Contribution of GABAergic inhibition to synaptic responses and LTD early in postnatal development in the rat superior colliculus

European Journal of Neuroscience

Volumn 20, Issue 5, 2004, Pages 1331-1340

  Mize, R Ranney ^a,b   Salt, Thomas E ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b LOUISIANA STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

GABA receptors; Retinal evoked potentials; Synaptic plasticity; Visual system

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID C RECEPTOR; 4 AMINOBUTYRIC ACID C RECEPTOR BLOCKING AGENT; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; PICROTOXIN;

ADRENERGIC RECEPTOR BLOCKING; AMPLITUDE MODULATION; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN SLICE; CONTROLLED STUDY; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; EVOKED VISUAL RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; FREQUENCY MODULATION; GABAERGIC TRANSMISSION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; NEUROMODULATION; NONHUMAN; POSTNATAL DEVELOPMENT; POSTSYNAPTIC INHIBITION; PRESYNAPTIC INHIBITION; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; RECEPTOR BLOCKING; RETINA DEVELOPMENT; SUPERIOR COLLICULUS;

ANIMALS; ANIMALS, NEWBORN; GABA ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; LONG-TERM DEPRESSION (PHYSIOLOGY); NEURAL INHIBITION; RATS; SUPERIOR COLLICULUS; SYNAPSES;

EID: 4544355023     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2004.03596.x     Document Type: Article

References (56)

