DOI QR코드

DOI QR Code

Distinct Developmental Features of Olfactory Bulb Interneurons

  • Kim, Jae Yeon (Department of Brain and Cognitive Sciences, Graduate School, Daegu Gyeongbuk Institute of Science and Technology) ;
  • Choe, Jiyun (Department of Brain and Cognitive Sciences, Graduate School, Daegu Gyeongbuk Institute of Science and Technology) ;
  • Moon, Cheil (Department of Brain and Cognitive Sciences, Graduate School, Daegu Gyeongbuk Institute of Science and Technology)
  • Received : 2020.01.30
  • Accepted : 2020.03.02
  • Published : 2020.03.31

Abstract

The olfactory bulb (OB) has an extremely higher proportion of interneurons innervating excitatory neurons than other brain regions, which is evolutionally conserved across species. Despite the abundance of OB interneurons, little is known about the diversification and physiological functions of OB interneurons compared to cortical interneurons. In this review, an overview of the general developmental process of interneurons from the angles of the spatial and temporal specifications was presented. Then, the distinct features shown exclusively in OB interneurons development and molecular machinery recently identified were discussed. Finally, we proposed an evolutionary meaning for the diversity of OB interneurons.

Keywords

References

  1. Alvarez-Buylla, A., Garcia-Verdugo, J.M., and Tramontin, A.D. (2001). A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2, 287-293. https://doi.org/10.1038/35067582
  2. Anderson, J.S., Carandini, M., and Ferster, D. (2000). Orientation tuning of input conductance, excitation, and inhibition in cat primary visual cortex. J. Neurophysiol. 84, 909-926. https://doi.org/10.1152/jn.2000.84.2.909
  3. Ashwin, C., Chapman, E., Howells, J., Rhydderch, D., Walker, I., and Baron-Cohen, S. (2014). Enhanced olfactory sensitivity in autism spectrum conditions. Mol. Autism 5, 53. https://doi.org/10.1186/2040-2392-5-53
  4. Bandler, R.C., Mayer, C., and Fishell, G. (2017). Cortical interneuron specification: the juncture of genes, time and geometry. Curr. Opin. Neurobiol. 42, 17-24. https://doi.org/10.1016/j.conb.2016.10.003
  5. Bartolini, G., Ciceri, G., and Marin, O. (2013). Integration of GABAergic interneurons into cortical cell assemblies: lessons from embryos and adults. Neuron 79, 849-864. https://doi.org/10.1016/j.neuron.2013.08.014
  6. Batista-Brito, R., Close, J., Machold, R., and Fishell, G. (2008). The distinct temporal origins of olfactory bulb interneuron subtypes. J. Neurosci. 28, 3966-3975. https://doi.org/10.1523/JNEUROSCI.5625-07.2008
  7. Batista-Brito, R. and Fishell, G. (2009). The developmental integration of cortical interneurons into a functional network. Curr. Top. Dev. Biol. 87, 81-118. https://doi.org/10.1016/S0070-2153(09)01203-4
  8. Bayer, S.A. (1983). 3H-thymidine-radiographic studies of neurogenesis in the rat olfactory bulb. Exp. Brain Res. 50, 329-340.
  9. Bovetti, S., Peretto, P., Fasolo, A., and De Marchis, S. (2007). Spatiotemporal specification of olfactory bulb interneurons. J. Mol. Histol. 38, 563-569. https://doi.org/10.1007/s10735-007-9111-8
  10. Burton, S.D. (2017). Inhibitory circuits of the mammalian main olfactory bulb. J. Neurophysiol. 118, 2034-2051. https://doi.org/10.1152/jn.00109.2017
