全部 标题 作者
关键词 摘要

OALib Journal期刊
ISSN: 2333-9721
费用:99美元

查看量下载量

相关文章

更多...
PLOS ONE  2012 

Development of GPCR Modulation of GABAergic Transmission in Chicken Nucleus Laminaris Neurons

DOI: 10.1371/journal.pone.0035831

Full-Text   Cite this paper   Add to My Lib

Abstract:

Neurons in the nucleus laminaris (NL) of birds act as coincidence detectors and encode interaural time difference to localize the sound source in the azimuth plane. GABAergic transmission in a number of CNS nuclei including the NL is subject to a dual modulation by presynaptic GABAB receptors (GABABRs) and metabotropic glutamate receptors (mGluRs). Here, using in vitro whole-cell patch clamp recordings from acute brain slices of the chick, we characterized the following important but unknown properties pertaining to such a dual modulation: (1) emergence of functional GABA synapses in NL neurons; (2) the temporal onset of neuromodulation mediated by GABABRs and mGluRs; and (3) the physiological conditions under which GABABRs and mGluRs are activated by endogenous transmitters. We found that (1) GABAAR-mediated synaptic responses were observed in about half of the neurons at embryonic day 11 (E11); (2) GABABR-mediated modulation of the GABAergic transmission was detectable at E11, whereas the modulation by mGluRs did not emerge until E15; and (3) endogenous activity of GABABRs was induced by both low- (5 or 10 Hz) and high-frequency (200 Hz) stimulation of the GABAergic pathway, whereas endogenous activity of mGluRs was induced by high- (200 Hz) but not low-frequency (5 or 10 Hz) stimulation of the glutamatergic pathway. Furthermore, the endogenous activity of mGluRs was mediated by group II but not group III members. Therefore, autoreceptor-mediated modulation of GABAergic transmission emerges at the same time when the GABA synapses become functional. Heteroreceptor-mediated modulation appears at a later time and is receptor type dependent in vitro.

