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.
Highlights
Synaptic transmission is dynamically modulated by G-proteincoupled receptors (GPCRs) acting as autoreceptors or heteroreceptors [1,2]
Onset of GABAAR responses in nucleus laminaris (NL) neurons Because neuromodulation mediated by GABAB receptors (GABABRs) activated by endogenous GABA relies on the presence of functional GABA synapses, we first characterized the onset of GABAergic transmission in the NL
Based on the anatomical data showing that GABA terminals to the NL have little presence at E9–11 and a few GABAergic fibers are present at E12–14 [20], we chose embryonic day 11 (E11) as the earliest age to study the onset of physiological responses mediated by GABAARs in NL neuron
Summary
Synaptic transmission is dynamically modulated by G-proteincoupled receptors (GPCRs) acting as autoreceptors or heteroreceptors [1,2] Found among these receptors are metabotropic glutamate receptors (mGluRs) [3,4,5] and type-B GABA receptors (GABABRs) [6,7], which are activated by the two most prevalent excitatory and inhibitory neurotransmitters in the vertebrate CNS, glutamate and GABA, respectively. A dual modulation of GABA release by both presynaptic GABABRs and mGluRs has been found in a number of CNS nuclei including two avian auditory nuclei involved in coding of temporal information of sounds [11,12,13] In such cases, GABABRs function as autoreceptors modulating GABA release via a use-dependent feedback mechanism, whereas mGluRs function as heteroreceptors modulating GABA release. Does the autoreceptor-mediated modulation emerge at the same time when the GABA synapses start functioning through postsynaptic ionotropic receptors? Which one appears first, the modulation mediated by autoreceptors or the modulation mediated by heteroreceptors? Are the physiological conditions, under which the heteroreceptors are activated by endogenous glutamate and exert their modulatory effects, similar to those for autoreceptors?
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