Abstract
Glutamate and GABA neurotransmission is mediated through various types of ionotropic and metabotropic receptors. In this review, we summarise some of our recent findings on the subcellular and subsynaptic localisation of GABAB and group I metabotropic glutamate receptors in the striatopallidal complex of monkeys. Polyclonal antibodies that specifically recognise GABABR1, mGluR1a and mGluR5 receptor subtypes were used for immunoperoxidase and pre-embedding immunogold techniques at the light and electron microscope levels. Both subtypes of group I mGluRs were expressed postsynaptically in striatal projection neurons and interneurons where they aggregate perisynaptically at asymmetric glutamatergic synapses and symmetric dopaminergic synaptic junctions. Moreover, they are also strongly expressed in the main body of symmetric synapses established by putative intrastriatal GABAergic terminals. In the globus pallidus, both receptor subtypes are found postsynaptically in the core of striatopallidal GABAergic synapses and perisynaptically at subthalamopallidal glutamatergic synapses. Finally, extrasynaptic labelling was commonly seen in the globus pallidus and the striatum.
Moderate to intense GABABR1 immunoreactivity was observed in the striatopallidal complex. At the electron microscope level, GABABR1 immunostaining was commonly found in neuronal cell bodies and dendrites. Many striatal dendritic spines also displayed GABABR1 immunoreactivity. Moreover, GABABR1-immunoreactive axons and axon terminals were frequently encountered. In the striatum, GABABR1-immunoreactive boutons resembled terminals of cortical origin, while in the globus pallidus, subthalamic-like terminals were labelled. Pre-embedding immunogold data showed that postsynaptic GABABR1 receptors are concentrated at extrasynaptic sites on dendrites, spines and somata in the striatopallidal complex, perisynaptically at asymmetric synapses and in the main body of symmetric striatopallidal synapses in the GPe and GPi. Consistent with the immunoperoxidase data, immunoparticles were found in the presynaptic grid of asymmetric synapses established by cortical- and subthalamic-like glutamatergic terminals.
These findings indicate that both GABA and glutamate metabotropic receptors are located to subserve various modulatory functions of the synaptic transmission in the primate striatopallidal complex. Furthermore, their pattern of localisation raises issues about their roles and mechanisms of activation in normal and pathological conditions. Because of their ‘modulatory’ functions, these receptors are ideal targets for chronic drug therapies in neurodegenerative diseases such as Parkinson's disease.
Keywords: Striatum, globus pallidus, subthalamic nucleus, corticostriatal projections, primates
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- Albin R. L., Makowiec R. L., Hollingsworth Z. R., Dure L. S., 4th, Penney J. B., Young A. B. Excitatory amino acid binding sites in the basal ganglia of the rat: a quantitative autoradiographic study. Neuroscience. 1992;46(1):35–48. doi: 10.1016/0306-4522(92)90006-n. [DOI] [PubMed] [Google Scholar]
- Albin R. L., Young A. B., Penney J. B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989 Oct;12(10):366–375. doi: 10.1016/0166-2236(89)90074-x. [DOI] [PubMed] [Google Scholar]
- Alexander G. E., Crutcher M. D. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 1990 Jul;13(7):266–271. doi: 10.1016/0166-2236(90)90107-l. [DOI] [PubMed] [Google Scholar]
- Araque A., Parpura V., Sanzgiri R. P., Haydon P. G. Tripartite synapses: glia, the unacknowledged partner. Trends Neurosci. 1999 May;22(5):208–215. doi: 10.1016/s0166-2236(98)01349-6. [DOI] [PubMed] [Google Scholar]
- Arias Montaño J. A., Martínez-Fong D., Aceves J. GABAB receptor activation partially inhibits N-methyl-D-aspartate-mediated tyrosine hydroxylase stimulation in rat striatal slices. Eur J Pharmacol. 1992 Aug 6;218(2-3):335–338. doi: 10.1016/0014-2999(92)90187-9. [DOI] [PubMed] [Google Scholar]
- Arluison M., Dietl M., Thibault J. Ultrastructural morphology of dopaminergic nerve terminals and synapses in the striatum of the rat using tyrosine hydroxylase immunocytochemistry: a topographical study. Brain Res Bull. 1984 Aug;13(2):269–285. doi: 10.1016/0361-9230(84)90128-x. [DOI] [PubMed] [Google Scholar]
- Asztely F., Erdemli G., Kullmann D. M. Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron. 1997 Feb;18(2):281–293. doi: 10.1016/s0896-6273(00)80268-8. [DOI] [PubMed] [Google Scholar]
- Attwell D., Barbour B., Szatkowski M. Nonvesicular release of neurotransmitter. Neuron. 1993 Sep;11(3):401–407. doi: 10.1016/0896-6273(93)90145-h. [DOI] [PubMed] [Google Scholar]
- Barbour B., Häusser M. Intersynaptic diffusion of neurotransmitter. Trends Neurosci. 1997 Sep;20(9):377–384. doi: 10.1016/s0166-2236(96)20050-5. [DOI] [PubMed] [Google Scholar]
- Baude A., Nusser Z., Roberts J. D., Mulvihill E., McIlhinney R. A., Somogyi P. The metabotropic glutamate receptor (mGluR1 alpha) is concentrated at perisynaptic membrane of neuronal subpopulations as detected by immunogold reaction. Neuron. 1993 Oct;11(4):771–787. doi: 10.1016/0896-6273(93)90086-7. [DOI] [PubMed] [Google Scholar]
- Bergles D. E., Diamond J. S., Jahr C. E. Clearance of glutamate inside the synapse and beyond. Curr Opin Neurobiol. 1999 Jun;9(3):293–298. doi: 10.1016/s0959-4388(99)80043-9. [DOI] [PubMed] [Google Scholar]
- Bergman H., Wichmann T., DeLong M. R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science. 1990 Sep 21;249(4975):1436–1438. doi: 10.1126/science.2402638. [DOI] [PubMed] [Google Scholar]
