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

Abstract

The hypothalamic suprachiasmatic nucleus (SCN) is the leading circadian pacemaker in mammals, which synchronizes with environmental light through the retinohypothalamic tract (RHT). Although the SCN regulates circadian rhythms before birth, postnatal synaptic changes are needed for the RHT-SCN pathway to achieve total functional development. However, it is unknown whether visual experience affects developmental maturation. Here, we studied the effects of constant darkness (DD) rearing on the physiology (at pre-and postsynaptic levels) of glutamatergic neurotransmission between RHT and SCN during postnatal development in rats.Upon recording spontaneous and evoked excitatory postsynaptic currents (EPSCs) by electrical stimulation of RHT fibers, we found that DD animals at early postnatal ages (P3-19) exhibited different frequencies of spontaneous EPSCs and lower synaptic performance (short-term depression, release sites, and recruitment of RHT fibers) when compared with their normal light/dark (LD) counterparts. At the oldest age evaluated (P30-35), there was a synaptic response strengthening (probability of release, vesicular re-filling rate, and reduced synaptic depression) in DD rats, which functionally equaled (or surmounted) that of LD animals. Control experiments evaluating EPSCs in ventral SCN neurons of LD rats during day and night revealed no significant differences in spontaneous or evoked EPSCs by high-frequency trains in the RHT at any postnatal age. Our results suggest that DD conditions induce a compensatory mechanism in the glutamatergic signaling of the circadian system to increase the chances of synchronization to light at adult ages, and that the synaptic properties of RHT terminals during postnatal development are not critically influenced by environmental light.

Developmental light deprivation transiently reduces the expression of vGluT2 and GluN2B in the rat ventral suprachiasmatic nucleus

“…By contrast, DD conditions induced a transitory lowering in the expression of GluN2B at the earliest postnatal age analyzed (P7–9), though this reduction was compensated at the later ages assayed. These results agree with our recent electrophysiological data, where there are no differences in the ratio of NMDA/AMPA‐kainate components between DD and control LD rats at P30‐35 (Reyes‐Mendez et al., 2021), implying that DD conditions do not affect the regulation of the postsynaptic protein GluN2B at older ages. However, a caveat of the present research is that the GluN2B antibody has not been tested in knockout animals or using the blocking peptide in immunohistochemical preparations.…”

“…Moreover, similar amount of c‐Fos positive cells in the SCN are found in animals maintained during the first 3 weeks of postnatal development in DD and light/dark (LD) conditions (Brooks, Waters, Farrington, & Canal, 2011). Recently, our electrophysiological studies support the idea that the amount of RHT fibers is similar between both lighting conditions (LD and DD), but the synaptic efficacy is higher in animals reared under DD conditions (Reyes‐Mendez et al., 2021). Therefore, in this study we investigated whether the expression in ventral SCN of vGluT2 and GluN2B is affected by light deprivation during postnatal development.…”

“…Experiments were performed in both pups and adult Wistar rats bred in our animal facilities from parents supplied by Harlan (Mexico). Animals from several postnatal (P) ages (P7–35 and one adult stage, P90) were submitted to normal light/dark (LD) cycles (12:12, lights on at 7:00 h) or DD (dim red light of 0.2 lux; Cambras, Canal, Cernuda‐Cernuda, Garcia‐Fernandez, & Diez‐Noguera, 2015; Reyes‐Mendez et al., 2021). Rat pups remained with their dam until the day of the trials or weaned at P21 and housed in pairs.…”