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J Physiol Volume 585, Number 3, 881-895, December 15, 2007 DOI: 10.1113/jphysiol.2007.145003
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NEUROSCIENCE

Cajal–Retzius cells in the mouse neocortex receive two types of pre- and postsynaptically distinct GABAergic inputs

 Knut Kirmse1, Anton Dvorzhak1, Christian Henneberger1, Rosemarie Grantyn1 and Sergei Kirischuk1

1 Institute of Neurophysiology, Johannes-Mueller-Center of Physiology, Charité-University-Medicine Berlin, Tucholskystr. 2, 10117 Berlin, Germany

Cajal–Retzius (CR) cells are principal cells of layer I in the developing neocortex. They are able to generate action potentials, make synaptic contacts in layer I and receive excitatory GABAergic inputs before birth. Although CR cells participate in neuronal network activity in layer I, the properties of their synaptic inputs are not yet characterized. We recorded miniature (mIPSCs) and evoked (eIPSCs) postsynaptic currents using the whole-cell patch-clamp technique. Most of CR cells displayed two types of mIPSCs, namely those with fast (mIPSCF) and slow (mIPSCS) rise kinetics. The mIPSCF mean amplitude was significantly larger than that of mIPSCS, while their decay rates were not different. Peak-scaled non-stationary noise analysis revealed that mIPSCS and mIPSCF differed in their weighted single-channel conductance. In addition, zolpidem (100 nM), a modulator of {alpha}1 subunit-containing GABAA receptors, selectively affected mIPSCS suggesting that different postsynaptic GABAA receptors mediate mIPSCF and mIPSCS. eIPSCs also split into two populations with different rise kinetics. Fast eIPSCs (eIPSCF) displayed higher paired-pulse ratio (PPR) and lower GABA release probability than slowly rising eIPSCs (eIPSCS). As CGP55845, a GABAB receptor antagonist, eliminated the observed difference in PPR, the lower release probability at IPSCF connections probably reflects a stronger tonic GABAB receptor-mediated inhibition of IPSCF synapses. At low (0.1 Hz) stimulation frequency both inputs can effectively convert presynaptic action potentials into postsynaptic ones; however, only IPSCF connections reliably transfer the presynaptic activity patterns at higher stimulation rates. Thus, CR cells receive two GABAergic inputs, which differ in the quantal amplitude, the probability of GABA release and the frequency dependence of signal transfer.

(Received 13 September 2007; accepted after revision 23 October 2007; first published online 25 October 2007)
Corresponding author S. Kirischuk: Institute of Neurophysiology, Johannes-Mueller-Center of Physiology, Charité-University-Medicine Berlin, Tucholskystr. 2, 10117 Berlin, Germany. Email: sergei.kirischuk{at}charite.de

K. Kirmse and A. Dvorzhak contributed equally to this work. This paper has online supplemental material.






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