- Bernard V., Bolam J. P. Subcellular and subsynaptic distribution of the NR1 subunit of the NMDA receptor in the neostriatum and globus pallidus of the rat: co-localization at synapses with the GluR2/3 subunit of the AMPA receptor. Eur J Neurosci. 1998 Dec;10(12):3721–3736. doi: 10.1046/j.1460-9568.1998.00380.x. [DOI] [PubMed] [Google Scholar]
- Bernard V., Somogyi P., Bolam J. P. Cellular, subcellular, and subsynaptic distribution of AMPA-type glutamate receptor subunits in the neostriatum of the rat. J Neurosci. 1997 Jan 15;17(2):819–833. doi: 10.1523/JNEUROSCI.17-02-00819.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Berthele A., Laurie D. J., Platzer S., Zieglgänsberger W., Tölle T. R., Sommer B. Differential expression of rat and human type I metabotropic glutamate receptor splice variant messenger RNAs. Neuroscience. 1998 Aug;85(3):733–749. doi: 10.1016/s0306-4522(97)00670-2. [DOI] [PubMed] [Google Scholar]
- Bettler B., Kaupmann K., Bowery N. GABAB receptors: drugs meet clones. Curr Opin Neurobiol. 1998 Jun;8(3):345–350. doi: 10.1016/s0959-4388(98)80059-7. [DOI] [PubMed] [Google Scholar]
- Blandini F., Porter R. H., Greenamyre J. T. Glutamate and Parkinson's disease. Mol Neurobiol. 1996 Feb;12(1):73–94. doi: 10.1007/BF02740748. [DOI] [PubMed] [Google Scholar]
- Bolam J. P., Powell J. F., Wu J. Y., Smith A. D. Glutamate decarboxylase-immunoreactive structures in the rat neostriatum: a correlated light and electron microscopic study including a combination of Golgi impregnation with immunocytochemistry. J Comp Neurol. 1985 Jul 1;237(1):1–20. doi: 10.1002/cne.902370102. [DOI] [PubMed] [Google Scholar]
- Bonanno G., Fassio A., Sala R., Schmid G., Raiteri M. GABA(B) receptors as potential targets for drugs able to prevent excessive excitatory amino acid transmission in the spinal cord. Eur J Pharmacol. 1998 Dec 4;362(2-3):143–148. doi: 10.1016/s0014-2999(98)00759-6. [DOI] [PubMed] [Google Scholar]
- Bonci A., Grillner P., Siniscalchi A., Mercuri N. B., Bernardi G. Glutamate metabotropic receptor agonists depress excitatory and inhibitory transmission on rat mesencephalic principal neurons. Eur J Neurosci. 1997 Nov;9(11):2359–2369. doi: 10.1111/j.1460-9568.1997.tb01653.x. [DOI] [PubMed] [Google Scholar]
- Bormann J. Electrophysiology of GABAA and GABAB receptor subtypes. Trends Neurosci. 1988 Mar;11(3):112–116. doi: 10.1016/0166-2236(88)90156-7. [DOI] [PubMed] [Google Scholar]
- Bowery N. G., Hill D. R., Hudson A. L., Doble A., Middlemiss D. N., Shaw J., Turnbull M. (-)Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature. 1980 Jan 3;283(5742):92–94. doi: 10.1038/283092a0. [DOI] [PubMed] [Google Scholar]
- Bowery N. G., Hudson A. L., Price G. W. GABAA and GABAB receptor site distribution in the rat central nervous system. Neuroscience. 1987 Feb;20(2):365–383. doi: 10.1016/0306-4522(87)90098-4. [DOI] [PubMed] [Google Scholar]
- Bowery N. G., Price G. W., Hudson A. L., Hill D. R., Wilkin G. P., Turnbull M. J. GABA receptor multiplicity. Visualization of different receptor types in the mammalian CNS. Neuropharmacology. 1984 Feb;23(2B):219–231. doi: 10.1016/0028-3908(84)90063-7. [DOI] [PubMed] [Google Scholar]
- Bradley S. R., Standaert D. G., Rhodes K. J., Rees H. D., Testa C. M., Levey A. I., Conn P. J. Immunohistochemical localization of subtype 4a metabotropic glutamate receptors in the rat and mouse basal ganglia. J Comp Neurol. 1999 Apr 28;407(1):33–46. [PubMed] [Google Scholar]
- Calabresi P., Mercuri N. B., De Murtas M., Bernardi G. Endogenous GABA mediates presynaptic inhibition of spontaneous and evoked excitatory synaptic potentials in the rat neostriatum. Neurosci Lett. 1990 Oct 2;118(1):99–102. doi: 10.1016/0304-3940(90)90258-b. [DOI] [PubMed] [Google Scholar]
- Calabresi P., Mercuri N. B., De Murtas M., Bernardi G. Involvement of GABA systems in feedback regulation of glutamate-and GABA-mediated synaptic potentials in rat neostriatum. J Physiol. 1991;440:581–599. doi: 10.1113/jphysiol.1991.sp018726. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Calabresi P., Pisani A., Mercuri N. B., Bernardi G. Heterogeneity of metabotropic glutamate receptors in the striatum: electrophysiological evidence. Eur J Neurosci. 1993 Oct 1;5(10):1370–1377. doi: 10.1111/j.1460-9568.1993.tb00923.x. [DOI] [PubMed] [Google Scholar]
- Calabresi P., Pisani A., Mercuri N. B., Bernardi G. The corticostriatal projection: from synaptic plasticity to dysfunctions of the basal ganglia. Trends Neurosci. 1996 Jan;19(1):19–24. doi: 10.1016/0166-2236(96)81862-5. [DOI] [PubMed] [Google Scholar]
- Carmignoto G., Pasti L., Pozzan T. On the role of voltage-dependent calcium channels in calcium signaling of astrocytes in situ. J Neurosci. 1998 Jun 15;18(12):4637–4645. doi: 10.1523/JNEUROSCI.18-12-04637.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Castelli M. P., Ingianni A., Stefanini E., Gessa G. L. Distribution of GABA(B) receptor mRNAs in the rat brain and peripheral organs. Life Sci. 1999;64(15):1321–1328. doi: 10.1016/s0024-3205(99)00067-3. [DOI] [PubMed] [Google Scholar]
- Charara A., Heilman T. C., Levey A. I., Smith Y. Pre- and postsynaptic localization of GABA(B) receptors in the basal ganglia in monkeys. Neuroscience. 2000;95(1):127–140. doi: 10.1016/s0306-4522(99)00409-1. [DOI] [PubMed] [Google Scholar]
- Chesselet M. F., Delfs J. M. Basal ganglia and movement disorders: an update. Trends Neurosci. 1996 Oct;19(10):417–422. doi: 10.1016/0166-2236(96)10052-7. [DOI] [PubMed] [Google Scholar]
