Vesicular glutamate transporters define two sets of glutamatergic afferents to the somatosensory thalamus and two thalamocortical projections in the mouse

Journal of Comparative Neurology

Volumn 507, Issue 2, 2008, Pages 1258-1276

  Graziano, Alessandro ^a   Liu, Xiao Bo ^a   Murray, Karl D ^a   Jones, Edward G ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

BNPI; Core matrix; Corticothalamic; DNPI; Medial lemniscus; Spinothalamic; Synapses

Indexed keywords

ANTIBODY; VESICULAR GLUTAMATE TRANSPORTER; VESICULAR GLUTAMATE TRANSPORTER 1; VESICULAR GLUTAMATE TRANSPORTER 2;

ARTICLE; ELECTRON MICROSCOPY; GENE EXPRESSION; IMMUNOCYTOCHEMISTRY; MEDIAL LEMNISCUS; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; SENSORY NERVE; SOMATOSENSORY CORTEX; SPINOTHALAMIC TRACT; SYNAPSE; SYNAPSE VESICLE; THALAMOCORTICAL TRACT; THALAMUS;

AFFERENT PATHWAYS; ANIMALS; BIOLOGICAL MARKERS; BRAIN MAPPING; BRAIN STEM; EFFERENT PATHWAYS; GENE EXPRESSION; GLUTAMIC ACID; IN SITU HYBRIDIZATION; MICE; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; PRESYNAPTIC TERMINALS; RNA, MESSENGER; SOMATOSENSORY CORTEX; SPINAL CORD; SYNAPTIC TRANSMISSION; VENTRAL THALAMIC NUCLEI; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 39649083368     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21592     Document Type: Article

References (84)

