Functional properties of spontaneous excitatory currents and encoding of light/dark transitions in horizontal cells of the mouse retina

As all visual information is represented in the spatio-temporal dynamics of transmitter release from photoreceptors and the combined postsynaptic responses of second-order neurons, appropriate synaptic transfer functions are fundamental for a meaningful perception of the visual world. The functional contribution of horizontal cells to gain control and organization of bipolar and ganglion cell receptive fields can only be evaluated with an in-depth understanding of signal processing in horizontal cells. Therefore, a horizontal slice preparation of the mouse retina was established to record from horizontal cell bodies with their dendritic fields intact and receiving functional synaptic input from cone photoreceptors. Horizontal cell bodies showed spontaneous excitatory currents (spEPSCs) of monophasic and more complex multi-peak waveforms. spEPSCs were induced by quantal release of glutamate from presynaptic cones with a unitary amplitude of 3 pA. Non-stationary noise analysis revealed that spEPSCs with a monoexponential decay were mediated by 7–8 glutamate receptors with a single-channel amplitude of 1.55 pA. Responses to photopic full-field illumination were characterized by reduction of a tonic inward current or hyperpolarization, inhibition of spEPSCs, followed by a fast and transient inward current at light offset. The response to periodic dark/light transitions of different frequencies was dependent on the adaptational status of the cell with a limiting frequency of 10 Hz. Both on and off components of the light response were mediated by AMPA and kainate receptors. Detailed analysis of horizontal cell synaptic physiology is a prerequisite for understanding signal coding and processing at the photoreceptor ribbon synapse.