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01-04-2021 | Original Article

Development of γ-aminobutyric acid-, glycine-, and glutamate-immunopositive boutons on the rat genioglossal motoneurons

Authors: Sang Kyoo Paik, Atsushi Yoshida, Yong Chul Bae

Published in: Brain Structure and Function | Issue 3/2021

Abstract

Detailed information about the development of excitatory and inhibitory synapses on the genioglossal (GG) motoneuron may help to understand the mechanism of fine control of GG motoneuron firing and the coordinated tongue movement during postnatal development. For this, we investigated the development of γ-aminobutyric acid (GABA)-immunopositive (GABA +), glycine + (Gly +), and glutamate + (Glut +) axon terminals (boutons) on the somata of rat GG motoneurons at a postnatal day 2 (P2), P6 and P18 by retrograde labeling of GG motoneurons with horseradish peroxidase, electron microscopic postembedding immunogold staining with GABA, Gly, and Glut antisera, and quantitative analysis. The number of boutons per GG motoneuron somata and the mean length of bouton apposition, measures of bouton size and synaptic covering percentage, were significantly increased from P2/P6 to P18. The number and fraction of GABA + only boutons of all boutons decreased significantly, whereas those of Gly + only boutons increased significantly from P2/P6 to P18, suggesting developmental switch from GABAergic to glycinergic synaptic transmission. The fraction of mixed GABA +/Gly + boutons of all boutons was the highest among inhibitory bouton types throughout the postnatal development. The fractions of excitatory and inhibitory boutons of all boutons remained unchanged during postnatal development. These findings reveal a distinct developmental pattern of inhibitory synapses on the GG motoneurons different from that on spinal or trigeminal motoneurons, which may have an important role in the regulation of the precise and coordinated movements of the tongue during the maturation of the oral motor system.

Apostolova G, Dechant G (2009) Development of neurotransmitter phenotypes in sympathetic neurons. Auton Neurosci 151:30–38. https://doi.org/10.1016/j.autneu.2009.08.012CrossRefPubMed

Aubrey KR (2016) Presynaptic control of inhibitory neurotransmitter content in VIAAT containing synaptic vesicles. Neurochem Int 98:94–102. https://doi.org/10.1016/j.neuint.2016.06.002CrossRefPubMed

Aubrey KR, Supplisson S (2018) Heterogeneous signaling at GABA and glycine co-releasing terminals. Front Synaptic Neurosci 10:40. https://doi.org/10.3389/fnsyn.2018.00040CrossRefPubMedPubMedCentral

Bae JY, Lee JS, Ko SJ, Cho YS, Rah JC, Cho HJ, Park MJ, Bae YC (2018) Extrasynaptic homomeric glycine receptors in neurons of the rat trigeminal mesencephalic nucleus. Brain Struct Funct 223:2259–2268. https://doi.org/10.1007/s00429-018-1607-3CrossRefPubMed

Berger AJ (2011) Development of synaptic transmission to respiratory motoneurons. Respir Physiol Neurobiol 179:34–42. https://doi.org/10.1016/j.resp.2011.03.002CrossRefPubMedPubMedCentral

Broman J, Anderson S, Ottersen OP (1993) Enrichment of glutamate-like immunoreactivity in primary afferent terminals throughout the spinal cord dorsal horn. Eur J Neurosci 5:1050–1061. https://doi.org/10.1111/j.1460-9568.1993.tb00958.xCrossRefPubMed

Carrascal L, Nieto-Gonzalez JL, Cameron WE, Torres B, Nunez-Abades PA (2005) Changes during the postnatal development in physiological and anatomical characteristics of rat motoneurons studied in vitro. Brain Res Brain Res Rev 49:377–387. https://doi.org/10.1016/j.brainresrev.2005.02.003CrossRefPubMed

Chery N, De Koninck Y (2000) GABA(B) receptors are the first target of released GABA at lamina I inhibitory synapses in the adult rat spinal cord. J Neurophysiol 84:1006–1011. https://doi.org/10.1152/jn.2000.84.2.1006CrossRefPubMed

Cragg BG (1975) The development of synapses in the visual system of the cat. J Comp Neurol 160:147–166. https://doi.org/10.1002/cne.901600202CrossRefPubMed

Dulcis D, Jamshidi P, Leutgeb S, Spitzer NC (2013) Neurotransmitter switching in the adult brain regulates behavior. Science 340:449–453. https://doi.org/10.1126/science.1234152CrossRefPubMed

Gao BX, Stricker C, Ziskind-Conhaim L (2001) Transition from GABAergic to glycinergic synaptic transmission in newly formed spinal networks. J Neurophysiol 86:492–502. https://doi.org/10.1152/jn.2001.86.1.492CrossRefPubMed

