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Article ; Online: The critical period: neurochemical and synaptic mechanisms shared by the visual cortex and the brain stem respiratory system.

Wong-Riley, Margaret T T

2021 Volume 288, Issue 1958, Page(s) 20211025

Abstract: The landmark studies of Wiesel and Hubel in the 1960's initiated a surge of investigations into the critical period of visual cortical development, when abnormal visual experience can alter cortical structures and functions. Most studies focused on the ... ...

Abstract	The landmark studies of Wiesel and Hubel in the 1960's initiated a surge of investigations into the critical period of visual cortical development, when abnormal visual experience can alter cortical structures and functions. Most studies focused on the visual cortex, with relatively little attention to subcortical structures. The goal of the present review is to elucidate neurochemical and synaptic mechanisms common to the critical periods of the visual cortex and the brain stem respiratory system in the
MeSH term(s)	Animals ; Brain Stem ; Neurogenesis ; Neurons ; Rats ; Respiratory System ; Visual Cortex
Language	English
Publishing date	2021-09-08
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	209242-6
ISSN	1471-2954 ; 0080-4649 ; 0962-8452 ; 0950-1193
ISSN (online)	1471-2954
ISSN	0080-4649 ; 0962-8452 ; 0950-1193
DOI	10.1098/rspb.2021.1025
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Article ; Online: Mechanisms underlying a critical period of respiratory development in the rat.

Wong-Riley, Margaret T T / Liu, Qiuli / Gao, Xiuping

Respiratory physiology & neurobiology

2019 Volume 264, Page(s) 40–50

Abstract: Twenty-five years ago, Filiano and Kinney (1994) proposed that a critical period of postnatal development constitutes one of the three risk factors for sudden infant death syndrome (SIDS). The underlying mechanism was poorly understood. In the last 17 ... ...

Abstract	Twenty-five years ago, Filiano and Kinney (1994) proposed that a critical period of postnatal development constitutes one of the three risk factors for sudden infant death syndrome (SIDS). The underlying mechanism was poorly understood. In the last 17 years, much has been uncovered on this period in the rat. Against several expected trends of development, abrupt neurochemical, metabolic, ventilatory, and electrophysiological changes occur in the respiratory system at P12-13. This results in a transient synaptic imbalance with suppressed excitation and enhanced inhibition, and the response to acute hypoxia is the weakest at this time, both at the cellular and system's levels. The basis for the synaptic imbalance is likely to be contributed by a reduced expression of brain-derived neurotrophic factor (BDNF) and its TrkB receptors in multiple brain stem respiratory-related nuclei during the critical period. Exogenous BDNF or a TrkB agonist partially reverses the synaptic imbalance, whereas a TrkB antagonist accentuates the imbalance. A transient down-regulation of pituitary adenylate cyclase-activating polypeptide (PACAP) at P12 in respiratory-related nuclei also contributes to the vulnerability of this period. Carotid body denervation during this time or perinatal hyperoxia merely delays and sometimes prolongs, but not eliminate the critical period. The rationale for the necessity of the critical period in postnatal development is discussed.
MeSH term(s)	Animals ; Brain-Derived Neurotrophic Factor/metabolism ; Hypoxia/metabolism ; Pituitary Adenylate Cyclase-Activating Polypeptide/metabolism ; Rats ; Receptor, trkB/agonists ; Receptor, trkB/antagonists & inhibitors ; Receptor, trkB/metabolism ; Respiratory Physiological Phenomena ; Solute Carrier Family 12, Member 2/metabolism
Chemical Substances	Bdnf protein, rat ; Brain-Derived Neurotrophic Factor ; Pituitary Adenylate Cyclase-Activating Polypeptide ; Slc12a2 protein, rat ; Solute Carrier Family 12, Member 2 ; Ntrk2 protein, rat (EC 2.7.10.1) ; Receptor, trkB (EC 2.7.10.1)
Language	English
Publishing date	2019-04-15
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	2077867-3
ISSN	1878-1519 ; 1569-9048
ISSN (online)	1878-1519
ISSN	1569-9048
DOI	10.1016/j.resp.2019.04.006
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Article ; Online: Pituitary adenylate cyclase-activating polypeptide: Postnatal development in multiple brain stem respiratory-related nuclei in the rat.

