Metabotropic glutamate receptors drive global persistent inhibition in the visual thalamus

Journal of Neuroscience

Volumn 33, Issue 6, 2013, Pages 2494-2506

  Pressler, R Todd ^a   Regehr, Wade G ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3, 5 DIHYDROXYPHENYLGLYCINE; 4 (3 PHOSPHONOPROPYL) 2 PIPERAZINECARBOXYLIC ACID; 6 NITRO 7 SULFAMOYLBENZO [F] QUINOXALINE 2, 3 DIONE; CALCIUM ION; MATRIX EXTRACELLULAR PHOSPHOGLYCOPROTEIN; METABOTROPIC RECEPTOR; UNCLASSIFIED DRUG;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONTROLLED STUDY; ELECTROPHYSIOLOGY; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; LATERAL GENICULATE BODY; MOUSE; NERVE CELL INHIBITION; NERVE CELL MEMBRANE STEADY POTENTIAL; NERVE CELL STIMULATION; NERVE POTENTIAL; NONHUMAN; PRIORITY JOURNAL; RETINA GANGLION CELL; SPIKE WAVE; THALAMOCORTICAL TRACT; THALAMUS;

ANIMALS; FEMALE; GAMMA-AMINOBUTYRIC ACID; GENICULATE BODIES; INHIBITORY POSTSYNAPTIC POTENTIALS; MALE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; ORGAN CULTURE TECHNIQUES; RECEPTORS, METABOTROPIC GLUTAMATE; RETINAL GANGLION CELLS; THALAMUS; VISUAL CORTEX; VISUAL PATHWAYS;

EID: 84873294613     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3458-12.2013     Document Type: Article

References (53)

