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The diverse functional roles and regulation of neuronal gap junctions in the retina

Nature Reviews Neuroscience volume 10, pages 495–506 (2009)Cite this article

Key Points

  • Electrical transmission through gap junctions forms a rapid form of inter-neuronal communication in the CNS.

  • Gap junctions are expressed by each of the five major neuron types in the retina and thus are positioned to play key parts in visual processing.

  • Retinal gap junctions are dynamically regulated by light acting through neuromodulators such as dopamine and nitric oxide.

  • Gap junctional coupling between cone photoreceptors decreases their intrinsic noise and thereby increase the sensitivity and fidelity of their signals.

  • Coupling between rod and cone photoreceptors creates a secondary pathway for rod signals to reach the ganglion cells. This secondary pathway extends the operation of the retina under dim light conditions.

  • Gap junctional coupling between rod photoreceptors is thought to average signals for transmission to ganglion cells that operate under certain dim light conditions such as dusk and dawn.

  • Horizontal cells are widely coupled through gap junctions to form an extensive electrical syncytium. Horizontal cell coupling is thought to form the initial mechanism for contrast detection in the visual system.

  • Gap junctions of the AII amacrine cells preserve the fidelity of the most sensitive retinal signals in the inner retina so that they can be transmitted to higher brain centres.

  • Electrical coupling between retinal ganglion cells synchronizes their light-evoked signals. This concerted activity is believed to compress information for more efficient transmission and thereby enable more information to be passed through the optic nerve.

  • Coupling of neighbouring direction-selective ganglion cells produces synchronous activity. However, the movement of intercellular current through the gap junctions is modulated based on the direction of stimulus movement. This modulation provides a mechanism by which coupled cells can encode specific information about an image.

Abstract

Electrical synaptic transmission through gap junctions underlies direct and rapid neuronal communication in the CNS. The diversity of functional roles that electrical synapses have is perhaps best exemplified in the vertebrate retina, in which gap junctions are formed by each of the five major neuron types. These junctions are dynamically regulated by ambient illumination and by circadian rhythms acting through light-activated neuromodulators such as dopamine and nitric oxide, which in turn activate intracellular signalling pathways in the retina.The networks formed by electrically coupled neurons are plastic and reconfigurable, and those in the retina are positioned to play key and diverse parts in the transmission and processing of visual information at every retinal level.

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Figure 1: Structure and molecular organization of gap junctions.
Figure 2: Neuromodulators affect gap junction conductances through intracellular pathways.
Figure 3: Gap junctions expressed by retinal neurons.
Figure 4: The three rod pathways in the mammalian retina.
Figure 5: Electrical coupling between AII amacrine cells is regulated by background light conditions.
Figure 6: Ganglion cell gap junctions underlie two patterns of concerted spike activity.
Figure 7: Synchronous activity of coupled ON direction-selective ganglion cells encodes the direction of moving light stimuli.

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Acknowledgements

The authors wish to acknowledge the National Eye Institute of the US National Institutes of Health for support of their research programmes (grants EY007360 (S.A.B.) and EY017832 (B.V.)).

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  1. Departments of Physiology & Neuroscience and Ophthalmology, New York University School of Medicine, 550 First Avenue, New York, 10016, New York, USA

    Stewart A. Bloomfield & Béla Völgyi

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Correspondence to Stewart A. Bloomfield.

Glossary

Amacrine cell

An interneuron located in the inner plexiform layer of the retina, at the level where bipolar cells and ganglion cells synapse.

Gap junction plaque

A collection of up to thousands of single gap junction channels.

Bipolar cell

A cell that receives information formed by the interactions of horizontal cells with cone or rod photoreceptors and conveys it to the inner retina. ON (cone or rod) bipolar cells respond to increases in intensity, whereas OFF cone bipolar cells respond to decreases in intensity.

All amacrine cell

A subtype of retinal amacrine cell with a small dendritic field that conveys the rod signal to cone bipolar cells.

Sign-inverting synapse

A synapse that inverts the polarity of the signal passed from the pre- to the postsynaptic neuron.

Sign-conserving synapse

A synapse that preserves the polarity of the signal passed from the pre- to the postsynaptic neuron.

Ganglion cells

The output neurons of the retina, the axons of which form the optic nerve. ON ganglion cells respond to increases in light intensity, whereas OFF ganglion cells respond to decreases in light intensity.

Scotopic

Relating to dim ambient light conditions under which only rod photoreceptors are active.

Horizontal cells

Retinal neurons that form a network just beneath the photoreceptors that is responsible for averaging visual activity over space and time, which is important for contrast signalling.

Receptive field

A dynamic area of the retina in which stimulus presentation leads to the response of a particular cell.

Ephaptic

Relating to the direct electrical interaction between neighbouring neurons, mediated by current flow through the extracellular space that separates them.

Mesopic

Relating to the ambient light condition under which both rod and cone photoreceptors are active.

Accessory optic system

A visuosensory pathway with a direct retinal input to the midbrain.

Optokinetic response

A compensatory eye movement that stabilizes an image on the retina during slow head rotation.

Pannexins

Proteins expressed in both vertebrates and invertebrates that can form intercellular gap junction channels.They are genetically related to the invertebrate innexin family but are not related to connexins.

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Bloomfield, S., Völgyi, B. The diverse functional roles and regulation of neuronal gap junctions in the retina. Nat Rev Neurosci 10, 495–506 (2009). https://doi.org/10.1038/nrn2636

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