Active Roles of Electrically Coupled Bipolar Cell Network in the Adult Retina

Arai, Iwao; Tanaka, Masashi; Tachibana, Makoto

doi:10.1523/jneurosci.1590-10.2010

Cited by 36 publications

(51 citation statements)

References 71 publications

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“…However, the experiment in Figure 3B–D cannot rule out additional contributions from direct coupling between bipolar cells (Arai et al, 2010; Cohen and Sterling, 1990) or coupling between bipolar cells and other amacrine cell types (Lee et al, 2015). …”

Section: Resultsmentioning

confidence: 94%

Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

Kuo

Schwartz

Rieke

2016

Neuron

102

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Summary Electrical and chemical synapses coexist in circuits throughout the CNS. Yet, it is not well understood how electrical and chemical synaptic transmission interact to determine the functional output of networks endowed with both types of synapse. We found that release of glutamate from bipolar cells onto retinal ganglion cells (RGCs) was strongly shaped by gap junction-mediated electrical coupling within the bipolar cell network of the mouse retina. Specifically, electrical synapses spread signals laterally between bipolar cells, and this lateral spread contributed to a nonlinear enhancement of bipolar cell output to visual stimuli presented closely in space and time. Our findings thus (1) highlight how electrical and chemical transmission can work in concert to influence network output, and (2) reveal a previously unappreciated circuit mechanism that increases RGC sensitivity to spatiotemporally correlated input, such as that produced by motion.

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Section: Resultsmentioning

confidence: 94%

Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

Kuo

Schwartz

Rieke

2016

Neuron

102

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“…Previously, gap junctions in teleost species were found and extensively studied in three primary locations – LMCE/M-cell mixed synapses (Tuttle et al, 1986; Nakajima et al, 1987; Lin and Faber, 1988; Pereda et al, 2003), at electrosensory and electromotor neurons of weakly electric fish (Bennett et al, 1963; Pappas and Bennett, 1966; Bennett et al, 1967a; Kriebel et al, 1969; Payton et al, 1969; Maler et al, 1981; Carr et al, 1986; Mathieson et al, 1987), and in retina (Witkovsky et al, 1974; Naka and Christensen, 1981; Kurz-Isler and Wolburg, 1986; Marc et al, 1988; Wolburg and Rohlmann, 1995; O'Brien et al, 2004; Kothmann et al, 2007; Arai et al, 2010), the latter of which has the greatest variety of synaptic configurations involving gap junctions, and which we do not address here. This prior focus of studies on a few CNS regions potentially left the impression that gap junctions are otherwise rare in the teleost CNS.…”

Section: Discussionmentioning

confidence: 99%

Heterotypic gap junctions at glutamatergic mixed synapses are abundant in goldfish brain

et al. 2015

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Gap junctions provide for direct intercellular electrical and metabolic coupling. The abundance of gap junctions at “large myelinated club ending” synapses on Mauthner cells of the teleost brain provided a convenient model to correlate anatomical and physiological properties of electrical synapses. There, presynaptic action potentials were found to evoke short-latency electrical “pre-potentials” immediately preceding their accompanying glutamate-induced depolarizations, making these the first unambiguously identified “mixed” (i.e., chemical plus electrical) synapses in the vertebrate CNS. We recently showed that gap junctions at these synapses exhibit asymmetric electrical resistance (i.e., electrical rectification), which we correlated with total molecular asymmetry of connexin composition in their apposing gap junction hemiplaques, with Cx35 restricted to axon terminal hemiplaques and Cx34.7 restricted to apposing Mauthner cell plasma membranes. We now show that similarly heterotypic neuronal gap junctions are abundant throughout goldfish brain, with labeling exclusively for Cx35 in presynaptic hemiplaques and exclusively for Cx34.7 in postsynaptic hemiplaques. Moreover, the vast majority of these asymmetric gap junctions occur at glutamatergic axon terminals. The widespread distribution of heterotypic gap junctions at glutamatergic mixed synapses throughout goldfish brain and spinal cord implies that pre- vs. postsynaptic asymmetry at electrical synapses evolved early in the chordate lineage. We propose that the advantages of the molecular and functional asymmetry of connexins at electrical synapses that are so prominently expressed in the teleost CNS are unlikely to have been abandoned in higher vertebrates. However, to create asymmetric coupling in mammals, where most gap junctions are composed of Cx36 on both sides, would require some other mechanism, such as differential phosphorylation of connexins on opposite sides of the same gap junction or on asymmetric differences in the complement of their scaffolding and regulatory proteins.

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“…In wt retina, electrical coupling is an integral part of the rod pathway (Deans et al, 2002). In addition, both bipolar (Zhang and Wu, 2009;Arai et al, 2010) and AII amacrine (Veruki and Hartveit, 2002) cells may also couple to each other. Three lines of evidence suggest that bipolar cells and/or AII amacrine cells in the rd1 retina form electrically coupled networks.…”

Section: Mechanisms Driving Autonomous Activitymentioning

confidence: 99%

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

Borowska¹,

Trenholm²,

Awatramani³

2011

J. Neurosci.

107

171

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The loss of photoreceptors during retinal degeneration (RD) is known to lead to an increase in basal activity in remnant neural networks. To identify the source of activity, we combined two-photon imaging with patch-clamp techniques to examine the physiological properties of morphologically identified retinal neurons in a mouse model of RD (rd1). Analysis of activity in rd1 ganglion cells revealed sustained oscillatory (ϳ10 Hz) synaptic activity in ϳ30% of all classes of cells. Oscillatory activity persisted after putative inputs from residual photoreceptor, rod bipolar cell, and inhibitory amacrine cell synapses were pharmacologically blocked, suggesting that presynaptic cone bipolar cells were intrinsically active. Examination of presynaptic rd1 ON and OFF bipolar cells indicated that they rested at relatively negative potentials (less than Ϫ50 mV). However, in approximately half the cone bipolar cells, low-amplitude membrane oscillation (ϳ5 mV, ϳ10 Hz) were apparent. Such oscillations were also observed in AII amacrine cells. Oscillations in ON cone bipolar and AII amacrine cells exhibited a weak apparent voltage dependence and were resistant to blockade of synaptic receptors, suggesting that, as in wild-type retina, they form an electrically coupled network. In addition, oscillations were insensitive to blockers of voltage-gated Ca 2ϩ channels (0.5 mM Cd 2ϩ and 0.5 mM Ni 2ϩ ), ruling out known mechanisms that underlie oscillatory behavior in bipolar cells. Together, these results indicate that an electrically coupled network of ON cone bipolar/AII amacrine cells constitutes an intrinsic oscillator in the rd1 retina that is likely to drive synaptic activity in downstream circuits.

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Active Roles of Electrically Coupled Bipolar Cell Network in the Adult Retina

Cited by 36 publications

References 71 publications

Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

Nonlinear Spatiotemporal Integration by Electrical and Chemical Synapses in the Retina

Heterotypic gap junctions at glutamatergic mixed synapses are abundant in goldfish brain

An Intrinsic Neural Oscillator in the Degenerating Mouse Retina

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