Abstract
BackgroundThe impact of a given presynaptic neuron on the firing probability of the postsynaptic neuron critically depends on the number of functional release sites that connect the two neurons. One way of determining the average functional synaptic connectivity onto a postsynaptic neuron is to compare the amplitudes of action potential dependent spontaneous synaptic currents with the amplitude of the synaptic currents that are independent of action potentials ("minis"). With this method it has been found that average synaptic connectivity between glutamatergic CA3 and CA1 pyramidal cells increases from single connections in the neonatal rat, to multiple connections in the young adult rat. On the other hand, γ-aminobutyric acid (GABA)ergic interneurons form multiple connections onto CA1 pyramidal cells already in the neonatal rat, and the degree of multiple GABAergic connectivity is preserved into adulthood. In the present study, we have examined the development of glutamate and GABA connectivity onto GABAergic CA1 stratum radiatum interneurons in the hippocampal slice, and compared this to the connectivity onto CA1 pyramidal neurons.ResultsIn GABAergic interneurons in the CA1 stratum radiatum, irrespective of developmental stage, we found that the average amplitude of action potential dependent spontaneous AMPA receptor-mediated synaptic currents were of the same magnitude as the mini AMPA receptor mediated synaptic currents. This finding indicates that these GABAergic interneurons, in contrast to the CA1 pyramidal neurons, preserve single glutamate connectivity throughout development. For GABA connectivity, on the other hand, we found multiple functional synaptic connections onto the interneurons, as onto the pyramidal cells.ConclusionsThe results presented here confirm that glutamate and GABA synaptic connectivity develop very differently in the hippocampal CA1 region. Thus, whereas average GABA connectivity is multiple throughout the development, glutamate connectivity is unitary early in development. Our results further suggest that the development of glutamate synaptic connectivity differs markedly between pyramidal cells and GABAergic interneurons in stratum radiatum, such that a given presynaptic glutamatergic cell appears not allowed to increase its connectivity onto the postsynaptic stratum radiatum interneuron, as it may do onto the postsynaptic CA1 pyramidal cell.
Highlights
The impact of a given presynaptic neuron on the firing probability of the postsynaptic neuron critically depends on the number of functional release sites that connect the two neurons
Connectivity at CA3-CA1 pyramidal cell connections Previous studies have shown that the average magnitude of spontaneous AMPA EPSCs in the presence of TTX and in the absence of TTX is the same in developing (< P10) rat CA1 pyramidal cells [4,15]
In mature CA1 pyramidal cells the magnitude of action potential dependent AMPA sEPSCs is about two times larger than that of the AMPA mEPSCs [4]
Summary
The impact of a given presynaptic neuron on the firing probability of the postsynaptic neuron critically depends on the number of functional release sites that connect the two neurons. These findings indicate that newly formed glutamatergic connections are restricted to one release site, whereas such restriction is lacking for newly formed GABAergic connections These conclusions have been obtained by comparing the average amplitude of spontaneous action potential dependent postsynaptic currents (sPSCs), to that of action potential independent PSCs (miniature PSCs, mPSCs or “minis”). This amplitude ratio is referred to as multiplicity [4], and if each presynaptic cell forms at most one synaptic contact with the postsynaptic cell the multiplicity will be 1. Studies in the CA3 and CA1 region have shown good resemblance between electrophysiological and morphological estimates of connectivity [10,11,12]
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