- Chevalier G., Deniau J. M. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci. 1990 Jul;13(7):277–280. doi: 10.1016/0166-2236(90)90109-n. [DOI] [PubMed] [Google Scholar]
- Chu D. C., Albin R. L., Young A. B., Penney J. B. Distribution and kinetics of GABAB binding sites in rat central nervous system: a quantitative autoradiographic study. Neuroscience. 1990;34(2):341–357. doi: 10.1016/0306-4522(90)90144-s. [DOI] [PubMed] [Google Scholar]
- Clarke N. P., Bolam J. P., Bevan M. D. Glutamate-enriched inputs from the mesopontine tegmentum to the entopeduncular nucleus in the rat. Eur J Neurosci. 1996 Jul;8(7):1363–1376. doi: 10.1111/j.1460-9568.1996.tb01599.x. [DOI] [PubMed] [Google Scholar]
- Clarke N. P., Bolam J. P. Distribution of glutamate receptor subunits at neurochemically characterized synapses in the entopeduncular nucleus and subthalamic nucleus of the rat. J Comp Neurol. 1998 Aug 3;397(3):403–420. [PubMed] [Google Scholar]
- Conn P. J., Pin J. P. Pharmacology and functions of metabotropic glutamate receptors. Annu Rev Pharmacol Toxicol. 1997;37:205–237. doi: 10.1146/annurev.pharmtox.37.1.205. [DOI] [PubMed] [Google Scholar]
- Davies J. Selective depression of synaptic excitation in cat spinal neurones by baclofen: an iontophoretic study. Br J Pharmacol. 1981 Feb;72(2):373–384. doi: 10.1111/j.1476-5381.1981.tb09137.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- DeLong M. R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990 Jul;13(7):281–285. doi: 10.1016/0166-2236(90)90110-v. [DOI] [PubMed] [Google Scholar]
- Diamond J. S., Jahr C. E. Transporters buffer synaptically released glutamate on a submillisecond time scale. J Neurosci. 1997 Jun 15;17(12):4672–4687. doi: 10.1523/JNEUROSCI.17-12-04672.1997. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dubinsky J. M. Development of inhibitory synapses among striatal neurons in vitro. J Neurosci. 1989 Nov;9(11):3955–3965. doi: 10.1523/JNEUROSCI.09-11-03955.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dubé L., Smith A. D., Bolam J. P. Identification of synaptic terminals of thalamic or cortical origin in contact with distinct medium-size spiny neurons in the rat neostriatum. J Comp Neurol. 1988 Jan 22;267(4):455–471. doi: 10.1002/cne.902670402. [DOI] [PubMed] [Google Scholar]
- Dzubay J. A., Jahr C. E. The concentration of synaptically released glutamate outside of the climbing fiber-Purkinje cell synaptic cleft. J Neurosci. 1999 Jul 1;19(13):5265–5274. doi: 10.1523/JNEUROSCI.19-13-05265.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fiorillo C. D., Williams J. T. Glutamate mediates an inhibitory postsynaptic potential in dopamine neurons. Nature. 1998 Jul 2;394(6688):78–82. doi: 10.1038/27919. [DOI] [PubMed] [Google Scholar]
- Fox S., Krnjević K., Morris M. E., Puil E., Werman R. Action of baclofen on mammalian synaptic transmission. Neuroscience. 1978;3(6):495–515. doi: 10.1016/0306-4522(78)90016-7. [DOI] [PubMed] [Google Scholar]
- Freund T. F., Powell J. F., Smith A. D. Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience. 1984 Dec;13(4):1189–1215. doi: 10.1016/0306-4522(84)90294-x. [DOI] [PubMed] [Google Scholar]
- Fritschy J. M., Meskenaite V., Weinmann O., Honer M., Benke D., Mohler H. GABAB-receptor splice variants GB1a and GB1b in rat brain: developmental regulation, cellular distribution and extrasynaptic localization. Eur J Neurosci. 1999 Mar;11(3):761–768. doi: 10.1046/j.1460-9568.1999.00481.x. [DOI] [PubMed] [Google Scholar]
- Gehlert D. R., Yamamura H. I., Wamsley J. K. gamma-Aminobutyric acidB receptors in the rat brain: quantitative autoradiographic localization using [3H](-)-baclofen. Neurosci Lett. 1985 May 14;56(2):183–188. doi: 10.1016/0304-3940(85)90126-0. [DOI] [PubMed] [Google Scholar]
- Gereau R. W., 4th, Conn P. J. Multiple presynaptic metabotropic glutamate receptors modulate excitatory and inhibitory synaptic transmission in hippocampal area CA1. J Neurosci. 1995 Oct;15(10):6879–6889. doi: 10.1523/JNEUROSCI.15-10-06879.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gerfen C. R., Engber T. M., Mahan L. C., Susel Z., Chase T. N., Monsma F. J., Jr, Sibley D. R. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science. 1990 Dec 7;250(4986):1429–1432. doi: 10.1126/science.2147780. [DOI] [PubMed] [Google Scholar]
- Gerfen C. R. The neostriatal mosaic: multiple levels of compartmental organization in the basal ganglia. Annu Rev Neurosci. 1992;15:285–320. doi: 10.1146/annurev.ne.15.030192.001441. [DOI] [PubMed] [Google Scholar]
- Glaum S. R., Miller R. J. Activation of metabotropic glutamate receptors produces reciprocal regulation of ionotropic glutamate and GABA responses in the nucleus of the tractus solitarius of the rat. J Neurosci. 1993 Apr;13(4):1636–1641. doi: 10.1523/JNEUROSCI.13-04-01636.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Greenamyre J. T., O'Brien C. F. N-methyl-D-aspartate antagonists in the treatment of Parkinson's disease. Arch Neurol. 1991 Sep;48(9):977–981. doi: 10.1001/archneur.1991.00530210109030. [DOI] [PubMed] [Google Scholar]
- Hanson J. E., Smith Y. Group I metabotropic glutamate receptors at GABAergic synapses in monkeys. J Neurosci. 1999 Aug 1;19(15):6488–6496. doi: 10.1523/JNEUROSCI.19-15-06488.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hashimoto T., Kuriyama K. In vivo evidence that GABA(B) receptors are negatively coupled to adenylate cyclase in rat striatum. J Neurochem. 1997 Jul;69(1):365–370. doi: 10.1046/j.1471-4159.1997.69010365.x. [DOI] [PubMed] [Google Scholar]