  11. Bushdid, C., Magnasco, M.O., Vosshall, L.B., and Keller, A. (2014). Humans can discriminate more than 1 trillion olfactory stimuli. Science 343, 1370-1372. https://doi.org/10.1126/science.1249168
  12. D'Amour, J.A. and Froemke, R.C. (2015). Inhibitory and excitatory spiketiming-dependent plasticity in the auditory cortex. Neuron 86, 514-528. https://doi.org/10.1016/j.neuron.2015.03.014
  13. Donato, F., Chowdhury, A., Lahr, M., and Caroni, P. (2015). Early- and late-born parvalbumin basket cell subpopulations exhibiting distinct regulation and roles in learning. Neuron 85, 770-786. https://doi.org/10.1016/j.neuron.2015.01.011
  14. Fairen, A., Cobas, A., and Fonseca, M. (1986). Times of generation of glutamic acid decarboxylase immunoreactive neurons in mouse somatosensory cortex. J. Comp. Neurol. 251, 67-83. https://doi.org/10.1002/cne.902510105
  15. Fang, W.Q., Chen, W.W., Jiang, L., Liu, K., Yung, W.H., Fu, A.K.Y., and Ip, N.Y. (2014). Overproduction of upper-layer neurons in the neocortex leads to autism-like features in mice. Cell Rep. 9, 1635-1643. https://doi.org/10.1016/j.celrep.2014.11.003
  16. Fertuzinhos, S., Krsnik, Z., Kawasawa, Y.I., Rasin, M.R., Kwan, K.Y., Chen, J.G., Judas, M., Hayashi, M., and Sestan, N. (2009). Selective depletion of molecularly defined cortical interneurons in human holoprosencephaly with severe striatal hypoplasia. Cereb. Cortex 19, 2196-2207. https://doi.org/10.1093/cercor/bhp009
  17. Fuentealba, L.C., Rompani, S.B., Parraguez, J.I., Obernier, K., Romero, R., Cepko, C.L., and Alvarez-Buylla, A. (2015). Embryonic origin of postnatal neural stem cells. Cell 161, 1644-1655. https://doi.org/10.1016/j.cell.2015.05.041
  18. Fujiwara, N. and Cave, J.W. (2016). Partial conservation between mice and humans in olfactory bulb interneuron transcription factor codes. Front. Neurosci. 10, 337.
  19. Galle, S.A., Courchesne, V., Mottron, L., and Frasnelli, J. (2013). Olfaction in the autism spectrum. Perception 42, 341-355. https://doi.org/10.1068/p7337
  20. Garcia, I., Quast, K.B., Huang, L., Herman, A.M., Selever, J., Deussing, J.M., Justice, N.J., and Arenkiel, B.R. (2014). Local CRH signaling promotes synaptogenesis and circuit integration of adult-born neurons. Dev. Cell 30, 645-659. https://doi.org/10.1016/j.devcel.2014.07.001
  21. Gomes, E., Pedroso, F.S., and Wagner, M.B. (2008). Auditory hypersensitivity in the autistic spectrum disorder. Pro Fono 20, 279-284. https://doi.org/10.1590/S0104-56872008000400013
  22. Greer, C.A. (1987). Golgi analyses of dendritic organization among denervated olfactory bulb granule cells. J. Comp. Neurol. 257, 442-452. https://doi.org/10.1002/cne.902570311
  23. Hansen, D.V., Lui, J.H., Flandin, P., Yoshikawa, K., Rubenstein, J.L., Alvarez-Buylla, A., and Kriegstein, A.R. (2013). Non-epithelial stem cells and cortical interneuron production in the human ganglionic eminences. Nat. Neurosci. 16, 1576-1587. https://doi.org/10.1038/nn.3541
  24. Hinds, J.W. (1968). Autoradiographic study of histogenesis in the mouse olfactory bulb. I. Time of origin of neurons and neuroglia. J. Comp. Neurol. 134, 287-304. https://doi.org/10.1002/cne.901340304
  25. Hu, J.S., Vogt, D., Sandberg, M., and Rubenstein, J.L. (2017). Cortical interneuron development: a tale of time and space. Development 144, 3867-3878. https://doi.org/10.1242/dev.132852
