GABAB receptor-mediated presynaptic inhibition reverses inter-columnar covariability of synaptic actions by intracortical axons in the rat barrel cortex

Simultaneous recordings from two L3 PCs in the stimulated (HC) and adjacent column (AC) showed that in response to paired stimulations of superficial L3, the L3 PC in HC displayed prominent PPD of EPSCs, whereas the L3 PC in AC displayed little PPD. The correlation between the pairs of 1st EPSCs was positive and that between the pairs of 2nd EPSCs was negative, indicating positive and negative covariabilities, respectively, of intracortical actions between two adjacent columns. Intracortical axons originating from pyramidal cells in layer 3 of the rat somatosensory cortex are shared between adjacent columns, and receive the presynaptic inhibition that is mediated by the GABAB receptor. Synaptic actions by intracortical axons of single layer 3 pyramidal cells covary between the two adjacent columns in response to stimulation of layer 3 of either column. We examined whether GABAB receptor‐mediated presynaptic inhibition affects the covariability of synaptic actions by intracortical axons between adjacent columns in slice preparations of the rat barrel cortex. Paired stimulations of superficial layer 3 evoked first and second excitatory postsynaptic currents (EPSCs) of varying amplitudes, yielding varying paired‐pulse depression of EPSCs in layer 3 pyramidal cells that were located in the stimulated column, but not in its adjacent column. The amplitude of the second EPSC was inversely proportional to that of the first EPSC in layer 3 pyramidal cells in the stimulated column, yielding a negative correlation coefficient between the first and second EPSCs. Baclofen and CGP55845 attenuated paired‐pulse depression and abolished the inverse relationship. Simultaneous recordings from two layer 3 pyramidal cells in the stimulated and adjacent columns revealed a positive correlation between the paired first EPSC amplitudes and a negative correlation between the paired second EPSC amplitudes, which, respectively, indicate the positive and negative covariability of synaptic actions by intracortical axons between the two adjacent columns. These results suggest that GABAB receptor‐mediated presynaptic inhibition can reverse the positive covariability of inter‐columnar synaptic actions, which may serve as a basis for inter‐columnar desynchronisation.