Gao XP, Liu QS, Liu Q, Wong-Riley MT (2011) Excitatory-inhibitory imbalance in hypoglossal neurons during the critical period of postnatal development in the rat. J Physiol 589:1991–2006. https://doi.org/10.1113/jphysiol.2010.198945CrossRefPubMedPubMedCentral

Habecker BA, Tresser SJ, Rao MS, Landis SC (1995) Production of sweat gland cholinergic differentiation factor depends on innervation. Dev Biol 167:307–316. https://doi.org/10.1006/dbio.1995.1025CrossRefPubMed

Hashimoto K, Kano M (2013) Synapse elimination in the developing cerebellum. Cell Mol Life Sci 70:4667–4680. https://doi.org/10.1007/s00018-013-1405-2CrossRefPubMedPubMedCentral

Hinds JW, Hinds PL (1976) Synapse formation in the mouse olfactory bulb. I. Quantitative studies. J Comp Neurol 169:15–40. https://doi.org/10.1002/cne.901690103CrossRefPubMed

Horner RL (2009) Emerging principles and neural substrates underlying tonic sleep-state-dependent influences on respiratory motor activity. Philos Trans R Soc Lond B Biol Sci 364:2553–2564. https://doi.org/10.1098/rstb.2009.0065CrossRefPubMedPubMedCentral

Inquimbert P, Rodeau JL, Schlichter R (2007) Differential contribution of GABAergic and glycinergic components to inhibitory synaptic transmission in lamina II and laminae III–IV of the young rat spinal cord. Eur J Neurosci 26:2940–2949. https://doi.org/10.1111/j.1460-9568.2007.05919.xCrossRefPubMed

Kolston J, Osen KK, Hackney CM, Ottersen OP, Storm-Mathisen J (1992) An atlas of glycine- and GABA-like immunoreactivity and colocalization in the cochlear nuclear complex of the guinea pig. Anat Embryol (Berl) 186:443–465CrossRef

Lim R, Alvarez FJ, Walmsley B (2000) GABA mediates presynaptic inhibition at glycinergic synapses in a rat auditory brainstem nucleus. J Physiol 525(Pt 2):447–459. https://doi.org/10.1111/j.1469-7793.2000.t01-1-00447.xCrossRefPubMedPubMedCentral

Liu Q, Wong-Riley MT (2005) Postnatal developmental expressions of neurotransmitters and receptors in various brain stem nuclei of rats. J Appl Physiol 98:1442–1457. https://doi.org/10.1152/japplphysiol.01301.2004CrossRefPubMed

Liu Q, Wong-Riley MT (2010) Postnatal development of N-methyl-d-aspartate receptor subunits 2A, 2B, 2C, 2D, and 3B immunoreactivity in brain stem respiratory nuclei of the rat. Neuroscience 171:637–654. https://doi.org/10.1016/j.neuroscience.2010.09.055CrossRefPubMedPubMedCentral

Liu X, Sood S, Liu H, Nolan P, Morrison JL, Horner RL (2003) Suppression of genioglossus muscle tone and activity during reflex hypercapnic stimulation by GABA(A) mechanisms at the hypoglossal motor nucleus in vivo. Neuroscience 116:249–259CrossRef

Lu T, Rubio ME, Trussell LO (2008) Glycinergic transmission shaped by the corelease of GABA in a mammalian auditory synapse. Neuron 57:524–535. https://doi.org/10.1016/j.neuron.2007.12.010CrossRefPubMed

Meng D, Li HQ, Deisseroth K, Leutgeb S, Spitzer NC (2018) Neuronal activity regulates neurotransmitter switching in the adult brain following light-induced stress. Proc Natl Acad Sci USA 115:5064–5071. https://doi.org/10.1073/pnas.1801598115CrossRefPubMed

Muller E, Triller A, Legendre P (2004) Glycine receptors and GABA receptor alpha 1 and gamma 2 subunits during the development of mouse hypoglossal nucleus. Eur J Neurosci 20:3286–3300. https://doi.org/10.1111/j.1460-9568.2004.03785.xCrossRefPubMed

Muller E, Le Corronc H, Triller A, Legendre P (2006) Developmental dissociation of presynaptic inhibitory neurotransmitter and postsynaptic receptor clustering in the hypoglossal nucleus. Mol Cell Neurosci 32:254–273. https://doi.org/10.1016/j.mcn.2006.04.007CrossRefPubMed

Nabekura J, Katsurabayashi S, Kakazu Y, Shibata S, Matsubara A, Jinno S, Mizoguchi Y, Sasaki A, Ishibashi H (2004) Developmental switch from GABA to glycine release in single central synaptic terminals. Nat Neurosci 7:17–23. https://doi.org/10.1038/nn1170CrossRefPubMed