1. 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 472:257-280.
2. Barroso-Chinea P, Castle M, Aymerich MS, Perez-Manso M, Erro E, Tunon 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.
3. 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.
4. Billups B. 2005. Colocalization of vesicular glutamate transporters in the rat superior olivary complex. Neurosci Lett 382:66-70.
5. Bolte S, Cordelieres FP. 2006. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 224:213-232.
6. Boulland JL, Qureshi T, Seal RP, Rafiki A, Gundersen V, Bergersen LH, Fremeau RT Jr, Edwards RH, Storm-Mathisen J, Chaudhry FA. 2004. Expression of the vesicular glutamate transporters during development indicates the widespread corelease of multiple neurotransmitters. J Comp Neurol 480:264-280.
7. Bourassa J, Deschênes M. 1995. Corticothalamic projections from the primary visual cortex in rats: a single fiber study using biocytin as an anterograde tracer. Neuroscience 66:253-263.
8. Bourassa J, Pinault D, Deschênes M. 1995. Corticothalamic projections from the cortical barrel field to the somatosensory thalamus in rats: a single-fibre study using biocytin as an anterograde tracer. Eur J Neurosci 7:19-30.
9. Broman J. 1994. Neurotransmitters in subcortical somatosensory pathways. Anat Embryol (Berl) 189:181-214.
10. Castro-Alamancos MA. 2002. Properties of primary sensory (lemniscal) synapses in the ventrobasal thalamus and the relay of high-frequency sensory inputs. J Neurophysiol 87:946-953.
11. Castro-Alamancos MA, Calcagnotto ME. 1999. Presynaptic long-term potentiation in corticothalamic synapses. J Neurosci 19:9090-9097.
12. Clements JR, Toth DD, Highfield DA, Grant SJ. 1991. Glutamate-like immunoreactivity is present within cholinergic neurons of the laterodorsal tegmental and pedunculopontine nuclei. Adv Exp Med Biol 295:127-142.
13. Commons KG, Beck SG, Bey VW. 2005. Two populations of glutamatergic axons in the rat dorsal raphe nucleus defined by the vesicular glutamate transporters 1 and 2. Eur J Neurosci 21:1577-1586.
14. Conti F, Candiracci C, Fattorini G. 2005. Heterogeneity of axon terminals expressing VGLUT1 in the cerebral neocortex. Arch Ital Biol 143:127-132.
15. Danik M, Cassoly E, Manseau F, Sotty F, Mouginot D, Williams S. 2005. Frequent coexpression of the vesicular glutamate transporter 1 and 2 genes, as well as coexpression with genes for choline acetyltransferase or glutamic acid decarboxylase in neurons of rat brain. J Neurosci Res 81:506-521.
16. De Gois S, Schafer MK, Defamie N, Chen C, Ricci A, Weihe E, Varoqui H, Erickson JD. 2005. Homeostatic scaling of vesicular glutamate and GABA transporter expression in rat neocortical circuits. J Neurosci 25:7121-7133.
17. Dyer CA, Hickey WF, Geisert EE Jr. 1991. Myelin/oligodendrocyte-specific protein: a novel surface membrane protein that associates with microtubules. J Neurosci Res 28:607-613.
18. 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.
19. 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.
20. 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.
21. 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.
22. Fujiyama F, Hioki H, Tomioka R, Taki K, Tamamaki N, Nomura S, Okamoto K, Kaneko T. 2003. Changes of immunocytochemical localization of vesicular glutamate transporters in the rat visual system after the retinofugal denervation 1. J Comp Neurol 465:234-249.
23. Fujiyama F, Kuramoto E, Okamoto K, Hioki H, Furuta T, Zhou L, Nomura S, Kaneko T. 2004. Presynaptic localization of an AMPA-type glutamate receptor in corticostriatal and thalamostriatal axon terminals. Eur J Neurosci 20:3322-3330.
24. Fyk-Kolodziej B, Dzhagaryan A, Qin P, Pourcho RG. 2004. Immunocytochemical localization of three vesicular glutamate transporters in the cat retina. J Comp Neurol 475:518-530.
25. Gargini C, Terzibasi E, Mazzoni F, Strettoi E. 2007. Retinal organization in the retinal degeneration 10 (rd10) mutant mouse: a morphological and ERG study. J Comp Neurol 500:222-238.
26. Gilmor ML, Nash NR, Roghani A, Edwards RH, Yi H, Hersch SM, Levey AI. 1996. Expression of the putative vesicular acetylcholine transporter in rat brain and localization in cholinergic synaptic vesicles. J Neurosci 16:2179-2190.
27. Golshani P, Liu XB, Jones EG. 2001. Differences in quantal amplitude reflect GluR4- subunit number at corticothalamic synapses on two populations of thalamic neurons. Proc Natl Acad Sci U S A 98:4172-4177.