  26. Huang, L., Ung, K., Garcia, I., Quast, K.B., Cordiner, K., Saggau, P., and Arenkiel, B.R. (2016). Task learning promotes plasticity of interneuron connectivity maps in the olfactory bulb. J. Neurosci. 36, 8856-8871. https://doi.org/10.1523/JNEUROSCI.0794-16.2016
  27. Igarashi, K.M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., Kobayakawa, R., Tanifuji, M., Sakano, H., Chen, W.R., et al. (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32, 7970-7985. https://doi.org/10.1523/JNEUROSCI.0154-12.2012
  28. Kao, C.F. and Lee, T. (2010). Birth time/order-dependent neuron type specification. Curr. Opin. Neurobiol. 20, 14-21. https://doi.org/10.1016/j.conb.2009.10.017
  29. Kay, L.M. and Sherman, S.M. (2007). An argument for an olfactory thalamus. Trends Neurosci. 30, 47-53. https://doi.org/10.1016/j.tins.2006.11.007
  30. Kepecs, A. and Fishell, G. (2014). Interneuron cell types are fit to function. Nature 505, 318-326. https://doi.org/10.1038/nature12983
  31. Kim, J.Y., Cho, B., and Moon, C. (2020). Timely inhibitory circuit formation controlled by Abl1 regulates innate olfactory behaviors in mouse. Cell Rep. 30, 187-201.e4. https://doi.org/10.1016/j.celrep.2019.12.004
  32. Lemasson, M., Saghatelyan, A., Olivo-Marin, J.C., and Lledo, P.M. (2005). Neonatal and adult neurogenesis provide two distinct populations of newborn neurons to the mouse olfactory bulb. J. Neurosci. 25, 6816-6825. https://doi.org/10.1523/JNEUROSCI.1114-05.2005
  33. Lepousez, G., Nissant, A., and Lledo, P.M. (2015). Adult neurogenesis and the future of the rejuvenating brain circuits. Neuron 86, 387-401. https://doi.org/10.1016/j.neuron.2015.01.002
  34. Lim, L., Mi, D., Llorca, A., and Marin, O. (2018). Development and functional diversification of cortical interneurons. Neuron 100, 294-313. https://doi.org/10.1016/j.neuron.2018.10.009
  35. Liu, G., Froudarakis, E., Patel, J.M., Kochukov, M.Y., Pekarek, B., Hunt, P.J., Patel, M., Ung, K., Fu, C.H., Jo, J., et al. (2019). Target specific functions of EPL interneurons in olfactory circuits. Nat. Commun. 10, 3369. https://doi.org/10.1038/s41467-019-11354-y
  36. Lledo, P.M., Merkle, F.T., and Alvarez-Buylla, A. (2008). Origin and function of olfactory bulb interneuron diversity. Trends Neurosci. 31, 392-400. https://doi.org/10.1016/j.tins.2008.05.006
  37. Lledo, P.M. and Valley, M. (2016). Adult olfactory bulb neurogenesis. Cold Spring Harb. Perspect. Biol. 8, a018945. https://doi.org/10.1101/cshperspect.a018945
  38. Lois, C. and Alvarez-Buylla, A. (1994). Long-distance neuronal migration in the adult mammalian brain. Science 264, 1145-1148. https://doi.org/10.1126/science.8178174
  39. Ma, Y., Hu, H., Berrebi, A.S., Mathers, P.H., and Agmon, A. (2006). Distinct subtypes of somatostatin-containing neocortical interneurons revealed in transgenic mice. J. Neurosci. 26, 5069-5082. https://doi.org/10.1523/JNEUROSCI.0661-06.2006
  40. Maccaferri, G. and Lacaille, J.C. (2003). Interneuron diversity series: hippocampal interneuron classifications--making things as simple as possible, not simpler. Trends Neurosci. 26, 564-571. https://doi.org/10.1016/j.tins.2003.08.002
