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D. K. Vaughan, K. A. Linberg, W. Li, M. Traub, G. P. Lewis, S. K. Fisher; Seasonal Dynamics of Cone Ribbon Synapses in Ground Squirrel Retina. Invest. Ophthalmol. Vis. Sci. 2008;49(13):1262. doi: https://doi.org/.
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© ARVO (1962-2015); The Authors (2016-present)
The tissues of hibernating mammals, e.g. ground squirrels (GSs), are resilient to the twin challenges of ischemia and reperfusion on a background of starvation. Hibernating GSs alternate between hypothermic torpor bouts (lasting 1-2 wk) interrupted by euthermic interbout arousals (lasting 10-12 hr). Metabolic adjustments occur in the weeks preceding hibernation and ensure that GSs emerge from hibernation with their faculties intact. Seasonal synaptic plasticity has been described in the hibernator’s brain in the form of reversible (mostly post-) synaptic protein dissociation (von der Ohe et al. 2007). Thirty years ago, electron microscope studies of the GS retina demonstrated that cone synaptic ribbons withdraw from the active zone during torpor and re-deploy upon arousal (Kuwabara 1975, Remé & Young 1977), a logical down-regulation of a tonically-active glutamatergic synapse (Schmitz et al. 2006) during months where the visual system isn’t needed. We re-examined GS ribbon synapses with immunoconfocal microscopy and extended the time-frame of the earlier studies to include the pre-hibernation period.
One wild-caught adult (aroused but had hibernated) was sacrificed in July. Otherwise, young of the year from the UW Oshkosh captive colony were used. Hibernation-naïve (aroused) GSs were sacrificed in August, October and November, whereas first-hibernation (torpid) GSs were sacrificed in October and December. Retinas were processed for in situ immunolabelling with anti-CtBP2 to identify synaptic ribbons (Schmitz et al. 2000).
In August/aroused retinas, CtBP2-immunoreactivity (IR) was evenly distributed in a narrow band along the base of the photoreceptor terminals - the presumed active zone. In December/torpid retinas, a single large punctum of CtBP2-IR per photoreceptor was observed displaced ~ 2 µm sclerad from the active zone, which retained minimal CtBP2-IR. In the adult retina collected in July, and in some November retinas, displaced CtBP2-IR punctae were observed, even though these animals were aroused.
Our data confirm the earlier studies on ribbon synapses of torpid and aroused GSs. Moreover, ribbon synapse disengagement in GS retina may be anticipatory. Seasonal plasticity of ribbon synapses may be neuroprotective if it reduces the risk of glutamate excitotoxicity, consistent with depressed glutamate levels in the torpid GS brain (Henry et al. 2007).
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