Expression of GABAergic and glutamatergic neurons after olfactory stimulation in the mouse piriform cortex during postnatal development

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Abstract

Introduction. The control of the survival and differentiation of immature neurons in the piriform cortex of rodents, which can transform into GABAergic and/or glutamatergic neurons under the influence of olfactory stimuli, is an important factor for prevention of neurological dysfunction.

The aim of the study was to assess the expression of GABAergic and glutamatergic neurons after olfactory stimulation (OS) in the mouse piriform cortex during postnatal development.

Materials and methods. The study was carried out on CD1 male mice aged 2 (n = 20; group Р2), 21 (n = 20; group Р21) and 60 (n = 20; group Р60) days. The mice were presented with olfactory stimuli, and brain tissue was collected for immunohistochemical analysis 2 hours, 24 hours and 7 days later, to assess glutamic acid decarboxylase 67 (GAD67) and vesicular glutamate transporter 1 (VGlut1) expression.

Results. OS in the group P2 animals increased VGlut1 expression in the first 2 hours after OS, followed by a return to baseline level by day 7, while GAD67 expression showed no significant changes. The animals in group P21 showed increased expression of VGlut1 and GAD67 two hours after OS, followed by a significant decrease. Expression of both molecules demonstrated a statistically significant increase in the group P60 animals 24 hours after OS, and remained at the same level on day 7 (GAD67) or returned to baseline levels (VGlut1).

Conclusion. OS increases the number of GABAergic (GAD67+) и glutamatergic (VGlut1+) neurons in the piriform cortex (P60). The predominance of glutamatergic effects is a possible mechanism for associative memory cell recruitment.

About the authors

Yulia A. Panina

Research Institute of Molecular Medicine and Pathobiochemistry, Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Author for correspondence.
Email: annaly-nevrologii@neurology.ru
ORCID iD: 0000-0002-8675-3489

Cand. Sci. (Med.), researcher

Russian Federation, Krasnoyarsk

Yulia A. Uspenskaya

Krasnoyarsk State Agrarian University

Email: annaly-nevrologii@neurology.ru
ORCID iD: 0000-0003-4386-9753

D. Sci. (Biol.), Associate Professor, Professor of the Institute of Applied Biotechnologies and Veterinary Medicine

Russian Federation, Krasnoyarsk

Olga L. Lopatina

Center for collective use Molecular & Cell Technologies, Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University

Email: annaly-nevrologii@neurology.ru
ORCID iD: 0000-0002-7884-2721

D. Sci. (Biol.), Associate Professor, leading researcher

Russian Federation, Krasnoyarsk

Alla B. Salmina

Research Institute of Molecular Medicine and Pathobiochemistry, Prof. V.F. Voino-Yasenetsky Krasnoyarsk State Medical University; Research Center of Neurology

Email: annaly-nevrologii@neurology.ru
ORCID iD: 0000-0003-4012-6348

D. Sci. (Med.), Prof., chief researcher, Head, Laboratory of experimental brain cytology, Department of brain sciences, chief researcher