Nagata S, Nakamura S, Nakayama K, Mochizuki A, Yamamoto M, Inoue T (2016) Postnatal changes in glutamatergic inputs of jaw-closing motoneuron dendrites. Brain Res Bull 127:47–55. https://doi.org/10.1016/j.brainresbull.2016.08.014CrossRefPubMed

O’Brien JA, Berger AJ (2001) The nonuniform distribution of the GABA(A) receptor alpha 1 subunit influences inhibitory synaptic transmission to motoneurons within a motor nucleus. J Neurosci 21:8482–8494CrossRef

O’Brien JA, Sebe JY, Berger AJ (2004) GABA(B) modulation of GABA(A) and glycine receptor-mediated synaptic currents in hypoglossal motoneurons. Respir Physiol Neurobiol 141:35–45. https://doi.org/10.1016/j.resp.2004.03.009CrossRefPubMed

O’Kusky JR (1998) Postnatal changes in the numerical density and total number of asymmetric and symmetric synapses in the hypoglossal nucleus of the rat. Brain Res Dev Brain Res 108:179–191. https://doi.org/10.1016/s0165-3806(98)00048-0CrossRefPubMed

Oshima S, Fukaya M, Masabumi N, Shirakawa T, Oguchi H, Watanabe M (2002) Early onset of NMDA receptor GluR epsilon 1 (NR2A) expression and its abundant postsynaptic localization in developing motoneurons of the mouse hypoglossal nucleus. Neurosci Res 43:239–250. https://doi.org/10.1016/s0168-0102(02)00035-4CrossRefPubMed

Ottersen OP, Storm-Mathisen J (1984) Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique. J Comp Neurol 229:374–392. https://doi.org/10.1002/cne.902290308CrossRefPubMed

Ottersen OP, Storm-Mathisen J, Madsen S, Skumlien S, Stromhaug J (1986) Evaluation of the immunocytochemical method for amino acids. Med Biol 64:147–158PubMed

Paik SK, Bae JY, Park SE, Moritani M, Yoshida A, Yeo EJ, Choi KS, Ahn DK, Moon C, Shigenaga Y, Bae YC (2007) Developmental changes in distribution of gamma-aminobutyric acid- and glycine-immunoreactive boutons on rat trigeminal motoneurons. I. Jaw-closing motoneurons. J Comp Neurol 503:779–789. https://doi.org/10.1002/cne.21423CrossRefPubMed

Paik SK, Park SK, Jin JK, Bae JY, Choi SJ, Yoshida A, Ahn DK, Bae YC (2011) Ultrastructural analysis of glutamate-immunopositive synapses onto the rat jaw-closing motoneurons during postnatal development. J Neurosci Res 89:153–161. https://doi.org/10.1002/jnr.22544CrossRefPubMed

Paik SK, Kwak WK, Bae JY, Na YK, Park SY, Yi HW, Ahn DK, Ottersen OP, Yoshida A, Bae YC (2012) Development of gamma-aminobutyric acid-, glycine-, and glutamate-immunopositive boutons on rat jaw-opening motoneurons. J Comp Neurol 520:1212–1226. https://doi.org/10.1002/cne.22771CrossRefPubMed

Paik SK, Yoo HI, Choi SK, Bae JY, Park SK, Bae YC (2019) Distribution of excitatory and inhibitory axon terminals on the rat hypoglossal motoneurons. Brain Struct Funct 224:1767–1779. https://doi.org/10.1007/s00429-019-01874-0CrossRefPubMed

Pang YW, Li JL, Nakamura K, Wu S, Kaneko T, Mizuno N (2006) Expression of vesicular glutamate transporter 1 immunoreactivity in peripheral and central endings of trigeminal mesencephalic nucleus neurons in the rat. J Comp Neurol 498:129–141. https://doi.org/10.1002/cne.21047CrossRefPubMed

Park SK, Lee DS, Bae JY, Bae YC (2016) Central connectivity of the chorda tympani afferent terminals in the rat rostral nucleus of the solitary tract. Brain Struct Funct 221:1125–1137. https://doi.org/10.1007/s00429-014-0959-6CrossRefPubMed

Park SK, Ko SJ, Paik SK, Rah JC, Lee KJ, Bae YC (2018) Vesicular glutamate transporter 1 (VGLUT1)- and VGLUT2-immunopositive axon terminals on the rat jaw-closing and jaw-opening motoneurons. Brain Struct Funct 223:2323–2334. https://doi.org/10.1007/s00429-018-1636-yCrossRefPubMed

