Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine Neurons

The mammalian olfactory bulb (OB) has a vast population of dopamine (DA) neurons, whose function is to increase odor discrimination through mostly inhibitory synaptic mechanisms. However, it is not well understood whether there is more than one neuronal type of OB DA neuron, how these neurons respon...

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Main Authors: Kirill S. Korshunov, Laura J. Blakemore, Richard Bertram, Paul Q. Trombley
Format: Article
Language:English
Published: Frontiers Media S.A. 2020-03-01
Series:Frontiers in Cellular Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fncel.2020.00060/full
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spelling doaj-8f20772b091c44e5ad40366ddc1f2fa32020-11-25T02:31:32ZengFrontiers Media S.A.Frontiers in Cellular Neuroscience1662-51022020-03-011410.3389/fncel.2020.00060512967Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine NeuronsKirill S. Korshunov0Kirill S. Korshunov1Laura J. Blakemore2Laura J. Blakemore3Richard Bertram4Richard Bertram5Paul Q. Trombley6Paul Q. Trombley7Program in Neuroscience, Florida State University, Tallahassee, FL, United StatesDepartment of Biological Science, Florida State University, Tallahassee, FL, United StatesProgram in Neuroscience, Florida State University, Tallahassee, FL, United StatesDepartment of Biological Science, Florida State University, Tallahassee, FL, United StatesProgram in Neuroscience, Florida State University, Tallahassee, FL, United StatesDepartment of Mathematics, Florida State University, Tallahassee, FL, United StatesProgram in Neuroscience, Florida State University, Tallahassee, FL, United StatesDepartment of Biological Science, Florida State University, Tallahassee, FL, United StatesThe mammalian olfactory bulb (OB) has a vast population of dopamine (DA) neurons, whose function is to increase odor discrimination through mostly inhibitory synaptic mechanisms. However, it is not well understood whether there is more than one neuronal type of OB DA neuron, how these neurons respond to different stimuli, and the ionic mechanisms behind those responses. In this study, we used a transgenic rat line (hTH-GFP) to identify fluorescent OB DA neurons for recording via whole-cell electrophysiology. These neurons were grouped based on their localization in the glomerular layer (“Top” vs. “Bottom”) with these largest and smallest neurons grouped by neuronal area (“Large” vs. “Small,” in μm2). We found that some membrane properties could be distinguished based on a neuron’s area, but not by its glomerular localization. All OB DA neurons produced a single action potential when receiving a sufficiently depolarizing stimulus, while some could also spike multiple times when receiving weaker stimuli, an activity that was more likely in Large than Small neurons. This single spiking activity is likely driven by the Na+ current, which showed a sensitivity to inactivation by depolarization and a relatively long time constant for the removal of inactivation. These recordings showed that Small neurons were more sensitive to inactivation of Na+ current at membrane potentials of −70 and −60 mV than Large neurons. The hyperpolarization-activated H-current (identified by voltage sags) was more pronounced in Small than Large DA neurons across hyperpolarized membrane potentials. Lastly, to mimic a more physiological stimulus, these neurons received ramp stimuli of various durations and current amplitudes. When stimulated with weaker/shallow ramps, the neurons needed less current to begin and end firing and they produced more action potentials at a slower frequency. These spiking properties were further analyzed between the four groups of neurons, and these analyses support the difference in spiking induced with current step stimuli. Thus, there may be more than one type of OB DA neuron, and these neurons’ activities may support a possible role of being high-pass filters in the OB by allowing the transmission of stronger odor signals while inhibiting weaker ones.https://www.frontiersin.org/article/10.3389/fncel.2020.00060/fulldopamineolfactory bulbelectrophysiologymembrane propertiesH-currentNa+ current
collection DOAJ
language English
format Article
sources DOAJ
author Kirill S. Korshunov
Kirill S. Korshunov
Laura J. Blakemore
Laura J. Blakemore
Richard Bertram
Richard Bertram
Paul Q. Trombley
Paul Q. Trombley
spellingShingle Kirill S. Korshunov
Kirill S. Korshunov
Laura J. Blakemore
Laura J. Blakemore
Richard Bertram
Richard Bertram
Paul Q. Trombley
Paul Q. Trombley
Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine Neurons
Frontiers in Cellular Neuroscience
dopamine
olfactory bulb
electrophysiology
membrane properties
H-current
Na+ current
author_facet Kirill S. Korshunov
Kirill S. Korshunov
Laura J. Blakemore
Laura J. Blakemore
Richard Bertram
Richard Bertram
Paul Q. Trombley
Paul Q. Trombley
author_sort Kirill S. Korshunov
title Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine Neurons
title_short Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine Neurons
title_full Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine Neurons
title_fullStr Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine Neurons
title_full_unstemmed Spiking and Membrane Properties of Rat Olfactory Bulb Dopamine Neurons
title_sort spiking and membrane properties of rat olfactory bulb dopamine neurons
publisher Frontiers Media S.A.
series Frontiers in Cellular Neuroscience
issn 1662-5102
publishDate 2020-03-01
description The mammalian olfactory bulb (OB) has a vast population of dopamine (DA) neurons, whose function is to increase odor discrimination through mostly inhibitory synaptic mechanisms. However, it is not well understood whether there is more than one neuronal type of OB DA neuron, how these neurons respond to different stimuli, and the ionic mechanisms behind those responses. In this study, we used a transgenic rat line (hTH-GFP) to identify fluorescent OB DA neurons for recording via whole-cell electrophysiology. These neurons were grouped based on their localization in the glomerular layer (“Top” vs. “Bottom”) with these largest and smallest neurons grouped by neuronal area (“Large” vs. “Small,” in μm2). We found that some membrane properties could be distinguished based on a neuron’s area, but not by its glomerular localization. All OB DA neurons produced a single action potential when receiving a sufficiently depolarizing stimulus, while some could also spike multiple times when receiving weaker stimuli, an activity that was more likely in Large than Small neurons. This single spiking activity is likely driven by the Na+ current, which showed a sensitivity to inactivation by depolarization and a relatively long time constant for the removal of inactivation. These recordings showed that Small neurons were more sensitive to inactivation of Na+ current at membrane potentials of −70 and −60 mV than Large neurons. The hyperpolarization-activated H-current (identified by voltage sags) was more pronounced in Small than Large DA neurons across hyperpolarized membrane potentials. Lastly, to mimic a more physiological stimulus, these neurons received ramp stimuli of various durations and current amplitudes. When stimulated with weaker/shallow ramps, the neurons needed less current to begin and end firing and they produced more action potentials at a slower frequency. These spiking properties were further analyzed between the four groups of neurons, and these analyses support the difference in spiking induced with current step stimuli. Thus, there may be more than one type of OB DA neuron, and these neurons’ activities may support a possible role of being high-pass filters in the OB by allowing the transmission of stronger odor signals while inhibiting weaker ones.
topic dopamine
olfactory bulb
electrophysiology
membrane properties
H-current
Na+ current
url https://www.frontiersin.org/article/10.3389/fncel.2020.00060/full
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