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01-06-2018 | Original Article

Vesicular glutamate transporter 1 (VGLUT1)- and VGLUT2-immunopositive axon terminals on the rat jaw-closing and jaw-opening motoneurons

Authors: Sook Kyung Park, Sang Jin Ko, Sang Kyoo Paik, Jong-Cheol Rah, Kea Joo Lee, Yong Chul Bae

Published in: Brain Structure and Function | Issue 5/2018

Abstract

To provide information on the glutamatergic synapses on the trigeminal motoneurons, which may be important for understanding the mechanism of control of jaw movements, we investigated the distribution of vesicular glutamate transporter (VGLUT)1-immunopositive (+) and VGLUT2 + axon terminals (boutons) on the rat jaw-closing (JC) and jaw-opening (JO) motoneurons, and their morphological determinants of synaptic strength by retrograde tracing, electron microscopic immunohistochemistry, and quantitative ultrastructural analysis. We found that (1) the large majority of VGLUT + boutons on JC and JO motoneurons were VGLUT2+, (2) the density of VGLUT1 + boutons terminating on JC motoneurons was significantly higher than that on JO motoneurons, (3) the density of VGLUT1 + boutons terminating on non-primary dendrites of JC motoneurons was significantly higher than that on somata or primary dendrites, whereas the density of VGLUT2 + boutons was not significantly different between JC and JO motoneurons and among various compartments of the postsynaptic neurons, and (4) the bouton volume, mitochondrial volume, and active zone area of the VGLUT1 + boutons forming synapses on JC motoneurons were significantly bigger than those of VGLUT2 + boutons. These findings suggest that JC and JO motoneurons receive glutamatergic input primarily from VGLUT2-expressing intrinsic neurons (premotoneurons), and may be controlled differently by neurons in the trigeminal mesencephalic nucleus and by glutamatergic premotoneurons.

We used the formula V (µ³) = \({\text{~}}\mathop \sum \nolimits_{{i=1}}^{n} 0.{\text{075A}}i{\text{~}}\) and Area (µ²) =\({\text{~}}\mathop \sum \nolimits_{{i=1}}^{n} 0.{\text{075}}Li{\text{~}}\): “V” is the volume of a bouton or mitochondria, “A” is the cross-sectional area of the bouton or mitochondria of the bouton measured in an individual section. “Area” is the active zone area of a bouton, “L” is length of presynaptic density of the bouton measured in an individual section. “n” is the number of sections in the series.

Alvarez FJ, Villalba RM, Zerda R, Schneider SP (2004) Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J Comp Neurol 472:257–280CrossRefPubMed

Alvarez FJ, Titus-Mitchell HE, Bullinger KL, Kraszpulski M, Nardelli P, Cope TC (2011) Permanent central synaptic disconnection of proprioceptors after nerve injury and regeneration. I. Loss of VGLUT1/IA synapses on motoneurons. J Neurophysiol 106:2450–2470CrossRefPubMedPubMedCentral

Atwood HL, Marin L (1983) Ultrastructure of synapses with different transmitter-releasing characteristics on motor axon terminals of a crab, Hyas areneas. Cell Tissue Res 231:103–115CrossRefPubMed

Bae YC, Nakagawa S, Yasuda K, Yabuta NH, Yoshida A, Pil PK, Moritani M, Chen K, Nagase Y, Takemura M, Shigenaga Y (1996) Electron microscopic observation of synaptic connections of jaw-muscle spindle and periodontal afferent terminals in the trigeminal motor and supratrigeminal nuclei in the cat. J Comp Neurol 374:421–435CrossRefPubMed

Bae YC, Nakamura T, Ihn HJ, Choi MH, Yoshida A, Moritani M, Honma S, Shigenaga Y (1999) Distribution pattern of inhibitory and excitatory synapses in the dendritic tree of single masseter alpha-motoneurons in the cat. J Comp Neurol 14:454–468CrossRef

Bae YC, Ihn HJ, Park MJ, Ottersen OP, Moritani M, Yoshida A, Shigenaga Y (2000) Identification of signal substances in synapses made between primary afferents and their associated axon terminals in the rat trigeminal sensory nuclei. J Comp Neurol 418:299–309CrossRefPubMed

Bae YC, Kim JP, Choi BJ, Park KP, Choi MK, Moritani M, Yoshida A, Shigenaga Y (2003) Synaptic organization of tooth pulp afferent terminals in the rat trigeminal sensory nuclei. J Comp Neurol 463:13–24CrossRefPubMed

