Molecular identity of periglomerular and short axon cells

Emi Kiyokage, Yu Zhen Pan, Zuoyi Shao, Kazuto Kobayashi, Gabor Szabo, Yuchio Yanagawa, Kunihiko Obata, Hideyuki Okano, Kazunori Toida, Adam C. Puche, Michael T. Shipley

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Abstract

Within glomeruli, the initial sites of synaptic integration in the olfactory pathway, olfactory sensory axons terminate on dendrites of projection and juxtaglomerular (JG) neurons. JG cells form at least two major circuits: the classic intraglomerular circuit consisting of external tufted (ET) and periglomerular (PG) cells and an interglomerular circuit comprised of the long-range connections of short axon (SA) cells. We examined the projections and the synaptic inputs of identified JG cell chemotypes using mice expressing green fluorescent protein (GFP) driven by the promoter for glutamic acid decarboxylase (GAD) 65 kDa, 67 kDa, or tyrosine hydroxylase (TH). Virtually all (97%) TH+ cells are also GAD67+ and are thus DAergic-GABAergic neurons. Using a combination of retrograde tracing, whole-cell patch-clamp recording, and single-cell three-dimensional reconstruction, we show that different JG cell chemotypes contribute to distinct microcircuits within or between glomeruli. GAD65+ GABAergic PG cells ramify principally within one glomerulus and participate in uniglomerular circuits. DAergic-GABAergic cells have extensive interglomerular projections. DAergic-GABAergic SA cells comprise two subgroups. One subpopulation contacts 5-12 glomeruli and is referred to as "oligoglomerular." Approximately one-third of these oligoglomerular DAergic SA cells receive direct olfactory nerve (ON) synaptic input, and the remaining two-thirds receive input via a disynaptic ON→ET→SA circuit. The second population of DAergic-GABAergic SA cells also disynaptic ON input and connect tens to hundreds of glomeruli in an extensive " polyglomerular" network. Although DAergic JG cells have traditionally been considered PG cells, their interglomerular connections argue that they are more appropriately classified as SA cells.

Original languageEnglish
Pages (from-to)1185-1196
Number of pages12
JournalJournal of Neuroscience
Volume30
Issue number3
DOIs
Publication statusPublished - 2010 Jan 20

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Axons
Olfactory Nerve
Tyrosine 3-Monooxygenase
GABAergic Neurons
Olfactory Pathways
Glutamate Decarboxylase
Dendrites
Green Fluorescent Proteins

ASJC Scopus subject areas

  • Neuroscience(all)
  • Medicine(all)

Cite this

Kiyokage, E., Pan, Y. Z., Shao, Z., Kobayashi, K., Szabo, G., Yanagawa, Y., ... Shipley, M. T. (2010). Molecular identity of periglomerular and short axon cells. Journal of Neuroscience, 30(3), 1185-1196. https://doi.org/10.1523/JNEUROSCI.3497-09.2010

Molecular identity of periglomerular and short axon cells. / Kiyokage, Emi; Pan, Yu Zhen; Shao, Zuoyi; Kobayashi, Kazuto; Szabo, Gabor; Yanagawa, Yuchio; Obata, Kunihiko; Okano, Hideyuki; Toida, Kazunori; Puche, Adam C.; Shipley, Michael T.

In: Journal of Neuroscience, Vol. 30, No. 3, 20.01.2010, p. 1185-1196.

Research output: Contribution to journalArticle

Kiyokage, E, Pan, YZ, Shao, Z, Kobayashi, K, Szabo, G, Yanagawa, Y, Obata, K, Okano, H, Toida, K, Puche, AC & Shipley, MT 2010, 'Molecular identity of periglomerular and short axon cells', Journal of Neuroscience, vol. 30, no. 3, pp. 1185-1196. https://doi.org/10.1523/JNEUROSCI.3497-09.2010
Kiyokage E, Pan YZ, Shao Z, Kobayashi K, Szabo G, Yanagawa Y et al. Molecular identity of periglomerular and short axon cells. Journal of Neuroscience. 2010 Jan 20;30(3):1185-1196. https://doi.org/10.1523/JNEUROSCI.3497-09.2010
Kiyokage, Emi ; Pan, Yu Zhen ; Shao, Zuoyi ; Kobayashi, Kazuto ; Szabo, Gabor ; Yanagawa, Yuchio ; Obata, Kunihiko ; Okano, Hideyuki ; Toida, Kazunori ; Puche, Adam C. ; Shipley, Michael T. / Molecular identity of periglomerular and short axon cells. In: Journal of Neuroscience. 2010 ; Vol. 30, No. 3. pp. 1185-1196.
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