Neuroglial and synaptic rearrangements associated with photic entrainment of the circadian clock in the suprachiasmatic nucleus

Abstract

Rhythmic biological functions in mammals are orchestrated by a circadian timekeeper in the suprachiasmatic nucleus of the hypothalamus (SCN) which precisely adjusts clock outputs to solar time through the process of photic synchronization. Entrainment to the 24-h light-dark cycle is known to act on the molecular loops which trigger circadian oscillations but is also thought to involve day-night adjustments in the intercellular phasing of the multiple component SCN oscillators. This view is supported by data showing that the SCN undergoes important rearrangements of its neuroglial architecture throughout the 24-h cycle. The present paper highlights our data showing in rat that the two main sources of SCN efferents, composed of neurons synthesizing either vasopressin (AVP) or vasoactive intestinal peptide (VIP), are differentially involved in day-night SCN neuroglial plasticity. We found that the synaptic inputs received by the VIP neurons, which are major integrators of photic signals in the retinorecipient SCN subregion, increased during the day while those received by the AVP neurons remained unchanged at day and night. Glutamatergic axons, known to convey photic information from the retina, together with nonglutamatergic axons, contribute to the synaptic remodellings on VIP neurons. Experimental data providing strong indication that these plastic events may subserve synchronization of the clock to the light-dark cycle and that the daily fluctuations of plasma glucocorticoid hormones may act as temporal endocrine signals that may modulate SCN neuroglial plasticity through the rhythmic release of serotonin are also reviewed.

The dynamics of GABA signaling: Revelations from the circadian pacemaker in the suprachiasmatic nucleus

“…Neither GAT-1 nor GAT-3 appear to change rhythmically over the day when measured in rats housed in a 24 h LD cycle. There is evidence however, although controversial, that neuroglial synaptic arrangements change rhythmically over the day in the SCN (Elliott and Nunez, 1994; Girardet et al, 2010). …”

Collective timekeeping among cells of the master circadian clock

“…In general, astrocytes provide physical support, release pro-survival factors, influence synaptic clearance, and produce gliotransmitters that interact with presynaptic and postsynaptic receptors (Faissner, et al 2010). Anatomical and functional evidence suggests that SCN astrocytes may influence light-induced resetting by regulating glutamate release from retinal terminals (Girardet, et al 2010; Lavaille and Serviere 1995; Lavialle, et al 2001; Moriya et al 2000; Tamada, et al 1998; van den Pol et al 1992). Interestingly, VIP and AVP neurons in the SCN core and shell compartments display differences in daily rhythms of glial coverage of dendrites, with higher coverage of VIP and AVP neurons during the night and day, respectively (Becquet et al 2008).…”

Sleep, clocks, and synaptic plasticity

“…There is also evidence of circadian rhythms in synaptic plasticity, in some cases driven by a master clock (in mammals, the suprachiasmatic nucleus [SCN]) and in other cases, by peripheral clocks. In the following sections, we review the evidence for circadian influences on synaptic plasticity outside the SCN (see [60] for discussion of plastic changes within the SCN). One consideration in assessing these studies is that it can be difficult to disentangle the effects of circadian time vs. brain state in a given measurement.…”