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

Abstract

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.

Signal transmission at invaginating cone photoreceptor synaptic contacts following deletion of the presynaptic cytomatrix protein Bassoon in mouse retina

“…The differences in synaptic activity and persistent inward currents between Bsn wt and Bsn ΔEx4/5 mice were clearly evident (Figure C,D). As shown previously, tonic activity at the synapse between cone photoreceptors and horizontal cells was entirely abolished by extracellular application of the AMPA/kainate receptor antagonist CNQX …”

“…As shown previously, tonic activity at the synapse between cone photoreceptors and horizontal cells was entirely abolished by extracellular application of the AMPA/kainate receptor antagonist CNQX. 26 Next, we measured synaptic charge transfer as an indicator of tonic synaptic vesicle release during 5-second intervals of continuous recording. In Bsn wt retina, significantly more charge was transferred to postsynaptic horizontal cells during the 5-second intervals ( Figure 1E,F).…”

Mechanisms, pools, and sites of spontaneous vesicle release at synapses of rod and cone photoreceptors

“…In control conditions, mEPSCs in this HC averaged 4.03 pA in amplitude. While smaller than mEPSCs found at many conventional synapses, they were similar in amplitude to mEPSCs reported previously in salamander and mammalian HCs (Maple et al ., ; Cadetti et al ., ; DeVries et al ., ; Feigenspan & Babai, ). Application of Cd 2+ plus dantrolene slightly reduced the mean amplitude of mEPSCs to 3.33 pA (Fig.…”

“…Postsynaptic properties of horizontal cell (HC) miniature excitatory post-synaptic currents (mEPSCs) have been characterized in a number of species (Maple et al, 1994;Hirasawa et al, 2001;Cadetti et al, 2005;Feigenspan & Babai, 2015), but there has been limited study of the presynaptic mechanisms regulating spontaneous release from photoreceptors. Because photoreceptors maintain relatively depolarized membrane potentials allowing continuous Ca 2+ channel activity, we considered that perhaps all spontaneous mEPSCs from photoreceptors might arise from Ca 2+ -dependent release.…”

Horizontal slices of mouse retina expose horizontal cells and their properties (Commentary on Feigenspan & Babai)

“…There have therefore been few published recordings from mouse HCs. To visualize HC somata and keep their processes intact, Feigenspan & Babai () developed a preparation in which they slice the retina horizontally along a plane parallel to the retinal surface. To do so, they embed small pieces of mouse retina in a block of low melting point agarose and then slice the retina into thin sections with a vibratome.…”