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CCKergic Tufted Cells Differentially Drive Two Anatomically Segregated Inhibitory Circuits in the Mouse Olfactory Bulb.
J Neurosci. 2020 Aug 05; 40(32):6189-6206.JN

Abstract

Delineation of functional synaptic connections is fundamental to understanding sensory processing. Olfactory signals are synaptically processed initially in the olfactory bulb (OB) where neural circuits are formed among inhibitory interneurons and the output neurons mitral cells (MCs) and tufted cells (TCs). TCs function in parallel with but differently from MCs and are further classified into multiple subpopulations based on their anatomic and functional heterogeneities. Here, we combined optogenetics with electrophysiology to characterize the synaptic transmission from a subpopulation of TCs, which exclusively express the neuropeptide cholecystokinin (CCK), to two groups of spatially segregated GABAergic interneurons, granule cells (GCs) and glomerular interneurons in mice of both sexes with four major findings. First, CCKergic TCs receive direct input from the olfactory sensory neurons (OSNs). This monosynaptic transmission exhibits high fidelity in response to repetitive OSN input. Second, CCKergic TCs drive GCs through two functionally distinct types of monosynaptic connections: (1) dendrodendritic synapses onto GC distal dendrites via their lateral dendrites in the superficial external plexiform layer (EPL); (2) axodendritic synapses onto GC proximal dendrites via their axon collaterals or terminals in the internal plexiform layer (IPL) on both sides of each bulb. Third, CCKergic TCs monosynaptically excite two subpopulations of inhibitory glomerular interneurons via dendrodendritic synapses. Finally, sniff-like patterned activation of CCKergic TCs induces robust frequency-dependent depression of the dendrodendritic synapses but facilitation of the axodendritic synapses. These results demonstrated important roles of the CCKergic TCs in olfactory processing by orchestrating OB inhibitory activities.SIGNIFICANCE STATEMENT Neuronal morphology and organization in the olfactory bulb (OB) have been extensively studied, however, the functional operation of neuronal interactions is not fully understood. We combined optogenetic and electrophysiological approaches to investigate the functional operation of synaptic connections between a specific population of excitatory output neuron and inhibitory interneurons in the OB. We found that these output neurons formed distinct types of synapses with two populations of spatially segregated interneurons. The functional characteristics of these synapses vary significantly depending on the presynaptic compartments so that these output neurons can dynamically rebalance inhibitory feedback or feedforward to other neurons types in the OB in response to dynamic rhythmic inputs.

Authors+Show Affiliations

Department of Anatomy and Neurobiology, Department of Radiology, University of Maryland School of Medicine, Baltimore, Maryland 21201.Department of Anatomy and Neurobiology, University of Maryland School of Medicine, Baltimore, Maryland 21201.Department of Anatomy, Howard University College of Medicine, Washington, DC 20059.Department of Anatomy, Howard University College of Medicine, Washington, DC 20059 shaolin.liu@howard.edu.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

32605937

Citation

Sun, Xicui, et al. "CCKergic Tufted Cells Differentially Drive Two Anatomically Segregated Inhibitory Circuits in the Mouse Olfactory Bulb." The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, vol. 40, no. 32, 2020, pp. 6189-6206.
Sun X, Liu X, Starr ER, et al. CCKergic Tufted Cells Differentially Drive Two Anatomically Segregated Inhibitory Circuits in the Mouse Olfactory Bulb. J Neurosci. 2020;40(32):6189-6206.
Sun, X., Liu, X., Starr, E. R., & Liu, S. (2020). CCKergic Tufted Cells Differentially Drive Two Anatomically Segregated Inhibitory Circuits in the Mouse Olfactory Bulb. The Journal of Neuroscience : the Official Journal of the Society for Neuroscience, 40(32), 6189-6206. https://doi.org/10.1523/JNEUROSCI.0769-20.2020
Sun X, et al. CCKergic Tufted Cells Differentially Drive Two Anatomically Segregated Inhibitory Circuits in the Mouse Olfactory Bulb. J Neurosci. 2020 Aug 5;40(32):6189-6206. PubMed PMID: 32605937.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - CCKergic Tufted Cells Differentially Drive Two Anatomically Segregated Inhibitory Circuits in the Mouse Olfactory Bulb. AU - Sun,Xicui, AU - Liu,Xiang, AU - Starr,Eric R, AU - Liu,Shaolin, Y1 - 2020/06/30/ PY - 2020/04/01/received PY - 2020/05/06/revised PY - 2020/05/21/accepted PY - 2021/02/05/pmc-release PY - 2020/7/2/pubmed PY - 2020/7/2/medline PY - 2020/7/2/entrez KW - inhibitory interneuron KW - neural circuits KW - olfactory bulb KW - projection neurons KW - synaptic plasticity KW - synaptic transmission SP - 6189 EP - 6206 JF - The Journal of neuroscience : the official journal of the Society for Neuroscience JO - J. Neurosci. VL - 40 IS - 32 N2 - Delineation of functional synaptic connections is fundamental to understanding sensory processing. Olfactory signals are synaptically processed initially in the olfactory bulb (OB) where neural circuits are formed among inhibitory interneurons and the output neurons mitral cells (MCs) and tufted cells (TCs). TCs function in parallel with but differently from MCs and are further classified into multiple subpopulations based on their anatomic and functional heterogeneities. Here, we combined optogenetics with electrophysiology to characterize the synaptic transmission from a subpopulation of TCs, which exclusively express the neuropeptide cholecystokinin (CCK), to two groups of spatially segregated GABAergic interneurons, granule cells (GCs) and glomerular interneurons in mice of both sexes with four major findings. First, CCKergic TCs receive direct input from the olfactory sensory neurons (OSNs). This monosynaptic transmission exhibits high fidelity in response to repetitive OSN input. Second, CCKergic TCs drive GCs through two functionally distinct types of monosynaptic connections: (1) dendrodendritic synapses onto GC distal dendrites via their lateral dendrites in the superficial external plexiform layer (EPL); (2) axodendritic synapses onto GC proximal dendrites via their axon collaterals or terminals in the internal plexiform layer (IPL) on both sides of each bulb. Third, CCKergic TCs monosynaptically excite two subpopulations of inhibitory glomerular interneurons via dendrodendritic synapses. Finally, sniff-like patterned activation of CCKergic TCs induces robust frequency-dependent depression of the dendrodendritic synapses but facilitation of the axodendritic synapses. These results demonstrated important roles of the CCKergic TCs in olfactory processing by orchestrating OB inhibitory activities.SIGNIFICANCE STATEMENT Neuronal morphology and organization in the olfactory bulb (OB) have been extensively studied, however, the functional operation of neuronal interactions is not fully understood. We combined optogenetic and electrophysiological approaches to investigate the functional operation of synaptic connections between a specific population of excitatory output neuron and inhibitory interneurons in the OB. We found that these output neurons formed distinct types of synapses with two populations of spatially segregated interneurons. The functional characteristics of these synapses vary significantly depending on the presynaptic compartments so that these output neurons can dynamically rebalance inhibitory feedback or feedforward to other neurons types in the OB in response to dynamic rhythmic inputs. SN - 1529-2401 UR - https://www.unboundmedicine.com/medline/citation/32605937/CCKergic_tufted_cells_differentially_drive_two_anatomically_segregated_inhibitory_circuits_in_the_mouse_olfactory_bulb L2 - http://www.jneurosci.org/cgi/pmidlookup?view=long&pmid=32605937 DB - PRIME DP - Unbound Medicine ER -
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