Park SK, Hong JH, Jung JK, Ko HG, Bae YC (2019a) Vesicular Glutamate Transporter 1 (VGLUT1)- and VGLUT2-containing terminals on the rat jaw-closing gamma-motoneurons. Exp Neurobiol 28:451–457. https://doi.org/10.5607/en.2019.28.4.451CrossRefPubMedPubMedCentral

Park SK, Devi AP, Bae JY, Cho YS, Ko HG, Kim DY, Bae YC (2019b) Synaptic connectivity of urinary bladder afferents in the rat superficial dorsal horn and spinal parasympathetic nucleus. J Comp Neurol 527:3002–3013. https://doi.org/10.1002/cne.24725CrossRefPubMed

Plowman L, Lauff DC, Berthon-Jones M, Sullivan CE (1990) Waking and genioglossus muscle responses to upper airway pressure oscillation in sleeping dogs. J Appl Physiol 68:2564–2573. https://doi.org/10.1152/jappl.1990.68.6.2564CrossRefPubMed

Ronnevi LO (1977) Spontaneous phagocytosis of boutons on spinal motoneurons during early postnatal development. An electron microscopical study in the cat. J Neurocytol 6:487–504. https://doi.org/10.1007/BF01205215CrossRef

Ronnevi LO (1979) Spontaneous phagocytosis of C-type synaptic terminals by spinal alpha-motoneurons in newborn kittens. An electron microscopic study. Brain Res 162:189–199. https://doi.org/10.1016/0006-8993(79)90283-xCrossRefPubMed

Sanes DH, Reh TA, Harris WA (2012) Synapse formation and function. In: Sanes DH, Reh TA, Harris WA (eds) Development of the nervous system, 3rd edn. Elsevier, Amsterdam, pp 209–248CrossRef

Singer JH, Berger AJ (2000) Development of inhibitory synaptic transmission to motoneurons. Brain Res Bull 53:553–560CrossRef

Stanek E 4th, Cheng S, Takatoh J, Han BX, Wang F (2014) Monosynaptic premotor circuit tracing reveals neural substrates for oro-motor coordination. Elife 3:e02511. https://doi.org/10.7554/eLife.02511CrossRefPubMedPubMedCentral

Travers JB, Yoo JE, Chandran R, Herman K, Travers SP (2005) Neurotransmitter phenotypes of intermediate zone reticular formation projections to the motor trigeminal and hypoglossal nuclei in the rat. J Comp Neurol 488:28–47. https://doi.org/10.1002/cne.20604CrossRefPubMed

Vaughn JE (1989) Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3:255–285. https://doi.org/10.1002/syn.890030312CrossRefPubMed

Vonhoff F, Keshishian H (2017) Activity-dependent synaptic refinement: new insights from Drosophila. Front Syst Neurosci 11:23. https://doi.org/10.3389/fnsys.2017.00023CrossRefPubMedPubMedCentral

Weinberg RJ, van Eyck SL (1991) A tetramethylbenzidine/tungstate reaction for horseradish peroxidase histochemistry. J Histochem Cytochem 39:1143–1148. https://doi.org/10.1177/39.8.1906909CrossRefPubMed

Whitney GM, Ohtake PJ, Simakajornboon N, Xue YD, Gozal D (2000) AMPA glutamate receptors and respiratory control in the developing rat: anatomic and pharmacological aspects. Am J Physiol Regul Integr Comp Physiol 278:R520-528. https://doi.org/10.1152/ajpregu.2000.278.2.R520CrossRefPubMed

Wojcik SM, Katsurabayashi S, Guillemin I, Friauf E, Rosenmund C, Brose N, Rhee JS (2006) A shared vesicular carrier allows synaptic corelease of GABA and glycine. Neuron 50:575–587. https://doi.org/10.1016/j.neuron.2006.04.016CrossRefPubMed

Wong-Riley MT, Liu Q (2005) Neurochemical development of brain stem nuclei involved in the control of respiration. Respir Physiol Neurobiol 149:83–98. https://doi.org/10.1016/j.resp.2005.01.011CrossRefPubMed

Yamane A (2005) Embryonic and postnatal development of masticatory and tongue muscles. Cell Tissue Res 322:183–189. https://doi.org/10.1007/s00441-005-0019-xCrossRefPubMed

Title: Development of γ-aminobutyric acid-, glycine-, and glutamate-immunopositive boutons on the rat genioglossal motoneurons
Authors: Sang Kyoo Paik
Atsushi Yoshida
Yong Chul Bae
Publication date: 01-04-2021
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 3/2021
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-021-02216-9

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Development of γ-aminobutyric acid-, glycine-, and glutamate-immunopositive boutons on the rat genioglossal motoneurons

Abstract

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Abstract

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