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Differential expression of VGLUT1 or VGLUT2 in the trigeminothalamic or trigeminocerebellar projection neurons in the rat

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Abstract

The vesicular glutamate transporters, VGLUT1 and VGLUT2, reportedly display complementary distribution in the rat brain. However, co-expression of them in single neurons has been reported in some brain areas. We previously found co-expression of VGLUT1 and VGLUT2 mRNAs in a number of single neurons in the principal sensory trigeminal nucleus (Vp) of the adult rat; the majority of these neurons sent their axons to the thalamic regions around the posteromedial ventral nucleus (VPM) and the posterior nuclei (Po). It is well known that trigeminothalamic (T-T) projection fibers arise not only from the Vp but also from the spinal trigeminal nucleus (Vsp), and that trigeminocerebellar (T-C) projection fibers take their origins from both of the Vp and Vsp. Thus, in the present study, we examined the expression of VGLUT1 and VGLUT2 in Vp and Vsp neurons that sent their axons to the VPM/Po regions or the cortical regions of the cerebellum. For this purpose, we combined fluorescence in situ hybridization (FISH) histochemistry with retrograde tract-tracing; immunofluorescence histochemistry was also combined with anterograde tract-tracing. The results indicate that glutamatergic Vsp neurons sending their axons to the cerebellar cortical regions mainly express VGLUT1, whereas glutamatergic Vsp neurons sending their axons to the thalamic regions express VGLUT2. The present data, in combination with those of our previous study, indicate that glutamatergic Vp neurons projecting to the cerebellar cortical regions express mainly VGLUT1, whereas the majority of glutamatergic Vp neurons projecting to the thalamus co-express VGLUT1 and VGLUT2.

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References

  • Barroso-Chinea P, Castle M, Aymerich MS, Pérez-Manso M, Erro E, Tuñon T, Lanciego JL (2007) Expression of the mRNAs encoding for the vesicular glutamate transporters 1 and 2 in the rat thalamus. J Comp Neurol 501:703–715

    Article  CAS  PubMed  Google Scholar 

  • Barroso-Chinea P, Castle M, Aymerich MS, Lanciego JL (2008) Expression of vesicular glutamate transporters 1 and 2 in the cells of origin of the rat thalamostriatal pathway. J Chem Neuroanat 35:101–107

    Article  CAS  PubMed  Google Scholar 

  • Bellocchio EE, Hu H, Pohorille A, Chan J, Pickel VM, Edwards RH (1998) The localization of the brain-specific inorganic phosphate transporter suggests a specific presynaptic role in glutamatergic transmission. J Neurosci 18:8648–8659

    CAS  PubMed  Google Scholar 

  • Bruce LL, McHaffie JG, Stein BE (1987) The organization of trigeminotectal and trigeminothalamic neurons in rodents: a double-labeling study with fluorescent dyes. J Comp Neurol 262:315–330

    Article  CAS  PubMed  Google Scholar 

  • Erzurumlu RS, Bates CA, Killackey HP (1980) Differential organization of thalamic projection cells in the brain stem trigeminal complex of the rat. Brain Res 198:427–433

    Article  CAS  PubMed  Google Scholar 

  • Falls WM, Rice RE, VanWagner JP (1985) The dorsomedial portion of trigeminal nucleus oralis (Vo) in the rat: cytology and projections to the cerebellum. Somatosens Res 3:89–118

    Article  CAS  PubMed  Google Scholar 

  • Feldman SG, Kruger L (1980) An axonal transport study of the ascending projection of medial lemniscal neurons in the rat. J Comp Neurol 192:427–454

    Article  CAS  PubMed  Google Scholar 

  • Fremeau RT Jr, Troyer MD, Pahner I, Nygaard GO, Tran CH, Reimer RJ, Bellocchio EE, Fortin D, Storm-Mathisen J, Edwards RH (2001) The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31:247–260

    Article  CAS  PubMed  Google Scholar 

  • Fremeau RT Jr, Kam K, Qureshi T, Johnson J, Copenhagen DR, Storm-Mathisen J, Chaudhry FA, Nicoll RA, Edwards RH (2004a) Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites. Science 304:1815–1819

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Fujiyama F, Furuta T, Kaneko T (2001) Immunocytochemical localization of candidates for vesicular glutamate transporters in the rat cerebral cortex. J Comp Neurol 435:379–387

    Article  CAS  PubMed  Google Scholar 

  • Fukushima T, Kerr FWL (1979) Organization of trigeminothalamic tracts and other thalamic afferent systems of the brainstem in the rat: presence of gelatinosa neurons with thalamic connections. J Comp Neurol 183:169–184

