Neurons containing gastrin-releasing peptide and vasoactive intestinal polypeptide are involved in the reception of the photic signal in the suprachiasmatic nucleus of the Syrian hamster: an immunocytochemical ultrastructural study

Abstract

In mammals, the suprachiasmatic nuclei are involved in the generation of biological rhythms and are synchronized by light input coming from the retina. The targets of retinal afferents and the involvement of neurons containing gastrin-releasing and vasoactive intestinal peptides in photic reception were investigated in the suprachiasmatic nuclei of the Syrian hamster by using light- and electron-microscopic immunocytochemistry. Cholera toxin was used to trace retinal fibers and Fos immunoreactivity to visualize cellular response to light stimulation. Ultrastructural observations were made in the intermediate third of the nuclei, the area of highest overlap for the immunoreactivities investigated. Gastrin-releasing peptide and vasoactive intestinal peptide cell bodies were localized in the ventral part of the nuclei; their dense immunoreactive fiber network often displayed synaptic contacts. Both neuropeptides were colocalized in elongated cells observed near the optic chiasm. Following a light pulse in the middle of the subjective night, Fos protein was expressed in most gastrin-releasing peptide perikarya and in some vasoactive intestinal peptide cells. Retinal terminals mostly occurred in the midline zone between the suprachiasmatic nuclei. Symmetrical or asymmetrical retinal synapses were observed on gastrin-releasing peptide-immunoreactive dendrites and somata, but never on vasoactive intestinal peptide neurons. These results are discussed in relation to the photic entrainment of the circadian clock.

Phenotype Matters: Identification of Light-Responsive Cells in the Mouse Suprachiasmatic Nucleus

“…The present study shows that 1 hr after a brief light pulse, most GFP cells (in the CalB::GFP mouse) in the SCN express Fos. Consistent with our results in mice, retinal terminals contact gastrin-releasing peptide cells in both rats and hamsters (Tanaka et al, 1997;Aioun et al, 1998). VIP cells of the SCN are also known to receive direct retinal input.…”

“…Estimates of the size and identity of this population of light-responsive cells range from 20 to 40% of SCN cells and vary depending on the assay used [electrophysiology (Sawaki, 1979;Meijer et al, 1986;Aggelopoulos and Meissl, 2000) or IEG expression (Earnest et al, 1993;Silver et al, 1996;Castel et al, 1997;Aioun et al, 1998)]. The present study shows that 1 hr after a brief light pulse, most GFP cells (in the CalB::GFP mouse) in the SCN express Fos.…”

“…In rats, 0 -10% of VIP cells, which lie in the ventrolateral retinorecipient SCN region, express Fos content after a light pulse (Earnest et al, 1993;Mikkelsen et al, 1994;Romijn et al, 1996). Retinal terminals on VIP cells have been observed in the rat but not in the hamster (Tanaka et al, 1993;Aioun et al, 1998). VIP, like gastrin-releasing peptide, is rhythmic in LD but not in DD, although the former peaks at night and the latter in the day (Shinohara et al, 1993).…”

Calbindin-D28K cells selectively contact intra-SCN neurons

“…All these cells may be part of the light entrainment mechanism in hamsters. CalB (Bryant et al, 2000) and GRP (Aioun et al, 1998) cells receive retinal terminals and presentation of a light pulse during the night induces c-Fos in about 80% of the CalB cells (Silver et al, 1996), 78% of the GRP cells and 60% of the VIP cells (Aioun et al, 1998). It is also known that administration of GRP (McArthur et al, 2000) or coadministration of VIP, peptide histidine isoleucine and GRP (Albers et al, 1991) induce phase-dependent resetting of the SCN that resembles the lightinduced phase response curve.…”

Gastrin-Releasing Peptide Promotes Suprachiasmatic Nuclei Cellular Rhythmicity in the Absence of Vasoactive Intestinal Polypeptide-VPAC2Receptor Signaling

“…Many neurochemicals are present in the rodent SCN, and some SCN neurons containing VIP also coexpress peptide histidine isoleucine, GABA, and gastrin-releasing peptide (GRP) (Albers et al, 1991;Zoeller et al, 1992;Romijn et al, 1996Romijn et al, , 1998Aioun et al, 1998;Kawamoto et al, 2003). GRP, acting via its BB 2 receptor, shares some of the resetting actions of VIP on the rodent SCN (Piggins et al, 1995;McArthur et al, 2000;Reed et al, 2001;Aida et al, 2002) and may potentiate the actions of VIP within the circadian pacemaker (Albers et al, 1991).…”