Liu, Qiuli / Wong-Riley, Margaret T T

Respiratory physiology & neurobiology

2018 Volume 259, Page(s) 149–155

Abstract: The pituitary adenylate cyclase-activating polypeptide (PACAP) plays an important role in anterior pituitary hormone secretion, neurotransmission, and the control of breathing. Mice lacking PACAP die suddenly mainly in the ... ...

Abstract	The pituitary adenylate cyclase-activating polypeptide (PACAP) plays an important role in anterior pituitary hormone secretion, neurotransmission, and the control of breathing. Mice lacking PACAP die suddenly mainly in the 2
MeSH term(s)	Age Factors ; Animals ; Animals, Newborn ; Brain Stem/anatomy & histology ; Brain Stem/growth & development ; Brain Stem/metabolism ; Female ; Gene Expression Regulation, Developmental/physiology ; Hypoxia/metabolism ; Male ; Neurons/metabolism ; Neuropil/cytology ; Neuropil/metabolism ; Pituitary Adenylate Cyclase-Activating Polypeptide/metabolism ; Rats ; Rats, Sprague-Dawley ; Respiration
Chemical Substances	Pituitary Adenylate Cyclase-Activating Polypeptide
Language	English
Publishing date	2018-10-22
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2077867-3
ISSN	1878-1519 ; 1569-9048
ISSN (online)	1878-1519
ISSN	1569-9048
DOI	10.1016/j.resp.2018.10.005
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Article: Alterations in synapses and mitochondria induced by acute or chronic intermittent hypoxia in the pre-Bötzinger complex of rats: an ultrastructural triple-labeling study with immunocytochemistry and histochemistry.

Kang, Junjun / Lu, Naining / Yang, Shoujing / Guo, Baolin / Zhu, Yuanyuan / Wu, Shengxi / Huang, Xiaofeng / Wong-Riley, Margaret T T / Liu, Ying-Ying

Frontiers in cellular neuroscience

2023 Volume 17, Page(s) 1132241

Abstract: Introduction: The pre-Bötzinger complex (pre-BötC), a kernel of inspiratory rhythmogenesis, is a heterogeneous network with excitatory glutamatergic and inhibitory GABAergic and glycinergic neurons. Inspiratory rhythm generation relies on synchronous ... ...

Abstract	Introduction: The pre-Bötzinger complex (pre-BötC), a kernel of inspiratory rhythmogenesis, is a heterogeneous network with excitatory glutamatergic and inhibitory GABAergic and glycinergic neurons. Inspiratory rhythm generation relies on synchronous activation of glutamatergic neuron, whilst inhibitory neurons play a critical role in shaping the breathing pattern, endowing the rhythm with flexibility in adapting to environmental, metabolic, and behavioral needs. Here we report ultrastructural alterations in excitatory, asymmetric synapses (AS) and inhibitory, symmetric synapses (SS), especially perforated synapses with discontinuous postsynaptic densities (PSDs) in the pre-BötC in rats exposed to daily acute intermittent hypoxia (dAIH) or chronic (C) IH. Methods: We utilized for the first time a combination of somatostatin (SST) and neurokinin 1 receptor (NK1R) double immunocytochemistry with cytochrome oxidase histochemistry, to reveal synaptic characteristics and mitochondrial dynamic in the pre-BötC. Results: We found perforated synapses with synaptic vesicles accumulated in distinct pools in apposition to each discrete PSD segments. dAIH induced significant increases in the PSD size of macular AS, and the proportion of perforated synapses. AS were predominant in the dAIH group, whereas SS were in a high proportion in the CIH group. dAIH significantly increased SST and NK1R expressions, whereas CIH led to a decrease. Desmosome-like contacts (DLC) were characterized for the first time in the pre-BötC. They were distributed alongside of synapses, especially SS. Mitochondria appeared in more proximity to DLC than synapses, suggestive of a higher energy demand of the DLC. Findings of single spines with dual AS and SS innervation provide morphological evidence of excitation-inhibition interplay within a single spine in the pre-BötC. In particular, we characterized spine-shaft microdomains of concentrated synapses coupled with mitochondrial positioning that could serve as a structural basis for synchrony of spine-shaft communication. Mitochondria were found within spines and ultrastructural features of mitochondrial fusion and fission were depicted for the first time in the pre-BötC. Conclusion: We provide ultrastructural evidence of excitation-inhibition synapses in shafts and spines, and DLC in association with synapses that coincide with mitochondrial dynamic in their contribution to respiratory plasticity in the pre-BötC.
Language	English
Publishing date	2023-06-16
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2452963-1
ISSN	1662-5102
ISSN	1662-5102
DOI	10.3389/fncel.2023.1132241
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Article ; Online: Transcriptional Regulation of Brain-derived Neurotrophic Factor Coding Exon IX: ROLE OF NUCLEAR RESPIRATORY FACTOR 2.