Russian Federation, Krasnoyarsk; Moscow

References

  1. Cassé F., Richetin K., Toni N. Astrocytes’ contribution to adult neurogenesis in physiology and Alzheimer’s disease. Front Cell Neurosci. 2018;12:432. doi: 10.3389/fncel.2018.00432. PMID: 30538622.
  2. Berg D.A., Su Y., Jimenez-Cyrus D. et al. A common embryonic origin of stem cells drives developmental and adult neurogenesis. Cell. 2019;177(3):654.e15–668.e15. doi: 10.1016/j.cell.2019.02.010. PMID: 30929900.
  3. Chareyron L.J., Amaral D.G., Lavenexa P. Selective lesion of the hippocampus increases the differentiation of immature neurons in the monkey amygdala. Proc Natl Acad Sci USA. 2016;113(50):14420–14425. doi: 10.1073/pnas.1604288113. PMID: 27911768.
  4. Lietzau G., Nyström T., Wang Z. et al. Western diet accelerates the impairment of odor-related learning and olfactory memory in the mouse. ACS Chem Neurosci. 2020;11(21):3590–3602. doi: 10.1021/acschemneuro.0c00466. PMID: 33054173.
  5. La Rosa C., Parolisi R., Bonfanti L. Brain structural plasticity: from adult neurogenesis to immature neurons. Front Neurosci. 2020;14:75. doi: 10.3389/fnins.2020.00075. PMID: 32116519.
  6. Rotheneichner P., Belles M., Benedetti B. et al. Cellular plasticity in the adult murine piriform cortex: continuous maturation of dormant precursors into excitatory neurons. Cereb Cortex. 2018;28(7):2610–2621. doi: 10.1093/cercor/bhy087. PMID: 29688272.
  7. Benedetti B., Dannehl D., König R. et al. Functional integration of neuronal precursors in the adult murine piriform cortex. Cereb Cortex. 2020;30(3):1499–1515. doi: 10.1093/cercor/bhz181. PMID: 31647533.
  8. Nacher J., Alonso-Llosa G., Rosell D., McEwen B. PSA-NCAM expression in the piriform cortex of the adult rat. Modulation by NMDA receptor antagonist administration. Brain Res. 2002;927(2):111–121. doi: 10.1016/s0006-8993(01)03241-3. PMID: 11821005.
  9. Coviello S., Gramuntell Y., Castillo-Gomez E., Nacher J. Effects of dopamine on the immature neurons of the adult rat piriform cortex. Front Neurosci. 2020;14:574234. doi: 10.3389/fnins.2020.574234. PMID: 33122993.
  10. Meissner-Bernard C., Dembitskaya Y., Venance L., Fleischmann A. Encoding of odor fear memories in the mouse olfactory cortex. Curr Biol. 2019;29(3):367–380.e4. doi: 10.1016/j.cub.2018.12.003. PMID: 30612908.
  11. Rubio A., Belles M., Belenguer G. et al. Characterization and isolation of immature neurons of the adult mouse piriform cortex. Dev Neurobiol. 2016;76(7):748–763. doi: 10.1002/dneu.22357. PMID: 26487449.
  12. He X., Zhang X.-M., Wu J. et al. Olfactory experience modulates immature neuron development in postnatal and adult guinea pig piriform cortex. Neuroscience. 2014; 259:101–112. doi: 10.1016/j.neuroscience.2013.11.056. PMID: 24316472.
  13. Bahuleyan B., Singh S. Olfactory memory impairment in neurodege- nerative diseases. J Clin Diagn Res. 2012;6(8):1437–1441. doi: 10.7860/JCDR/2012/3408.2382. PMID: 23205370.
  14. Van den Bergh B.R.H., Dahnke R., Mennes M. Prenatal stress and the developing brain: risks for neurodevelopmental disorders. Dev Psychopathol. 2018;30(3):743–762. doi: 10.1017/S0954579418000342. PMID: 30068407.
  15. Mouly A.M., Sullivan R. Memory and plasticity in the olfactory system: from infancy to adulthood. In: Menini A. (eds.). The neurobiology of olfaction. Boca Raton, 2010:367–392.
  16. Van der Linden C.J., Gupta P., Bhuiya A.I. et al. Olfactory stimulation regu-lates the birth of neurons that express specific odorant receptors. Cell Reports. 2020;33(1):108210. doi: 10.1016/j.celrep.2020.108210. PMID: 33027656.
  17. Bartocci M., Winberg J., Ruggiero C. et al. Activation of olfactory cortex in newborn infants after odor stimulation: a functional near-infrared spectroscopy study. Pediatr Res. 2000;48(1):18–23. doi: 10.1203/00006450-200007000-00006. PMID: 10879795.
