Original Research ARTICLE
Activity-dependent endogenous taurine release facilitates excitatory neurotransmission in the neocortical marginal zone of neonatal rats
- 1Department of Neurophysiology, Hamamatsu University School of Medicine, Hamamatsu, Japan
- 2Institute of Physiology, University Medical Center of the Johannes Gutenberg-University, Mainz, Germany
- 3Department of Psychology and Behavioral Neuroscience, Hamamatsu University School of Medicine, Hamamatsu, Japan
- 4Department of Occupational Therapy, Tokoha University, Hamamatsu, Japan
In the developing cerebral cortex, the marginal zone (MZ), consisting of early-generated neurons such as Cajal-Retzius cells, plays an important role in cell migration and lamination. There is accumulating evidence of widespread excitatory neurotransmission mediated by γ-aminobutyric acid (GABA) in the MZ. Cajal-Retzius cells express not only GABAA receptors but also α2/β subunits of glycine receptors, and exhibit glycine receptor-mediated depolarization due to high [Cl−]i. However, the physiological roles of glycine receptors and their endogenous agonists during neurotransmission in the MZ are yet to be elucidated. To address this question, we performed optical imaging from the MZ using the voltage-sensitive dye JPW1114 on tangential neocortical slices of neonatal rats. A single electrical stimulus evoked an action-potential-dependent optical signal that spread radially over the MZ. The amplitude of the signal was not affected by glutamate receptor blockers, but was suppressed by either GABAA or glycine receptor antagonists. Combined application of both antagonists nearly abolished the signal. Inhibition of Na+, K+-2Cl− cotransporter by 20 µM bumetanide reduced the signal, indicating that this transporter contributes to excitation. Analysis of the interstitial fluid obtained by microdialysis from tangential neocortical slices with high-performance liquid chromatography revealed that GABA and taurine, but not glycine or glutamate, were released in the MZ in response to the electrical stimulation. The ambient release of taurine was reduced by the addition of a voltage-sensitive Na+ channel blocker. Immunohistochemistry and immunoelectron microscopy indicated that taurine was stored both in Cajal-Retzius and non-Cajal-Retzius cells in the MZ, but was not localized in presynaptic structures. Our results suggest that activity-dependent non-synaptic release of endogenous taurine facilitates excitatory neurotransmission through activation of glycine receptors in the MZ.
Keywords: taurine, GABAA receptor, glycine receptor, marginal zone, NKCC1, GABA, microdialysis
Citation: Qian T, Chen R, Nakamura M, Furukawa T, Kumada T, Akita T, Kilb W, Luhmann HJ, Nakahara D and Fukuda A (2014) Activity-dependent endogenous taurine release facilitates excitatory neurotransmission in the neocortical marginal zone of neonatal rats. Front. Cell. Neurosci. 8:33. doi: 10.3389/fncel.2014.00033
Received: 18 December 2013; Accepted: 22 January 2014;
Published online: 10 February 2014.
Edited by:Laura Cancedda, Istituto Italiano di Tecnologia, Italy
Reviewed by:Katsushige Sato, Komazawa Women’s University, Japan
Ping Liu, University of Connecticut Health Center, USA
Copyright © 2014 Qian, Chen, Nakamura, Furukawa, Kumada, Akita, Kilb, Luhmann, Nakahara and Fukuda. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Atsuo Fukuda, Department of Neurophysiology, Hamamatsu University School of Medicine, 20-1 Handayama 1-chome, Higashi-ku, Hamamatsu, Shizuoka 431-3192, Japan e-mail: firstname.lastname@example.org