28. Graybiel AM, Ragsdale CW Jr. 1979. Fiber connections of the basal ganglia. Prog Brain Res 51:237-283.
29. Graziano A, Jones EG. 2004. Widespread thalamic terminations of fibers arising in the superficial medullary dorsal horn of monkeys and their relation to calbindin immunoreactivity. J Neurosci 24:248-256.
30. Groome N, Dawkes A, Barry R, Hruby R, Alvord E. 1988. New monoclonal antibodies reactive with defined sequential epitopes in human myelin basic protein. J Neuroimmunol 19:305-315.
31. Hartig W, Riedel A, Grosche J, Edwards RH, Fremeau RT Jr, Harkany T, Brauer K, Arendt T. 2003. Complementary distribution of vesicular glutamate transporters 1 and 2 in the nucleus accumbens of rat: relationship to calretinin-containing extrinsic innervation and calbindin-immunoreactive neurons. J Comp Neurol 465:1-10.
32. Helmchen F, Borst JG, Sakmann B. 1997. Calcium dynamics associated with a single action potential in a CNS presynaptic terminal. Biophys J 72:1458-1471.
33. 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.
34. 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.
35. 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.
36. +-dependent inorganic phosphate cotransporter (DNPI) in the rat forebrain. Brain Res Mol Brain Res 83:34-43.
37. 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. Brain Res Mol Brain Res 107:23-31.
38. Hoogland PV, Welker E, Van der Loos H. 1987. Organization of the projections from barrel cortex to thalamus in mice studied with Phaseolus vulgaris-leucoagglutinin and HRP. Exp Brain Res 68:73-87.
39. Hur EE, Zaborszky L. 2005. VGluT2 afferents to the medial prefrontal and primary somatosensory cortices: a combined retrograde tracing in situ hybridization. J Comp Neurol 483:351-373.
40. Jones EG. 1975. Some aspects of the organization of the thalamic reticular complex. J Comp Neurol 162:285-308.
41. Jones EG. 1998. Viewpoint: the core and matrix of thalamic organization. Neuroscience 85:331-345.
42. Jones EG. 2007. The thalamus, 2nd ed. Cambridge, UK: Cambridge University Press.
43. Kaneko T, Mizuno N. 1988. Immunohistochemical study of glutaminase-containing neurons in the cerebral cortex and thalamus of the rat. J Comp Neurol 267:590-602.
44. 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.
45. Katz B, Miledi R. 1968. The role of calcium in neuromuscular facilitation. J Physiol 195:481-492.
46. Land PW, Kyonka E, Shamalla-Hannah L. 2004. Vesicular glutamate transporters in the lateral geniculate nucleus: expression of VGLUT2 by retinal terminals. Brain Res 996:251-254.
47. 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 468:380-394.
48. Lavoie B, Parent A. 1994. Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J Comp Neurol 344:190-209.
49. Levine JM, Stallcup WB. 1987. Plasticity of developing cerebellar cells in vitro studied with antibodies against the NG2 antigen. J Neurosci 7:2721-2731.
50. Levine JM, Stincone F, Lee YS. 1993. Development and differentiation of glial precursor cells in the rat cerebellum. Glia 7:307-321.
51. Li JL, Fujiyama F, Kaneko T, Mizuno N. 2003a. Expression of vesicular glutamate transporters, VGluT1 and VGluT2, in axon terminals of nociceptive primary afferent fibers in the superficial layers of the medullary and spinal dorsal horns of the rat 13. J Comp Neurol 457:236-249.
52. Li JL, Xiong KH, Dong YL, Fujiyama F, Kaneko T, Mizuno N. 2003b. Vesicular glutamate transporters, VGluT1 and VGluT2, in the trigeminal ganglion neurons of the rat, with special reference to coexpression. J Comp Neurol 463:212-220.
53. 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.
54. Lindström S, Wróbel A. 1990. Frequency dependent corticofugal excitation of principal cells in the cat's dorsal lateral geniculate nucleus. Exp Brain Res 79:313-318.
55. Liu XB, Honda CN, Jones EG. 1995. Distribution of four types of synapse on physiologically identified relay neurons in the ventral posterior thalamic nucleus of the cat. J Comp Neurol 352:69-91.
56. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA. 1992. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 103:857-862.
57. Melone M, Burette A, Weinberg RJ. 2005. Light microscopic identification and immunocytochemical characterization of glutamatergic synapses in brain sections. J Comp Neurol 492:495-509.
