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

Abstract

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.