- Hazrati L. N., Parent A., Mitchell S., Haber S. N. Evidence for interconnections between the two segments of the globus pallidus in primates: a PHA-L anterograde tracing study. Brain Res. 1990 Nov 12;533(1):171–175. doi: 10.1016/0006-8993(90)91813-v. [DOI] [PubMed] [Google Scholar]
- Hazrati L. N., Parent A. The striatopallidal projection displays a high degree of anatomical specificity in the primate. Brain Res. 1992 Oct 2;592(1-2):213–227. doi: 10.1016/0006-8993(92)91679-9. [DOI] [PubMed] [Google Scholar]
- Hill D. R., Bowery N. G. 3H-baclofen and 3H-GABA bind to bicuculline-insensitive GABA B sites in rat brain. Nature. 1981 Mar 12;290(5802):149–152. doi: 10.1038/290149a0. [DOI] [PubMed] [Google Scholar]
- Hill D. R. GABAB receptor modulation of adenylate cyclase activity in rat brain slices. Br J Pharmacol. 1985 Jan;84(1):249–257. [PMC free article] [PubMed] [Google Scholar]
- Houamed K. M., Kuijper J. L., Gilbert T. L., Haldeman B. A., O'Hara P. J., Mulvihill E. R., Almers W., Hagen F. S. Cloning, expression, and gene structure of a G protein-coupled glutamate receptor from rat brain. Science. 1991 May 31;252(5010):1318–1321. doi: 10.1126/science.1656524. [DOI] [PubMed] [Google Scholar]
- Ikarashi Y., Yuzurihara M., Takahashi A., Hirohisa Ishimaru, Shiobara T., Maruyama Y. Modulation of acetylcholine release via GABAA and GABAB receptors in rat striatum. Brain Res. 1999 Jan 16;816(1):238–240. doi: 10.1016/s0006-8993(98)01163-9. [DOI] [PubMed] [Google Scholar]
- Isaacson J. S., Solís J. M., Nicoll R. A. Local and diffuse synaptic actions of GABA in the hippocampus. Neuron. 1993 Feb;10(2):165–175. doi: 10.1016/0896-6273(93)90308-e. [DOI] [PubMed] [Google Scholar]
- Jo Y. H., Schlichter R. Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat Neurosci. 1999 Mar;2(3):241–245. doi: 10.1038/6344. [DOI] [PubMed] [Google Scholar]
- Jonas P., Bischofberger J., Sandkühler J. Corelease of two fast neurotransmitters at a central synapse. Science. 1998 Jul 17;281(5375):419–424. doi: 10.1126/science.281.5375.419. [DOI] [PubMed] [Google Scholar]
- Jones K. A., Borowsky B., Tamm J. A., Craig D. A., Durkin M. M., Dai M., Yao W. J., Johnson M., Gunwaldsen C., Huang L. Y. GABA(B) receptors function as a heteromeric assembly of the subunits GABA(B)R1 and GABA(B)R2. Nature. 1998 Dec 17;396(6712):674–679. doi: 10.1038/25348. [DOI] [PubMed] [Google Scholar]
- Karbon E. W., Enna S. J. Characterization of the relationship between gamma-aminobutyric acid B agonists and transmitter-coupled cyclic nucleotide-generating systems in rat brain. Mol Pharmacol. 1985 Jan;27(1):53–59. [PubMed] [Google Scholar]
- Kaupmann K., Huggel K., Heid J., Flor P. J., Bischoff S., Mickel S. J., McMaster G., Angst C., Bittiger H., Froestl W. Expression cloning of GABA(B) receptors uncovers similarity to metabotropic glutamate receptors. Nature. 1997 Mar 20;386(6622):239–246. doi: 10.1038/386239a0. [DOI] [PubMed] [Google Scholar]
- Kaupmann K., Malitschek B., Schuler V., Heid J., Froestl W., Beck P., Mosbacher J., Bischoff S., Kulik A., Shigemoto R. GABA(B)-receptor subtypes assemble into functional heteromeric complexes. Nature. 1998 Dec 17;396(6712):683–687. doi: 10.1038/25360. [DOI] [PubMed] [Google Scholar]
- Kawaguchi Y., Wilson C. J., Emson P. C. Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J Neurosci. 1990 Oct;10(10):3421–3438. doi: 10.1523/JNEUROSCI.10-10-03421.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kemp J. M., Powell T. P. The cortico-striate projection in the monkey. Brain. 1970;93(3):525–546. doi: 10.1093/brain/93.3.525. [DOI] [PubMed] [Google Scholar]
- Kerner J. A., Standaert D. G., Penney J. B., Jr, Young A. B., Landwehrmeyer G. B. Expression of group one metabotropic glutamate receptor subunit mRNAs in neurochemically identified neurons in the rat neostriatum, neocortex, and hippocampus. Brain Res Mol Brain Res. 1997 Sep;48(2):259–269. doi: 10.1016/s0169-328x(97)00102-2. [DOI] [PubMed] [Google Scholar]
- Kerr D. I., Ong J. GABAB receptors. Pharmacol Ther. 1995;67(2):187–246. doi: 10.1016/0163-7258(95)00016-a. [DOI] [PubMed] [Google Scholar]
- Kincaid A. E., Penney J. B., Jr, Young A. B., Newman S. W. Evidence for a projection from the globus pallidus to the entopeduncular nucleus in the rat. Neurosci Lett. 1991 Jul 8;128(1):121–125. doi: 10.1016/0304-3940(91)90774-n. [DOI] [PubMed] [Google Scholar]
- Kinoshita A., Shigemoto R., Ohishi H., van der Putten H., Mizuno N. Immunohistochemical localization of metabotropic glutamate receptors, mGluR7a and mGluR7b, in the central nervous system of the adult rat and mouse: a light and electron microscopic study. J Comp Neurol. 1998 Apr 13;393(3):332–352. [PubMed] [Google Scholar]
- Kinzie J. M., Saugstad J. A., Westbrook G. L., Segerson T. P. Distribution of metabotropic glutamate receptor 7 messenger RNA in the developing and adult rat brain. Neuroscience. 1995 Nov;69(1):167–176. doi: 10.1016/0306-4522(95)00244-d. [DOI] [PubMed] [Google Scholar]
- Kita H. GABAergic circuits of the striatum. Prog Brain Res. 1993;99:51–72. doi: 10.1016/s0079-6123(08)61338-2. [DOI] [PubMed] [Google Scholar]
- Kita H., Kitai S. T. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol. 1987 Jun 15;260(3):435–452. doi: 10.1002/cne.902600309. [DOI] [PubMed] [Google Scholar]
- Kita H., Kitai S. T. Intracellular study of rat globus pallidus neurons: membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res. 1991 Nov 15;564(2):296–305. doi: 10.1016/0006-8993(91)91466-e. [DOI] [PubMed] [Google Scholar]
