Distributed forebrain sites mediate melatonin-induced short-day responses in Siberian hamsters

Abstract

The pineal hormone melatonin (MEL) is the key initiator in regulating seasonal photoperiodic responses; however, the central sites that mediate short day (SD) winter-like responses, such as testicular regression and decreases in white adipose tissue (WAT) mass, by Siberian hamsters are not precisely known. WAT is innervated by the sympathetic nervous system, and several forebrain sites that are part of the sympathetic nervous system outflow to WAT coexpress MEL(1a) receptor mRNA [e.g. suprachiasmatic nucleus, subzona incerta (SubZi), dorsomedial nucleus of the hypothalamus, nucleus reunions and paraventricular nuclei of the thalamus]. We tested the involvement of these sites in MEL-triggered SD responses. A long duration, SD-like MEL signal was applied site specifically for 5 wk, with sc and third ventricle MEL application serving as positive controls. Whereas SD MEL signals delivered to each of these sites were able to induce testicular regression, all but the paraventricular nuclei of the thalamus also trigger SD-induced decreases in body mass. Third ventricle, sc, suprachiasmatic nucleus, or SubZi MEL application also decreased WAT mass, and only sc and SubZi MEL application decreased food intake. Collectively these data suggest a distributed system of MEL-sensitive brain sites sufficient to mediate these SD responses, the redundancy of which suggests its importance for appropriate seasonal responses critical for overwintering.

Figure 1

Representative schematic drawings of cannulation placement in the SCN (n = 15), SubZi (n = 15), third ventricle (3rd V; n = 28), DMH (n = 10), PVT (n = 16), and the ReN (n = 18). Black dot, Correct placement (hit, depicted unilaterally or as midline structure); summing junction, incorrect placement (miss; SCN, n = 2; SubZi, n = 3; third ventricle (3rd V), n = 1; DMH, n = 1; PVT, n = 2; ReN, n = 5). Not indicated is one ReN cannulated individual with cannulation misplacement too far anterior into the anterior commissure, and the misplacements for the SubZi were located in the ReN, 3rd V, and DMH.

Figure 2

A, Mean ± sem percent change of testes mass (grams) from MEL-treated Siberian hamsters vs. their controls (saline or beeswax treated) in the SCN [n = 13 (six MEL)], SubZi [n = 12 (five MEL)], third ventricle [3rd V; n = 27 (15 MEL)], DMH [n = 9 (four MEL)], PVT [n = 13 (six MEL)], and the ReN [n = 14 (six MEL)]. *, P < 0.05 vs. controls. B, Correlation of percent change of testes mass and serum testosterone concentrations (nanograms per milliliter) for all animals [absolute values of control animals for testes and testosterone, respectively: sc: 0.84 ± 0.06 g, 5.32 ± 1.32 ng/ml; 3rd V: 0.69 ± 0.05 g, 6.36 ± 1.14 ng/ml; SCN: 0.79 ± 0.09 g, 2.93 ± 1.29 ng/ml; SubZi: 0.77 ± 0.06 g, 1.15 ± 0.29 ng/ml; DMH: 0.66 ± 0.08 g, 2.19 ± 0.87 ng/ml; PVT: 0.82 ± 0.05 g, 4.09 ± 1.52 ng/ml; ReN: 0.94 ± 0.08 g, 3.32 ± 0.89 ng/ml].

Figure 3

Mean ± sem percent change of fat pad mass (grams) in MEL-treated Siberian hamsters compared with controls (saline or beeswax treated) in the SCN [n = 13 (six MEL)], SubZi [n = 12 (five MEL)], third ventricle [3rd V; n = 19(8 MEL)], DMH [n = 9 (four MEL)], PVT [n = 13 (six MEL)], and the ReN [n = 12 (four MEL)]. *, P < 0.05 vs. controls [absolute values of controls for EWAT, IWAT, and RWAT mass, respectively: sc: 0.95 ± 0.08, 0.74 ± 0.05, 0.2 ± 0.03 g; 3rd V: 0.88 ± 0.06, 0.65 ± 0.04, 0.18 ± 0.01 g; SCN: 0.92 ± 0.08, 0.56 ± 0.06, 0.15 ± 0.02 g; SubZi: 0.76 ± 0.02, 0.52 ± 0.06, 0.15 ± 0.02 g; DMH: 0.78 ± 0.09, 0.57 ± 0.09, 0.19 ± 0.03; PVT: 0.89 ± 0.05, 0.73 ± 0.05, 0.19 ± 0.02; ReN: 0.78 ± 0.06, 0.54 ± 0.04, 0.13 ± 0.01 g].