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Depolarizing chloride gradient in developing cochlear nucleus neurons: underlying mechanism and implication for
M Witte1, T Reinert2, B Dietz2
1Institute of Biology, Faculty of Biosciences, Pharmacy and Psychology, University of Leipzig, Germany; Institute of Neuroanatomy, University Medical Center Göttingen, Germany.
Neuroscience
|January 7, 2014
Summary
The sodium-potassium-chloride cotransporter 1 (NKCC1) loads chloride into developing neurons, causing depolarizing effects from GABA and glycine. This shifts to hyperpolarizing effects as NKCC1 downregulates and KCC2 matures.
Area of Science:
- Neuroscience
- Developmental Biology
- Cellular Physiology
Background:
- Chloride homeostasis is critical for inhibitory neurotransmission by GABA and glycine.
- Neuronal responses to GABA/glycine shift from depolarizing to hyperpolarizing during early postnatal development.
- The mechanisms underlying the initial depolarizing chloride gradient in developing neurons were previously unknown.
Purpose of the Study:
- To identify the chloride-loading transporter responsible for depolarizing GABA/glycine effects in early postnatal spherical bushy cells.
- To elucidate the developmental shift in chloride homeostasis and its impact on neuronal signaling.
Main Methods:
- Gramicidin-perforated patch-clamp recordings.
- Non-invasive chloride and calcium imaging.
- Immunohistochemistry.
Main Results:
- The 1Na(+):1K(+):2Cl(-) cotransporter 1 (NKCC1) was identified as the primary chloride loader in early postnatal (P3-5) spherical bushy cells.
- GABA/muscimol-induced calcium signaling was dependent on NKCC1 activity and chloride accumulation.
- Adult-like low intracellular chloride concentrations are established by the second postnatal week via NKCC1 downregulation and KCC2 activity.
Conclusions:
- NKCC1 is the major contributor to the depolarizing action of GABA/glycine during early development in the cochlear nucleus.
- The developmental shift in chloride gradient involves a coordinated downregulation of NKCC1 and upregulation of KCC2.
- This study clarifies a key mechanism in the maturation of inhibitory neurotransmission.
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