Seasonal neuroplasticity in the songbird telencephalon: A role for melatonin

Abstract

Neuroplasticity in the vocal control system of songbirds is strongly inf luenced by seasonal f luctuations in circulating testosterone. These seasonally plastic telencephalic structures are implicated in the learning and production of song in songbirds. The role of the indoleamine melatonin in seasonal adaptations in birds has remained unclear. In this experiment, European starlings were castrated to remove the neuromodulating activity of gonadal steroids and were exposed to different photoperiods to induce reproductive states characteristic of different seasonal conditions. Long days increased the volume of the song-control nucleus high vocal center compared with its volume on short days. Exogenous melatonin attenuated the long-day-induced volumetric increase in high vocal center and also decreased the volume of another song-control nucleus, area X. This effect was observed regardless of reproductive state. To our knowledge, this is the first direct evidence of a role for melatonin in functional plasticity within the central nervous system of vertebrates.European starlings (Sturnus vulgaris) are highly photoperiodic (1). Reproductive activity occurs in the spring as day length is increasing (i.e., photostimulation occurs), but is subsequently curtailed by the onset of photorefractoriness during exposure to long day lengths. During the onset of photorefractoriness, the hypothalamo-pituitary-gonadal (HPG) axis becomes inactive and the gonads regress (2). Starlings remain refractory to long day lengths until short days are experienced in the winter; the HPG axis slowly becomes responsive again in the absence of a long day photostimulus, in preparation for increasing day length and consequent full reproductive activity in the spring. It must be noted that these centrally mediated different reproductive states are not mediated by seasonal changes in gonadal steroids and still occur at the levels of the hypothalamus and the pituitary gland, even in the absence of gonads (2). Coincident with changes in reproductive activity, seasonal neuroplasticity now documented in several species of oscine songbirds occurs within discrete telencephalic nuclei that are involved in song learning and production (3-7). Increases in the volumes of these song-control nuclei largely depend on seasonal increases in circulating testosterone (T) and its metabolites (8-10) that are directly related to the annual reproductive cycles of these birds (11). These seasonal changes in volumes of the song-control nuclei are associated with changes in cell size and cell number in various song-control nuclei (12).Recent studies suggest that there are gonad-and Tindependent seasonal changes in the volumes of song nuclei (13-15). To date, it has been unclear what factors might be contributing to these T-independent neuronal changes. A complex suite of physiological events occurs during the onset of photorefractoriness (2). These include changes in circulating concentrations of photoperiodically controlled hormones other than T. There are also alt...

Seasonal-like growth and regression of the avian song control system: Neural and behavioral plasticity in adult male Gambel’s white-crowned sparrows

“…In castrated male starlings, American tree sparrows, and dark-eyed juncos and Gambel's whitecrowned sparrows, LD photoperiod is sufficient to promote at least partial growth of some song control system nuclei volumes (Bernard et al, 1997;Smith et al, 1997;Bentley et al, 1999;Dloniak and Deviche, 2001). In castrated male house finches, LD photoperiod is sufficient to induce growth of RA but not HVC (Strand and Deviche, 2007).…”

Tracking the seasons: the internal calendars of vertebrates

“…Pinealectomy prevents the long day-induced increase in nesting behaviour of male ring doves (Streptopelia risoria;McDonald 1982). In castrated European starlings, constant release melatonin implants prevent photorefractory-induced changes in the immune system (Bentley et al 1998a) and long dayinduced increases in the high vocal centre (HVc), a brain nucleus important for birdsong (Bentley et al 1999). Again, these effects may be of pharmacological rather than physiological significance.…”

The effects of light pollution on biological rhythms of birds: an integrated, mechanistic perspective

“…http://eproofing.springer.com/journals/printpage.php?token=TaHBL3K0MzivtP9dyZh Egm 9e46Xwx0IBI6tHxA9LzbhUEWXGZXsg 9/27 they are stimulated by increasing daylength (Bentley et al 1999 ). Last, melatonin has been shown to stimulate the release of gonadotropic inhibitory hormone (GnIH) from the avian hypothalamus, a process that inhibits seasonal breeding (Tsutsui et al 2006 ).…”

“…First, melatonin can stimulate cell mediated immune responses typical of winter, while increasing daylength dampens the immune system during reproduction (Bentley et al 1998 ). Second, melatonin can directly affect the plasticity of the avian song control system (Bentley et al 1999; Cassone et al 2008 ). In particular, melatonin receptors have been identified in the forebrain song control nucleus, Area X.…”