1. Aamodt, S.M., Shi, J., Colonnese, M.T., Veras, W. & Constantine-Paton, M. (2000) Chronic NMDA exposure accelerates development of GABAergic inhibition in the superior colliculus. J. Neurophysiol., 83, 1580-1591.
2. A but not glutamate receptors. Br. J. Pharmacol., 115, 527-533.
3. Arakawa, T. & Okada, Y. (1988) Excitatory and inhibitory action of GABA on synaptic transmission in slices of guinea pig superior colliculus. Eur. J. Pharmacol., 158, 217-224.
4. Artola, A., Brocher, S. & Singer, W. (1990) Different voltage-dependent thresholds for inducing long-term depression and long-term potentiation in slices of rat visual cortex. Nature, 347, 69-72.
5. Artola, A. & Singer, W. (1987) Long-term potentiation and NMDA receptors in rat visual cortex. Nature, 330, 649-652.
6. Binns, K.E. & Salt, T.E. (1997a) Post eye opening maturation of visual receptive field diameters in the superior colliculus of normal- and dark-reared rats. Dev. Brain Res., 58, 263-266.
7. B receptors in visual processing in the rat superior colliculus. J. Physiol. (Lond.), 504, 629-639.
8. C receptor function in the mammalian superior colliculus. Eur. J. Neurosci., 14, 1185-1193.
9. C receptors in the rat superior colliculus and pretectum participate in synaptic neurotransmission. J. Neurophysiol., 89, 2035-2045.
10. Caillard, O., Ben-Ari, Y. & Gaiarsa, J.L. (2000) Activation of presynaptic and postsynaptic ryanodine-sensitive calcium stores is required for the induction of long-term depression at GABAergic synapses in the neonatal rat hippocampus. J. Neurosci., 20, 1-5.
11. Choi, S.-Y., Morales, B., Lee, H.-K. & Kirkwood, A. (2002) Absence of long-term depression in the visual cortex of glutamic acid decarboxylase-65 knock-out mice. J. Neurosci., 11, 5271-5276.
12. 2+ influx in the induction of homosynaptic long-term depression in hippocampal CA1 pyramidal neurons. Learn. Mem., 3, 160-169.
13. Clark, S.E., Garret, M. & Platt, B. (2001) Postnatal alterations of GABA receptor profiles in the rat superior colliculus. Neuroscience, 104, 441-454.
14. Connor, J.A., Petrozzino, J., Pozzo-Miller, L.D. & Otani, S. (1999) Calcium signals in long-term potentiation and long-term depression. Can. J. Physiol. Pharmacol., 77, 722-734.
15. B receptors: a new paradigm in G protein signaling. Mol. Cell. Neurosci., 16, 296-312.
16. Edwards, M.A., Schneider, G.E. & Caviness, V.S. Jr (1986) Development of the crossed retinocollicular projection in the mouse. J. Comp. Neurol., 248, 410-421.
17. Fosse, V.M., Heggelund, P. & Fonnum, F. (1989) Postnatal development of glutamatergic, GABAergic, and cholinergic neurotransmitter phenotypes in the visual cortex, lateral geniculate nucleus, pulvinar, and superior colliculus in cats. J. Neurosci., 9, 426-435.
18. Godement, P., Salaun, J. & Imbert, M. (1984) Prenatal and postnatal development of retinogeniculate and retinocollicular projections in the mouse. J. Comp. Neurol., 230, 552-575.
19. Grassi, S., Della Torre, G., Capocchi, G., Zampolini, M. & Pettorossi, V.E. (1995) The role of GABA in NMDA-dependent long term depression (LTD) of rat medial vestibular nuclei. Brain. Res., 699, 183-191.
20. Hirai, H. & Okada, Y. (1993) Ipsilateral corticotectal pathway inhibits the formation of long-term potentiation (LTP) in the rat superior colliculus through GABAergic mechanism. Brain. Res., 95, 23-30.
21. Huang, J.Z., Kirkwood, A., Pizzorusso, T., Porciatti, V., Morales, B., Bear, M.F., Maffei, L. & Tonegawa, S. (1999) BDNF regulates the maturation of inhibition and the critical period of plasticity in mouse visual cortex. Cell. 98, 739-755.
22. Juttner, R., Henneberger, C., Grantyn, R. & Rothe, T. (2001b) Early onset of glutamatergic and GABAergic synaptic activity in the visual layers of the rodent superior colliculus. Int. J. Dev. Neurosci., 19, 255-261.
23. Juttner, R., Meier, J. & Grantyn, R. (2001a) Slow IPSC kinetics, low levels of alpha1 subunit expression and paired-pulse depression are distinct properties of neonatal inhibitory GABAergic synaptic connections in the mouse superior colliculus. Eur. J. Neurosci., 13, 2088-2098.
24. C receptors to GABAergic synaptic transmission in rat collicular slices and cultures. Eur. J. Neurosci., 18, 752-758.
25. Kirkwood, A. & Bear, M.F. (1994) Homosynaptic long-term depression in the visual cortex. J. Neurosci., 14, 3404-3412.
26. Kraszewski, K. & Grantyn, R. (1992) Development of GABAergic connections in vitro: increasing efficacy of synaptic transmission is not accompanied by changes in miniature currents. J. Neurobiol., 23, 766-781.
27. Kvale, I., Fosse, V.M. & Fonnum, F. (1983) Development of neurotransmitter parameters in lateral geniculate body, superior colliculus and visual cortex of the albino rat. Brain Res., 283, 137-145.
28. Land, P.W. & Lund, R.D. (1979) Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. Science, 205, 698-700.
29. Lo, F.-S. & Mize, R.R. (1999) Retinal input induces three firing patterns in neurons of the superficial colliculus of neonatal rats. J. Neurophysiol., 81, 954-958.
30. 2+ channel activity and long-term depression during refinement of the retinocollicular pathway in developing rodent superior colliculus. J. Neurosci., 20, 1-6.