    Article  CAS  PubMed  Google Scholar 

  • Furuta T, Timofeeva E, Nakamura K, Okamoto-Furuta K, Togo M, Kaneko T, Deschênes M (2008) Inhibitory gating of vibrissal inputs in the brainstem. J Neurosci 28:1789–1797

    Article  CAS  PubMed  Google Scholar 

  • 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 518:3149–3168

    Article  CAS  PubMed  Google Scholar 

  • 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 507:1258–1276

    Article  CAS  PubMed  Google Scholar 

  • Guy N, Chalus M, Dallel R, Voisin DL (2005) Both oral and caudal parts of the spinal trigeminal nucleus project to the somatosensory thalamus in the rat. Eur J Neurosci 21:741–754

    Article  PubMed  Google Scholar 

  • Hayashi H, Sumino R, Sessle BJ (1984) Functional organization of trigeminal subnucleus interpolaris: nociceptive and innocuous afferent inputs, projections to thalamus, cerebellum, and spinal cord, and descending modulation from periaqueductal gray. J Neurophysiol 51:890–905

    CAS  PubMed  Google Scholar 

  • Herzog E, Bellenchi GC, Gras C, Bernard V, Ravassard P, Bedet C, Gasnier B, Giros B, EL Mestikawy S (2001) The existence of a second vesicular glutamate transporter specifies subpopulations of glutamatergic neurons. J Neurosci 21:RC181 (1–6)

    Google Scholar 

  • Herzog E, Takamori S, Jahn R, Brose N, Wojcik SM (2006) Synaptic and vesicular co-localization of the glutamate transporters VGLUT1 and VGLUT2 in the mouse hippocampus. J Neurochem 99:1011–1018

    Article  CAS  PubMed  Google Scholar 

  • Hioki H, Fujiyama F, Taki K, Tomioka R, Furuta T, Tamamaki N, Kaneko T (2003) Differential distribution of vesicular glutamate transporters in the rat cerebellar cortex. Neuroscience 117:1–6

    Article  CAS  PubMed  Google Scholar 

  • Hisano S, Sawada K, Kawano M, Kanemoto M, Xiong G, Mogi K, Sakata-Haga H, Takeda J, Fukui Y, Nogami H (2002) Expression of inorganic phosphate/vesicular glutamate transporters (BNPI/VGLUT1 and DNPI/VGLUT2) in the cerebellum and precerebellar nuclei of the rat. Mol Brain Res 107:23–31

    Article  CAS  PubMed  Google Scholar 

  • Huerta MF, Frankfurter A, Harting JK (1983) Studies of the principal sensory and spinal trigeminal nuclei of the rat: projections to the superior colliculus, inferior olive, and cerebellum. J Comp Neurol 220:147–167

    Article  CAS  PubMed  Google Scholar 

  • Ikeda M (1979) Projections from the spinal and the principal sensory nuclei of the trigeminal nerve to the cerebellar cortex in the cat, as studied by retrograde transport of horseradish peroxidase. J Comp Neurol 184:567–586

    Article  CAS  PubMed  Google Scholar 

  • Jacquin MF, Mooney RD, Rhoades RW (1986) Morphology, response properties, and collateral projections of trigeminothalamic neurons in brainstem subnucleus interpolaris of rat. Exp Brain Res 61:457–468

    Article  CAS  PubMed  Google Scholar 

  • Jacquin MF, Barcia M, Rhoades BW (1989) Structure–function relationships in rat brainstem subnucleus interpolaris: IV. Projection neurons. J Comp Neurol 282:45–62

    Article  CAS  PubMed  Google Scholar 

  • Joseph JW, Shambes GM, Gibson JM, Welker W (1978) Tactile projections to granule cells in caudal vermis of the rat’s cerebellum. Brain Behav Evol 15:141–149

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Kaneko T, Fujiyama F, Hioki H (2002) Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J Comp Neurol 444:39–62

    Article  CAS  PubMed  Google Scholar 

  • Kemplay S, Webster KE (1989) A quantitative study of the projections of the gracile, cuneate and trigeminal nuclei and of the medullary reticular formation to the thalamus in the rat. Neuroscience 32:153–167

    Article  CAS  PubMed  Google Scholar 

  • Kimoto Y, Satoh K, Sakumoto T, Tohyama M, Shimizu N (1978) Afferent fiber connections from the lower brain stem to the rat cerebellum by the horseradish peroxidase method combined with MAO staining, with special reference to noradrenergic neurons. J Hirnforsch 19:85–100