1. Abramowitz J, Birnbaumer L (2009) Physiology and pathophysiology of canonical transient receptor potential channels. FASEB J 23:297-328. Medline
2. Acuna-Goycolea C, Brenowitz SD, Regehr WG (2008) Active dendritic conductances dynamically regulate GABA release from thalamic interneurons. Neuron 57:420-431. CrossRef Medline
3. Antal M, Acuna-Goycolea C, Pressler RT, Blitz DM, Regehr WG (2010) Cholinergic activation of M2 receptors leads to context-dependent modulation of feed forward inhibition in the visual thalamus. PLoS Biol 8:e1000348. CrossRef Medline
4. Barlow HB, Levick WR (1969) Changes in the maintained discharge with adaptation level in the cat retina. J Physiol 202:699-718. Medline
5. Batchelor AM, Madge DJ, Garthwaite J (1994) Synaptic activation of metabotropic glutamate receptors in the parallel fibre-Purkinje cell pathway in rat cerebellar slices. Neuroscience 63:911-915. CrossRef Medline
6. Berry MJ, Warland DK, Meister M (1997) The structure and precision of retinal spike trains. Proc Natl Acad Sci U S A 94:5411-5416. CrossRef Medline
7. Blitz DM, Regehr WG (2005) Timing and specificity of feed-forward inhibition within the LGN. Neuron 45:917-928. CrossRef Medline
8. Bloomfield SA, Sherman SM (1989) Dendritic current flow in relay cells and interneurons of the cat's lateral geniculate nucleus. Proc Natl Acad Sci U S A 86:3911-3914. CrossRef Medline
9. Brenowitz SD, Regehr WG (2007) Reliability and heterogeneity of calcium signaling at single presynaptic boutons of cerebellar granule cells. J Neurosci 27:7888-7898. CrossRef Medline
10. Cleland BG, Levick WR, Sanderson KJ (1973) Properties of sustained and transient ganglion cells in the cat retina. J Physiol 228:649-680. Medline
11. Congar P, Leinekugel X, Ben-Ari Y, Crépel V (1997) A long-lasting calciumactivated nonselective cationic current is generated by synaptic stimulation or exogenous activation of group I metabotropic glutamate receptors in CA1 pyramidal neurons. J Neurosci 17:5366-5379. Medline
12. Cox CL, Sherman SM (2000) Control of dendritic outputs of inhibitory interneurons in the lateral geniculate nucleus. Neuron 27:597-610. CrossRef Medline
13. Cox CL, Zhou Q, Sherman SM (1998) Glutamate locally activates dendritic outputs of thalamic interneurons. Nature 394:478-482. CrossRef Medline
14. Crandall SR, Cox CL (2012) Local dendrodendritic inhibition regulates fast synaptic transmission in visual thalamus. J Neurosci 32:2513-2522. CrossRef Medline
15. Crépel V, Aniksztejn L, Ben-Ari Y, Hammond C (1994) Glutamate metabotropic receptors increase a Ca(2+)-activated nonspecific cationic current in CA1 hippocampal neurons. J Neurophysiol 72:1561-1569. Medline
16. Dugué GP, Dumoulin A, Triller A, Dieudonné S (2005) Target-dependent use of co-released inhibitory transmitters at central synapses. J Neurosci 25:6490-6498. CrossRef Medline
17. Egorov AV, Hamam BN, Fransén E, Hasselmo ME, Alonso AA (2002) Graded persistent activity in entorhinal cortex neurons. Nature 420:173-178. CrossRef Medline
18. Enroth-Cugell C, Robson JG (1966) The contrast sensitivity of retinal ganglion cells of the cat. J Physiol 187:517-552. Medline
19. Errington AC, di Giovanni G, Crunelli V, Cope DW (2011) MGluR control of interneuron output regulates feedforward tonic GABAA inhibition in the visual thalamus. J Neurosci 31:8669-8680. CrossRef Medline
20. Godwin DW, van Horn SC, Eriir A, Sesma M, Romano C, Sherman SM (1996) Ultrastructural localization suggests that retinal and cortical inputs access different metabotropic glutamate receptors in the lateral geniculate nucleus. J Neurosci 16:8181-8192. Medline
21. Govindaiah, Cox CL (2004) Synaptic activation of metabotropic glutamate receptors regulates dendritic outputs of thalamic interneurons. Neuron 41:611-623. CrossRef Medline
22. Govindaiah G, Cox CL (2006) Metabotropic glutamate receptors differentially regulate GABAergic inhibition in thalamus. J Neurosci 26:13443-13453. CrossRef Medline
23. Hamos JE, Van Horn SC, Raczkowski D, Uhlrich DJ, Sherman SM (1985) Synaptic connectivity of a local circuit neurone in lateral geniculate nucleus of the cat. Nature 317:618-621. CrossRef Medline
24. Hull C, Regehr WG (2012) Identification of an inhibitory circuit that regulates cerebellar Golgi cell activity. Neuron 73:149-158. CrossRef Medline
25. Jones EG (2007) The thalamus. Cambridge, UK: Cambridge UP.
26. Kanichay RT, Silver RA (2008) Synaptic and cellular properties of the feedforward inhibitory circuit within the input layer of the cerebellar cortex. J Neurosci 28:8955-8967. CrossRef Medline
27. Karakossian MH, Otis TS (2004) Excitation of cerebellar interneurons by group I metabotropic glutamate receptors. J Neurophysiol 92:1558-1565. CrossRef Medline
28. Kuffler SW, Fitzhugh R, Barlow HB (1957) Maintained activity in the cat's retina in light and darkness. J Gen Physiol 40:683-702. CrossRef Medline
29. Mastronarde DN (1983) Interactions between ganglion cells in cat retina. J Neurophysiol 49:350-365. Medline
30. Mastronarde DN (1989) Correlated firing of retinal ganglion cells. Trends Neurosci 12:75-80. CrossRef Medline
31. Meister M, Berry MJ 2nd (1999) The neural code of the retina. Neuron 22:435-450. CrossRef Medline
32. Meister M, Lagnado L, Baylor DA (1995) Concerted signaling by retinal ganglion cells. Science 270:1207-1210. CrossRef Medline
33. 2+ levels via the phospholipase C transduction pathway in cultured Purkinje neurons. J Neurophysiol 78:63-75. Medline
34. Norton TT, Godwin DW (1992) Inhibitory GABAergic control of visual signals at the lateral geniculate nucleus. Prog Brain Res 90:193-217. CrossRef Medline
35. Norton TT, Holdefer RN, Godwin DW (1989) Effects of bicuculline on receptive field center sensitivity of relay cells in the lateral geniculate nucleus. Brain Res 488:348-352. CrossRef Medline
36. Ohara PT, Lieberman AR, Hunt SP, Wu JY (1983) Neural elements containing glutamic acid decarboxylase (GAD) in the dorsal lateral geniculate nucleus of the rat; immunohistochemical studies by light and electron microscopy. Neuroscience 8:189-211. CrossRef Medline
37. Pin JP, Duvoisin R (1995) The metabotropic glutamate receptors: structure and functions. Neuropharmacology 34:1-26. CrossRef Medline
38. Pressler RT, Strowbridge BW (2006) Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49:889-904. CrossRef Medline
39. Rafols JA, Valverde F (1973) The structure of the dorsal lateral geniculate nucleus in the mouse. A Golgi and electron microscopic study. J Comp Neurol 150:303-332. CrossRef Medline
40. Salt TE, Binns KE, Turner JP, Gasparini F, Kuhn R (1999) Antagonism of the mGlu5 agonist 2-chloro-5-hydroxyphenylglycine by the novel selective mGlu5 antagonist 6-methyl-2-(phenylethynyl)-pyridine (MPEP) in the thalamus. Br J Pharmacol 127:1057-1059. CrossRef Medline
41. Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Usedependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385:630-634. CrossRef Medline
42. Shepherd GM (2004) The synaptic organization of the brain. Oxford: Oxford UP.
43. Sherman SM (2004) Interneurons and triadic circuitry of the thalamus. Trends Neurosci 27:670-675. CrossRef Medline
44. Sherman SM, Guillery RW (1996) Functional organization of thalamocortical relays. J Neurophysiol 76:1367-1395. Medline
45. Sherman SM, Guillery RW (2006) Exploring the thalamus and its role in cortical function. Cambridge, MA: MIT.
46. Sillito AM (1992) GABA mediated inhibitory processes in the function of the geniculo-striate system. Prog Brain Res 90:349-384. CrossRef Medline
47. Sillito AM, Kemp JA (1983) The influence of GABAergic inhibitory processes on the receptive field structure of X and Y cells in cat dorsal lateral geniculate nucleus (dLGN). Brain Res 277:63-77. CrossRef Medline
48. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T (2003) Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 467:60-79. CrossRef Medline
49. Tempia F, Miniaci MC, Anchisi D, Strata P (1998) Postsynaptic current mediated by metabotropic glutamate receptors in cerebellar Purkinje cells. J Neurophysiol 80:520-528. Medline
50. Usrey WM, Reppas JB, Reid RC (1999) Specificity and strength of retinogeniculate connections. J Neurophysiol 82:3527-3540. Medline
51. Zhang Z, Reboreda A, Alonso A, Barker PA, Séguéla P (2011) TRPC channels underlie cholinergic plateau potentials and persistent activity in entorhinal cortex. Hippocampus 21:386-397. CrossRef Medline
52. Zorumski CF, Mennerick S, Que J (1996) Modulation of excitatory synaptic transmission by low concentrations of glutamate in cultured rat hippocampal neurons. J Physiol 494:465-477. Medline
53. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405. CrossRef Medline