Synchronous inhibitory synaptic inputs to layer II/III pyramidal neurons in the murine barrel cortex

Abstract

The barrel cortex exhibits obvious columnar organization. Although GABAergic inhibition plays a critical role in regulating neural excitation in response to mechanical stimuli applied to whiskers, the profiles of synchronous events for inhibitory synaptic transmission in intracolumnar and transcolumnar pyramidal neurons remain unknown. To explore a functional mechanism of synchronous inhibition of pyramidal neurons, we performed paired whole-cell patch-clamp recordings and recorded spontaneous inhibitory postsynaptic currents (sIPSCs) from layer II/III pyramidal neurons. A cross-correlogram of sIPSCs (1 ms bin) was used to detect synchronous sIPSCs. Synchronous neuron pairs were defined as those whose peak number of sIPSCs between −3 and 3 ms exceeded the mean + 2 SD of the number of sIPSCs in the period of −50 to 50 ms minus the number in that of −3 to 3 ms period. In the recording of pyramidal neurons located in the same column (intracolumn), 61.5% of neuron pairs were classified as synchronous neuron pairs, while 52.6% of pyramidal neuron pairs in adjacent columns (transcolumn) were defined as synchronous neuron pairs. The amplitude of synchronous sIPSCs was comparable to that of asynchronous sIPSCs in asynchronous neuron pairs, whereas that of synchronous sIPSCs was larger than that of asynchronous sIPSCs in synchronous neuron pairs. Synchronicity of sIPSCs did not depend on the distance of neuron pairs. These results suggest that layer II/III pyramidal neurons receive synchronous inhibitory synaptic inputs generated by a certain type of GABAergic interneuron that induces large IPSCs in pyramidal neurons, likely to be fast-spiking cells.