Elsevier

Neuroscience

Volume 164, Issue 3, 15 December 2009, Pages 1009-1019
Neuroscience

Cellular Neuroscience
Research Paper
Regulation of glutamatergic and GABAergic neurotransmission in the chick nucleus laminaris: role of N-type calcium channels

https://doi.org/10.1016/j.neuroscience.2009.09.013Get rights and content

Abstract

Neurons in the chicken nucleus laminaris (NL), the third order auditory nucleus involved in azimuth sound localization, receive bilaterally segregated (ipsilateral vs contralateral) glutamatergic excitation from the cochlear nucleus magnocellularis and GABAergic inhibition from the ipsilateral superior olivary nucleus (SON). Here, I investigate the voltage-gated calcium channels (VGCCs) that trigger the excitatory and the inhibitory transmission in the NL. Whole-cell recordings were performed in acute brainstem slices. The excitatory transmission was predominantly mediated by N-type VGCCs, as the specific N-type blocker ω-Conotoxin-GVIA (ω-CTx-GVIA, 1–2.5 μM) inhibited excitatory postsynaptic currents (EPSCs) by ∼90%. Blockers for P/Q- and L-type VGCCs produced no inhibition, and blockade of R-type VGCCs produced a small inhibition. In individual cells, the effect of each VGCC blocker on the EPSC elicited by activation of the ipsilateral input was the same as that on the EPSC elicited by activation of the contralateral input, and the two EPSCs had similar kinetics, suggesting physiological symmetry between the two glutamatergic inputs to single NL neurons. The inhibitory transmission in NL neurons was almost exclusively mediated by N-type VGCCs, as ω-CTx-GVIA (1 μM) produced a ∼90% reduction of inhibitory postsynaptic currents, whereas blockers for other VGCCs produced no inhibition. In conclusion, N-type VGCCs play a dominant role in triggering both the excitatory and the inhibitory transmission in the NL, and the presynaptic VGCCs that mediate the two bilaterally segregated glutamatergic inputs to individual NL neurons are identical. These features may play a role in optimizing coincidence detection in NL neurons.

Section snippets

Slice preparation and in vitro whole-cell recordings

Fertilized chicken eggs (Gallus domesticus) were purchased from Purdue University (West Lafayette, IN) and incubated using an RX2 Auto Turner (Lyon Electric Co., Chula Vista, CA, USA). Brainstem slices (250–300 μm in thickness) were prepared from late embryos (E18–E21) and early hatchlings (P6–P9) as previously described (Reyes et al., 1994, Tang et al., 2009), with modification of the artificial cerebrospinal fluid (ACSF) components used for dissection and cutting of the brain tissue. The

Effects of Ca2+ channel blockers on the excitatory transmission in the NL

The dorsal and ventral glutamatergic pathways to the NL were activated by the delivery of two separate electrical stimulations using two stimulus setups (Fig. 1C), with an inter-stimulus interval of 75 ms. This interval is long enough to avoid any interactions between the two EPSCs, as responses elicited by the individual stimuli alone were the same as those elicited when both stimuli were presented at the interval of 75 ms (data not shown). Stimulus intensities were adjusted to give rise to

Discussion

The main finding of this study is that N-type VGCCs play a dominant role in triggering both the excitatory and the inhibitory transmission in NL neurons. Furthermore, I found that the same types of VGCCs mediate the ipsilateral and the contralateral glutamatergic transmission in individual NL neurons, and that the ipsilateral and the contralateral EPSCs have the same kinetics. Herein, I provide the first evidence at the cellular level of physiological symmetry between the two segregated

Acknowledgments

This work was supported by Northeastern Ohio Universities Colleges of Medicine and Pharmacy startup funds, and the National Institute on Deafness and other Communication Disorders Grant R01 DC008984 to YL. The author thanks Dr. Hongxiang Gao for technical assistance, Ms. Susan Motts and Dr. Kyle Nakamoto for taking the photographs presented in Fig. 1, and Dr. Zheng-Quan Tang and the anonymous reviewer for critical comments on an earlier version of the manuscript.

References (56)

  • J.H. Ye et al.

    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

    (2006)
  • H. Agmon-Snir et al.

    The role of dendrites in auditory coincidence detection

    Nature

    (1998)
  • M. Barnes-Davis et al.

    Calcium channels triggering transmitter release in the rat medial superior olive

    Hear Res

    (2001)
  • B.P. Bean

    Neurotransmitter inhibition of neuronal calcium currents by changes in channel voltage dependence

    Nature

    (1989)
  • L.M. Boland et al.

    Omega-Conotoxin block of N-type calcium channels in frog and rat sympathetic neurons

    J Neurosci

    (1994)
  • R.M. Burger et al.

    The avian superior olivary nucleus provides divergent inhibitory input to parallel auditory pathways

    J Comp Neurol

    (2005)
  • W.A. Catterall et al.

    International union of pharmacologyXLVIII. Nomenclature and structure-function relationships of voltage-gated calcium channels

    Pharmacol Rev

    (2005)
  • H.M. Colecraft et al.

    G-protein inhibition of N- and P/Q-type calcium channels: distinctive elementary mechanisms and their functional impact

    J Neurosci

    (2001)
  • H.M. Colecraft et al.

    Differential occurrence of reluctant openings in G-protein-inhibited N- and P/Q-type calcium channels

    J Gen Physiol

    (2000)
  • K.P. Currie et al.

    Differential facilitation of N- and P/Q-type calcium channels during trains of action potential-like waveforms

    J Physiol

    (2002)
  • V.K. Dasika et al.

    Simple models show the general advantages of dendrites in coincidence detection

    J Neurophysiol

    (2007)
  • K. Funabiki et al.

    The role of GABAergic inputs for coincidence detection in the neurones of nucleus laminaris of the chick

    J Physiol

    (1998)
  • V. Grau-Serrat et al.

    Modeling coincidence detection in nucleus laminaris

    Biol Cybern

    (2003)
  • L. Gray et al.

    Development of absolute thresholds in chickens

    J Acoust Soc Am

    (1985)
  • C.G. Inchauspe et al.

    Changes in synaptic transmission properties due to the expression of N-type calcium channels at the calyx of Held synapse of mice lacking P/Q-type calcium channels

    J Physiol

    (2007)
  • C.G. Inchauspe et al.

    Functional compensation of P/Q by N-type channels blocks short-term plasticity at the calyx of Held presynaptic terminal

    J Neurosci

    (2004)
  • T. Ishikawa et al.

    Presynaptic N-type and P/Q-type Ca2+ channels mediating synaptic transmission at the calyx of Held of mice

    J Physiol

    (2005)
  • S. Iwasaki et al.

    Developmental changes in calcium channel types mediating synaptic transmission in rat auditory brainstem

    J Physiol

    (1998)
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