31. Lo, F.-S. & Mize, R.R. (2002) Properties of LTD and LTP of retinocollicular synaptic transmission in the developing rat superior colliculus. Eur. J. Neurosci., 15, 1421-1432.
32. Lund, R.D. & Lund, J.S. (1972) Development of synaptic patterns in the superior colliculus of the rat. Brain Res., 42, 1-20.
33. Mize, R.R. (1988) Immunocytochemical localization of gamma-aminobutyric acid (GABA) in the cat superior colliculus. J. Comp. Neurol., 276, 169-187.
34. Mize, R.R., Jeon, C.-J., Harnada, O.J. & Spencer, R.F. (1991) Organization of neurons labeled by antibodies to gamma-aminobutyric acid (GABA) in the superior colliculus of the rhesus monkey. Vis. Neurosci., 6, 75-92.
35. Mize, R.R. & Lo, F.-S. (2000) Nitric oxide, impulse activity, and neurotrophins in visual system development. Brain Res., 886, 15-32.
36. Mize, R.R., Whitworth, R.H., Nunes-Cardozo, B. & van der Want, J. (1994) Ultrastructural organization of GABA in the rabbit superior colliculus revealed by quantitative post-embedding immunocytochemistry. J. Comp. Neurol., 341, 273-287.
37. Nishiyama, M., Hong, K., Mikoshiba, K., Poo, M.M. & Kato, K. (2000) Calcium stores regulate the polarity and input specificity of synaptic modification. Nature, 408, 584-588.
38. O'Leary, D.D., Fawcett, J.W. & Cowan, W.M. (1986) Topographic targeting errors in the retinocollicular projection and their elimination by selective ganglion cell death. J. Neurosci., 6, 3692-3705.
39. Olpe, H.R. & Karlsson, G. (1990) The effects of baclofen and two GABAB-receptor antagonists on long-term potentiation. Naunyn Schmiedebergs Arch. Pharmacol., 342, 194-197.
40. 2+ entry and synaptic activation of metabotropic glutamate receptors for the induction of long-term depression in adult rat hippocampus. J. Physiol. (Lond.), 511, 761-770.
41. Pinard, R., Benfares, J. & Lanoir, J. (1991) Electron microscopic study of GABA-immunoreactive neuronal processes in the superficial gray layer of the rat superior colliculus: their relationships with degenerating retinal nerve endings. J. Neurocytol., 20, 262-276.
42. Platt, B. & Withington, D.J. (1998) GABA-induced long-term potentiation in the guinea-pig superior colliculus. Neuropharmacology, 37, 1111-1122.
43. Rammes, G., Eder, M., Dodt, H.U., Kochs, E. & Zieglgansberger, W. (2001) Long-term depression in the basolateral amygdala of the mouse involves the activation of interneurons. Neuroscience, 107, 85-97.
44. Reece, L.J. & Lim, C.H. (1998) Onset of optic nerve conduction and synaptic potentials in superior colliculus of fetal rats studied in vitro. Dev. Brain Res., 106, 25-38.
45. Schmidt, M., Boller, M., Ozen, G. & Hall, W.C.W.C. (2001) Disinhibition in rat superior colliculus mediated by GABAc receptors. J. Neurosci., 21, 691-699.
46. Shi, J., Aamodt, S.M. & Constantine-Paton, M. (1997) Temporal correlations between functional and molecular changes in NMDA receptors and GABA neurotransmission in the superior colliculus. J. Neurosci., 17, 6264-6276.
47. Simon, D.K. & O'Leary, D.D. (1992) Development of topographic order in the mammalian retinocollicular projection. J. Neurosci., 12, 1212-1232.
48. Simon, D.K., Prusky, G.T., O'Leary, D.D. & Constantine-Paton, M. (1992) N-methyl-D-aspartate receptor antagonists disrupt the formation of a mammalian neural map. Proc. Natl Acad. Sci. USA, 89, 10593-10597.
49. Thompson, I. & Holt, C. (1989) Effects of intraocular tetrodotoxin on the development of the retinocollicular pathway in the Syrian hamster. J. Comp. Neurol., 282, 371-388.
50. Tropea, D., Sermasi, E. & Domenici, L. (1999) Synaptic plasticity of feedback connections in rat visual cortex. Dev. Brain Res., 118, 61-67.
51. Wang, J., Liu, S., Haditsch, U., Tu, W., Cochrnae, K., Ahmadian, G., Tran, L., Paw, J., Wang, Y., Mansuy, I., Salter, M.M. & Lu, Y.M. (2003) Interaction of calcineurin and type-0A GABA receptor gamma 2 subunits produces long-term depression at CA1 inhibitory synapses. J. Neurosci., 23, 826-836.
52. Warton, S.S., Perousansky, M. & Grantyn, R. (1990) Development of GABAergic synaptic connections in vivo and in cultures from the rat superior colliculus. Dev. Brain Res., 52, 95-111.
53. Wu, H.H., Cork, R.J. & Mize, R.R. (2000b) Normal development of the ipsilateral retinocollicular pathway and its disruption in double endothelial and neuronal nitric oxide synthase gene knockout mice. J. Comp. Neurol., 426, 651-665.
54. Wu, H.H., Cork, R.J., Shuman, D., Huang, P.L. & Mize, R.R. (2000a) Refinement of the ipsilateral retinocollicular projection is delayed in double endothelial and neuronal nitric oxide synthase gene knockout mice. Dev. Brain Res., 120, 105-111.
55. Yu, T.P., McKinney, S., Lester, H.A. & Davidson, N. (2001) Gamma-aminobutyric acid type A receptors modulate cAMP-mediated long-term potentiation and long-term depression at monosynaptic CA3-CA1 synapses. Proc. Natl Acad. Sci. USA, 98, 5264-5265.
56. Zhang, D., Pan, Z.H., Zhang, X., Brideau, A.D. & Lipton, S.A. (1995) Cloning of a gamma-aminobutyric acid type C receptor subunit in rat retina with a methionine residue critical for picrotoxinin channel block. Proc. Natl Acad. Sci. USA, 92, 11756-11760.