- Kita H. Responses of globus pallidus neurons to cortical stimulation: intracellular study in the rat. Brain Res. 1992 Aug 28;589(1):84–90. doi: 10.1016/0006-8993(92)91164-a. [DOI] [PubMed] [Google Scholar]
- Kosinski C. M., Standaert D. G., Testa C. M., Penney J. B., Jr, Young A. B. Expression of metabotropic glutamate receptor 1 isoforms in the substantia nigra pars compacta of the rat. Neuroscience. 1998 Oct;86(3):783–798. doi: 10.1016/s0306-4522(97)00654-4. [DOI] [PubMed] [Google Scholar]
- Kullmann D. M., Asztely F. Extrasynaptic glutamate spillover in the hippocampus: evidence and implications. Trends Neurosci. 1998 Jan;21(1):8–14. doi: 10.1016/s0166-2236(97)01150-8. [DOI] [PubMed] [Google Scholar]
- Kullmann D. M., Min M. Y., Asztely F., Rusakov D. A. Extracellular glutamate diffusion determines the occupancy of glutamate receptors at CA1 synapses in the hippocampus. Philos Trans R Soc Lond B Biol Sci. 1999 Feb 28;354(1381):395–402. doi: 10.1098/rstb.1999.0392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kuner R., Köhr G., Grünewald S., Eisenhardt G., Bach A., Kornau H. C. Role of heteromer formation in GABAB receptor function. Science. 1999 Jan 1;283(5398):74–77. doi: 10.1126/science.283.5398.74. [DOI] [PubMed] [Google Scholar]
- Le Moine C., Normand E., Bloch B. Phenotypical characterization of the rat striatal neurons expressing the D1 dopamine receptor gene. Proc Natl Acad Sci U S A. 1991 May 15;88(10):4205–4209. doi: 10.1073/pnas.88.10.4205. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Le Moine C., Normand E., Guitteny A. F., Fouque B., Teoule R., Bloch B. Dopamine receptor gene expression by enkephalin neurons in rat forebrain. Proc Natl Acad Sci U S A. 1990 Jan;87(1):230–234. doi: 10.1073/pnas.87.1.230. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Levine M. S., Hull C. D., Buchwald N. A. Pallidal and entopeduncular intracellular responses to striatal, cortical, thalamic, and sensory inputs. Exp Neurol. 1974 Sep;44(3):448–460. doi: 10.1016/0014-4886(74)90208-8. [DOI] [PubMed] [Google Scholar]
- Levy R., Hazrati L. N., Herrero M. T., Vila M., Hassani O. K., Mouroux M., Ruberg M., Asensi H., Agid Y., Féger J. Re-evaluation of the functional anatomy of the basal ganglia in normal and Parkinsonian states. Neuroscience. 1997 Jan;76(2):335–343. doi: 10.1016/s0306-4522(96)00409-5. [DOI] [PubMed] [Google Scholar]
- Lovinger D. M., McCool B. A. Metabotropic glutamate receptor-mediated presynaptic depression at corticostriatal synapses involves mGLuR2 or 3. J Neurophysiol. 1995 Mar;73(3):1076–1083. doi: 10.1152/jn.1995.73.3.1076. [DOI] [PubMed] [Google Scholar]
- Lovinger D. M. Trans-1-aminocyclopentane-1,3-dicarboxylic acid (t-ACPD) decreases synaptic excitation in rat striatal slices through a presynaptic action. Neurosci Lett. 1991 Aug 5;129(1):17–21. doi: 10.1016/0304-3940(91)90710-b. [DOI] [PubMed] [Google Scholar]
- Lu X. Y., Ghasemzadeh M. B., Kalivas P. W. Regional distribution and cellular localization of gamma-aminobutyric acid subtype 1 receptor mRNA in the rat brain. J Comp Neurol. 1999 May 3;407(2):166–182. doi: 10.1002/(sici)1096-9861(19990503)407:2<166::aid-cne2>3.0.co;2-j. [DOI] [PubMed] [Google Scholar]
- Lujan R., Nusser Z., Roberts J. D., Shigemoto R., Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur J Neurosci. 1996 Jul;8(7):1488–1500. doi: 10.1111/j.1460-9568.1996.tb01611.x. [DOI] [PubMed] [Google Scholar]
- Makoff A. Molecular cloning of human GABABR1 and its tissue distribution. Brain Res Mol Brain Res. 1999 Jan 22;64(1):137–140. doi: 10.1016/s0169-328x(98)00316-7. [DOI] [PubMed] [Google Scholar]
- Manzoni O., Bockaert J. Metabotropic glutamate receptors inhibiting excitatory synapses in the CA1 area of rat hippocampus. Eur J Neurosci. 1995 Dec 1;7(12):2518–2523. doi: 10.1111/j.1460-9568.1995.tb01051.x. [DOI] [PubMed] [Google Scholar]
- Margeta-Mitrovic M., Mitrovic I., Riley R. C., Jan L. Y., Basbaum A. I. Immunohistochemical localization of GABA(B) receptors in the rat central nervous system. J Comp Neurol. 1999 Mar 15;405(3):299–321. doi: 10.1002/(sici)1096-9861(19990315)405:3<299::aid-cne2>3.0.co;2-6. [DOI] [PubMed] [Google Scholar]
- Martin L. J., Blackstone C. D., Huganir R. L., Price D. L. Cellular localization of a metabotropic glutamate receptor in rat brain. Neuron. 1992 Aug;9(2):259–270. doi: 10.1016/0896-6273(92)90165-a. [DOI] [PubMed] [Google Scholar]
- Masu M., Tanabe Y., Tsuchida K., Shigemoto R., Nakanishi S. Sequence and expression of a metabotropic glutamate receptor. Nature. 1991 Feb 28;349(6312):760–765. doi: 10.1038/349760a0. [DOI] [PubMed] [Google Scholar]
- Misgeld U., Bijak M., Jarolimek W. A physiological role for GABAB receptors and the effects of baclofen in the mammalian central nervous system. Prog Neurobiol. 1995 Jul;46(4):423–462. doi: 10.1016/0301-0082(95)00012-k. [DOI] [PubMed] [Google Scholar]
- Moratalla R., Bowery N. G. Chronic lesion of corticostriatal fibers reduces GABAB but not GABAA binding in rat caudate putamen: an autoradiographic study. Neurochem Res. 1991 Mar;16(3):309–315. doi: 10.1007/BF00966094. [DOI] [PubMed] [Google Scholar]
- Morishita W., Kirov S. A., Alger B. E. Evidence for metabotropic glutamate receptor activation in the induction of depolarization-induced suppression of inhibition in hippocampal CA1. J Neurosci. 1998 Jul 1;18(13):4870–4882. doi: 10.1523/JNEUROSCI.18-13-04870.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Muñoz A., Huntsman M. M., Jones E. G. GABA(B) receptor gene expression in monkey thalamus. J Comp Neurol. 1998 Apr 27;394(1):118–126. doi: 10.1002/(sici)1096-9861(19980427)394:1<118::aid-cne9>3.0.co;2-3. [DOI] [PubMed] [Google Scholar]