  41. Marco, E.J., Hinkley, L.B., Hill, S.S., and Nagarajan, S.S. (2011). Sensory processing in autism: a review of neurophysiologic findings. Pediatr. Res. 69(5 Pt 2), 48R-54R. https://doi.org/10.1203/PDR.0b013e3182130c54
  42. Mayer, C., Jaglin, X.H., Cobbs, L.V., Bandler, R.C., Streicher, C., Cepko, C.L., Hippenmeyer, S., and Fishell, G. (2015). Clonally related forebrain interneurons disperse broadly across both functional areas and structural boundaries. Neuron 87, 989-998. https://doi.org/10.1016/j.neuron.2015.07.011
  43. Mirich, J.M., Williams, N.C., Berlau, D.J., and Brunjes, P.C. (2002). Comparative study of aging in the mouse olfactory bulb. J. Comp. Neurol. 454, 361-372. https://doi.org/10.1002/cne.10426
  44. Mori, K. (1987). Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog. Neurobiol. 29, 275-320. https://doi.org/10.1016/0301-0082(87)90024-4
  45. Muthusamy, N., Zhang, X., Johnson, C.A., Yadav, P.N., and Ghashghaei, H.T. (2017). Developmentally defined forebrain circuits regulate appetitive and aversive olfactory learning. Nat. Neurosci. 20, 20-23. https://doi.org/10.1038/nn.4452
  46. Nagayama, S., Homma, R., and Imamura, F. (2014). Neuronal organization of olfactory bulb circuits. Front. Neural Circuits 8, 98. https://doi.org/10.3389/fncir.2014.00098
  47. Orona, E., Scott, J.W., and Rainer, E.C. (1983). Different granule cell populations innervate superficial and deep regions of the external plexiform layer in rat olfactory bulb. J. Comp. Neurol. 217, 227-237. https://doi.org/10.1002/cne.902170209
  48. Osterhout, J.A., El-Danaf, R.N., Nguyen, P.L., and Huberman, A.D. (2014). Birthdate and outgrowth timing predict cellular mechanisms of axon target matching in the developing visual pathway. Cell Rep. 8, 1006-1017. https://doi.org/10.1016/j.celrep.2014.06.063
  49. Paredes, M.F., James, D., Gil-Perotin, S., Kim, H., Cotter, J.A., Ng, C., Sandoval, K., Rowitch, D.H., Xu, D., McQuillen, P.S., et al. (2016). Extensive migration of young neurons into the infant human frontal lobe. Science 354, aaf7073. https://doi.org/10.1126/science.aaf7073
  50. Petreanu, L. and Alvarez-Buylla, A. (2002). Maturation and death of adultborn olfactory bulb granule neurons: role of olfaction. J. Neurosci. 22, 6106-6113. https://doi.org/10.1523/JNEUROSCI.22-14-06106.2002
  51. Price, J.L. and Powell, T.P. (1970). The morphology of the granule cells of the olfactory bulb. J. Cell Sci. 7, 91-123. https://doi.org/10.1242/jcs.7.1.91
  52. Puelles, L. and Rubenstein, J.L. (1993). Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggest a neuromeric organization. Trends Neurosci. 16, 472-479. https://doi.org/10.1016/0166-2236(93)90080-6
  53. Rall, W., Shepherd, G.M., Reese, T.S., and Brightman, M.W. (1966). Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp. Neurol. 14, 44-56. https://doi.org/10.1016/0014-4886(66)90023-9
  54. Ramon y Cajal, S., DeFelipe, J., and Jones, E.G. (1988). Cajal on the Cerebral Cortex: An Annotated Translation of the Complete Writings (New York: Oxford University Press).
  55. Rubenstein, J.L., Martinez, S., Shimamura, K., and Puelles, L. (1994). The embryonic vertebrate forebrain: the prosomeric model. Science 266, 578-580. https://doi.org/10.1126/science.7939711
  56. Rymar, V.V. and Sadikot, A.F. (2007). Laminar fate of cortical GABAergic interneurons is dependent on both birthdate and phenotype. J. Comp. Neurol. 501, 369-380. https://doi.org/10.1002/cne.21250