Nair, Bindu / Wong-Riley, Margaret T T

The Journal of biological chemistry

2016 Volume 291, Issue 43, Page(s) 22583–22593

Abstract: Brain-derived neurotrophic factor (BDNF) is an active neurotrophin abundantly expressed throughout the nervous system. It plays an important role in synaptic transmission, plasticity, neuronal proliferation, differentiation, survival, and death. The Bdnf ...

Abstract	Brain-derived neurotrophic factor (BDNF) is an active neurotrophin abundantly expressed throughout the nervous system. It plays an important role in synaptic transmission, plasticity, neuronal proliferation, differentiation, survival, and death. The Bdnf gene in rodents has eight non-coding exons and only a single coding exon (IX). Despite its recognized regulation by neuronal activity, relatively little is known about its transcriptional regulation, and even less about the transcription factor candidates that may play such a role. The goal of the present study was to probe for such a candidate that may regulate exon IX in the rat Bdnf gene. Our in silico analysis revealed tandem binding sites for nuclear respiratory factor 2 (NRF-2) on the promoter of exon IX. NRF-2 is of special significance because it co-regulates the expressions of mediators of energy metabolism (cytochrome c oxidase) and mediators of neuronal activity (glutamatergic receptors). To test our hypothesis that NRF-2 also regulates the Bdnf gene, we performed electrophoretic mobility shift assay (EMSA), chromatin immunoprecipitation (ChIP), promoter cloning, and site-directed mutagenesis, real-time quantitative PCR (RT-qPCR), and Western blotting analysis. Results indicate that NRF-2 functionally regulates exon IX of the rat Bdnf gene. The binding sites of NRF-2 are conserved between rats and mice. Overexpressing NRF-2 up-regulated the expression of Bdnf exon IX, whereas knocking down NRF-2 down-regulated such expression. These findings are consistent with our hypothesis that NRF-2, in addition to regulating the coupling between neuronal activity and energy metabolism, also regulates the expression of BDNF, which is intimately associated with energy-demanding neuronal activity.
MeSH term(s)	Animals ; Brain-Derived Neurotrophic Factor/biosynthesis ; Brain-Derived Neurotrophic Factor/genetics ; Energy Metabolism/physiology ; Exons/physiology ; Gene Expression Regulation/physiology ; Gene Knockdown Techniques ; Mice ; NF-E2-Related Factor 2/genetics ; NF-E2-Related Factor 2/metabolism ; Neurons/metabolism ; Rats ; Response Elements/physiology ; Transcription, Genetic/physiology
Chemical Substances	Brain-Derived Neurotrophic Factor ; NF-E2-Related Factor 2 ; Nfe2l2 protein, rat
Language	English
Publishing date	2016-09-13
Publishing country	United States
Document type	Journal Article
ZDB-ID	2997-x
ISSN	1083-351X ; 0021-9258
ISSN (online)	1083-351X
ISSN	0021-9258
DOI	10.1074/jbc.M116.742304
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Article: Bigenomic regulation of cytochrome c oxidase in neurons and the tight coupling between neuronal activity and energy metabolism.

Wong-Riley, Margaret T T

Advances in experimental medicine and biology

2012 Volume 748, Page(s) 283–304

Abstract: Cytochrome c oxidase is the terminal enzyme of the mitochondrial electron transport chain, without which oxidative metabolism cannot be carried to completion. It is one of only four unique, bigenomic proteins in mammalian cells. The holoenzyme is made up ...