    CAS  PubMed  Google Scholar 

  • Kobayashi Y (1995) Distribution and size of cerebellar and thalamic projection neurons in the trigeminal principal sensory nucleus and adjacent nuclei in the rat. Acta Anat Nippon 70:156–171

    CAS  PubMed  Google Scholar 

  • Kuramoto E, Furuta T, Nakamura KC, Unzai T, Hioki H, Kaneko T (2009) Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb Cortex 19:2065–2077

    Article  PubMed  Google Scholar 

  • Liguz-Lecznar M, Skangiel-Kramska J (2007) Vesicular glutamate transporters VGLUT1 and VGLUT2 in the developing mouse barrel cortex. Int J Dev Neurosci 25:107–114

    Article  CAS  PubMed  Google Scholar 

  • Mantle-St.John LA, Tracey DJ (1987) Somatosensory nuclei in the brainstem of the rat: independent projections to the thalamus and cerebellum. J Comp Neurol 255:259–271

    Article  CAS  PubMed  Google Scholar 

  • Matsushita M, Ikeda M, Okado N (1982) The cells of origin of the trigeminothalamic, trigeminospinal and trigeminocerebellar projections in the cat. Neuroscience 7:1439–1454

    Article  CAS  PubMed  Google Scholar 

  • Mizuno N (1970) Projection fibers from the main sensory trigeminal nucleus and the supratrigeminal region. J Comp Neurol 139:457–472

    Article  CAS  PubMed  Google Scholar 

  • Nakamura K, Hioki H, Fujiyama F, Kaneko T (2005) Postnatal changes of vesicular glutamate transporter (VGLUT)1 and VGLUT2 immunoreactivities and their colocalization in the mouse forebrain. J Comp Neurol 492:262–288

    Article  Google Scholar 

  • Nakamura K, Watakabe A, Hioki H, Fujiyama F, Tanaka Y, Yamamori T, Kaneko T (2008) Transiently increased colocalization of vesicular glutamate transporters 1 and 2 at single axon terminals during postnatal development of mouse neocortex: a quantitative analysis with correlation coefficient. Eur J Neurosci 28:1032–1046

    Article  Google Scholar 

  • Ni B, Wu X, Yan GM, Wang J, Paul SM (1995) Regional expression and cellular localization of the Na+-dependent inorganic phosphate cotransporter of rat brain. J Neurosci 15:5789–5799

    CAS  PubMed  Google Scholar 

  • Oliveira ALR, Hydling F, Olsson E, Shi T, Edwards RH, Fujiyama F, Kaneko T, Hökfeld 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 50:117–129

    Article  CAS  PubMed  Google Scholar 

  • Palay SL, Chan-Palay V (1974) Cerebellar cortex. Cytology and organization. Springer, New York

    Book  Google Scholar 

  • 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 512:595–612

    Article  PubMed  Google Scholar 

  • Patrick GW, Haines DE (1982) Cerebellar afferents to paramedian lobule from the trigeminal complex in Tupaia glis: a horseradish peroxidase (HRP) study. J Morphol 172:209–222

    Article  CAS  PubMed  Google Scholar 

  • Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, 6th edn. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Peschanski M (1984) Trigeminal afferents to the diencephalon in the rat. Neuroscience 12:465–487

    Article  CAS  PubMed  Google Scholar 

  • Phelan KD, Falls WM (1991) A comparison of the distribution and morphology of thalamic, cerebellar and spinal projection neurons in rat trigeminal nucleus interpolaris. Neuroscience 40:497–511

    Article  CAS  PubMed  Google Scholar 

  • Saigal RP, Karamanlidis AN, Voogd J, Mangana O, Michaloudi H (1980) Secondary trigeminocerebellar projections in sheep studied with the horseradish peroxidase tracing method. J Comp Neurol 189:537–553

    Article  CAS  PubMed  Google Scholar 

  • Sakata-Haga H, Kanemoto M, Maruyama D, Hoshi K, Mogi K, Narita M, Okado N, Ikeda Y, Nogami H, Fukui Y, Kojima I, Takeda J, Hisano S (2001) Differential localization and colocalization of two neuron-types of sodium-dependent inorganic phosphate cotransporters in rat forebrain. Brain Res 902:143–155

    Article  CAS  PubMed  Google Scholar 

  • Shambes GM, Beermann DH, Welker W (1978a) Multiple tactile areas in cerebellar cortex: another patchy cutaneous projection to granule cell columns in rats. Brain Res 157:123–128