References

[1]  de Jong AP, Verhage M (2009) Presynaptic signal transduction pathways that modulate synaptic transmission. Curr Opin Neurobiol 19: 245–253.
[2]  Stephens GJ (2009) G-protein-coupled-receptor-mediated presynaptic inhibition in the cerebellum. Trends Pharmacol Sci 30: 421–430.
[3]  Cartmell J, Schoepp DD (2000) Regulation of neurotransmitter release by metabotropic glutamate receptors. J Neurochem 75: 889–907.
[4]  Nicoletti F, Bockaert J, Collingridge GL, Conn PJ, Ferraguti F, et al. (2011) Metabotropic glutamate receptors: from the workbench to bedside. Neuropharmacology 60: 1017–1041.
[5]  Niswender CM, Conn PJ (2010) Metabotropic glutamate receptors: physiology, pharmacology, and disease. Annu Rev Pharmacol Toxicol 50: 295–322.
[6]  Chalifoux JR, Carter AG (2011) GABAB receptor modulation of synaptic function. Curr Opin Neurobiol 21: 339–344.
[7]  Ulrich D, Bettler B (2007) GABAB receptors: synaptic functions and mechanisms of diversity. Curr Opin Neurobiol 17: 298–303.
[8]  Fujino K, Oertel D (2003) Bidirectional synaptic plasticity in the cerebellum-like mammalian dorsal cochlear nucleus. Proc Natl Acad Sci 100: 265–270.
[9]  Luo B, Wang HT, Su YY, Wu SH, Chen L (2011) Activation of presynaptic GABAB receptors modulates GABAergic and glutamatergic inputs to the medial geniculate body. Hear Res 280: 157–165.
[10]  Sanes DH, McGee J, Walsh EJ (1998) Metabotropic glutamate receptor activation modulates sound level processing in the cochlear nucleus. J Neurophysiol 80: 209–217.
[11]  Lu Y, Burger RM, Rubel EW (2005) GABAB receptor activation modulates GABAA receptor-mediated inhibition in chicken nucleus magnocellularis neurons. J Neurophysiol 93: 1429–1438.
[12]  Lu Y (2007) Endogenous mGluR activity suppresses GABAergic transmission in avian cochlear nucleus magnocellularis neurons. J Neurophysiol 97: 1018–1029.
[13]  Tang ZQ, Gao H, Lu Y (2009) Control of a depolarizing GABAergic input in an auditory coincidence detection circuit. J Neurophysiol 102: 1672–1683.
[14]  Hyson RL (2005) The analysis of interaural time differences in the chick brain stem. Physiol Behav 86: 297–305.
[15]  Rubel EW, Fritzsch B (2002) Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25: 51–101.
[16]  Hendricks SJ, Rubel EW, Nishi R (2006) Formation of the avian nucleus magnocellularis from the auditory anlage. J Comp Neurol 498(4): 433–442.
[17]  Young SR, Rubel EW (1983) Frequency-specific projections of individual neurons in chick brainstem auditory nuclei. J Neurosci 3(7): 1373–1378.
[18]  Gao H, Lu Y (2008) Early development of intrinsic and synaptic properties of chicken nucleus laminaris neurons. Neuroscience 153: 131–143.
[19]  Sanchez JT, Wang Y, Rubel EW, Barria A (2010) Development of glutamatergic synaptic transmission in binaural auditory neurons. J Neurophysiol 104: 1774–1789.
[20]  Code RA, Burd GD, Rubel EW (1989) Development of GABA immunoreactivity in brainstem auditory nuclei of the chick: ontogeny of gradients in terminal staining. J Comp Neurol 284: 504–518.
[21]  Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R (2007) GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87: 1215–1284.
[22]  Barbour B, H?usser M (1997) Intersynaptic diffusion of neurotransmitter. Trends Neurosci 20: 377–384.
[23]  Galvan A, Kuwajima M, Smith Y (2006) Glutamate and GABA receptors and transporters in the basal ganglia: what does their subsynaptic localization reveal about their function? Neuroscience 143: 351–375.
[24]  Tang ZQ, Dinh EH, Shi W, Lu Y (2011) Ambient GABA-activated tonic inhibition sharpens auditory coincidence detection via a depolarizing shunting mechanism. J Neurosci 31: 6121–6131.
[25]  Ye JH, Zhang J, Xiao C, Kong JQ (2006) Patch-clamp studies in the CNS illustrate a simple new method for obtaining viable neurons in rat brain slices: glycerol replacement of NaCl protects CNS neurons. J Neurosci Methods 158: 251–259.
[26]  Barry PH (1994) JPCalc, a software package for calculating liquid junction potential corrections in patch-clamp, intracellular, epithelial and bilayer measurements and for correcting junction potential measurements. J Neurosci Methods 51: 107–116.
[27]  Burger RM, Cramer KS, Pfeiffer JD, Rubel EW (2005) Avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways. J Comp Neurol 481: 6–18.
[28]  Lachica EA, Rübsamen R, Rubel EW (1994) GABAergic terminals in nucleus magnocellularis and laminaris originate from the superior olivary nucleus. J Comp Neurol 348: 403–418.
[29]  Yang L, Monsivais P, Rubel EW (1999) The superior olivary nucleus and its influence on nucleus laminaris: a source of inhibitory feedback for coincidence detection in the avian auditory brainstem. J Neurosci 19: 2313–2325.
