The Olfactory Critical Period is Determined by Activity-dependent Sema7A/PlxnC1 Signaling Within Glomeruli

Overview

Journal Elife

Specialty Biology

Date 2021 Mar 29

PMID 33780330

Citations 14

Authors

Nobuko Inoue

Hirofumi Nishizumi

Rumi Ooyama

Kazutaka Mogi

Katsuhiko Nishimori

Takefumi Kikusui

Hitoshi Sakano

Affiliations

Soon will be listed here.

Abstract

In mice, early exposure to environmental odors affects social behaviors later in life. A signaling molecule, Semaphorin 7A (Sema7A), is induced in the odor-responding olfactory sensory neurons. Plexin C1 (PlxnC1), a receptor for Sema7A, is expressed in mitral/tufted cells, whose dendrite-localization is restricted to the first week after birth. Sema7A/PlxnC1 signaling promotes post-synaptic events and dendrite selection in mitral/tufted cells, resulting in glomerular enlargement that causes an increase in sensitivity to the experienced odor. Neonatal odor experience also induces positive responses to the imprinted odor. Knockout and rescue experiments indicate that oxytocin in neonates is responsible for imposing positive quality on imprinted memory. In the oxytocin knockout mice, the sensitivity to the imprinted odor increases, but positive responses cannot be promoted, indicating that Sema7A/PlxnC1 signaling and oxytocin separately function. These results give new insights into our understanding of olfactory imprinting during the neonatal critical period.

Citing Articles

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References

Sakano H . Neural map formation in the mouse olfactory system. Neuron. 2010; 67(4):530-42. DOI: 10.1016/j.neuron.2010.07.003. View

Insel T . The challenge of translation in social neuroscience: a review of oxytocin, vasopressin, and affiliative behavior. Neuron. 2010; 65(6):768-79. PMC: 2847497. DOI: 10.1016/j.neuron.2010.03.005. View

Gire D, Franks K, Zak J, Tanaka K, Whitesell J, Mulligan A . Mitral cells in the olfactory bulb are mainly excited through a multistep signaling path. J Neurosci. 2012; 32(9):2964-75. PMC: 3467005. DOI: 10.1523/JNEUROSCI.5580-11.2012. View

Takayanagi Y, Yoshida M, Bielsky I, Ross H, Kawamata M, Onaka T . Pervasive social deficits, but normal parturition, in oxytocin receptor-deficient mice. Proc Natl Acad Sci U S A. 2005; 102(44):16096-101. PMC: 1276060. DOI: 10.1073/pnas.0505312102. View

Hooks B, Chen C . Critical periods in the visual system: changing views for a model of experience-dependent plasticity. Neuron. 2007; 56(2):312-26. DOI: 10.1016/j.neuron.2007.10.003. View

Yogev S, Shen K . Cellular and molecular mechanisms of synaptic specificity. Annu Rev Cell Dev Biol. 2014; 30:417-37. DOI: 10.1146/annurev-cellbio-100913-012953. View

Hong W, Luo L . Genetic control of wiring specificity in the fly olfactory system. Genetics. 2014; 196(1):17-29. PMC: 3872183. DOI: 10.1534/genetics.113.154336. View

Nakashima A, Ihara N, Shigeta M, Kiyonari H, Ikegaya Y, Takeuchi H . Structured spike series specify gene expression patterns for olfactory circuit formation. Science. 2019; 365(6448). DOI: 10.1126/science.aaw5030. View

Liu A, Urban N . Prenatal and Early Postnatal Odorant Exposure Heightens Odor-Evoked Mitral Cell Responses in the Mouse Olfactory Bulb. eNeuro. 2017; 4(5). PMC: 5613225. DOI: 10.1523/ENEURO.0129-17.2017. View

10.

Smith A, Korgan A, Young W . Oxytocin delivered nasally or intraperitoneally reaches the brain and plasma of normal and oxytocin knockout mice. Pharmacol Res. 2019; 146:104324. PMC: 6679720. DOI: 10.1016/j.phrs.2019.104324. View

11.

Tsuboi A, Imai T, Kato H, Matsumoto H, Igarashi K, Suzuki M . Two highly homologous mouse odorant receptors encoded by tandemly-linked MOR29A and MOR29B genes respond differently to phenyl ethers. Eur J Neurosci. 2010; 33(2):205-13. DOI: 10.1111/j.1460-9568.2010.07495.x. View

12.

Nishimori K, Young L, Guo Q, Wang Z, Insel T, Matzuk M . Oxytocin is required for nursing but is not essential for parturition or reproductive behavior. Proc Natl Acad Sci U S A. 1996; 93(21):11699-704. PMC: 38121. DOI: 10.1073/pnas.93.21.11699. View

13.

Wilson D, Sullivan R . Neurobiology of associative learning in the neonate: early olfactory learning. Behav Neural Biol. 1994; 61(1):1-18. DOI: 10.1016/s0163-1047(05)80039-1. View

14.

Leung C, Coulombe P, Reed R . Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat Neurosci. 2007; 10(6):720-6. DOI: 10.1038/nn1882. View

15.

Sannino S, Chini B, Grinevich V . Lifespan oxytocin signaling: Maturation, flexibility, and stability in newborn, adolescent, and aged brain. Dev Neurobiol. 2016; 77(2):158-168. DOI: 10.1002/dneu.22450. View

16.

Graziadei P, Monti Graziadei G . Neurogenesis and plasticity of the olfactory sensory neurons. Ann N Y Acad Sci. 1985; 457:127-42. DOI: 10.1111/j.1749-6632.1985.tb20802.x. View

17.

Logan D, Brunet L, Webb W, Cutforth T, Ngai J, Stowers L . Learned recognition of maternal signature odors mediates the first suckling episode in mice. Curr Biol. 2012; 22(21):1998-2007. PMC: 3494771. DOI: 10.1016/j.cub.2012.08.041. View

18.

Spooren W, Schoeffter P, Gasparini F, Kuhn R, Gentsch C . Pharmacological and endocrinological characterisation of stress-induced hyperthermia in singly housed mice using classical and candidate anxiolytics (LY314582, MPEP and NKP608). Eur J Pharmacol. 2002; 435(2-3):161-70. DOI: 10.1016/s0014-2999(01)01562-x. View

19.

Mennella J, Jagnow C, Beauchamp G . Prenatal and postnatal flavor learning by human infants. Pediatrics. 2001; 107(6):E88. PMC: 1351272. DOI: 10.1542/peds.107.6.e88. View

20.

Andersson K . Neurotransmitters: central and peripheral mechanisms. Int J Impot Res. 2000; 12 Suppl 4:S26-33. DOI: 10.1038/sj.ijir.3900574. View