Response attenuation during coincident afferent excitatory inputs

The linearity of the synaptic summation of two unitary excitatory synaptic events was investigated during whole cell recordings from retinal target neurons in an eye-attached isolated brain stem preparation. Pairs of unitary excitatory postsynaptic potentials (EPSPs) were evoked by bipolar stimulation electrodes that were directed to two distinct foci on the retinal surface based on the visual receptive field boundaries. The interval between stimulation of each retinal site was incremented by 0.5-1 ms to quantify the time course of nonlinear summation using an exponential fit. Response facilitation was never observed; however, the coincident arrival of synaptic inputs caused a response attenuation in 26 of the 37 pairs studied. Twelve of the 26 pairs had time constants of their attenuation that were similar to the time constants of the decaying phases of the first EPSPs of each pair. This suggests that the attenuation of these 12 pairs may be entirely due to voltage-dependent mechanisms, such as a reduction in driving force or a change of the activity of voltage-sensitive channels. On the other hand, the 14 other pairs had their time constant of attenuation shorter than the time constants of the decaying phase of the first EPSP. In fact, the attenuation time constants were often closer to the time constants of the decaying phases of the first excitatory postsynaptic currents of each pair. This finding suggests that the attenuation of these 14 pairs involve a shunting mechanism due to the opening of synaptic channels. The presence of this conductance-dependent mechanism is supported by the finding of asymmetric effects on the time course of attenuation when the stimulation sequence was reversed. These results are discussed in terms of the processing by neurons of coincident excitatory inputs onto spatially distinct points of their dendritic trees.