[30]  Lanza M, Fassio A, Gemignani A, Bonanno G, Raiteri M (1993) CGP 52432: a novel potent and selective GABAB autoreceptor antagonist in rat cerebral cortex. Eur J Pharmacol 237: 191–195.
[31]  Drew GM, Mitchell VA, Vaughan CW (2008) Glutamate spillover modulates GABAergic synaptic transmission in the rat midbrain periaqueductal grey via metabotropic glutamate receptors and endocannabinoid signaling. J Neurosci 28: 808–815.
[32]  Nishino E, Yamada R, Kuba H, Hioki H, Furuta T, et al. (2008) Sound-intensity-dependent compensation for the small interaural time difference cue for sound source localization. J Neurosci 28: 7153–7164.
[33]  Pinheiro PS, Mulle C (2008) Presynaptic glutamate receptors: physiological functions and mechanisms of action. Nat Rev Neurosci 9: 423–436.
[34]  Fukui I, Sato T, Ohmori H (2006) Improvement of phase information at low sound frequency in nucleus magnocellularis of the chicken. J Neurophysiol 96: 633–641.
[35]  Warchol ME, Dallos P (1990) Neural coding in the chick cochlear nucleus. J Comp Physiol [A] 166: 721–734.
[36]  Scanziani M, Salin PA, Vogt KE, Malenka RC, Nicoll RA (1997) Use-dependent increases in glutamate concentration activate presynaptic metabotropic glutamate receptors. Nature 385: 630–634.
[37]  Shimamoto K, Lebrun B, Yasuda-Kamatani Y, Sakaitani M, Shigeri Y, et al. (1998) DL-threo-beta-benzyloxyaspartate, a potent blocker of excitatory amino acid transporters. Mol Pharmacol 53: 195–201.
[38]  Tsukada S, Iino M, Takayasu Y, Shimamoto K, Ozawa S (2005) Effects of a novel glutamate transporter blocker, (2S, 3S)-3-[3-[4-(trifluoromethyl) benzoylamino] benzyloxy] aspartate (TFB-TBOA), on activities of hippocampal neurons. Neuropharmacology 48: 479–491.
[39]  Toms NJ, Jane DE, Kemp MC, Bedingfield JS, Roberts PJ (1996) The effects of (RS)-alpha-cyclopropyl-4-phosphonophenyl?glycine((RS)-CPPG), a potent and selective metabotropic glutamate receptor antagonist. Br J Pharmacol 119: 851–854.
[40]  Saunders JC, Coles RB, Gates GR (1973) The development of auditory evoked responses in the cochlea and cochlear nuclei of the chick. Brain Res 63: 59–74.
[41]  Lippe WR (1994) Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14: 1486–1495.
[42]  Bellone C, Lüscher C, Mameli M (2008) Mechanisms of synaptic depression triggered by metabotropic glutamate receptors. Cell Mol Life Sci 65: 2913–2923.
[43]  Gladding CM, Fitzjohn SM, Molnár E (2009) Metabotropic glutamate receptor-mediated long-term depression: molecular mechanisms. Pharmacol Rev 61: 395–412.
[44]  Asztely F, Erdemli G, Kullmann DM (1997) Extrasynaptic glutamate spillover in the hippocampus: dependence on temperature and the role of active glutamate uptake. Neuron 18: 281–293.
[45]  Kullmann DM (2000) Spillover and synaptic cross talk mediated by glutamate and GABA in the mammalian brain. Prog Brain Res 125: 339–351.
[46]  Mitchell SJ, Silver RA (2000) Glutamate spillover suppresses inhibition by activating presynaptic mGluRs. Nature 404: 498–502.
[47]  Okubo Y, Iino M (2011) Visualization of glutamate as a volume transmitter. J Physiol 589: 481–488.
[48]  Smith ZD (1981) Organization and development of brain stem auditory nuclei of the chicken: dendritic development in N. Laminaris. J Comp Neurol 203: 309–333.
[49]  Smith DJ, Rubel EW (1979) Organization and development of brain stem auditory nuclei of the chicken: dendritic gradients in nucleus laminaris. J Comp Neurol 186: 213–239.
[50]  Korn MJ, Koppel SJ, Cramer KS (2011) Astrocyte-secreted factors modulate a gradient of primary dendritic arbors in nucleus laminaris of the avian auditory brainstem. PloS One 6(11): e27383.
[51]  Parks TN, Collins P, Conlee JW (1983) Morphology and origin of axonal endings in nucleus laminaris of the chicken. J Comp Neurol 214: 32–42.
[52]  Tabor KM, Wong RO, Rubel EW (2011) Topography and morphology of the inhibitory projection from superior olivary nucleus to nucleus laminaris in chickens (Gallus gallus). J Comp Neurol 519: 358–375.
[53]  Parks TN (1981) Morphology of axosomatic endings in an avian cochlear nucleus: nucleus magnocellularis of the chicken. J Comp Neurol 203: 425–440.
[54]  Zhang S, Trussell LO (1994) A characterization of excitatory postsynaptic potentials in the avian nucleus magnocellularis. J Neurophysiol 72(2): 705–718.
[55]  Ryugo DK, Parks TN (2003) Primary innervation of the avian and mammalian cochlear nucleus. Brain Res Bull 60: 435–456.
[56]  Panatier A, Poulain DA, Oliet SH (2004) Regulation of transmitter release by high-affinity group III mGluRs in the supraoptic nucleus of the rat hypothalamus. Neuropharmacology 47: 333–341.

Full-Text

Contact Us

service@oalib.com

QQ:3279437679

WhatsApp +8615387084133