Time‐matched pre‐ and postsynaptic changes of GABAergic synaptic transmission in the developing mouse superior colliculus

Abstract

Developmental changes in the kinetics of GABAergic postsynaptic currents have been reported for various brain structures. However, it has remained unclear whether these modifications are matched by presynaptic changes. We addressed this question by analysing evoked IPSCs (eIPSCs) in mouse superior colliculus slices between postnatal day (P) 1 and 22. eIPSCs were elicited by electrical stimulation and measured in the whole-cell patch-clamp configuration. IPSCs were analysed using the binomial model of synaptic transmission. The readily releasable pool (RRP, N) was estimated from the cumulative eIPSC amplitude histograms during 50-Hz stimulation. Median delayed IPSC (dIPSC) amplitude was used as a quantal amplitude (q) estimate. The mean release probability (p) was determined as the mean eIPSC amplitude divided by the product of RRP and q. The experiments revealed that GABAergic synapses pass through two distinct periods of functional adjustment: (i) P1-3 (coincidental with the onset of glutamatergic spontaneous activity and a switch from depolarizing to hyperpolarizing GABA action) displayed a significant decrease of p, associated with an increase in the paired-pulse ratio (eIPSC(2)/eIPSC(1)); and (ii) P6-15 (the period before and shortly after eye opening) is characterized by a drastic reduction of IPSC duration. On the presynaptic side, it was accompanied by a down-regulation of asynchronous release in favour of stimulus-locked synchronous release. We conclude that postsynaptic modifications of GABAergic synaptic transmission in the superior colliculus (SC) are indeed accompanied by presynaptic changes, and this may guarantee the necessary efficacy of inhibition during the developmental reconstruction of the synaptic network in the SC.