  18. Liu Y., Gao Z., Chen C. et al. Piriform cortical glutamatergic and GABAergic neurons express coordinated plasticity for whisker-induced odor recall. Oncotarget. 2017;8(56):95719–95740. doi: 10.18632/oncotarget.21207. PMID: 29221161.
  19. Sarma A.A., Richard M.B., Greer C.A. Developmental dynamics of piriform cortex. Cereb Cortex. 2011;21(6):1231–1245. doi: 10.1093/cercor/bhq199. PMID: 21041199.
  20. Navarro D., Alvarado M., Figueroa A. et al. Distribution of GABAergic neurons and VGluT1 and VGAT immunoreactive boutons in the ferret (mustela putorius) piriform cortex and endopiriform nucleus. Comparison with visual areas 17, 18 and 19. Front Neuroanat. 2019;13:54. doi: 10.3389/fnana.2019. 00054. PMID: 31213994.
  21. Ben-Ari Y. The GABA excitatory/inhibitory developmental sequence: a personal journey. Neuroscience. 2014;279:187–219. doi: 10.1016/j.neuroscience.2014.08.001. PMID: 25168736.
  22. Plachez C., Puche A.C. Early specification of GAD67 subventricular derived olfactory interneurons. J Mol Histol. 2012;43(2):215–221. doi: 10.1007/s10735-012-9394-2. PMID: 22389027.
  23. Yuan T.F., Liang Y.X., So K.F. Occurrence of new neurons in the piriform cortex. Front Neuroanat. 2014;8:167. doi: 10.3389/fnana.2014.00167. PMID: 25653597.
  24. Bovetti S., Veyrac A., Peretto P. et al. Olfactory enrichment influences adult neurogenesis modulating GAD67 and plasticity-related molecules expression in newborn cells of the olfactory bulb. PLoS One. 2009;4(7):e6359. doi: 10.1371/journal.pone.0006359. PMID: 19626121.
  25. Komleva Iu.K., Salmina A.B., Prokopenko S.V. et al. Changes in structural and functional plasticity of the brain induced by environmental enrichment. Vestn Ross Akad Med Nauk. 2013;(6):39–48. doi: 10.15690/vramn.v68i6.672. PMID: 24340634.
  26. Lopatina O.L., Panina Y.A., Malinovskaya N.A., Salmina A.B. Early life stress and brain plasticity: from molecular alterations to aberrant memory and behavior. Rev Neurosci. 2020;32(2):131–142. doi: 10.1515/revneuro-2020-0077. PMID: 33550784.
  27. Danik M., Cassoly E., Manseau F. et al. Frequent coexpression of the vesicu- lar glutamate transporter 1 and 2 genes, as well as coexpression with genes for choline acetyltransferase or glutamic acid decarboxylase in neurons of rat brain. J Neurosci Res. 2005;81(4):506–521. doi: 10.1002/jnr.20500. PMID: 15983996.
  28. Hnasko T.S., Edwards R.H. Neurotransmitter corelease: mechanism and physiological role. Annu Rev Physiol. 2012;74:225–243. doi: 10.1146/annurev-physiol-020911-153315. PMID: 22054239.
  29. Zimmermann J., Herman M.A., Rosenmund C. Co-release of glutamate and GABA from single vesicles in GABAergic neurons exogenously expressing VGLUT3. Front Synaptic Neurosci. 2015;7:16. doi: 10.3389/fnsyn.2015.00016. PMID: 26441632.

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2. Fig. 1. VGlut1 and GAD67 expression on the piriform cortex cells of animals (Р60) in the control group (А) and experimental groups, 2 hours (В), 24 hours (С) and 7 days (D) after OS.

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3. Fig. 2. Number of cells (%) expressing VGlut1 (А), GAD67 (В) and coexpressing GAD67 and VGlut1 (С) in the piriform cortex of animals in the control and experimental groups, 2 hours, 24 hours and 7 days after OS. Five animals, 5 sections from each animal, 5 fields of view in each group. The sample contained 25 specimens. *р < 0.01 (one-way ANOVA with a subsequent post-hoc Bonferroni test).

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Copyright (c) 2022 Panina Y.A., Uspenskaya Y.A., Lopatina O.L., Salmina A.B.

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