Selective synaptic connections in the retinal pathway for night vision

Abstract

The mammalian retina encodes visual information in dim light using rod photoreceptors and a specialized circuit: rods→rod bipolar cells→AII amacrine cell. The AII amacrine cell uses sign-conserving electrical synapses to modulate ON cone bipolar cell terminals and sign-inverting chemical (glycinergic) synapses to modulate OFF cone cell bipolar terminals; these ON and OFF cone bipolar terminals then drive the output neurons, retinal ganglion cells (RGCs), following light increments and decrements, respectively. The AII amacrine cell also makes direct glycinergic synapses with certain RGCs, but it is not well established how many types receive this direct AII input. Here, we investigated functional AII amacrine→RGC synaptic connections in the retina of the guinea pig (Cavia porcellus) by recording inhibitory currents from RGCs in the presence of ionotropic glutamate receptor (iGluR) antagonists. This condition isolates a specific pathway through the AII amacrine cell that does not require iGluRs: cone→ON cone bipolar cell→AII amacrine cell→RGC. These recordings show that AII amacrine cells make direct synapses with OFF Alpha, OFF Delta and a smaller OFF transient RGC type that co-stratifies with OFF Alpha cells. However, AII amacrine cells avoid making synapses with numerous RGC types that co-stratify with the connected RGCs. Selective AII connections ensure that a privileged minority of RGC types receives direct input from the night-vision pathway, independent from OFF bipolar cell activity. Furthermore, these results illustrate the specificity of retinal connections, which cannot be predicted solely by co-stratification of dendrites and axons within the inner plexiform layer.

Electrical Coupling of Heterotypic Ganglion Cells in the Mammalian Retina

“…In addition, the primary dendrites of these cells stratified just beneath the dendritic plexus of ON starburst amacrine cells. These features were highly suggestive of the sON ␣-RGCs in the guinea pig retina (Demb et al, 1999;Manookin et al, 2008;Beaudoin et al, 2019). The putative sON ␣-RGC cell body locations matched the recording locations of the large sON type derived from the electrical signals of the cells on the multielectrode array ( Fig.…”

ERG Responses in Mice with Deletion of the Synaptic Ribbon Component RIBEYE

“…The lack of difference between the mice groups under photopic conditions may reflect the smaller amplitudes of responses elicited following light adaptation and the differential contributions of rod and cone photoreceptor synaptic signaling that also include OFF responses. 11 , 46 – 49 The OFF responses in the outer retina originate at some distance from ribbon release sites and thus might be less dependent on the presence of the synaptic ribbon. Homeostatic mechanisms in the cone pathway, as have been observed in the inner ear (e.g., increased postsynaptic density sizes), might also contribute to the lack of defect in the photopic ERG.…”

The ARMS2 A69S Polymorphism Is Associated with Delayed Rod-Mediated Dark Adaptation in Eyes at Risk for Incident Age-Related Macular Degeneration

“…Further, the methods just mentioned assay specific neurophysiologic mechanisms of the night vision system, including rod sensitivity, lateral interaction with cones, and rod signal convergence onto cone-driven pathways. [59][60][61] Genes that influence these other visual functions in AMD will be sought in future studies.…”