Experience-Independent Development of the Hamster Circadian Visual System

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.

Light stimulation during postnatal development is not determinant for glutamatergic neurotransmission from the retinohypothalamic tract to the suprachiasmatic nucleus in rats

“…Likewise, there is consensus that light deprivation (even over a long period of time) during development does not modify circadian rhythm synchronization to light at adult stages (Brooks et al, 2011;Palma-Gomez et al, 2018;Smith & Canal, 2009), thereby suggesting an unaltered connectivity between the RHT and SCN neurons. Moreover, a similar amount of stained RHT nerve endings that impinge on SCN neurons have been found in both light-exposed or ocular-deprived animals (Kampf-Lassin et al, 2011). These findings envisage the relevance of spontaneous neural activity in the development of the nonimage-forming visual system.…”

“…In the circadian system, the effects of visual experience on the physiology of the RHT‐SCN pathway remain to be investigated. Behavioral experiments have shown that animals reared in constant darkness (DD) during early development do not affect the ability of SCN neurons to synchronize to light at adult stages (Brooks et al., 2011; Palma‐Gomez et al., 2018; Smith & Canal, 2009), even if eye‐occluded conditions are maintained for a long time (Kampf‐Lassin et al., 2011). These findings suggest that light stimulation is not critical for RHT fibers to connect and be synaptically efficient with SCN neurons, which reinforces the notion that the synaptic wiring occurring during early development in a DD environment depends only on endogenous neural activity (Katz & Crowley, 2002).…”

Refinement but Not Maintenance of Visual Receptive Fields Is Independent of Visual Experience

“…As a burrowing rodent species, Syrian hamster pups may not experience light until later than carnivore or primate species. Indeed, Syrian hamsters develop normal circadian systems without visual experience (Kampf-Lassin et al 2011). Alternatively, the RFs of cats, rats, and mice in previous studies may have refined normally during development but enlarged by the time of recording.…”

The Biological Clock in Gray Mouse Lemur: Adaptive, Evolutionary and Aging Considerations in an Emerging Non-human Primate Model

“…Despite a general pattern of the PRC that is similar in gray mouse lemurs and rodents, nocturnal and diurnal rodent species exhibit phase delays almost twice as long as those of the gray mouse lemurs, as observed in the golden Hamster (Pohl, 1984) or in mice and rats (Pittendrigh and Daan, 1976b). This characteristic may be a typical primate trait, since similar observations have been made in other primate species, such as owl monkeys ( Aotus lemurinus ) (Rauth-Widmann et al, 1991), marmosets ( Callithrix jacchus ) (Wechselberger and Erkert, 1994) or squirrel monkeys ( Saimiri sciureus ) (Hoban and Sulzman, 1985).…”

“…To sustain circadian signals intracellularly, the negative-feedback loops between Clock/Bmal1 heterodimers and Per and Cry gene transcription are thought to be identical in diurnal and nocturnal mammals (Yu et al, 2002; Duong et al, 2011; Lande-Diner et al, 2013; Bollinger and Schibler, 2014). In addition, studies conducted in night-active and day-active mammalian species reveal that the phase-shifting effect of light is mainly efficient during the night period, regardless of the chronotype (Pohl, 1984; Takahashi et al, 1984; Hoban and Sulzman, 1985; Slotten et al, 2005; Shuboni and Yan, 2010). In the daytime, light exerts no synchronization effect during the previously described dead zone of the PRC, located between two windows of responsiveness to illumination.…”