Day‐length encoding through tonic photic effects in the retinorecipient SCN region

Abstract

The circadian clock in the suprachiasmatic nucleus (SCN) plays a critical role in seasonal processes by sensing ambient photoperiod. To explore how it measures daylength, we assessed the state of SCN oscillators using markers for neuronal activity (c-FOS) and the clock protein (PER1) in Syrian hamsters housed in long (LD, 16:8hr light:dark) versus short days (SD, 8:16hr light:dark). During SD, there was no detectable phase dispersion across the rostro-caudal extent of the nucleus. In contrast, during LD, rhythms in the caudal SCN phase led those in the mid-and rostral SCN by 4-8 h and 8-12 h, respectively. Importantly, some neurons in the retinorecipient core SCN were unique in that they were FOS-positive during the dark phase in LD, but not SD. Transfer of LD animals to constant darkness or skeleton photoperiod revealed that dark phase FOS expression depends on tonic light exposure rather than on intrinsic clock properties. By transferring animals from SD to LD, we next discovered that there are two separate populations of SCN cells one responding to acute and the other to tonic light exposure. The results suggest that the SCN's seasonal encoding of day-length entails reorganization of its constituent oscillators by a subgroup of neurons in the SCN core that respond to tonic photic cues.

Expression of clock genes in the suprachiasmatic nucleus: Effect of environmental lighting conditions

“…This is consistent in all species examined, regardless of whether the animals are reproductively photoperiodic [91,[97][98][99][100] or not [101][102][103]. The results on other clock genes, including Cry1, Cry2, Bmal1 and clock are less consistent, which could either reflect species difference (rat, Syrian hamster, Siberian hamster) or differences in photoperiodic history or condition [91,99,103].…”

“…However, such correlation between the SCN sub region and activity component was not seen in another in vitro study using Per2-luc animals [107]. Analyzing the PER1 expression ex vivo, at five spatial levels from the rostral to the caudal end of hamster SCN, revealed an orderly phase distribution of the SCN oscillators along the rostral-caudal axis corresponding to day-length [100]. Meanwhile, the core SCN showed low amplitude expression in phase with that in the shell under both long-and short-photoperiods [100].…”

“…Marked regional differences in clock gene expression have been observed along the rostral-caudal axis of the SCN, both in vivo [91,100,104] and in vitro [105][106][107]. In short photoperiod, the rostral and caudal remain in similar phases; while in long photoperiod, the clock gene expression in the caudal phase leads that in the rostral SCN [91,[104][105][106].…”

“…Analyzing the PER1 expression ex vivo, at five spatial levels from the rostral to the caudal end of hamster SCN, revealed an orderly phase distribution of the SCN oscillators along the rostral-caudal axis corresponding to day-length [100]. Meanwhile, the core SCN showed low amplitude expression in phase with that in the shell under both long-and short-photoperiods [100]. The results demonstrated a gradient in the phase of SCN cell oscillators from the rostral to caudal end of the nucleus, and indicated that day-length determined not only the waveform of the SCN as a whole, but also the phase distribution of individual oscillator cells within the SCN (Fig.…”

The suprachiasmatic nuclei as a seasonal clock

“…Moreover, in hamsters a striking difference 329 in c-Fos expression in the ventral SCN during the dark phase was 330 found between hamsters housed in a long and short photoperiods 331 (Yan and Silver, 2008). 332 The dorsomedial sub-region of the SCN (i.e., the ''shell'' of the 333 SCN) does not receive direct light input Long photoperiod Short photoperiod van den Pol, 1991;Guido et al, 1999a,b;335 Sumova et al, 1998); instead, this sub-region receives non-photic 336 input from the cortex, basal forebrain, and hypothalamus (Jac 337 et al, 2000;van den Pol, 1991; (Yan and Silver, 2008;Reddy et al, 2002;Nagano et al, 347 2003). Accordingly, the dorsal SCN lacks a light-induced up-regula-348 tion of c-fos mRNA levels; however, the dorsal SCN has sponta-349 neous rhythmic expression of c-fos and the protein product c-Fos 350 (Sumova et al, 1998).…”