58. Miyazaki T, Fukaya M, Shimizu H, Watanabe M. 2003. Subtype switching of vesicular glutamate transporters at parallel fibre-Purkinje cell synapses in developing mouse cerebellum. Eur J Neurosci 17:2563-2572.
59. Moechars D, Weston MC, Leo S, Callaerts-Vegh Z, Goris I, Daneels G, Buist A, Cik M, van der SP, Kass S, Meert T, D'Hooge R, Rosenmund C, Hampson RM. 2006. Vesicular glutamate transporter VGLUT2 expression levels control quantal size and neuropathic pain. J Neurosci 26:12055-12066.
60. Montana V, Ni Y, Sunjara V, Hua X, Parpura V. 2004. Vesicular glutamate transporter-dependent glutamate release from astrocytes. J Neurosci 24: 2633-2642.
61. Nahmani M, Erişir A. 2005. VGluT2 immunochemistry identifies thalamocortical terminals in layer 4 of adult and developing visual cortex. J Comp Neurol 484:458-473.
62. 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 492:263-288.
63. Ni B, Rosteck PR, Jr., Nadi NS, Paul SM. 1994. Cloning and expression of a cDNA encoding a brain-specific Na(+)-dependent inorganic phosphate cotransporter. Proc Natl Acad Sci U S A 91:5607-5611.
64. Ojima H. 1994. Terminal morphology and distribution of corticothalamic fibers originating from layers 5 and 6 of cat primary auditory cortex. Cereb Cortex 4:646-663.
65. 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 50:117-129.
66. Persson S, Boulland JL, Aspling M, Larsson M, Fremeau RT Jr, Edwards RH, Storm-Mathisen J, Chaudhry FA, Broman J. 2006. Distribution of vesicular glutamate transporters 1 and 2 in the rat spinal cord, with a note on the spinocervical tract. J Comp Neurol 497:683-701.
67. Raju DV, Shah DJ, Wright TM, Hall RA, Smith Y. 2006. Differential synaptology of vGluT2-containing thalamostriatal afferents between the patch and matrix compartments in rats. J Comp Neurol 499:231-243.
68. Regehr WG, Atluri PP. 1995. Calcium transients in cerebellar granule cell presynaptic terminals. Biophys J 68:2156-2170.
69. Regher WG, Stevens CF. 2001. Physiology of synaptic transmission and short-term plasticity. In Südhof TC, Stevens CF, editors. Synapses. Baltimore, MD: The Johns Hopkins University Press.
70. Ridler T, Calvard S. 1978. Picture thresholding using an iterative selection method. IEEE Trans Systems Man Cybernet 8:629-632.
71. 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.
72. Steriade M. 2000. Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101:243-276.
73. Steriade M, Paré D, Parent A, Smith Y. 1988. Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey. Neuroscience 25:47-67.
74. Takamori S, Rhee JS, Rosenmund C, Jahn R. 2001. Identification of differentiation-associated brain-specific phosphate transporter as a second vesicular glutamate transporter (VGluT2). J Neurosci 21: RC182.
75. Todd AJ, Hughes DI, Polgar 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 17:13-27.
76. Van Horn SC, Erişir A, Sherman SM. 2000. Relative distribution of synapses in the A-laminae of the lateral geniculate nucleus of the cat. J Comp Neurol 416:509-520.
77. Varoqui H, Schafer 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 22:142-155.
78. von Krosigk M, Monckton JE, Reiner PB, McCormick DA. 1999. Dynamic properties of corticothalamic excitatory postsynaptic potentials and thalamic reticular inhibitory postsynaptic potentials in thalamocortical neurons of the guinea-pig dorsal lateral geniculate nucleus. Neuroscience 91:7-20.
79. Wässle H, Regus-Leidig H, Haverkamp S. 2006. Expression of the vesicular glutamate transporter vGluT2 in a subset of cones of the mouse retina. J Comp Neurol 496:544-555.
80. Willis WD, Zhang X, Honda CN, Giesler GJ. 2001. Projections from the marginal zone and deep dorsal horn to the ventrobasal nuclei of the primate thalamus. Pain 92:267-276.
81. Wilson NR, Kang J, Hueske EV, Leung T, Varoqui H, Murnick JG, Erickson JD, Liu G. 2005. Presynaptic regulation of quantal size by the vesicular glutamate transporter VGLUT1. J Neurosci 25:6221-6234.
82. Wojcik SM, Rhee JS, Herzog E, Sigler A, Jahn R, Takamori S, Brose N, Rosenmund C. 2004. An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size. Proc Natl Acad Sci U S A 101:7158-7163.
83. Yeterian EH, Pandya DN. 1994. Laminar origin of striatal and thalamic projections of the prefrontal cortex in rhesus monkeys. Exp Brain Res 99:383-398.
84. Zhou J, Nannapaneni N, Shore S. 2007. Vesicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus. J Comp Neurol 500:777-787.