Spontaneous action potential activity and synaptic currents in the embryonic turtle cerebral cortex

Abstract

We used loose-patch and whole-cell recording techniques to study the development of spontaneous action potential activity and spontaneous excitatory and inhibitory synaptic currents in embryonic neurons in the cerebral hemispheres of turtles. Sporadic action potential activity appeared early in development at stage 17, soon after morphologically identifiable pyramidal and nonpyramidal neurons were first observed in the cortex. As the cortical plate matured in midembryonic stages, action potential activity became more regular and fell into one of two distinct patterns, tonic and intermittent high-frequency firing. Spontaneous excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs) appeared at developmental stages 18 and 20, respectively, after action potential activity was established. EPSCs and IPSCs exhibited characteristic ionic dependence and pharmacology throughout development. EPSCs reversed in direction at the equilibrium potential for cations and were sensitive to 6-cyano-7-nitroquinoxaline-2,3-dione, an antagonist of the non-NMDA type of glutamate receptor. IPSCs reversed at the equilibrium potential for chloride and were sensitive to bicuculline methiodide, a GABAA receptor antagonist. Spontaneous synaptic currents differed in their time course of development and in waveform parameters. Spontaneous synaptic currents differed in their time course of development and in waveform parameters. Spontaneous EPSCs appeared at stage 18 and increased progressively in frequency, from 0.2 +/- 0.1 Hz at stage 20 to 3.2 +/- 2.0 Hz at stage 26 (hatching), while spontaneous IPSCs appeared at stage 20 and surpassed EPSCs in frequency, increasing to 7.1 +/- 1.6 Hz at stage 26. EPSCs exhibited stable amplitudes during development, with a mean conductance of 126 +/- 20 pS at stage 26, while IPSCs increased in mean amplitude, from 180 +/- 12 pS at stage 18 to 260 +/- 44 pS at stage 26. The rise time to peak conductance of both types of synaptic currents increased with developmental time, for EPSCs increasing from 1.5 +/- 0.5 msec at stage 20 to 2.7 +/- 0.6 msec at stage 26 and for IPSCs increasing from 2.9 +/- 0.2 msec at stage 18 to 6.2 +/- 0.8 msec at stage 26. While the decay time constants increased for EPSCs, from 3.9 +/- 1.2 msec at stage 20 to 8.7 +/- 2.3 msec at stage 26, decay time constants for IPSCs showed a decreasing trend from 24.0 +/- 5.2 msec at stage 18 to 18.4 +/- 5.3 msec at stage 26. The excitatory and inhibitory synaptic currents were sensitive to the sodium channel blocker TTX and were thus dependent, in part, on spontaneous action potential activity.(ABSTRACT TRUNCATED AT 400 WORDS)

Temporal coherency between receptor expression, neural activity and AP-1-dependent transcription regulatesDrosophilamotoneuron dendrite development

“…9). Similarly, Xenopus optic tectal and turtle cortical neurons receive glutamatergic and GABAergic inputs as soon as the first dendrites are formed (Wu et al, 1996;Blanton and Kriegstein, 1991). In vertebrates, early synaptic inputs and neurotransmitters play essential roles in dendrite development (Bestman et al, 2008).…”

Synchronized Paroxysmal Activity in the Developing Thalamocortical Network Mediated by Corticothalamic Projections and “Silent” Synapses

“…We observed paroxysmal activity in the cortex as early as postnatal day 2, at a stage when only layers V and V I have formed, and synaptogenesis is only beginning. Spontaneous synaptic currents have been recorded in neocortical slices in very early postnatal stages (Blanton and Kriegstein 1991;K im et al, 1995), but it has generally been assumed that synaptic connectivity at these stages is incomplete or insufficiently dense to maintain synchronized network or paroxysmal activity. By suppressing inhibition and increasing transmitter release, we have shown that very early postnatal cortical circuitry can indeed support the existence of synchronized activity, mainly through activation of silent synapses.…”

Slow Kinetics of Miniature IPSCs during Early Postnatal Development in Granule Cells of the Dentate Gyrus

“…Previous studies have shown that GABAergic neurons are born prenatally (Schlessinger et al, 1978;Amaral and Kurz, 1985;Lubbers et al, 1985), and by the end of the first postnatal week, they make synaptic contacts on granule cell dendrites as well as somata (Lubbers and Frotscher, 1988;Ribak, 1988, 1990). Although GABAergic responses have been shown to occur in developing hippocampal and cortical pyramidal cells (Mueller et al, 1984;Kriegstein et al, 1987;Janigro and Schwartzkroin, 1988;Ben-Ari et al, 1989;Gaiarsa et al, 1990;Blanton and Kriegstein, 1991;Luhmann and Prince, 1991;Zhang et al, 1991;Hosokawa et al, 1994;Fleidervish and Gutnick, 1995), the functional properties of the early GABA A receptormediated synaptic transmission in the late-developing dentate granule cells are not well understood. The data presented here demonstrate that the overwhelming majority of dentate granule cells of the early postnatal rat possess functionally active GABAergic synaptic inputs [interestingly, no glutamatergic synaptic events can be observed at this time in granule cells (our unpublished observations)], similar to CA1 and CA3 pyramidal cells (Ben-Ari et al, 1989;Hosokawa et al, 1994;Gaiarsa et al, 1995).…”