Glia Regulate the Development, Function, and Plasticity of the Visual System From Retina to Cortex

Abstract

Visual experience is mediated through a relay of finely-tuned neural circuits extending from the retina, to retinorecipient nuclei in the midbrain and thalamus, to the cortex which work together to translate light information entering our eyes into a complex and dynamic spatio-temporal representation of the world. While the experience-dependent developmental refinement and mature function of neurons in each major stage of the vertebrate visual system have been extensively characterized, the contributions of the glial cells populating each region are comparatively understudied despite important findings demonstrating that they mediate crucial processes related to the development, function, and plasticity of the system. In this article we review the mechanisms for neuron-glia communication throughout the vertebrate visual system, as well as functional roles attributed to astrocytes and microglia in visual system development and processing. We will also discuss important aspects of glial function that remain unclear, integrating the knowns and unknowns about glia in the visual system to advance new hypotheses to guide future experimental work.

Keywords: Müller glia; astrocyte; microglia; neuron–glia interactions; ocular dominance plasticity; retina; visual cortex; visual system.

FIGURE 1

Schematic representations of the vertebrate visual system and the astrocytes and microglia populating each area. (A) Overview of the vertebrate visual system showing the connectivity between major visual areas, in fish and frogs, the retina and optic tectum; and in mammals, the retina, superior colliculus, lateral geniculate nucleus, and the primary visual cortex. (B) Cellular organization of the retina showing Müller glia and microglia. (C) Cellular organization of the optic tectum/developing superior colliculus showing radial astrocytes and microglia. (D) Cellular organization of the lateral geniculate nucleus showing astrocytes and microglia. (E) Cellular organization of the primary visual cortex showing astrocytes and microglia.

FIGURE 2

Overview of the signaling mechanisms implicated in neuron-glia communication and interactions throughout the vertebrate visual system. Representative microglial cell (Left, orange), pre- and postsynaptic terminals (Middle, blue), and Müller glial cell/radial astrocyte/astrocyte (Right, purple) expressing a variety of receptors, transporters, channels, and signaling proteins relevant to their functions across the visual system.