Stereotypic Tracer Coupling Patterns of the Ganglion Cell Subtypes in the Mouse Retina

Abstract

Purpose:: To study the tracer coupling pattern of the various subtypes of ganglion cell (GC) in the mouse retina.

Methods:: Individual GC cell bodies were targeted in a flattened retinal-scleral preparation of the mouse (C57BL6) under infrared visualization. The tracer Neurobiotin was iontophoresed intracellularly into the GCs using a sinusoidal current for 15 minutes. The morphology and coupling pattern of injected GCs were revealed by standard peroxidase histology.

Results:: Over 200 GC injections provided a sizeable database for examining the coupling pattern of most, if not all, GC subtypes in the mouse retina based on the classification scheme of Sun et al. (2002). We found that C1 and D1 GCs were uncoupled, whereas most other GC subtypes displayed one of six stereotypic coupling patterns: (1) the A2_O (OFF alpha) and B3_O GCs showed both homologous coupling to GC neighbors and heterologous coupling to amacrine cells (ACs) with somata located in the INL; (2) the B1, C2_O, C4 and C6 GC subtype displayed heterologous coupling to ACs with somata located in the INL; (3) the A1, A2_I (ON alpha), B3_I, C2_I and C3 (melanopsin-expressing) GC subtypes displayed heterologous coupling to ACs with somata displaced to the GCL; (4) the B4 and C5 subtype of GCs showed heterologous coupling to ACs in both the INL and the GCL; (5) the D2 (ON-OFF direction selective) GCs showed only homologous coupling to their GC neighbors and; (6) the B2 GC subtype showed homologous coupling to other B2 cells and heterologous coupling to ACs in both the INL and the GCL. In addition, the coupling patterns of a few other GC subtypes not characterized by Sun et al. (2002) were studied. Despite the variability in GC coupling, some general tendencies were found: (a) GCs that stratified in the ON sublamina of the IPL were coupled to ACs with somata displaced to the GCL, whereas those stratifying in the OFF sublamina were coupled to ACs with cell bodies in the INL and ; (b) homologous coupling of GC neighbors occurred only for subtypes that stratified in the OFF sublamina (OFF and ON-OFF cells).

Conclusions:: Our data indicate that each GC subtype displays a stereotypic coupling pattern, which in combination with the soma/dendritic morphology and dendritic stratification can be used for unequivocal cell identification. In addition, the prevalence of GC coupling suggests that electrical synaptic transmission via gap junctions plays a major role in shaping the light-evoked GC responses in the mouse retina.

Keywords: ganglion cells • gap junctions/coupling • retinal connections, networks, circuitry