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Center for Cellular and Molecular Neurobiology Research Group in Behavioral Neuroendocrinology University of Liège B-4000 Liège, Belgium
Address all correspondence and requests for reprints to: Jacques Balthazart, Center for Cellular and Molecular Neurobiology, Research Group in Behavioral Neuroendocrinology, University of Liège, 1 Avenue de l’Hopital (Bat B36), B-4000 Liège, Belgium. E-mail: jbalthazart{at}ulg.ac.be.
To ensure their survival and successful competition with other species, animals must select an optimal time for engaging in reproduction. Achieving this goal requires the analysis of complex signals from the environment and the transmission to the reproductive hypothalamo-pituitary-gonadal axis of the relevant information. The paper by Maney et al. (1) in this issue identifies key loci in the neural circuits mediating this task and, in this way, demonstrates how different types of information contribute to the full ovarian development in female songbirds.
Successful breeding involves selecting the optimal period of the year in terms of resources availability but also synchronizing this activity with a potential partner of the opposite sex. In species living in the temperate zone, changes in the daily photoperiod provide an accurate predictor of seasons and, thus, future breeding conditions. Therefore, it is not surprising that many species have developed a capacity to "read" the photoperiod and determine their breeding period based on this information (2). Depending on the duration required for a fertilized egg to develop into an independent young and the period in this development when energy requirements are maximal, species have adapted to engage in reproduction either during the early spring, as done by many birds who will then benefit from the abundance of food during the end of spring and summer, or in the fall, as observed, for example, in sheep, in which the embryo will develop in its mother’s womb during winter, but the young lamb will benefit from the tender and fast-growing grass in the following spring. The formal properties of the photoperiodic response and parts of the brain circuits underlying this capacity to adjust reproduction to changes in the photoperiod (the initial predictive information; see Ref. 3) are reasonably well understood and surprisingly quite similar for species breeding in increasing photoperiods during the spring, such as starlings, or in decreasing photoperiods during the fall, such as sheep (4, 5).
However, these photoperiodic mechanisms only provide a relatively coarse determination of the breeding phenology. It was discovered that many additional factors such as temperature, food, or sexual partner availability and behavior (called "Supplementary, Synchronizing or Modifying factors") are able to adjust the egg laying date of females to optimize breeding success during the broadly defined reproductive period, and synchronize the activity of the male and female in the breeding pair (3, 6, 7). For example, in birds it was established more than 50 yr ago that species such as the canary or ringdove synchronize their breeding behavior and physiology with the behavior of their partner (8, 9).
The relative importance of photoperiod and of supplementary cues in timing reproduction varies as a function of the species biology. For example, birds living at low latitudes normally experience minimal changes in day length. It has often been assumed that these species are not very sensitive to variations in photoperiod (however, for more recent contradicting data, see Ref. 10) and use other cues such as rainfall [zebra finches, Taeniopygia guttata (11)] or the behavior of their partner [ringdove, Streptopelia risoria (8, 12)] as initial predictive information. Temperate zone species are in contrast very photoperiodic but will also modify their precise breeding date in response to cues such as a partner’s vocalizations (7, 13), abrupt changes in weather conditions (14, 15), or food availability (6, 16). However, these effects of supplementary information can be masked in laboratory conditions if the photoperiodic stimulation is too intense (17).
Sophisticated behavioral analyses in ringdoves indicated that visual and vocal aspects of the male courtship behavior play additive roles in promoting ovarian development in the courted female over a period of 1 wk (18). Subsequent work even demonstrated that female ovarian growth actually results from the perception by the female of her own vocalizations produced in response to male calls (19). Many studies performed on a range of avian species have now confirmed the stimulatory effects of male vocalizations on ovarian function over a period of weeks. The brain mechanisms and neural circuits mediating these effects of male song and other supplementary cues on male and female reproductive physiology are, so far, poorly documented (however, see Ref. 20).
In the present manuscript, Maney et al. (1) demonstrate that in female white-throated sparrows (Zonotrichia albicollis), social signals (male songs) that are known to modulate the timing of reproduction significantly increase plasma LH concentrations and activate the mediobasal hypothalamus (MBH), as revealed by the detection of the immediate early gene (IEG) egr-1, also known as Zenk in birds (21). Both effects are observed within an hour after the initiation of song playback, indicating the existence of a much faster neuroendocrine response than previously thought. Much of the previous work on this topic assessed the stimulatory effects of male song on female reproductive endocrinology by measuring after a few weeks, increases in ovarian size or the diameter of the largest ovarian follicles. With the advent of LH RIA, it was shown that increases in ovarian/follicle size were associated with an increased LH secretion, but, with a few exception (e.g. Ref. 20), studies only assessed this effect after latencies of a few days if not weeks rather than minutes or hours, as done here.
The increases in LH plasma concentrations are in all probability triggered by increases in GnRH secretion, and, as a consequence, it has long been assumed that the preoptic GnRH neurons represent the target where information about photoperiod and additional cues must converge to regulate reproduction. Meddle and Follett (22) demonstrated that exposure to a single long day enhances in Japanese quail expression of the IEG c-fosin the basal tuberal hypothalamus, in parallel with the increase in plasma LH concentrations, but no report has described such an increase in the preoptic area (i.e. the location of GnRH neuronal perikarya). This suggests that the photoperiodic information increases GnRH secretion by activating tuberal neurons that stimulate its release (they presumably project on GnRH fibers in the tuberal region and median eminence), rather than by changing the secretion of this peptide in the corresponding cell bodies. These results are consistent with lesion studies indicating that the photoperiodic response in quail can be blocked by lesions of the basal tuberal hypothalamus (23). Interestingly, lesions in the tuberal hypothalamus that block photoperiod-induced gonadal growth in males leave the GnRH projection from the preoptic area to the median eminence intact, indicating that the lesioned cell population is distinct from, but probably projects on, the GnRH neurons/fibers (24). Maney et al. (1) demonstrate here that neurons in the same brain region are also activated by the playback of conspecific male song (Fig. 1
).
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The identification of this point of convergence between photoperiodic and social cues opens new avenues for research on the circuit integrating environmental and neuroendocrine information. Remaining questions that can now be addressed include:
1) Are cells activated by light and by male songs completely different, or do some of these cells react to both types of stimuli? Do they also react to other supplementary cues, such as temperature or the presence/absence of food?
2) What is the phenotype of these cells? Are they neurons or glial cells? Both types of cells were activated in the MBH and median eminence, respectively, during a study of the photoperiodic induction of LH secretion (25). What kind of transmitters and neuropeptides do they express? Could some of them be part of the kisspeptin neuronal system (26) that plays a key role in controlling GnRH release?
3) Do these cell project directly or indirectly to GnRH fibers, and what kind of inputs do they receive? How are they connected to the ear and photoreceptors (eye, hypothalamic photoreceptors)?
The present study by Maney et al. (1) leaves open a large number of these questions but provides an excellent experimental model that will now allow their study in future experiments.
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Disclosure Statement: The author has nothing to disclose.
Abbreviations: IEG, Immediate early gene; MBH, mediobasal hypothalamus.
Received September 14, 2007.
Accepted for publication September 18, 2007.
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