Abstract	Cytochrome c oxidase is the terminal enzyme of the mitochondrial electron transport chain, without which oxidative metabolism cannot be carried to completion. It is one of only four unique, bigenomic proteins in mammalian cells. The holoenzyme is made up of three mitochondrial-encoded and ten nuclear-encoded subunits in a 1:1 stoichiometry. The ten nuclear subunit genes are located in nine different chromosomes. The coordinated regulation of such a multisubunit, multichromosomal, bigenomic enzyme poses a challenge. It is especially so for neurons, whose mitochondria are widely distributed in extensive dendritic and axonal processes, resulting in the separation of the mitochondrial from the nuclear genome by great distances. Neuronal activity dictates COX activity that reflects protein amount, which, in turn, is regulated at the transcriptional level. All 13 COX transcripts are up- and downregulated by neuronal activity. The ten nuclear COX transcripts and those for Tfam and Tfbms important for mitochondrial COX transcripts are transcribed in the same transcription factory. Bigenomic regulation of all 13 transcripts is mediated by nuclear respiratory factors 1 and 2 (NRF-1 and NRF-2). NRF-1, in addition, also regulates critical neurochemicals of glutamatergic synaptic transmission, thereby ensuring the tight coupling of energy metabolism and neuronal activity at the molecular level in neurons.
MeSH term(s)	Animals ; Electron Transport Complex IV/physiology ; Energy Metabolism ; GA-Binding Protein Transcription Factor/physiology ; Glutamic Acid/physiology ; Humans ; Neurons/enzymology ; Neurons/physiology ; Nuclear Respiratory Factor 1/physiology ; Transcription, Genetic
Chemical Substances	GA-Binding Protein Transcription Factor ; Nuclear Respiratory Factor 1 ; Glutamic Acid (3KX376GY7L) ; Electron Transport Complex IV (EC 1.9.3.1)
Language	English
Publishing date	2012-06-23
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ISSN	2214-8019 ; 0065-2598
ISSN (online)	2214-8019
ISSN	0065-2598
DOI	10.1007/978-1-4614-3573-0_12
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Article: Specificity protein 4 (Sp4) transcriptionally regulates inhibitory GABAergic receptors in neurons.

Nair, Bindu / Johar, Kaid / Priya, Anusha / Wong-Riley, Margaret T T

Biochimica et biophysica acta

2016 Volume 1863, Issue 1, Page(s) 1–9

Abstract: Previous studies in our laboratory have shown that the neuron-specific specificity protein 4 (Sp4) transcriptionally regulates many excitatory neurotransmitter receptor subunit genes, such as those for GluN1, GluN2A, and GluN2B of N-methyl-d-aspartate ( ... ...

