Attenuation of inhibitory synaptic transmission by glial dysfunction in rat thalamus

Synapse

Volumn 65, Issue 12, 2011, Pages 1298-1308

  Yang, Sunggu ^a,b   Cox, Charles L ^a,b,c  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c UNIVERSITY OF ILLINOIS   (United States)

Author keywords

Glutamine; Inhibition; Thalamic reticular nucleus; Thalamus

Indexed keywords

4 AMINOBUTYRIC ACID; FLUOROCITRIC ACID; GLUTAMIC ACID; GLUTAMINE;

ABSENCE; AMINO ACID TRANSPORT; ANIMAL TISSUE; AROUSAL; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; GLIA; NONHUMAN; PRIORITY JOURNAL; RAT; SYNAPTIC TRANSMISSION; THALAMUS;

ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; EPILEPSY, ABSENCE; GLUTAMIC ACID; NEURAL INHIBITION; NEUROGLIA; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPTIC TRANSMISSION; THALAMUS;

EID: 80053902399     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20964     Document Type: Article

References (43)

1. Ahlsen G, Lindstrom S, Lo FS. 1985. Interaction between inhibitory pathways to principal cells in the lateral geniculate nucleus of the cat. Exp Brain Res 58: 134-143.
2. Armano S, Coco S, Bacci A, Pravettoni E, Schenk U, Verderio C, Varoqui H, Erickson JD, Matteoli M. 2002. Localization and functional relevance of system a neutral amino acid transporters in cultured hippocampal neurons. J Biol Chem 277: 10467-10473.
3. Bacci A, Sancini G, Verderio C, Armano S, Pravettoni E, Fesce R, Franceschetti S, Matteoli M. 2002. Block of glutamate-glutamine cycle between astrocytes and neurons inhibits epileptiform activity in hippocampus. J Neurophysiol 88: 2302-2310.
4. Broberger C, McCormick DA. 2005. Excitatory effects of thyrotropin-releasing hormone in the thalamus. J Neurosci 25: 1664-1673.
5. Bryant AS, Li B, Beenhakker MP, Huguenard JR. 2009. Maintenance of thalamic epileptiform activity depends on the astrocytic glutamate-glutamine cycle. J Neurophysiol 102: 2880-2888.
6. Chaudhry FA, Reimer RJ, Krizaj D, Barber D, Storm-Mathisen J, Copenhagen DR, Edwards RH. 1999. Molecular analysis of system N suggests novel physiological roles in nitrogen metabolism and synaptic transmission. Cell 99: 769-780.
7. Chaudhry FA, Schmitz D, Reimer RJ, Larsson P, Gray AT, Nicoll R, Kavanaugh M, Edwards RH. 2002. Glutamine uptake by neurons: Interaction of protons with system a transporters. J Neurosci 22: 62-72.
8. Chiu CS, Brickley S, Jensen K, Southwell A, McKinney S, Cull-Candy S, Mody I, Lester HA. 2005. GABA transporter deficiency causes tremor, ataxia, nervousness, and increased GABA-induced tonic conductance in cerebellum. J Neurosci 25: 3234-3245.
9. Cox CL, Huguenard JR, Prince DA. 1997. Nucleus reticularis neurons mediate diverse inhibitory effects in thalamus. Proc Natl Acad Sci USA 94: 8854-8859.
10. Crunelli V, Blethyn KL, Cope DW, Hughes SW, Parri HR, Turner JP, Toth TI, Williams SR. 2002. Novel neuronal and astrocytic mechanisms in thalamocortical loop dynamics. Philos Trans R Soc Lond B Biol Sci 357: 1675-1693.
11. Eid T, Thomas MJ, Spencer DD, Runden-Pran E, Lai JC, Malthankar GV, Kim JH, Danbolt NC, Ottersen OP, de Lanerolle NC. 2004. Loss of glutamine synthetase in the human epileptogenic hippocampus: Possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy. Lancet 363: 28-37.
12. Fricke MN, Jones-Davis DM, Mathews GC. 2007. Glutamine uptake by System A transporters maintains neurotransmitter GABA synthesis and inhibitory synaptic transmission. J Neurochem 102: 1895-1904.
13. Hale PT, Sefton AJ, Baur LA, Cottee LJ. 1982. Interrelations of the rat's thalamic reticular and dorsal lateral geniculate nuclei. Exp Brain Res 45: 217-229.
14. Helms G, Ciumas C, Kyaga S, Savic I. 2006. Increased thalamus levels of glutamate and glutamine (Glx) in patients with idiopathic generalised epilepsy. J Neurol Neurosurg Psychiatry 77: 489-494.
15. Jensen K, Chiu CS, Sokolova I, Lester HA, Mody I. 2003. GABA transporter-1 (GAT1)-deficient mice: Differential tonic activation of GABAA versus GABAB receptors in the hippocampus. J Neurophysiol 90: 2690-2701.
16. Jin H, Wu H, Osterhaus G, Wei J, Davis K, Sha D, Floor E, Hsu CC, Kopke RD, Wu JY. 2003. Demonstration of functional coupling between gamma -aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles. Proc Natl Acad Sci USA 100: 4293-4298.