- Nakanishi S. Metabotropic glutamate receptors: synaptic transmission, modulation, and plasticity. Neuron. 1994 Nov;13(5):1031–1037. doi: 10.1016/0896-6273(94)90043-4. [DOI] [PubMed] [Google Scholar]
- Ng G. Y., Clark J., Coulombe N., Ethier N., Hebert T. E., Sullivan R., Kargman S., Chateauneuf A., Tsukamoto N., McDonald T. Identification of a GABAB receptor subunit, gb2, required for functional GABAB receptor activity. J Biol Chem. 1999 Mar 19;274(12):7607–7610. doi: 10.1074/jbc.274.12.7607. [DOI] [PubMed] [Google Scholar]
- Nicoletti F., Meek J. L., Iadarola M. J., Chuang D. M., Roth B. L., Costa E. Coupling of inositol phospholipid metabolism with excitatory amino acid recognition sites in rat hippocampus. J Neurochem. 1986 Jan;46(1):40–46. doi: 10.1111/j.1471-4159.1986.tb12922.x. [DOI] [PubMed] [Google Scholar]
- Nicoletti F., Wroblewski J. T., Novelli A., Alho H., Guidotti A., Costa E. The activation of inositol phospholipid metabolism as a signal-transducing system for excitatory amino acids in primary cultures of cerebellar granule cells. J Neurosci. 1986 Jul;6(7):1905–1911. doi: 10.1523/JNEUROSCI.06-07-01905.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nisenbaum E. S., Berger T. W., Grace A. A. Depression of glutamatergic and GABAergic synaptic responses in striatal spiny neurons by stimulation of presynaptic GABAB receptors. Synapse. 1993 Jul;14(3):221–242. doi: 10.1002/syn.890140306. [DOI] [PubMed] [Google Scholar]
- Nisenbaum E. S., Berger T. W., Grace A. A. Presynaptic modulation by GABAB receptors of glutamatergic excitation and GABAergic inhibition of neostriatal neurons. J Neurophysiol. 1992 Feb;67(2):477–481. doi: 10.1152/jn.1992.67.2.477. [DOI] [PubMed] [Google Scholar]
- Nusser Z., Mulvihill E., Streit P., Somogyi P. Subsynaptic segregation of metabotropic and ionotropic glutamate receptors as revealed by immunogold localization. Neuroscience. 1994 Aug;61(3):421–427. doi: 10.1016/0306-4522(94)90421-9. [DOI] [PubMed] [Google Scholar]
- Nusser Z., Sieghart W., Somogyi P. Segregation of different GABAA receptors to synaptic and extrasynaptic membranes of cerebellar granule cells. J Neurosci. 1998 Mar 1;18(5):1693–1703. doi: 10.1523/JNEUROSCI.18-05-01693.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ohishi H., Akazawa C., Shigemoto R., Nakanishi S., Mizuno N. Distributions of the mRNAs for L-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J Comp Neurol. 1995 Oct 2;360(4):555–570. doi: 10.1002/cne.903600402. [DOI] [PubMed] [Google Scholar]
- Ohishi H., Shigemoto R., Nakanishi S., Mizuno N. Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J Comp Neurol. 1993 Sep 8;335(2):252–266. doi: 10.1002/cne.903350209. [DOI] [PubMed] [Google Scholar]
- Ohishi H., Shigemoto R., Nakanishi S., Mizuno N. Distribution of the messenger RNA for a metabotropic glutamate receptor, mGluR2, in the central nervous system of the rat. Neuroscience. 1993 Apr;53(4):1009–1018. doi: 10.1016/0306-4522(93)90485-x. [DOI] [PubMed] [Google Scholar]
- Olianas M. C., Onali P. GABA(B) receptor-mediated stimulation of adenylyl cyclase activity in membranes of rat olfactory bulb. Br J Pharmacol. 1999 Feb;126(3):657–664. doi: 10.1038/sj.bjp.0702349. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olpe H. R., Karlsson G., Pozza M. F., Brugger F., Steinmann M., Van Riezen H., Fagg G., Hall R. G., Froestl W., Bittiger H. CGP 35348: a centrally active blocker of GABAB receptors. Eur J Pharmacol. 1990 Oct 2;187(1):27–38. doi: 10.1016/0014-2999(90)90337-6. [DOI] [PubMed] [Google Scholar]
- Ottersen O. P., Landsend A. S. Organization of glutamate receptors at the synapse. Eur J Neurosci. 1997 Nov;9(11):2219–2224. doi: 10.1111/j.1460-9568.1997.tb01640.x. [DOI] [PubMed] [Google Scholar]
- Parent A., Charara A., Pinault D. Single striatofugal axons arborizing in both pallidal segments and in the substantia nigra in primates. Brain Res. 1995 Nov 6;698(1-2):280–284. doi: 10.1016/0006-8993(95)01017-p. [DOI] [PubMed] [Google Scholar]
- Parpura V., Basarsky T. A., Liu F., Jeftinija K., Jeftinija S., Haydon P. G. Glutamate-mediated astrocyte-neuron signalling. Nature. 1994 Jun 30;369(6483):744–747. doi: 10.1038/369744a0. [DOI] [PubMed] [Google Scholar]
- Pearce B., Albrecht J., Morrow C., Murphy S. Astrocyte glutamate receptor activation promotes inositol phospholipid turnover and calcium flux. Neurosci Lett. 1986 Dec 23;72(3):335–340. doi: 10.1016/0304-3940(86)90537-9. [DOI] [PubMed] [Google Scholar]
- Petralia R. S., Wang Y. X., Niedzielski A. S., Wenthold R. J. The metabotropic glutamate receptors, mGluR2 and mGluR3, show unique postsynaptic, presynaptic and glial localizations. Neuroscience. 1996 Apr;71(4):949–976. doi: 10.1016/0306-4522(95)00533-1. [DOI] [PubMed] [Google Scholar]
- Petralia R. S., Wang Y. X., Singh S., Wu C., Shi L., Wei J., Wenthold R. J. A monoclonal antibody shows discrete cellular and subcellular localizations of mGluR1 alpha metabotropic glutamate receptors. J Chem Neuroanat. 1997 Jul;13(2):77–93. doi: 10.1016/s0891-0618(97)00023-9. [DOI] [PubMed] [Google Scholar]
- Pin J. P., Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology. 1995 Jan;34(1):1–26. doi: 10.1016/0028-3908(94)00129-g. [DOI] [PubMed] [Google Scholar]
- Pisani A., Calabresi P., Centonze D., Bernardi G. Activation of group III metabotropic glutamate receptors depresses glutamatergic transmission at corticostriatal synapse. Neuropharmacology. 1997 Jun;36(6):845–851. doi: 10.1016/s0028-3908(96)00177-3. [DOI] [PubMed] [Google Scholar]
