Dendrodendritic Electrical Synapses between Mammalian Retinal Ganglion Cells

Abstract

Electrical synapses between ␣-type ganglion cells were detected using combined techniques of dual patch-clamp recordings, intracellular labeling, electron microscopy, and channel subunit connexin immunocytochemistry in the albino rat retina. After intracellular injection of Neurobiotin into ␣-cells of inner (ON-center) and outer (OFF-center) ramifying types, measurement of tracer coupling resulted in a preferentially homologous occurrence among cells of the same morphological type (n ϭ 19 of 24). In high-voltage as well as conventional electron microscopic analysis, direct dendrodendritic gap junctions (average size, 0.86 m long) were present in contact sites between tracer-coupled ␣-cells. In simultaneous dual whole-cell recordings from pairs of neighboring ␣-cells, these cells generated TTX-sensitive sustained spiking against extrinsic current injection, and bidirectional electrical synapses (maximum coupling coefficient, 0.32) with symmetrical junction conductance (average, 1.35 nS) were observed in pairs with cells of the same morphological type. Precise temporal synchronization of spike activity (average time delay, 2.7 msec) was detected when depolarizing currents were simultaneously injected into the pairs. To address whether physiologically identified electrical synapses constitute gap junctional connectivity between cell pairs, identified neuronal connexin36 immunoreactivity was undertaken in Lucifer yellow-labeled cell pairs after patch-clamp recordings. All ␣-cells expressed connexin36, and confocal laser-scanning imaging demonstrated that connexin36 is primarily located at dendritic crossings between electrically coupled cells (seven sites in a pair, on average). These results give conclusive evidence for electrical synapses via dendrodendritic gap junctions involving connexin36 in ␣ retinal ganglion cells of the same physiological type.

The Structure of Multi-Neuron Firing Patterns in Primate Retina

“…2 B). This synchronized firing in the absence of time-varying stimulation (also known as "noise correlations") resembles observations in other species and indicates functional connectivity attributable to common inputs and/or reciprocal connections in the retina (Arnett, 1978;Johnsen and Levine, 1983;Mastronarde, 1983b;Meister et al, 1995;DeVries and Baylor, 1997;Brivanlou et al, 1998;Hidaka et al, 2004). Anticorrelation between ON and OFF parasol cells was also observed (data not shown) (Mastronarde, 1983a), but subsequent analysis will be restricted to cells of the same type.…”

“…1 A). Conversely, several lines of evidence indicate that synchronized firing can originate from pairwise, adjacent interactions: gap junction coupling between adjacent RGCs, electrical coupling of neighboring RGCs via an intermediate amacrine cell, or common synaptic inputs from bipolar or amacrine cells to neighboring RGCs (Mastronarde, 1983b;Dacey and Brace, 1992;Jacoby et al, 1996;Brivanlou et al, 1998;Hu and Bloomfield, 2003;Hidaka et al, 2004;Schubert et al, 2005;Volgyi et al, 2005). Thus, interactions among multiple RGCs over large spatial scales may simply reflect the combined effect of pairwise, adjacent interactions (see Fig.…”

Dopaminergic modulation of tracer coupling in a ganglion-amacrine cell network

“…The presence of direct gap junctions between α ganglion cells has been demonstrated in rat (Hidaka et al, 2002(Hidaka et al, , 2004. The rabbit OFF α cells appear similar, as the existence of direct ganglion-ganglion gap junctions is suggested by the presence of short latency correlated spikes between pairs of OFF α ganglion cells (DeVries, 1999;Hu & Bloomfield, 2003), the occasional finding in this study of coupled ganglion cells brighter than any coupled amacrine cell, and the existence of a diffusion coefficient specific for direct ganglion-ganglion gap junctions that can be differentially modulated.…”

“…The evidence comes from demonstrations of correlated spiking (Mastronarde, 1983a(Mastronarde, , 1983bMeister et al, 1995;DeVries, 1999), tracer coupling (Vaney, 1991;Dacey & Brace, 1992;, 1999, light microscopy (Hidaka et al, 2002(Hidaka et al, , 2004Schubert et al, 2005aSchubert et al, , 2005b, and electron microscopy (Jacoby et al, 1996). Some ganglion cells are coupled to their neighbors of the same type, some are coupled to amacrine cells, and some are coupled to both.…”

“…In rabbit retinas, the presence of short latencies in the peak of spike cross-correlograms of OFF α ganglion cells, which are tracer-coupled, but not in ON α ganglion cells, which are not, suggest that OFF α ganglion cells are directly coupled to one another (DeVries, 1999;Hu & Bloomfield, 2003). Moreover, there is evidence from rat retina that there are direct gap junctions between α ganglion cells (Hidaka et al, 2002(Hidaka et al, , 2004. The OFF α ganglion cell connexin appears to be connexin36 in rats (Hidaka et al, 2002), but the identity of the connexin is controversial in mice (Schubert et al, 2005a;Völgyi et al, 2005).…”