Balschun D, Moechars D, Callaerts-Vegh Z, Vermaercke B, Van Acker N, Andries L, D’Hooge R (2010) Vesicular glutamate transporter VGLUT1 has a role in hippocampal long-term potentiation and spatial reversal learning. Cereb Cortex 20:684–693CrossRefPubMed

Dittman JS, Regehr WG (1998) Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J Neurosci 18:6147–6162CrossRefPubMed

Enomoto A, Kogo M, Koizumi H, Ishihama K, Yamanishi T (2002) Localization of premotoneurons for an NMDA-induced repetitive rhythmical activity to TMNs. Neuroreport 13:2303–2307CrossRefPubMed

Faunes M, Oñate-Ponce A, Fernández-Collemann S, Henny P (2016) Excitatory and inhibitory innervation of the mouse orofacial motor nuclei: A stereological study. J Comp Neurol 524:738–758CrossRefPubMed

Fremeau RT Jr, Voglmaier S, Seal RP, Edwards RH (2004) VGLUTs define subsets of excitatory neurons and suggest novel roles for glutamate. Trends Neurosci 27:98–103CrossRefPubMed

Ge SN, Ma YF, Hioki H, Wei YY, Kaneko T, Mizuno N, Gao GD, Li JL (2010) Coexpression of VGLUT1 and VGLUT2 in trigeminothalamic projection neurons in the principal sensory trigeminal nucleus of the rat. J Comp Neurol 518:3149–3168CrossRefPubMed

Graziano A, Liu XB, Murray KD, Jones EG (2008) Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse. J Comp Neurol 507:1258–1276CrossRefPubMed

Hackett TA, Takahata T, Balaram P (2011) VGLUT1 and VGLUT2 mRNA expression in the primate auditory pathway. Hear Res 274:129–141CrossRefPubMed

Hessler NA, Shirke AM, Malinow R (1993) The probability of transmitter release at a mammalian central synapse. Nature 366:569–572CrossRefPubMed

Hughes DI, Polgár E, Shehab SA, Todd AJ (2004) Peripheral axotomy induces depletion of the vesicular glutamate transporter VGLUT1 in central terminals of myelinated afferent fibres in the rat spinal cord. Brain Res 1017:69–76CrossRefPubMed

Hur EE, Edwards RH, Rommer E, Zaborszky L (2009) Vesicular glutamate transporter 1 and vesicular glutamate transporter 2 synapses on cholinergic neurons in the sublenticular gray of the rat basal forebrain: a double-label electron microscopic study. Neuroscience 164:1721–1731CrossRefPubMedPubMedCentral

Kaneko T, Fujiyama F (2002) Complementary distribution of vesicular glutamate transporters in the central nervous system. Neurosci Res 42:243–250CrossRefPubMed

Katakura N, Chandler SH (1990) An iontophoretic analysis of the pharmacologic mechanisms responsible for trigeminal motoneuronal discharge during masticatory-like activity in the guinea pig. J Neurophysiol 63:356–369CrossRefPubMed

Kidokoro Y, Kubota K, Shuto S, Sumino R (1968) Reflex organization of cat masticatory muscles. J Neurophysiol 31:695–708CrossRefPubMed

Kim YS, Park JH, Choi SJ, Bae JY, Ahn DK, McKemy DD, Bae YC (2014) Central connectivity of transient receptor potential melastatin 8-expressing axons in the brain stem and spinal dorsal horn. PLoS One 9:e94080CrossRefPubMedPubMedCentral

Kishimoto H, Bae YC, Yoshida A, Moritani M, Takemura M, Nakagawa S, Nagase Y, Wada T, Sessle BJ, Shigenaga Y (1998) Central distribution of synaptic contacts of primary and secondary jaw muscle spindle afferents in the trigeminal motor nucleus of the cat. J Comp Neurol 391:50–63CrossRefPubMed

Kogo M, Funk GD, Chandler SH (1996) Rhythmical oral-motor activity recorded in an in vitro brainstem preparation. Somatosens Mot Res 13:39–48CrossRefPubMed

Landry M, Bouali-Benazzouz R, El Mestikawy S, Ravassard P, Nagy F (2004) Expression of vesicular glutamate transporters in rat lumbar spinal cord, with a note on dorsal root ganglia. J Comp Neurol 468:380–394CrossRefPubMed

Li JL, Xiong KH, Dong YL, Fujiyama F, Kaneko T, Mizuno N (2003) Vesicular glutamate transporters, VGluT1 and VGluT2, in the trigeminal ganglion neurons of the rat, with special reference to coexpression. J Comp Neurol 463:212–220CrossRefPubMed

Liguz-Lecznar M, Skangiel-Kramska J (2007) Vesicular glutamate transporters (VGLUTs): the three musketeers of glutamatergic system. Acta Neurobiol Exp (Wars) 67:207–218