- Porter J. T., McCarthy K. D. Astrocytic neurotransmitter receptors in situ and in vivo. Prog Neurobiol. 1997 Mar;51(4):439–455. doi: 10.1016/s0301-0082(96)00068-8. [DOI] [PubMed] [Google Scholar]
- Rainnie D. G., Holmes K. H., Shinnick-Gallagher P. Activation of postsynaptic metabotropic glutamate receptors by trans-ACPD hyperpolarizes neurons of the basolateral amygdala. J Neurosci. 1994 Nov;14(11 Pt 2):7208–7220. doi: 10.1523/JNEUROSCI.14-11-07208.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reimann W. Inhibition by GABA, baclofen and gabapentin of dopamine release from rabbit caudate nucleus: are there common or different sites of action? Eur J Pharmacol. 1983 Oct 28;94(3-4):341–344. doi: 10.1016/0014-2999(83)90425-9. [DOI] [PubMed] [Google Scholar]
- Ribak C. E., Vaughn J. E., Roberts E. The GABA neurons and their axon terminals in rat corpus striatum as demonstrated by GAD immunocytochemistry. J Comp Neurol. 1979 Sep 15;187(2):261–283. doi: 10.1002/cne.901870203. [DOI] [PubMed] [Google Scholar]
- Romano C., Sesma M. A., McDonald C. T., O'Malley K., Van den Pol A. N., Olney J. W. Distribution of metabotropic glutamate receptor mGluR5 immunoreactivity in rat brain. J Comp Neurol. 1995 May 8;355(3):455–469. doi: 10.1002/cne.903550310. [DOI] [PubMed] [Google Scholar]
- Rothstein J. D., Dykes-Hoberg M., Pardo C. A., Bristol L. A., Jin L., Kuncl R. W., Kanai Y., Hediger M. A., Wang Y., Schielke J. P. Knockout of glutamate transporters reveals a major role for astroglial transport in excitotoxicity and clearance of glutamate. Neuron. 1996 Mar;16(3):675–686. doi: 10.1016/s0896-6273(00)80086-0. [DOI] [PubMed] [Google Scholar]
- Rusakov D. A., Kullmann D. M. Extrasynaptic glutamate diffusion in the hippocampus: ultrastructural constraints, uptake, and receptor activation. J Neurosci. 1998 May 1;18(9):3158–3170. doi: 10.1523/JNEUROSCI.18-09-03158.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sadikot A. F., Parent A., François C. Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a PHA-L study of subcortical projections. J Comp Neurol. 1992 Jan 8;315(2):137–159. doi: 10.1002/cne.903150203. [DOI] [PubMed] [Google Scholar]
- Sadikot A. F., Parent A., Smith Y., Bolam J. P. Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity. J Comp Neurol. 1992 Jun 8;320(2):228–242. doi: 10.1002/cne.903200207. [DOI] [PubMed] [Google Scholar]
- Sawynok J., Labella F. S. GABA and baclofen potentiate the K+-evoked release of methionine-enkephalin from rat striatal slices. Eur J Pharmacol. 1981 Mar 12;70(2):103–110. doi: 10.1016/0014-2999(81)90204-1. [DOI] [PubMed] [Google Scholar]
- Seabrook G. R., Howson W., Lacey M. G. Electrophysiological characterization of potent agonists and antagonists at pre- and postsynaptic GABAB receptors on neurones in rat brain slices. Br J Pharmacol. 1990 Dec;101(4):949–957. doi: 10.1111/j.1476-5381.1990.tb14186.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Seabrook G. R., Howson W., Lacey M. G. Subpopulations of GABA-mediated synaptic potentials in slices of rat dorsal striatum are differentially modulated by presynaptic GABAB receptors. Brain Res. 1991 Oct 25;562(2):332–334. doi: 10.1016/0006-8993(91)90642-9. [DOI] [PubMed] [Google Scholar]
- Shen K. Z., Johnson S. W. Presynaptic GABAB and adenosine A1 receptors regulate synaptic transmission to rat substantia nigra reticulata neurones. J Physiol. 1997 Nov 15;505(Pt 1):153–163. doi: 10.1111/j.1469-7793.1997.153bc.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shigemoto R., Nomura S., Ohishi H., Sugihara H., Nakanishi S., Mizuno N. Immunohistochemical localization of a metabotropic glutamate receptor, mGluR5, in the rat brain. Neurosci Lett. 1993 Nov 26;163(1):53–57. doi: 10.1016/0304-3940(93)90227-c. [DOI] [PubMed] [Google Scholar]
- Shink E., Bevan M. D., Bolam J. P., Smith Y. The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience. 1996 Jul;73(2):335–357. doi: 10.1016/0306-4522(96)00022-x. [DOI] [PubMed] [Google Scholar]
- Shink E., Smith Y. Differential synaptic innervation of neurons in the internal and external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey. J Comp Neurol. 1995 Jul 17;358(1):119–141. doi: 10.1002/cne.903580108. [DOI] [PubMed] [Google Scholar]
- Smith Y., Bennett B. D., Bolam J. P., Parent A., Sadikot A. F. Synaptic relationships between dopaminergic afferents and cortical or thalamic input in the sensorimotor territory of the striatum in monkey. J Comp Neurol. 1994 Jun 1;344(1):1–19. doi: 10.1002/cne.903440102. [DOI] [PubMed] [Google Scholar]
- Smith Y., Bevan M. D., Shink E., Bolam J. P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience. 1998 Sep;86(2):353–387. doi: 10.1016/s0306-4522(98)00004-9. [DOI] [PubMed] [Google Scholar]
- Smith Y., Bolam J. P. Neurons of the substantia nigra reticulata receive a dense GABA-containing input from the globus pallidus in the rat. Brain Res. 1989 Jul 24;493(1):160–167. doi: 10.1016/0006-8993(89)91011-1. [DOI] [PubMed] [Google Scholar]
- Smith Y., Wichmann T., DeLong M. R. Synaptic innervation of neurones in the internal pallidal segment by the subthalamic nucleus and the external pallidum in monkeys. J Comp Neurol. 1994 May 8;343(2):297–318. doi: 10.1002/cne.903430209. [DOI] [PubMed] [Google Scholar]
- Smolders I., De Klippel N., Sarre S., Ebinger G., Michotte Y. Tonic GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely moving rat. Eur J Pharmacol. 1995 Sep 15;284(1-2):83–91. doi: 10.1016/0014-2999(95)00369-v. [DOI] [PubMed] [Google Scholar]
