Abstract
Experience-dependent functional plasticity is a hallmark of the primary visual system, but it is not known if analogous mechanisms govern development of the circadian visual system. Here we investigated molecular, anatomical, and behavioral consequences of complete monocular light deprivation during extended intervals of postnatal development in Syrian hamsters. Hamsters were raised in constant darkness and opaque contact lenses were applied shortly after eye opening and prior to the introduction of a light-dark cycle. In adulthood, previously-occluded eyes were challenged with visual stimuli. Whereas image-formation and motion-detection were markedly impaired by monocular occlusion, neither entrainment to a light-dark cycle, nor phase-resetting responses to shifts in the light-dark cycle were affected by prior monocular deprivation. Cholera toxin-b subunit fluorescent tract-tracing revealed that in monocularly-deprived hamsters the density of fibers projecting from the retina to the suprachiasmatic nucleus (SCN) was comparable regardless of whether such fibers originated from occluded or exposed eyes. In addition, long-term monocular deprivation did not attenuate light-induced c-Fos expression in the SCN. Thus, in contrast to the thalamocortical projections of the primary visual system, retinohypothalamic projections terminating in the SCN develop into normal adult patterns and mediate circadian responses to light largely independent of light experience during development. The data identify a categorical difference in the requirement for light input during postnatal development between circadian and non-circadian visual systems.
Highlights
Organisms coordinate physiology and behavior to anticipate daily changes in the environment
Experiment 1: Verification of deprivation manipulation To evaluate the efficacy of lens occluders, and to determine whether light entering through the eye contralateral to the occluder stimulates the retina of the occluded eye, unilaterallydenervated hamsters were exposed to light pulses in the presence or absence or an occluder in the non-denervated eye
No decrements were evident in a previously-occluded eye’s ability to induce suprachiasmatic nucleus (SCN) c-Fos expression in response to a brief, non-saturating light pulse, and no obvious anatomical changes were evident in the density of the retinohypothalamic tract (RHT) projecting from monocularly occluded eyes to the SCN
Summary
Organisms coordinate physiology and behavior to anticipate daily changes in the environment. Illumination level is the parameter of light input most important in stimulating the RHT and in driving SCN phaseresetting responses [6]. This stands in contrast to the primary visual system, comprised of the polysynaptic projection from retina to thalamus to visual cortex, which processes patterned input consisting of color, contour and motion, but is relatively poorer at perceiving changes in brightness [7]. The RHT and SCN constitute a distinct circadian visual system [8], which is sufficient [9] and necessary [10,11] for circadian entrainment to light
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