Circadian Regulation of Bird Song, Call, and Locomotor Behavior by Pineal Melatonin in the Zebra Finch

Abstract

As both a photoreceptor and pacemaker in the avian circadian clock system, the pineal gland is crucial for maintaining and synchronizing overt circadian rhythms in processes such as locomotor activity and body temperature through its circadian secretion of the pineal hormone melatonin. In addition to receptor presence in circadian and visual system structures, high-affinity melatonin binding and receptor mRNA are present in the song control system of male oscine passeriform birds. The present study explores the role of pineal melatonin in circadian organization of singing and calling behavior in comparison to locomotor activity under different lighting conditions. Similar to locomotor activity, both singing and calling behavior were regulated on a circadian basis by the central clock system through pineal melatonin, since these behaviors free-ran with a circadian period and since pinealectomy abolished them in constant environmental conditions. Further, rhythmic melatonin administration restored their rhythmicity. However, the rates by which these behaviors became arrhythmic and the rates of their entrainment to rhythmic melatonin administration differed among locomotor activity, singing and calling under constant dim light and constant bright light. Overall, the study demonstrates a role for pineal melatonin in regulating circadian oscillations of avian vocalizations in addition to locomotor activity. It is suggested that these behaviors might be controlled by separable circadian clockworks and that pineal melatonin entrains them all through a circadian clock.

Melatonin action in a midbrain vocal-acoustic network

“…In support of an inhibitory role of melatonin in vocalization of diurnally active species, melatonin treatment in songbirds mimics the effect of short days by decreasing song nuclei volumes (Bentley et al, 1999;Cassone et al, 2008). Furthermore, daily melatonin treatment in pinealectomized zebra finches kept in constant dim light entrained song and call activity to occur during periods without melatonin (Wang et al, 2012). Our results in nocturnally active midshipman fish showed that fictive call duration was increased in 5LL+2-IMel animals, especially in the lateral midbrain (Fig.…”

“…rhythm in song and call behaviors has only recently been shown (Wang et al, 2012), even though melatonin influence on song nuclei volume and the expression of melatonin receptors in song nuclei has been well documented (Bentley, 2003;Bentley and Ball, 2000;Bentley et al, 1999;Bentley et al, 2013;Cassone et al, 1995;Cassone et al, 2008;Gahr and Kosar, 1996;Jansen et al, 2005;Whitfield-Rucker and Cassone, 1996). Additionally, melatonin inhibited the spontaneous firing rate of a vocal premotor nucleus in the zebra finch, suggesting that it can act directly on vocal circuits to influence vocal patterning (Jansen et al, 2005).…”

Comparative Neurobiology of Sound Production in Fishes

“…It remains to be shown that melatonin receptors are expressed in vocal brain regions as seen in songbirds (Gahr and Kosar 1996;Bentley and Ball 2000;Jansen et al 2005) and whether receptor expression levels change across the day. Future work also needs to test whether fish vocalizations are under endogenous circadian control by recording vocal behavior under constant photo-regimes, which has recently been demonstrated in a songbird (Wang et al 2012). Thus, although we have some evidence for a melatonin-sensitive vocal network, the cascade of cellular events leading to daily and seasonally rhythmic vocal behaviors remain to be defined.…”

Differential Expression of Melatonin Receptor Subtypes MelIa, MelIb and MelIc in Relation to Melatonin Binding in the Male Songbird Brain

“…song deteriorates after sleep and is recovered during the day, allowing modifications of learned motor patterns [Shank and Margoliash, 2008;Deregnaucourt et al, 2012]. However, recent work in zebra finches has shown that melatonin is capable of influencing circadian rhythms of vocal activity independently of locomotor activity, suggesting that there are clocks within the song system that are modulated by melatonin [Wang et al, 2012]. In agreement with the latter hypothesis, the differential expression of melatonin subtypes in separate brain regions suggests that melatonin does not simply switch the brain to a 'night' status but act on target areas to regulate behavioral patterns according to area-specific receptivity.…”

“…Melatonin might be implicated in thermoregulatory adaptation during migration [Carere et al, 2010;Fusani et al, 2011]. Recent studies have suggested a direct role of melatonin in controlling the pattern of song [Deregnaucourt et al, 2012], and it has been suggested that melatonin modulates suboscillators that are located within the song nuclei and control circadian rhythms of singing and calling [Wang et al, 2012].…”