Lund JP, Sadeghi S, Athanassiadis T, Caram Salas N, Auclair F, Thivierge B, Arsenault I, Rompré P, Westberg KG, Kolta A (2010) Assessment of the potential role of muscle spindle mechanoreceptor afferents in chronic muscle pain in the rat masseter muscle. PLoS One 5:e11131CrossRefPubMedPubMedCentral

Malet M, Brumovsky PR (2015) VGLUTs and glutamate synthesis-focus on DRG neurons and pain. Biomolecules 5:3416–3137CrossRefPubMedPubMedCentral

Matesz C (1994) Synaptic relations of the trigeminal motoneurons in a frog (Rana esculenta). Eur J Morphol 32:117–121PubMed

Oliveira AL, Hydling F, Olsson E, Shi T, Edwards RH, Fujiyama F, Kaneko T, Hökfelt T, Cullheim S, Meister B (2003) Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 50:117–129CrossRefPubMed

Paik SK, Kim SK, Choi SJ, Yang ES, Ahn SH, Bae YC (2012) Vesicular glutamate transporters in axons that innervate the human dental pulp. J Endod 38:470–474CrossRefPubMed

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 498:129–141CrossRefPubMed

Pang YW, Ge SN, Nakamura KC, Li JL, Xiong KH, Kaneko T, Mizuno N (2009) Axon terminals expressing vesicular glutamate transporter VGLUT1 or VGLUT2 within the trigeminal motor nucleus of the rat: origins and distribution patterns. J Comp Neurol 512:595–612CrossRefPubMed

Peters A, Palay SL, Webster HdeF (1991) The fine structure of the nervous system, 3rd edn. Oxford university press, New York, pp 70–100

Propst JW, Ko CP (1987) Correlations between active zone ultrastructure and synaptic function studied with freeze-fracture of physiologically identified neuromuscular junctions. J Neurosci 7:3654–3664CrossRefPubMed

Rosenmund C, Clements JD, Westbrook GL (1993) Nonuniform probability of glutamate release at a hippocampal synapse. Science 262:754–757CrossRefPubMed

Shepherd GM, Koch C (1990) Appendix: Dendritic electrotonus and synaptic integration. In: Shepherd GM (ed) The synaptic organization of the brain. Oxford university press, New York, pp 439–473

Todd AJ, Hughes DI, Polgár E, Nagy GG, Mackie M, Ottersen OP, Maxwell DJ (2003) The expression of vesicular glutamate transporters VGLUT1 and VGLUT2 in neurochemically defined axonal populations in the rat spinal cord with emphasis on the dorsal horn. Eur J Neurosci 17:13–27CrossRefPubMed

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 488:28–47CrossRefPubMed

Varoqui H, Schäfer MK, Zhu H, Weihe E, Erickson JD (2002) Identification of the differentiation-associated Na+/PI transporter as a novel vesicular glutamate transporter expressed in a distinct set of glutamatergic synapses. J Neurosci 22:142–155CrossRefPubMed

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

Wu SX, Koshimizu Y, Feng YP, Okamoto K, Fujiyama F, Hioki H, Li YQ, Kaneko T, Mizuno N (2004) Vesicular glutamate transporter immunoreactivity in the central and peripheral endings of muscle-spindle afferents. Brain Res 1011:247–251CrossRefPubMed

Yeo EJ, Cho YS, Paik SK, Yoshida A, Park MJ, Ahn DK, Moon C, Kim YS, Bae YC (2010) Ultrastructural analysis of the synaptic connectivity of TRPV1-expressing primary afferent terminals in the rat trigeminal caudal nucleus. J Comp Neurol 518:4134–4146CrossRefPubMed

Yeow MB, Peterson EH (1991) Active zone organization and vesicle content scale with bouton size at a vertebrate central synapse. J Comp Neurol 307:475–486CrossRefPubMed

Title: Vesicular glutamate transporter 1 (VGLUT1)- and VGLUT2-immunopositive axon terminals on the rat jaw-closing and jaw-opening motoneurons
Authors: Sook Kyung Park
Sang Jin Ko
Sang Kyoo Paik
Jong-Cheol Rah
Kea Joo Lee
Yong Chul Bae
Publication date: 01-06-2018
Publisher: Springer Berlin Heidelberg
Published in: Brain Structure and Function / Issue 5/2018
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI: https://doi.org/10.1007/s00429-018-1636-y

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Vesicular glutamate transporter 1 (VGLUT1)- and VGLUT2-immunopositive axon terminals on the rat jaw-closing and jaw-opening motoneurons

Abstract

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Abstract

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