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Spatial distribution of synapses on tyrosine hydroxylase-expressing juxtaglomerular cells in the mouse olfactory glomerulus.
J Comp Neurol 2017; 525(5):1059-1074JC

Abstract

Olfactory sensory axons converge in specific glomeruli where they form excitatory synapses onto dendrites of mitral/tufted (M/T) and juxtaglomerular (JG) cells, including periglomerular (PG), external tufted (ET), and superficial-short axon cells. JG cells consist of heterogeneous subpopulations with different neurochemical, physiological, and morphological properties. Among JG cells, previous electron microscopic (EM) studies have shown that the majority of synaptic inputs to tyrosine hydroxylase (TH)-immunoreactive neurons were asymmetrical synapses from olfactory nerve (ON) terminals. However, recent physiological results revealed that 70% of dopaminergic/γ-aminobutyric acid (GABA)ergic neurons received polysynaptic inputs via ET cells, whereas the remaining 30% received monosynaptic ON inputs. To understand the discrepancies between EM and physiological data, we used serial EM analysis combined with confocal laser scanning microscope images to examine the spatial distribution of synapses on dendrites using mice expressing enhanced green fluorescent protein under the control of the TH promoter. The majority of synaptic inputs to TH-expressing JG cells were from ON terminals, and they preferentially targeted distal dendrites from the soma. On the other hand, the numbers of non-ON inputs were fewer and targeted proximal dendrites. Furthermore, individual TH-expressing JG cells formed serial synapses, such as M/T→TH→another presumed M/T or ON→TH→presumed M/T, but not reciprocal synapses. Serotonergic fibers also associated with somatic regions of TH neurons, displaying non-ON profiles. Thus, fewer proximal non-ON synapses provide more effective inputs than large numbers of distal ON synapses and may occur on the physiologically characterized population of dopaminergic-GABAergic neurons (70%) that receive their most effective inputs indirectly via an ON→ET→TH circuit. J. Comp. Neurol. 525:1059-1074, 2017. © 2017 Wiley Periodicals, Inc.

Authors+Show Affiliations

Department of Anatomy, Kawasaki Medical School, Kurashiki, Okayama, 701-0192, Japan.Department of Molecular Genetics, Institute of Biomedical Sciences, Fukushima Medical University School of Medicine, Fukushima, 960-1295, Japan.Department of Anatomy, Kawasaki Medical School, Kurashiki, Okayama, 701-0192, Japan. Research Center for Ultra-High Voltage Electron Microscopy, Osaka University, Mihogaoka, Ibaraki, Osaka, 567-0047, Japan.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

27864931

Citation

Kiyokage, Emi, et al. "Spatial Distribution of Synapses On Tyrosine Hydroxylase-expressing Juxtaglomerular Cells in the Mouse Olfactory Glomerulus." The Journal of Comparative Neurology, vol. 525, no. 5, 2017, pp. 1059-1074.
Kiyokage E, Kobayashi K, Toida K. Spatial distribution of synapses on tyrosine hydroxylase-expressing juxtaglomerular cells in the mouse olfactory glomerulus. J Comp Neurol. 2017;525(5):1059-1074.
Kiyokage, E., Kobayashi, K., & Toida, K. (2017). Spatial distribution of synapses on tyrosine hydroxylase-expressing juxtaglomerular cells in the mouse olfactory glomerulus. The Journal of Comparative Neurology, 525(5), pp. 1059-1074. doi:10.1002/cne.24147.
Kiyokage E, Kobayashi K, Toida K. Spatial Distribution of Synapses On Tyrosine Hydroxylase-expressing Juxtaglomerular Cells in the Mouse Olfactory Glomerulus. J Comp Neurol. 2017 Apr 1;525(5):1059-1074. PubMed PMID: 27864931.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Spatial distribution of synapses on tyrosine hydroxylase-expressing juxtaglomerular cells in the mouse olfactory glomerulus. AU - Kiyokage,Emi, AU - Kobayashi,Kazuto, AU - Toida,Kazunori, Y1 - 2017/01/10/ PY - 2016/06/28/received PY - 2016/10/13/revised PY - 2016/10/13/accepted PY - 2016/11/20/pubmed PY - 2017/9/30/medline PY - 2016/11/20/entrez KW - RRID: AB_11180610 KW - RRID: AB_2315522 KW - RRID: AB_2336889 KW - RRID: AB_572263 KW - RRID: AB_94936 KW - RRID: IMSR-RBRC02095 KW - RRID: nif-0000-10294 KW - electron microscopy KW - juxtaglomerular cell KW - olfactory bulb KW - synapse KW - tyrosine hydroxylase SP - 1059 EP - 1074 JF - The Journal of comparative neurology JO - J. Comp. Neurol. VL - 525 IS - 5 N2 - Olfactory sensory axons converge in specific glomeruli where they form excitatory synapses onto dendrites of mitral/tufted (M/T) and juxtaglomerular (JG) cells, including periglomerular (PG), external tufted (ET), and superficial-short axon cells. JG cells consist of heterogeneous subpopulations with different neurochemical, physiological, and morphological properties. Among JG cells, previous electron microscopic (EM) studies have shown that the majority of synaptic inputs to tyrosine hydroxylase (TH)-immunoreactive neurons were asymmetrical synapses from olfactory nerve (ON) terminals. However, recent physiological results revealed that 70% of dopaminergic/γ-aminobutyric acid (GABA)ergic neurons received polysynaptic inputs via ET cells, whereas the remaining 30% received monosynaptic ON inputs. To understand the discrepancies between EM and physiological data, we used serial EM analysis combined with confocal laser scanning microscope images to examine the spatial distribution of synapses on dendrites using mice expressing enhanced green fluorescent protein under the control of the TH promoter. The majority of synaptic inputs to TH-expressing JG cells were from ON terminals, and they preferentially targeted distal dendrites from the soma. On the other hand, the numbers of non-ON inputs were fewer and targeted proximal dendrites. Furthermore, individual TH-expressing JG cells formed serial synapses, such as M/T→TH→another presumed M/T or ON→TH→presumed M/T, but not reciprocal synapses. Serotonergic fibers also associated with somatic regions of TH neurons, displaying non-ON profiles. Thus, fewer proximal non-ON synapses provide more effective inputs than large numbers of distal ON synapses and may occur on the physiologically characterized population of dopaminergic-GABAergic neurons (70%) that receive their most effective inputs indirectly via an ON→ET→TH circuit. J. Comp. Neurol. 525:1059-1074, 2017. © 2017 Wiley Periodicals, Inc. SN - 1096-9861 UR - https://www.unboundmedicine.com/medline/citation/27864931/Spatial_distribution_of_synapses_on_tyrosine_hydroxylase_expressing_juxtaglomerular_cells_in_the_mouse_olfactory_glomerulus_ L2 - https://doi.org/10.1002/cne.24147 DB - PRIME DP - Unbound Medicine ER -