Abstract
BackgroundActivity in neurons drives afferent competition that is critical for the refinement of nascent neural circuits. In ferrets, when an eye is lost in early development, surviving retinogeniculate afferents from the spared eye spread across the thalamus in a manner that is dependent on spontaneous retinal activity. However, how this spontaneous activity, also known as retinal waves, might dynamically regulate afferent terminal targeting remains unknown.MethodsWe recorded retinal waves from retinae ex vivo using multi-electrode arrays. Retinae came from ferrets who were binocular or who had one eye surgically removed at birth. Linear mixed effects models were used to investigate the effects of early monocular enucleation on retinal wave activity.ResultsWhen an eye is removed at birth, spontaneous bursts of action potentials by retinal ganglion cells (RGCs) in the surviving eye are shorter in duration. The shortening of RGC burst duration results in decreased pairwise RGC correlations across the retina and is associated with the retinal wave-dependent spread of retinogeniculate afferents previously reported in enucleates.ConclusionOur findings show that removal of the competing eye modulates retinal waves and could underlie the dynamic regulation of competition-based refinement during retinogeniculate development.
Highlights
Activity in neurons drives afferent competition that is critical for the refinement of nascent neural circuits
The reduction in burst duration was for the most part consistent across retinae recorded at temperatures of either 34 °C (binocular, 2.76 ± 1.42; monocular, 1.82 ± 0.91; mean ± STD; binocular, N = 731, 7 retinae; monocular, N = 592, 6 retinae; T(1317) = 3.90, P = 9.952 × 10− 5, linear mixed-effects model with log transformation) or 37 °C (binocular, 1.79 ± 0.83; monocular, 1.46 ± 1.07; mean ± STD; binocular, N = 447, 6 retinae; monocular, N = 409, 5 retinae; T(850) = 3.37, P = 0.00078, linear a b
We show that the removal of the competing eye alters the duration of retinal wave associated retinal ganglion cell (RGC) bursts, which has impacts on RGC correlation
Summary
Activity in neurons drives afferent competition that is critical for the refinement of nascent neural circuits. Neural activity that is essential for early stages of visual system development originates from spontaneous processes [1, 4,5,6] and appears to facilitate circuit refinement by driving Hebbian-like competition for synaptic partners between innervating neurons [7,8,9]. This activity-dependent refinement results in the precise mapping of sensory areas, for example by establishing eye-specific laminae and fine-scale retinotopy across visual areas [1, 4]. Retinal wave associated bursts of action potentials by retinal ganglion cells in the surviving eye were shorter as were the number of spikes
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