Abstract
Neural circuit development is an activity-dependent process. This activity can be spontaneous, such as the retinal waves that course across the mammalian embryonic retina, or it can be sensory-driven, such as the activation of retinal ganglion cells (RGCs) by visual stimuli. Whichever the source, neural activity provides essential instruction to the developing circuit. Indeed, experimentally altering activity has been shown to impact circuit development and function in many different ways and in many different model systems. In this review, we contemplate the idea that retinal waves in amniotes, the animals that develop either in ovo or utero (namely reptiles, birds and mammals) could be an evolutionary adaptation to life on land, and that the anamniotes, animals whose development is entirely external (namely the aquatic amphibians and fish), do not display retinal waves, most likely because they simply don’t need them. We then review what is known about the function of both retinal waves and visual stimuli on their respective downstream targets, and predict that the experience-dependent development of the tadpole visual system is a blueprint of what will be found in future studies of the effects of spontaneous retinal waves on instructing development of retinorecipient targets such as the superior colliculus (SC) and the lateral geniculate nucleus.
Highlights
Spontaneous neural activity, defined here as self-generated electrical activity that is not driven by afferent input, exists in many amniote sensory systems during their development
We first focus on the role of spontaneous retinal waves in amniotes, how they could be an evolutionary adaptation to developing on dry land in eggs or in utero, and recent findings about the consequence of these waves on their downstream targets
Visual experience plays a critical function in the development and maturation of the visual circuitry in anamniotes, including the development of the topographic retinotectal projection, retinotectal synaptic properties, tectal neuronal morphological development, as well as broader properties of tectal circuitry including connectivity underlying recurrent activity
Summary
Spontaneous neural activity, defined here as self-generated electrical activity that is not driven by afferent input, exists in many amniote sensory systems during their development. While spontaneous retinal waves have been well described and studied in embryonic retinas of amniotes such as turtles (Sernagor and Grzywacz, 1996, 1999), chicks (Wong et al, 1998), ferrets (Meister et al, 1991; Wong et al, 1993), rodents (Torborg and Feller, 2005; Ackman et al, 2012) and primates (Warland et al, 2006), this spontaneous patterned activity is not present in the retina of amphibians (Demas et al, 2012) nor fish (Kolls and Meyer, 2002) This dichotomy suggests the intriguing possibility that retinal waves are an evolutionary adaptation in response to the transition from life in the water to life on the land, when the transparent jelly coat of the aquatic anamniote embryo was replaced by a hard opaque shell for birds and reptiles, or a uterus for mammals. Emerging evidence indicates parallels between the role of visual stimulation in anamniotes and retinal waves in amniotes
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