Abstract	Previous studies in our laboratory have shown that the neuron-specific specificity protein 4 (Sp4) transcriptionally regulates many excitatory neurotransmitter receptor subunit genes, such as those for GluN1, GluN2A, and GluN2B of N-methyl-d-aspartate (NMDA) receptors and Gria2 of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors. It also regulates Atp1a1 and Atp1b1 subunit genes of Na(+)/K(+)-ATPase, a major energy-consuming enzyme, as well as all 13 subunits of cytochrome c oxidase (COX), an important energy-generating enzyme. Thus, there is a tight coupling between energy consumption, energy production, and excitatory neuronal activity at the transcriptional level in neurons. The question is whether inhibitory neurotransmitter receptors are also regulated by Sp4. In the present study, we tested our hypothesis that Sp4 regulates receptor subunit genes of a major inhibitory neurotransmitter, GABA, specifically GABAA receptors. By means of multiple approaches, including in silico analysis, electrophoretic mobility shift and supershift assays, real-time quantitative PCR, chromatin immunoprecipitation, promoter mutational analysis, over-expression and shRNA of Sp4, functional assays, and western blots, we found that Sp4 functionally regulates the transcription of Gabra1 (GABAA α1) and Gabra2 (GABAA α2), but not Gabra3 (GABAA α3) subunit genes. The binding sites of Sp4 are conserved among rats, humans, and mice. Thus, our results substantiate our hypothesis that Sp4 plays a key role in regulating the transcription of GABAA receptor subunit genes. They also indicate that Sp4 is in a position to transcriptionally regulate the balance between excitatory and inhibitory neurochemical expressions in neurons.
MeSH term(s)	Animals ; Cells, Cultured ; GABAergic Neurons/cytology ; GABAergic Neurons/metabolism ; Gene Expression Regulation/physiology ; Mice ; Rats ; Receptors, AMPA/biosynthesis ; Receptors, AMPA/genetics ; Receptors, N-Methyl-D-Aspartate/biosynthesis ; Receptors, N-Methyl-D-Aspartate/genetics ; Sodium-Potassium-Exchanging ATPase/biosynthesis ; Sodium-Potassium-Exchanging ATPase/genetics ; Sp4 Transcription Factor/genetics ; Sp4 Transcription Factor/metabolism ; Transcription, Genetic/physiology
Chemical Substances	Atp1b1 protein, rat ; Receptors, AMPA ; Receptors, N-Methyl-D-Aspartate ; Sp4 Transcription Factor ; Sp4 protein, rat ; glutamate receptor ionotropic, AMPA 2 ; Atp1a1 protein, rat (EC 3.6.1.-) ; Sodium-Potassium-Exchanging ATPase (EC 3.6.3.9)
Language	English
Publishing date	2016-01
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	60-7
ISSN	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650 ; 0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
ISSN (online)	1879-2596 ; 1879-260X ; 1872-8006 ; 1879-2642 ; 1879-2618 ; 1879-2650
ISSN	0006-3002 ; 0005-2728 ; 0005-2736 ; 0304-4165 ; 0167-4838 ; 1388-1981 ; 0167-4889 ; 0167-4781 ; 0304-419X ; 1570-9639 ; 0925-4439 ; 1874-9399
DOI	10.1016/j.bbamcr.2015.10.005
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Article: Energy metabolism of the visual system.

Wong-Riley, Margaret T T

Eye and brain

2010 Volume 2, Page(s) 99–116

Abstract: The visual system is one of the most energetically demanding systems in the brain. The currency of energy is ATP, which is generated most efficiently from oxidative metabolism in the mitochondria. ATP supports multiple neuronal functions. Foremost is ... ...

Abstract	The visual system is one of the most energetically demanding systems in the brain. The currency of energy is ATP, which is generated most efficiently from oxidative metabolism in the mitochondria. ATP supports multiple neuronal functions. Foremost is repolarization of the membrane potential after depolarization. Neuronal activity, ATP generation, blood flow, oxygen consumption, glucose utilization, and mitochondrial oxidative metabolism are all interrelated. In the retina, phototransduction, neurotransmitter utilization, and protein/organelle transport are energy-dependent, yet repolarization-after-depolarization consumes the bulk of the energy. Repolarization in photoreceptor inner segments maintains the dark current. Repolarization by all neurons along the visual pathway following depolarizing excitatory glutamatergic neurotransmission preserves cellular integrity and permits reactivation. The higher metabolic activity in the magno- versus the parvo-cellular pathway, the ON- versus the OFF-pathway in some (and the reverse in other) species, and in specialized functional representations in the visual cortex all reflect a greater emphasis on the processing of specific visual attributes. Neuronal activity and energy metabolism are tightly coupled processes at the cellular and even at the molecular levels. Deficiencies in energy metabolism, such as in diabetes, mitochondrial DNA mutation, mitochondrial protein malfunction, and oxidative stress can lead to retinopathy, visual deficits, neuronal degeneration, and eventual blindness.
Language	English
Publishing date	2010-07-22
Publishing country	New Zealand
Document type	Journal Article
ZDB-ID	2587460-3
ISSN	1179-2744
ISSN	1179-2744
DOI	10.2147/EB.S9078
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Article ; Online: Gender considerations in ventilatory and metabolic development in rats: special emphasis on the critical period.

Liu, Qiuli / Wong-Riley, Margaret T T

Respiratory physiology & neurobiology

2013 Volume 188, Issue 2, Page(s) 200–207

Abstract: In rats, a critical period exists around postnatal day (P) 12-13, when an imbalance between heightened inhibition and suppressed excitation led to a weakened ventilatory and metabolic response to acute hypoxia. An open question was whether the two ... ...