- Somogyi P., Fritschy J. M., Benke D., Roberts J. D., Sieghart W. The gamma 2 subunit of the GABAA receptor is concentrated in synaptic junctions containing the alpha 1 and beta 2/3 subunits in hippocampus, cerebellum and globus pallidus. Neuropharmacology. 1996;35(9-10):1425–1444. doi: 10.1016/s0028-3908(96)00086-x. [DOI] [PubMed] [Google Scholar]
- Sontheimer H., Black J. A., Waxman S. G. Voltage-gated Na+ channels in glia: properties and possible functions. Trends Neurosci. 1996 Aug;19(8):325–331. doi: 10.1016/0166-2236(96)10039-4. [DOI] [PubMed] [Google Scholar]
- Starr M. S. Glutamate/dopamine D1/D2 balance in the basal ganglia and its relevance to Parkinson's disease. Synapse. 1995 Apr;19(4):264–293. doi: 10.1002/syn.890190405. [DOI] [PubMed] [Google Scholar]
- Steinhäuser C., Gallo V. News on glutamate receptors in glial cells. Trends Neurosci. 1996 Aug;19(8):339–345. doi: 10.1016/0166-2236(96)10043-6. [DOI] [PubMed] [Google Scholar]
- Sulzer D., Joyce M. P., Lin L., Geldwert D., Haber S. N., Hattori T., Rayport S. Dopamine neurons make glutamatergic synapses in vitro. J Neurosci. 1998 Jun 15;18(12):4588–4602. doi: 10.1523/JNEUROSCI.18-12-04588.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Surmeier D. J., Reiner A., Levine M. S., Ariano M. A. Are neostriatal dopamine receptors co-localized? Trends Neurosci. 1993 Aug;16(8):299–305. doi: 10.1016/0166-2236(93)90103-s. [DOI] [PubMed] [Google Scholar]
- Surmeier D. J., Song W. J., Yan Z. Coordinated expression of dopamine receptors in neostriatal medium spiny neurons. J Neurosci. 1996 Oct 15;16(20):6579–6591. doi: 10.1523/JNEUROSCI.16-20-06579.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Takeshita Y., Harata N., Akaike N. Suppression of K+ conductance by metabotropic glutamate receptor in acutely dissociated large cholinergic neurons of rat caudate putamen. J Neurophysiol. 1996 Sep;76(3):1545–1558. doi: 10.1152/jn.1996.76.3.1545. [DOI] [PubMed] [Google Scholar]
- Tallaksen-Greene S. J., Kaatz K. W., Romano C., Albin R. L. Localization of mGluR1a-like immunoreactivity and mGluR5-like immunoreactivity in identified populations of striatal neurons. Brain Res. 1998 Jan 12;780(2):210–217. doi: 10.1016/s0006-8993(97)01141-4. [DOI] [PubMed] [Google Scholar]
- Testa C. M., Friberg I. K., Weiss S. W., Standaert D. G. Immunohistochemical localization of metabotropic glutamate receptors mGluR1a and mGluR2/3 in the rat basal ganglia. J Comp Neurol. 1998 Jan 5;390(1):5–19. [PubMed] [Google Scholar]
- Testa C. M., Standaert D. G., Young A. B., Penney J. B., Jr Metabotropic glutamate receptor mRNA expression in the basal ganglia of the rat. J Neurosci. 1994 May;14(5 Pt 2):3005–3018. doi: 10.1523/JNEUROSCI.14-05-03005.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Veenman C. L., Albin R. L., Richfield E. K., Reiner A. Distributions of GABAA, GABAB, and benzodiazepine receptors in the forebrain and midbrain of pigeons. J Comp Neurol. 1994 Jun 8;344(2):161–189. doi: 10.1002/cne.903440202. [DOI] [PubMed] [Google Scholar]
- Verkhratsky A., Kettenmann H. Calcium signalling in glial cells. Trends Neurosci. 1996 Aug;19(8):346–352. doi: 10.1016/0166-2236(96)10048-5. [DOI] [PubMed] [Google Scholar]
- Waldvogel H. J., Fritschy J. M., Mohler H., Faull R. L. GABA(A) receptors in the primate basal ganglia: an autoradiographic and a light and electron microscopic immunohistochemical study of the alpha1 and beta2,3 subunits in the baboon brain. J Comp Neurol. 1998 Aug 3;397(3):297–325. doi: 10.1002/(sici)1096-9861(19980803)397:3<297::aid-cne1>3.0.co;2-y. [DOI] [PubMed] [Google Scholar]
- White J. H., Wise A., Main M. J., Green A., Fraser N. J., Disney G. H., Barnes A. A., Emson P., Foord S. M., Marshall F. H. Heterodimerization is required for the formation of a functional GABA(B) receptor. Nature. 1998 Dec 17;396(6712):679–682. doi: 10.1038/25354. [DOI] [PubMed] [Google Scholar]
- White L. E., Hodges H. D., Carnes K. M., Price J. L., Dubinsky J. M. Colocalization of excitatory and inhibitory neurotransmitter markers in striatal projection neurons in the rat. J Comp Neurol. 1994 Jan 15;339(3):328–340. doi: 10.1002/cne.903390303. [DOI] [PubMed] [Google Scholar]
- Wichmann T., DeLong M. R. Functional and pathophysiological models of the basal ganglia. Curr Opin Neurobiol. 1996 Dec;6(6):751–758. doi: 10.1016/s0959-4388(96)80024-9. [DOI] [PubMed] [Google Scholar]
- Wilkin G. P., Hudson A. L., Hill D. R., Bowery N. G. Autoradiographic localization of GABAB receptors in rat cerebellum. Nature. 1981 Dec 10;294(5841):584–587. doi: 10.1038/294584a0. [DOI] [PubMed] [Google Scholar]
- Wilson J. S., Wilson J. A. Baclofen attenuates hyperpolarizing not depolarizing responses of caudate neurons in cat. Brain Res. 1985 Sep 9;342(2):396–400. doi: 10.1016/0006-8993(85)91145-x. [DOI] [PubMed] [Google Scholar]
- Wojcik W. J., Neff N. H. gamma-aminobutyric acid B receptors are negatively coupled to adenylate cyclase in brain, and in the cerebellum these receptors may be associated with granule cells. Mol Pharmacol. 1984 Jan;25(1):24–28. [PubMed] [Google Scholar]
- Wurtz R. H., Hikosaka O. Role of the basal ganglia in the initiation of saccadic eye movements. Prog Brain Res. 1986;64:175–190. doi: 10.1016/S0079-6123(08)63412-3. [DOI] [PubMed] [Google Scholar]
- Yoon K. W., Rothman S. M. The modulation of rat hippocampal synaptic conductances by baclofen and gamma-aminobutyric acid. J Physiol. 1991 Oct;442:377–390. doi: 10.1113/jphysiol.1991.sp018798. [DOI] [PMC free article] [PubMed] [Google Scholar]
