Molecular identity of periglomerular and short axon cells.
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.
Kiyokage
Emi
E
Department of Anatomy and Neurobiology, University of Maryland, School of Medicine, Baltimore, Maryland 21201, USA.
Pan
Yu-Zhen
YZ
Shao
Zuoyi
Z
Kobayashi
Kazuto
K
Szabo
Gabor
G
Yanagawa
Yuchio
Y
Obata
Kunihiko
K
Okano
Hideyuki
H
Toida
Kazunori
K
Puche
Adam C
AC
Shipley
Michael T
MT
D000596:Amino Acids / Q000378:metabolism; D000818:Animals; D001369:Axons / Q000502:physiology*; D001703:Biophysics; D004558:Electric Stimulation; D019706:Excitatory Postsynaptic Potentials / Q000502:physiology; D005968:Glutamate Decarboxylase / Q000235:genetics; D049452:Green Fluorescent Proteins / Q000235:genetics; D008239:Lysine / Q000031:analogs & derivatives / Q000378:metabolism; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D008959:Models, Neurological; D009415:Nerve Net / Q000166:cytology / Q000378:metabolism; D009833:Olfactory Pathways / Q000166:cytology*; D018408:Patch-Clamp Techniques / Q000379:methods; D011984:Sensory Receptor Cells / Q000145:classification* / Q000166:cytology* / Q000378:metabolism; D013266:Stilbamidines / Q000378:metabolism; D014446:Tyrosine 3-Monooxygenase / Q000235:genetics
C049774:2-hydroxy-4,4'-diamidinostilbene, methanesulfonate salt; D000596:Amino Acids; D013266:Stilbamidines; C098463:dolaisoleucine; D049452:Green Fluorescent Proteins; D014446:Tyrosine 3-Monooxygenase; D005968:Glutamate Decarboxylase; C402565:glutamate decarboxylase 1; C401141:glutamate decarboxylase 2; C013411:biocytin; D008239:Lysine