    Article  CAS  PubMed  Google Scholar 

  • Shambes GM, Gibson JM, Welker W (1978b) Fractured somatotopy in granule cell tactile areas of rat cerebellar hemispheres revealed by micromapping. Brain Behav Evol 15:94–140

    Article  CAS  PubMed  Google Scholar 

  • Shigenaga Y, Nakatani Z, Nishimori T, Suemune S, Kuroda R, Matano S (1983) The cells of origin of cat trigeminothalamic projections: especially in the caudal medulla. Brain Res 277:201–222

    Article  CAS  PubMed  Google Scholar 

  • Silverman JD, Kruger L (1985) Projections of the rat trigeminal sensory nuclear complex demonstrated by multiple fluorescent dye retrograde transport. Brain Res 361:383–388

    Article  CAS  PubMed  Google Scholar 

  • Somana R, Kotchabhakdi N, Walberg F (1980) Cerebellar afferents from the trigeminal sensory nuclei in the cat. Exp Brain Res 38:57–64

    Article  CAS  PubMed  Google Scholar 

  • Somers D, Panneton WM (1984) Heterogeneity of neurons in the subnucleus interpolaris of the cat. Brain Res 309:335–340

    Article  CAS  PubMed  Google Scholar 

  • Steindler DA (1977) Trigemino-cerebellar projections in normal and reeler mutant mice. Neurosci Lett 6:293–300

    Article  CAS  PubMed  Google Scholar 

  • Steindler DA (1985) Trigeminocerebellar, trigeminotectal, and trigeminothalamic projections: a double retrograde axonal tracing study in the mouse. J Comp Neurol 237:155–175

    Article  CAS  PubMed  Google Scholar 

  • Van Ham JJ, Yeo CH (1992) Somatosensory trigeminal projections to the inferior olive, cerebellum and other precerebellar nuclei in rabbits. Eur J Neurosci 4:302–317

    Article  PubMed  Google Scholar 

  • Varoqui H, Schäfer MKH, 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 22:142–155

    CAS  PubMed  Google Scholar 

  • Waite PME (2004) Trigeminal sensory system. In: Paxinos G (ed) The rat nervous system, 3rd edn. Elsevier Academic Press, Amsterdam, pp 817–851

    Google Scholar 

  • Watakabe A, Ohsawa S, Hashikawa T, Yamamori T (2006) Binding and complementary expression patterns of semaphorin 3E and plexin D1 in the mature neocortices of mice and monkeys. J Comp Neurol 499:258–273

    Article  CAS  PubMed  Google Scholar 

  • Watson CRR, Switzer RC III (1978) Trigeminal projections to cerebellar tactile areas in the rat-origin mainly from n. interpolaris and n. principalis. Neurosci Lett 10:77–82

    Article  CAS  PubMed  Google Scholar 

  • Woolston DC, Kassel J, Gibson JM (1981) Trigeminocerebellar mossy fiber branching to granule cell layer patches in the rat cerebellum. Brain Res 209:255–269

    Article  CAS  PubMed  Google Scholar 

  • Woolston DC, La Londe JR, Gibson JM (1982) Comparison of response properties of cerebellar- and thalamic-projecting interpolaris neurons. J Neurophysiol 48:160–173

    CAS  PubMed  Google Scholar 

  • Yasui Y, Itoh K, Mizuno N, Nomura S, Takada M, Konishi A, Kudo M (1983) The posteromedial ventral nucleus of the thalamus (VPM) of the cat: direct ascending projections to the cytoarchitectonic subdivisions. J Comp Neurol 220:219–228

    Article  CAS  PubMed  Google Scholar 

  • Yeo CH, Hardiman MJ, Glickstein M (1985) Classical conditioning of the nictitating membrane response of the rabbit. III. Connections of cerebellar lobule HVI. Exp Brain Res 60:114–126

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by National Natural Science Foundation of China (Grant 81070900 to J.-L. Li), Key Subject of Traditional Chinese Medicine Scientific Research of Military (No.10 ZYZ35 to J.-L. Li), Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (24500408, 23123510 to H. Hioki; 22300113, 23650175, 23115101 to T. Kaneko).

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Correspondence to Guo-Dong Gao or Jin-Lian Li.

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S.-N. Ge, Z.-H. Li and J. Tang contributed equally to this work.

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Ge, SN., Li, ZH., Tang, J. et al. Differential expression of VGLUT1 or VGLUT2 in the trigeminothalamic or trigeminocerebellar projection neurons in the rat. Brain Struct Funct 219, 211–229 (2014). https://doi.org/10.1007/s00429-012-0495-1

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