  57. Takahashi, H., Ogawa, Y., Yoshihara, S., Asahina, R., Kinoshita, M., Kitano, T., Kitsuki, M., Tatsumi, K., Okuda, M., Tatsumi, K., et al. (2016). A subtype of olfactory bulb interneurons is required for odor detection and discrimination behaviors. J. Neurosci. 36, 8210-8227. https://doi.org/10.1523/JNEUROSCI.2783-15.2016
  58. Tonacci, A., Billeci, L., Tartarisco, G., Ruta, L., Muratori, F., Pioggia, G., and Gangemi, S. (2017). [Formula: see text]Olfaction in autism spectrum disorders: a systematic review. Child Neuropsychol. 23, 1-25. https://doi.org/10.1080/09297049.2015.1081678
  59. Torigoe, M., Yamauchi, K., Kimura, T., Uemura, Y., and Murakami, F. (2016). Evidence that the laminar fate of LGE/CGE-derived neocortical interneurons is dependent on their progenitor domains. J. Neurosci. 36, 2044-2056. https://doi.org/10.1523/JNEUROSCI.3550-15.2016
  60. Tseng, C.S., Chao, H.W., Huang, H.S., and Huang, Y.S. (2017). Olfactory-experience- and developmental-stage-dependent control of CPEB4 regulates c-Fos mRNA translation for granule cell survival. Cell Rep. 21, 2264-2276. https://doi.org/10.1016/j.celrep.2017.10.100
  61. Wamsley, B. and Fishell, G. (2017). Genetic and activity-dependent mechanisms underlying interneuron diversity. Nat. Rev. Neurosci. 18, 299-309. https://doi.org/10.1038/nrn.2017.30
  62. Wang, J.Y., Ledley, F., Goff, S., Lee, R., Groner, Y., and Baltimore, D. (1984). The mouse c-abl locus: molecular cloning and characterization. Cell 36, 349-356. https://doi.org/10.1016/0092-8674(84)90228-9
  63. Yoshihara, S., Takahashi, H., Nishimura, N., Kinoshita, M., Asahina, R., Kitsuki, M., Tatsumi, K., Furukawa-Hibi, Y., Hirai, H., Nagai, T., et al. (2014). Npas4 regulates Mdm2 and thus Dcx in experience-dependent dendritic spine development of newborn olfactory bulb interneurons. Cell Rep. 8, 843-857. https://doi.org/10.1016/j.celrep.2014.06.056
  64. Yoshihara, S., Takahashi, H., Nishimura, N., Naritsuka, H., Shirao, T., Hirai, H., Yoshihara, Y., Mori, K., Stern, P.L., and Tsuboi, A. (2012). 5T4 glycoprotein regulates the sensory input-dependent development of a specific subtype of newborn interneurons in the mouse olfactory bulb. J. Neurosci. 32, 2217-2226. https://doi.org/10.1523/JNEUROSCI.5907-11.2012
  65. Zapiec, B., Dieriks, B.V., Tan, S., Faull, R.L.M., Mombaerts, P., and Curtis, M.A. (2017). A ventral glomerular deficit in Parkinson's disease revealed by whole olfactory bulb reconstruction. Brain 140, 2722-2736. https://doi.org/10.1093/brain/awx208
  66. Zozulya, S., Echeverri, F., and Nguyen, T. (2001). The human olfactory receptor repertoire. Genome Biol. 2, RESEARCH0018.

Cited by

  1. Unraveling the Role of Dopaminergic and Calretinin Interneurons in the Olfactory Bulb vol.15, 2020, https://doi.org/10.3389/fncir.2021.718221
  2. COVID-19 and Parkinson’s disease: Defects in neurogenesis as the potential cause of olfactory system impairments and anosmia vol.115, 2021, https://doi.org/10.1016/j.jchemneu.2021.101965
  3. Environmental enrichment ameliorates high-fat diet induced olfactory deficit and decrease of parvalbumin neurons in the olfactory bulb in mice vol.179, 2020, https://doi.org/10.1016/j.brainresbull.2021.11.015