  • Ming, G. L., & Song, H. (2011). Adult neurogenesis in the mammalian brain: Significant answers and significant questions. Neuron, 70(4), 687–702. https://doi.org/10.1016/j.neuron.2011.05.001
  • Moreno, M. M., Linster, C., Escanilla, O., Sacquet, J., Didier, A., & Mandairon, N. (2009). Olfactory perceptual learning requires adult neurogenesis. Proceedings of the National Academy of Sciences of the United States of America, 106(42), 17980–17985. https://doi.org/10.1073/pnas.0907063106
  • Mori, K., von Campenhause, H., & Yoshihara, Y. (2000). Zonal organization of the mammalian main and accessory olfactory systems. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 355(1404), 1801–1812. https://doi.org/10.1098/rstb.2000.0736
  • Nishi, M., Horii-Hayashi, N., Sasagawa, T., & Matsunaga, W. (2013). Effects of early life stress on brain activity: Implications from maternal separation model in rodents. General and Comparative Endocrinology, 181, 306–309. https://doi.org/10.1016/j.ygcen.2012.09.024
  • Nunez-Parra, A., Pugh, V., & Araneda, R. C. (2011). Regulation of adult neurogenesis by behavior and age in the accessory olfactory bulb. Molecular and Cellular Neurosciences, 47(4), 274–285. https://doi.org/10.1016/j.mcn.2011.05.003
  • Oboti, L., Savalli, G., Giachino, C., De Marchis, S., Panzica, G. C., Fasolo, A., & Peretto, P. (2009). Integration and sensory experience-dependent survival of newly-generated neurons in the accessory olfactory bulb of female mice. The European Journal of Neuroscience, 29(4), 679–692. https://doi.org/10.1111/j.1460-9568.2009.06614.x
  • Petreanu, L., & Alvarez-Buylla, A. (2002). Maturation and death of adult-born olfactory bulb granule neurons: Role of olfaction. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 22(14), 6106–6113. https://doi.org/10.1523/JNEUROSCI.22-14-06106.2002
  • Plotsky, P. M., Thrivikraman, K. V., Nemeroff, C. B., Caldji, C., Sharma, S., & Meaney, M. J. (2005). Long-term consequences of neonatal rearing on central corticotropin-releasing factor systems in adult male rat offspring. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 30(12), 2192–2204. https://doi.org/10.1038/sj.npp.1300769
  • Portillo, W., Unda, N., Camacho, F. J., Sánchez, M., Corona, R., Arzate, D. M., Díaz, N. F., & Paredes, R. G. (2012). Sexual activity increases the number of newborn cells in the accessory olfactory bulb of male rats. Frontiers in Neuroanatomy, 6, 25. https://doi.org/10.3389/fnana.2012.00025
  • Rochefort, C., & Lledo, P. M. (2005). Short-term survival of newborn neurons in the adult olfactory bulb after exposure to a complex odor environment. The European Journal of Neuroscience, 22(11), 2863–2870. https://doi.org/10.1111/j.1460-9568.2005.04486.x
  • Roque, S., Mesquita, A. R., Palma, J. A., Sousa, N., & Correia-Neves, M. (2014). The behavioral and immunological impact of maternal separation: a matter of timing. Frontiers in Behavioral Neuroscience, 8, 1–10. https://doi.org/10.3389/fnbeh.2014.00192
  • Saghatelyan, A., Roux, P., Migliore, M., Rochefort, C., Desmaisons, D., Charneau, P., Shepherd, G. M., & Lledo, P. M. (2005). Activity-dependent adjustments of the inhibitory network in the olfactory bulb following early postnatal deprivation. Neuron, 46(1), 103–116. https://doi.org/10.1016/j.neuron.2005.02.016
  • Schmidt, M., Enthoven, L., van Woezik, J. H., Levine, S., de Kloet, E. R., & Oitzl, M. S. (2004). The dynamics of the hypothalamic-pituitary-adrenal axis during maternal deprivation. Journal of Neuroendocrinology, 16(1), 52–57. https://doi.org/10.1111/j.1365-2826.2004.01123.x
  • Schneider, N. Y., Chaudy, S., Epstein, A. L., Viollet, C., Benani, A., Pénicaud, L., Grosmaître, X., Datiche, F., & Gascuel, J. (2020). Centrifugal projections to the main olfactory bulb revealed by transsynaptic retrograde tracing in mice. The Journal of Comparative Neurology, 528(11), 1805–1819. https://doi.org/10.1002/cne.24846
  • Smeyne, R. J., Curran, T., & Morgan, J. I. (1992). Temporal and spatial expression of a fos-lacZ transgene in the developing nervous system. Brain Research. Molecular Brain Research, 16(1–2), 158–162. https://doi.org/10.1016/0169-328x(92)90206-q
  • Stanton, M. E., Gutierrez, Y. R., & Levine, S. (1988). Maternal deprivation potentiates pituitary-adrenal stress responses in infant rats. Behavioral Neuroscience, 102(5), 692–700. https://doi.org/10.1037//0735-7044.102.5.692
  • Suárez, R., García-González, D., & de Castro, F. (2012). Mutual influences between the main olfactory and vomeronasal systems in development and evolution. Frontiers in Neuroanatomy, 6, 50. https://doi.org/10.3389/fnana.2012.00050
  • Takahashi, L. K. (2014). Olfactory systems and neural circuits that modulate predator odor fear. Frontiers in Behavioral Neuroscience, 8, 72. https://doi.org/10.3389/fnbeh.2014.00072
  • Trinh, K., & Storm, D. R. (2003). Vomeronasal organ detects odorants in absence of signaling through main olfactory epithelium. Nature Neuroscience, 6(5), 519–525. https://doi.org/10.1038/nn1039
  • Zurawicki, L. (2010). Neuromarketing: Exploring the brain of the consumer (p. 22). Springer Science & Business Media.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.