17. Jones EG. 1985. The thalamus. New York: Plenum Press.
18. Larrosa B, Pastor J, Lopez-Aguado L, Herreras O. 2006. A role for glutamate and glia in the fast network oscillations preceding spreading depression. Neuroscience 141: 1057-1068.
19. Lee J, Tommerdahl M, Favorov OV, Whitsel BL. 2005. Optically recorded response of the superficial dorsal horn: Dissociation from neuronal activity, sensitivity to formalin-evoked skin nociceptor activation. J Neurophysiol 94: 852-864.
20. Lee KH, McCormick DA. 1996. Abolition of spindle oscillations by serotonin and norepinephrine in the ferret lateral geniculate and perigeniculate nuclei in vitro. Neuron 17: 309-321.
21. Lee KH, McCormick DA. 1997. Modulation of spindle oscillations by acetylcholine, cholecystokinin and 1S, 3R-ACPD in the ferret lateral geniculat and perigeniculate nuclei in vitro. Neuroscience 77: 335-350.
22. Lee SH, Cox CL. 2003. Vasoactive intestinal peptide selectively depolarizes thalamic relay neurons and attenuates intrathalamic rhythmic activity. J Neurophysiol 90: 1224-1234.
23. Lee SH, Cox CL. 2006. Excitatory actions of vasoactive intestinal peptide on mouse thalamocortical neurons are mediated by VPAC2 receptors. J Neurophysiol 96: 858-871.
24. Lee SM, Friedberg MH, Ebner FF. 1994. The role of GABA-mediated inhibition in the rat ventral posterior medial thalamus. I. Assessment of receptive field changes following thalamus reticular nucleus lesions. J Neurophysiol 71: 1702-1715.
25. Liang SL, Carlson GC, Coulter DA. 2006. Dynamic regulation of synaptic GABA release by the glutamate-glutamine cycle in hippocampal area CA1. J Neurosci 26: 8537-8548.
26. Mathews GC, Diamond JS. 2003. Neuronal glutamate uptake contributes to GABA synthesis and inhibitory synaptic strength. J Neurosci 23: 2040-2048.
27. Parri HR, Gould TM, Crunelli V. 2001. Spontaneous astrocytic Ca2+ oscillations in situ drive NMDAR-mediated neuronal excitation. Nat Neurosci 4: 803-812.
28. Paulsen RE, Contestabile A, Villani L, Fonnum F. 1987. An in vivo model for studying function of brain tissue temporarily devoid of glial cell metabolism: The use of fluorocitrate. J Neurochem 48: 1377-1385.
29. Petroff OA, Errante LD, Rothman DL, Kim JH, Spencer DD. 2002. Glutamate-glutamine cycling in the epileptic human hippocampus. Epilepsia 43: 703-710.
30. Sepkuty JP, Cohen AS, Eccles C, Rafiq A, Behar K, Ganel R, Coulter DA, Rothstein JD. 2002. A neuronal glutamate transporter contributes to neurotransmitter GABA synthesis and epilepsy. J Neurosci 22: 6372-6379.
31. Sherman SM, Guillery RW. 2001. Exploring the thalamus. San Diego: Academic Press.
32. Shosaku A, Kayama Y, Sumitomo I, Sugitani M, Iwama K. 1989. Analysis of recurrent inhibitory circuit in rat thalamus: Neurophysiology of the thalamic reticular nucleus. Prog Neurobiol 32: 77-102.
33. Steriade M, Llinas R. 1988. The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68: 649-742.
34. Steriade M, McCormick DA, Sejnowski TJ. 1993. Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679-685.
35. Steriade M, Jones EG, McCormick DA. 1997. Thalamus. Vol. 1:Organization and function. New York: Elsevier.
36. Stringer JL, Aribi AM. 2003. Effects of glial toxins on extracellular acidification in the hippocampal CA1 region in vivo. Epilepsy Res 54: 163-170.
37. Sun QQ, Huguenard JR, Prince DA. 2002. Somatostatin inhibits thalamic network oscillations in vitro: Actions on the GABAergic neurons of the reticular nucleus. J Neurosci 22: 5374-5386.
38. Tani H, Bandrowski AE, Parada I, Wynn M, Huguenard JR, Prince DA, Reimer RJ. 2007. Modulation of epileptiform activity by glutamine and system A transport in a model of post-traumatic epilepsy. Neurobiol Dis 25: 230-238.
39. von Krosigk M, Bal T, McCormick DA. 1993. Cellular mechanisms of a synchronized oscillation in the thalamus. Science 261: 361-364.
40. Waniewski RA, Martin DL. 1998. Preferential utilization of acetate by astrocytes is attributable to transport. J Neurosci 18: 5225-5233.
41. Wetherington J, Serrano G, Dingledine R. 2008. Astrocytes in the epileptic brain. Neuron 58: 168-178.
42. Yang S, Cox CL. 2007. Modulation of inhibitory activity by nitric oxide in the thalamus. J Neurophysiol 97: 3386-3395.
43. Yang S, Cox CL. 2008. Excitatory and anti-oscillatory actions of nitric oxide in thalamus. J Physiol 586: 3617-3628.