Heterogeneous glutamatergic receptor mRNA expression across phrenic motor neurons in rats

The diaphragm muscle comprises various types of motor units that are recruited in an orderly fashion governed by the intrinsic electrophysiological properties (membrane capacitance as a function of somal surface area) of phrenic motor neurons (PhMNs). Glutamate is the main excitatory neurotransmitte...

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Bibliographic Details
Published in:Journal of neurochemistry 2020-06, Vol.153 (5), p.586-598
Main Authors: Rana, Sabhya, Sieck, Gary C., Mantilla, Carlos B.
Format: Article
Language:English
Subjects:
Animals
Aspartic acid
Density
Diaphragm
Female
Fluorescence
Fluorescence in situ hybridization
Gene Expression
glutamate
Glutamatergic transmission
Glutamic acid receptors (ionotropic)
Male
Membrane capacitance
Motor neurons
Motor Neurons - metabolism
motor unit recruitment
Motor units
Muscles
N-Methyl-D-aspartic acid receptors
neuromotor control
Neurons
Neurotransmission
neurotransmitter
Neurotransmitters
phrenic motor neurons
Phrenic Nerve - metabolism
Rats
Rats, Sprague-Dawley
Receptors
Receptors, AMPA - biosynthesis
Receptors, AMPA - genetics
Receptors, N-Methyl-D-Aspartate - biosynthesis
Receptors, N-Methyl-D-Aspartate - genetics
Recruitment
Recruitment, Neurophysiological - physiology
respiration
RNA, Messenger - biosynthesis
RNA, Messenger - genetics
Surface area
α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid
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Summary:The diaphragm muscle comprises various types of motor units that are recruited in an orderly fashion governed by the intrinsic electrophysiological properties (membrane capacitance as a function of somal surface area) of phrenic motor neurons (PhMNs). Glutamate is the main excitatory neurotransmitter at PhMNs and acts primarily via fast acting AMPA and N‐methyl‐D‐aspartic acid (NMDA) receptors. Differences in receptor expression may also contribute to motor unit recruitment order. We used single cell, multiplex fluorescence in situ hybridization to determine glutamatergic receptor mRNA expression across PhMNs based on their somal surface area. In adult male and female rats (n = 9) PhMNs were retrogradely labeled for analyses (n = 453 neurons). Differences in the total number and density of mRNA transcripts were evident across PhMNs grouped into tertiles according to somal surface area. A ~ 25% higher density of AMPA (Gria2) and NMDA (Grin1) mRNA expression was evident in PhMNs in the lower tertile compared to the upper tertile. These smaller PhMNs likely comprise type S motor units that are recruited first to accomplish lower force, ventilatory behaviors. In contrast, larger PhMNs with lower volume densities of AMPA and NMDA mRNA expression presumably comprise type FInt and FF motor units that are recruited during higher force, expulsive behaviors. Furthermore, there was a significantly higher cytosolic NMDA mRNA expression in small PhMNs suggesting a more important role for NMDA‐mediated glutamatergic neurotransmission at smaller PhMNs. These results are consistent with the observed order of motor unit recruitment and suggest a role for glutamatergic receptors in support of this orderly recruitment. Cover Image for this issue: doi: 10.1111/jnc.14747. Orderly recruitment of motor units permits generation of graded levels of force necessary for a range of motor behaviors. There is considerable evidence that motor units innervating the main inspiratory muscle in mammals, the diaphragm muscle, are recruited according to the size principle (i.e., phrenic motor neurons with smaller surface area recruited first). The present study examined differences in the expression of excitatory glutamatergic (AMPA and NMDA) receptors across phrenic motor neurons of varying size and found size‐dependent differences in receptor mRNA density across phrenic motor neurons which may contribute to the orderly recruitment of diaphragm motor units. Cover Image for this issue: doi: 1
ISSN:0022-3042
1471-4159
DOI:10.1111/jnc.14881