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The Journal of Neuroscience, October 3, 2007, 27(40):10860-10869; doi:10.1523/JNEUROSCI.2744-07.2007

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Cellular/Molecular
Sequential Postsynaptic Maturation Governs the Temporal Order of GABAergic and Glutamatergic Synaptogenesis in Rat Embryonic Cultures

Lunbin Deng,^1,2 * Jun Yao,^1,2 * Cheng Fang,^1,2,3 Ning Dong,^1,2 Bernhard Luscher,^1,2,3,4 and Gong Chen^1,2

¹Department of Biology, ²The Huck Institutes of Life Sciences, ³Department of Biochemistry and Molecular Biology, and ⁴Department of Psychiatry, Pennsylvania State University, University Park, Pennsylvania 16802

Correspondence should be addressed to Dr. Gong Chen, Department of Biology, 201 Life Sciences Building, The Huck Institutes of Life Sciences, Pennsylvania State University, University Park, PA 16802. Email: gongchen{at}psu.edu

Sequential formation of GABAergic and glutamatergic synapses is thought to be crucial for constructing the stereotypic neural networks during brain development. However, why GABAergic synapses are formed earlier than glutamatergic synapses in the developing brain is not well understood. We used electrophysiology and fluorescence imaging to study GABAergic and glutamatergic synaptogenesis in embryonic hypothalamic cultures, which contain 40% GABAergic and 60% glutamatergic neurons. The newly dissociated embryonic hypothalamic neurons contained a significant pool of functional GABA_A receptors but a very low level of glutamate receptors. Within the first week of culture, the time course of GABAergic synaptogenesis in embryonic neurons coincided with that of presynaptic vesicle cycling, but both measurements lagged behind the detection of functional GABA_A receptors. Remarkably, the GABA_A receptors of newly dissociated embryonic neurons can be rapidly clustered into postsynaptic apparatus and generate functional synaptic currents within 4–6 h when cocultured with mature neurons. Consistent with earlier expression of GABA_A receptors in immature neurons, synaptic GABAergic events were always detected before the onset of glutamatergic events in both purely embryonic and heterochronic cultures. Interestingly, overexpression of glutamate receptors in embryonic neurons not only increased whole-cell glutamate currents but also significantly increased the frequency of excitatory synaptic events. We conclude that the sequential formation of GABAergic and glutamatergic synapses in immature neurons is likely governed by a sequential expression of GABA_A and glutamate receptors during neuronal development.

Key words: GABAergic synapse; GABA_A receptor; glutamatergic synapse; presynaptic; postsynaptic; culture; hypothalamus

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Received Feb. 10, 2007; revised Aug. 16, 2007; accepted Aug. 16, 2007.

Correspondence should be addressed to Dr. Gong Chen, Department of Biology, 201 Life Sciences Building, The Huck Institutes of Life Sciences, Pennsylvania State University, University Park, PA 16802. Email: gongchen{at}psu.edu

This article has been cited by other articles:

				C. M. Root, N. A. Velazquez-Ulloa, G. C. Monsalve, E. Minakova, and N. C. Spitzer Embryonically Expressed GABA and Glutamate Drive Electrical Activity Regulating Neurotransmitter Specification J. Neurosci., April 30, 2008; 28(18): 4777 - 4784. [Abstract] [Full Text] [PDF]

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