AII (Rod) Amacrine Cells Form a Network of Electrically Coupled Interneurons in the Mammalian Retina

Abstract

AII (rod) amacrine cells in the mammalian retina are reciprocally connected via gap junctions, but there is no physiological evidence that demonstrates a proposed function as electrical synapses. In whole-cell recordings from pairs of AII amacrine cells in a slice preparation of the rat retina, bidirectional, nonrectifying electrical coupling was observed in all pairs with overlapping dendritic trees (average conductance approximately 700 pS). Coupling displayed characteristics of a low-pass filter, with no evidence for amplification of spike-evoked electrical postsynaptic potentials by active conductances. Coincidence detection, as well as precise temporal synchronization of subthreshold membrane potential oscillations and TTX-sensitive spiking, was commonly observed. These results indicate a unique mode of operation and integrative capability of the network of AII amacrine cells.

Electrical synapses between AII amacrine cells in the retina: Function and modulation

“…The electrical coupling can mediate precise synchronization of subthreshold membrane potential fluctuations and spiking that could serve as a substrate for coincidence detection in visual processing (Veruki and Hartveit, 2002a). Using dynamic clamp electrophysiology, we have also demonstrated that the magnitude of the junctional conductance quantitatively predicts the observed coupling characteristics (Veruki et al, 2008).…”

“…Ultrastructural investigations have revealed that AII amacrine cells are postsynaptic to other types of amacrine cells throughout the IPL (Strettoi et al, 1992), but the specific identity of the presynaptic amacrine cells is not known, except that they are not other AII amacrine cells as there is no physiological evidence for chemical synapses between these cells (Veruki and Hartveit, 2002a). Strettoi et al (1992) found evidence that the presynaptic inputs corresponded to two morphologically distinct types, potentially corresponding to glycinergic and GABAergic amacrine cells.…”

“…Dual, whole-cell, voltage-clamp recordings between pairs of electrically coupled cells can be used to measure junctional conductances both at the single-channel level and at the macroscopic level (Galarreta and Hestrin, 1999;Gibson et al, 1999;Neyton and Trautmann, 1985). Apart from the indirect evidence from tracer coupling via chemical diffusion and visual receptive field measurements, the first direct evidence for functional electrical synapses between AII amacrine cells was obtained in our laboratory by dual patch-clamp recording from pairs of AII amacrine cells in rat retinal slices (Veruki and Hartveit, 2002a). The recordings demonstrated bidirectional, non-rectifying electrical coupling between these cells, with an average junctional conductance (G j ) of ~700 pS (range from about 300 to about 1500 pS).…”

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

“…In contrast, oscillations were not observed in wt AII amacrine cells (n ϭ 4) (Fig. 7 B, D) (Manookin et al, 2008;Murphy and Rieke, 2008;Münch et al, 2009) (but see Veruki and Hartveit, 2002). Figure 7B illustrates the relatively stable baseline of a wt AII amacrine cell.…”

Selective Ablation of a Class of Amacrine Cells Alters Spatial Processing in the Retina

“…This is smaller than the size of the extended surrounds and thus argues that individual NPY cells cannot, by themselves, be generating a large surround. Rather, the NPY cells may be forming a gap junction-coupled population or regulating one because several amacrine cell populations are known to couple (Hampson et al, 1992;Menger and Wässle, 2000;Li et al, 2002;Veruki and Hartveit, 2002).…”