Intrinsic plasticity induced by group II metabotropic glutamate receptors via enhancement of high-threshold KV currents in sound localizing neurons.
Acoustic Stimulation/methods; Action Potentials/drug effects/physiology; Animals; Auditory Pathways/drug effects/*physiology; Brain/drug effects/physiology; Chick Embryo; Glutamic Acid/metabolism; metabotropic glutamate receptor; Metabotropic Glutamate/agonists/*metabolism; neuromodulation; Neuronal Plasticity/drug effects/*physiology; Neurons/drug effects/*physiology; nucleus laminaris; Patch-Clamp Techniques; Potassium Channels; Potassium/metabolism; Protein Kinase C/metabolism; Receptors; Sound Localization/drug effects/*physiology; Tissue Culture Techniques; Type C Phospholipases/metabolism; voltage-gated potassium channel; Voltage-Gated/*metabolism
Intrinsic plasticity has emerged as an important mechanism regulating neuronal excitability and output under physiological and pathological conditions. Here, we report a novel form of intrinsic plasticity. Using perforated patch clamp recordings, we examined the modulatory effects of group II metabotropic glutamate receptors (mGluR II) on voltage-gated potassium (KV) currents and the firing properties of neurons in the chicken nucleus laminaris (NL), the first central auditory station where interaural time cues are analyzed for sound localization. We found that activation of mGluR II by synthetic agonists resulted in a selective increase of the high-threshold KV currents. More importantly, synaptically released glutamate (with reuptake blocked) also enhanced the high-threshold KV currents. The enhancement was frequency-coding region dependent, being more pronounced in low-frequency neurons compared to middle- and high-frequency neurons. The intracellular mechanism involved the Gbetagamma signaling pathway associated with phospholipase C and protein kinase C. The modulation strengthened membrane outward rectification, sharpened action potentials, and improved the ability of NL neurons to follow high-frequency inputs. These data suggest that mGluR II provides a feedforward modulatory mechanism that may regulate temporal processing under the condition of heightened synaptic inputs.
Hamlet W R; Lu Y
Neuroscience
2016
2016-06
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1016/j.neuroscience.2016.03.010" target="_blank" rel="noreferrer noopener">10.1016/j.neuroscience.2016.03.010</a>
Synaptic Inhibition in Avian Interaural Level Difference Sound Localizing Neurons.
Female; Male; Animals; Acoustic Stimulation/methods; Tissue Culture Techniques; Chick Embryo; Patch-Clamp Techniques; *dorsal nucleus of the lateral lemniscus; *GABAA receptor; *interaural level difference; *reversal potential; *synaptic inhibition; Anions/metabolism; Avian Proteins/metabolism; Brain Stem/cytology/drug effects/*physiology; Chlorides/metabolism; Electric Stimulation; gamma-Aminobutyric Acid/metabolism; Intracellular Space/drug effects/metabolism; Neural Inhibition/drug effects/*physiology; Neurons/cytology/drug effects/*physiology; Sound Localization/drug effects/*physiology; Symporters/metabolism; Synaptic Transmission/drug effects/*physiology; Receptors; GABA-A/metabolism; Glycine/metabolism
Synaptic inhibition plays a fundamental role in the neural computation of the interaural level difference (ILD), an important cue for the localization of high-frequency sound. Here, we studied the inhibitory synaptic currents in the chicken posterior portion of the dorsal nucleus of the lateral lemniscus (LLDp), the first binaural level difference encoder of the avian auditory pathway. Using whole-cell recordings in brain slices, we provide the first evidence confirming a monosynaptic inhibition driven by direct electrical and chemical stimulation of the contralateral LLDp, establishing the reciprocal inhibitory connection between the two LLDps, a long-standing assumption in the field. This inhibition was largely mediated by GABAA receptors; however, functional glycine receptors were also identified. The reversal potential for the Cl(-) channels measured with gramicidin-perforated patch recordings was hyperpolarizing (-88 mV), corresponding to a low intracellular Cl(-) concentration (5.2 mm). Pharmacological manipulations of KCC2 (outwardly Cl(-) transporter) activity demonstrate that LLDp neurons can maintain a low intracellular Cl(-) concentration under a high Cl(-) load, allowing for the maintenance of hyperpolarizing inhibition. We further demonstrate that hyperpolarizing inhibition was more effective at regulating cellular excitability than depolarizing inhibition in LLDp neurons.
Curry Rebecca J; Lu Yong
eNeuro
2016
2016-12
Article information provided for research and reference use only. All rights are retained by the journal listed under publisher and/or the creator(s).
<a href="http://doi.org/10.1523/ENEURO.0309-16.2016" target="_blank" rel="noreferrer noopener">10.1523/ENEURO.0309-16.2016</a>