Abstract	In rats, a critical period exists around postnatal day (P) 12-13, when an imbalance between heightened inhibition and suppressed excitation led to a weakened ventilatory and metabolic response to acute hypoxia. An open question was whether the two genders follow the same or different developmental trends throughout the first 3 postnatal weeks and whether the critical period exists in one or both genders. The present large-scale, in-depth ventilatory and metabolic study was undertaken to address this question. Our data indicated that: (1) the ventilatory and metabolic rates in both normoxia and acute hypoxia were comparable between the two genders from P0 to P21; thus, gender was never significant as a main effect; and (2) the age effect was highly significant in all parameters studies for both genders, and both genders exhibited a significantly weakened response to acute hypoxia during the critical period. Thus, the two genders have comparable developmental trends, and the critical period exists in both genders in rats.
MeSH term(s)	Age Factors ; Animals ; Animals, Newborn ; Body Temperature ; Body Weight ; Carbon Dioxide/metabolism ; Female ; Hypoxia/physiopathology ; Male ; Oxygen Consumption/physiology ; Rats ; Rats, Sprague-Dawley ; Respiratory Mechanics/physiology ; Sex Characteristics ; Tidal Volume/physiology
Chemical Substances	Carbon Dioxide (142M471B3J)
Language	English
Publishing date	2013-06-21
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	2077867-3
ISSN	1878-1519 ; 1569-9048
ISSN (online)	1878-1519
ISSN	1569-9048
DOI	10.1016/j.resp.2013.06.013
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Article ; Online: Postnatal development of glycine receptor subunits α1, α2, α3, and β immunoreactivity in multiple brain stem respiratory-related nuclear groups of the rat.

Liu, Qiuli / Wong-Riley, Margaret T T

Brain research

2013 Volume 1538, Page(s) 1–16

Abstract: The respiratory system is immature at birth and significant development occurs postnatally. A critical period of respiratory development occurs in rats around postnatal days 12-13, when enhanced inhibition dominates over suppressed excitation. The ... ...

Abstract	The respiratory system is immature at birth and significant development occurs postnatally. A critical period of respiratory development occurs in rats around postnatal days 12-13, when enhanced inhibition dominates over suppressed excitation. The mechanisms underlying the heightened inhibition are not fully understood. The present study tested our hypothesis that the inhibition is marked by a switch in glycine receptor subunits from neonatal to adult form around the critical period. An in-depth immunohistochemical and single neuron optical densitometric study was undertaken on four respiratory-related nuclear groups (the pre-Bötzinger complex, nucleus ambiguus, hypoglossal nucleus, and ventrolateral subnucleus of solitary tract nucleus), and a non-respiratory cuneate nucleus in P2-21 rats. Our data revealed that in the respiratory-related nuclear groups: (1) the expressions of GlyRα2 and GlyRα3 were relatively high at P2, but declined after 1-1½ weeks to their lowest levels at P21; (2) the expression of GlyRα1 increased with age and reached significance at P12; and (3) the expression of GlyRβ rose from P2 to P12 followed by a slight decline until P21. No distinct increase in GlyRα1 at P12 was noted in the cuneate nucleus. Thus, there is a switch in dominance of expression from neonatal GlyRα2/α3 to the adult GlyRα1 and a heightened expression of GlyRα1 around the critical period in all respiratory-related nuclear groups, thereby supporting enhanced inhibition at that time. The rise in the expression of GlyRβ around P12 indicates that it plays an important role in forming the mature heteropentameric glycine receptors in these brain stem nuclear groups.
MeSH term(s)	Animals ; Brain Stem/chemistry ; Brain Stem/cytology ; Brain Stem/growth & development ; Female ; Male ; Rats ; Rats, Sprague-Dawley ; Receptors, Glycine/analysis ; Receptors, Glycine/immunology ; Respiratory Physiological Phenomena
Chemical Substances	Glra2 protein, rat ; Glrb protein, rat ; Receptors, Glycine ; glycine receptor alpha3 subunit
Language	English
Publishing date	2013-09-27
Publishing country	Netherlands
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	1200-2
ISSN	1872-6240 ; 0006-8993
ISSN (online)	1872-6240
ISSN	0006-8993
DOI	10.1016/j.brainres.2013.09.028
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