Due to the wealth and the variety of the observed gap junc-tions,Vaney (1994)suggested that the vertebrate retina should be viewed as a stack of planar neuronal arrays with vertical links. In that context, the present review detailed how each retinal cell type forms electrically coupled planar mosaics, how coupled ar-rays are interlaced with each other and how the electrically cou-pled neuronal networks act upon vertical signal processing throughout the retina. This article has also summarized results from various vertebrates, and has aimed to reveal evolutionary trends. However, a comprehensive phylogenetic comparison was not possible, since the available dataset was rather incomplete:(i) the early electrophysiological studies were primarily carried out in lower vertebrates (due to technical difficulties); (ii) recent ad-vances in molecular biology provided the opportunity to identify connexins but mainly popular mammalian models were studied;
(iii) in this dataset, lower vertebrates are represented by only a few model species. Nevertheless, we can still point out a number of general features and trends followed by most examined verte-brate species.
First, the cell types that contact each other via electrical syn-apses are conserved throughout vertebrate evolution. Thus, rod-to-rod, rod-to-cone, cone-to-cone, horizontal-to-horizontal, bipolar-to-bipolar, amacrine-to-amacrine, amacrine-to-ganglion and ganglion-to-ganglion cell contacts are ubiquitous across all verte-brate retinas. The only (known) exception is the mammalian pri-mary rod pathway that incorporates two gap junctions (AIIeAII and AIIeON cone bipolar cell), which are consequently uniquely mammalian features. Apart from the latter AII-bipolar cell contact, no other amacrine-to-bipolar cell gap junction has been discovered in vertebrates, not even in mammals.
Second, gap junctions located in particular retinal circuits play largely the same roles in retinal information processing in all examined vertebrates, again, with the sole exception of the mam-malian specific rod pathway. Gap junctions in this latter pathway process feed forward signaling, which is a unique feature in the retina and very rare within the entire central nervous system. Be-sides mammalian rod pathways, however, the functions of the rest of the retinal gap junctions are peculiarly similar in all vertebrates. It is clear, for example that all vertebrate horizontal cells utilize con-nexin subunits (Cx50, Cx57 or their orthologs) that possess high unitary conductance and/or are capable of forming extensive pla-ques to provide extremely high transmembrane conductance (in the nSemS range) for intercellular signaling. In contrast, other retinal cell types form gap junctions with moderate (1000e2000 pS) or low conductances (<800 pS), including most neurons in the inner retina and photoreceptors in the outer retina, respectively. These latter contacts are composed of Cx36, Cx45 subunits, some of which show about the lowest unitary conductances. This obvious difference in gap junctional conductance between horizontal cells and other retinal cell types corresponds nicely with the observed difference in the diameters of tracer-coupled arrays of these reti-nal neurons. Whereas horizontal cells display extended syncytia in the outer retina, most inner retinal neurons and photoreceptors form rather constrained tracer-coupled arrays restricted to direct neighbors. One exception from this tendency though is the exten-ded coupling of so-called wide-field amacrine cells in the inner retina of all examined species. These cells often form extended lattices involving up to a few hundred amacrine cells in one tracer coupled array. However, connexin makeup and conductance levels of the underlying gap junctions are yet to be determined. Generally speaking, apart from hard wiring provided by the fast synaptic transmitters and soft wiring contributed primarily by aminergic, NOergic and peptidergic systems, electrical coupling may subserve
as the skeleton of lateral processing, determining important func-tions such as signal averaging and synchronization.
Third, the modulation of gap junctions formed by retinal neurons follows the same patterns, including the dopamine/D1 mediated reduction or D2mediated increase in gap junction conductance. In addition, some contacts, including those between horizontal cells, are modulated by changes in extracellular NO concentrations as well. Since the production and release of both dopamine and NO are under the control of light adaptation levels and/or circadian rhyth-micity, the conductance of various gap junctions are dynamically modulated. Apart from the effects of the ambient background light level, conductance of most gap junctions is sensitive to changes in pH and/or the intracellular concentration of Caþþ. Therefore, the functioning of gap junctions is controlled by the changes in the environment as well as the internal condition of the living system.
Fourth, the observed species’ differences in the connexin makeup of gap junctions are also minor. The highest variety is found among horizontal-to-horizontal cell contacts of vertebrates but this diversity is largely due to the numerous ortholog connexins used in horizontal cell lattices of various species. It is important to point out that one canfind many different connexins in the inner retina as well (Cx36, Cx45, Cx30.2 etc.), although this variety is likely due to the diversity of inner retinal cell types rather than divergent evolution. In fact, we found that the genetical distances among connexin paralogs are larger than those of the orthologs expressed in the same circuit of various vertebrates (Fig. 1). This is in line with thefinding ofEastman et al. (2006)who detected high sequence similarity of even the most variable C-terminal tail of the
>400 myr separated zebrafish and mammalian ortholog Cx se-quences, even though many paralogs were not close relatives.
Based on theirfindings, they suggested that a stronger selection occurred for C-terminus function in orthologs, as opposed to a relaxed selection on one of the paralogs following gene duplica-tions. Such relaxed selection likely allowed divergence of connexins and facilitated novel gene evolution. The close homology of orthologs but not paralogs supports the view that the function determines the utilized connexin (Cruciani and Mikalsen, 2006) and not the phylogenetic group (DeBoer and Van der Heyden, 2005). In fact, connexin orthologs display very similar biophysical and physiological properties; in consequence, the fact that they are utilized in similar contacts further reinforces the equivalent roles they play in the vision of various vertebrates. In summary, all reviewed aspects of vertebrate retinal gap junctions appear remarkably conservative. This implies that the architecture of the electrically coupled neuronal networks in the retina is as old as the retinal circuitry itself. It seems fair to conclude, therefore, that gap junctions have been an integral component of retinal circuitry from the inception of vertebrate eye formation.
Acknowledgments
This study was supported by SROP-4.2.2/B-10/1-2010-0029 and SROP-4.2.1.B-10/2/KONV-2010-0002, and the Hungarian Academy by awarding OTKA K100144 to R.G and OTKA K105247 and the János Bolyai Fellowship to B.V. Authors are indebted to Dr. Paul Witkovsky with his style and grammar corrections and for pro-fessional advices.
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