Neuroendocrine regulation of gonadotropin secretion in seasonally breeding birds

Abstract

Seasonally breeding birds detect environmental signals, such as light, temperature, food availability, and presence of mates to time reproduction. Hypothalamic neurons integrate external and internal signals, and regulate reproduction by releasing neurohormones to the pituitary gland. The pituitary gland synthesizes and releases gonadotropins which in turn act on the gonads to stimulate gametogenesis and sex steroid secretion. Accordingly, how gonadotropin secretion is controlled by the hypothalamus is key to our understanding of the mechanisms of seasonal reproduction. A hypothalamic neuropeptide, gonadotropin-releasing hormone (GnRH), activates reproduction by stimulating gonadotropin synthesis and release. Another hypothalamic neuropeptide, gonadotropin-inhibitory hormone (GnIH), inhibits gonadotropin synthesis and release directly by acting on the pituitary gland or indirectly by decreasing the activity of GnRH neurons. Therefore, the next step to understand seasonal reproduction is to investigate how the activities of GnRH and GnIH neurons in the hypothalamus and their receptors in the pituitary gland are regulated by external and internal signals. It is possible that locally-produced triiodothyronine resulting from the action of type 2 iodothyronine deiodinase on thyroxine stimulates the release of gonadotropins, perhaps by action on GnRH neurons. The function of GnRH neurons is also regulated by transcription of the GnRH gene. Melatonin, a nocturnal hormone, stimulates the synthesis and release of GnIH and GnIH may therefore regulate a daily rhythm of gonadotropin secretion. GnIH may also temporally suppress gonadotropin secretion when environmental conditions are unfavorable. Environmental and social milieus fluctuate seasonally in the wild. Accordingly, complex interactions of various neuronal and hormonal systems need to be considered if we are to understand the mechanisms underlying seasonal reproduction.

Keywords: gonadotropin-inhibitory hormone; gonadotropin-releasing hormone; gonadotropins; hypothalamus-pituitary-gonadal axis; melatonin; seasonal reproduction; stress; thyroid hormone.

Figure 1

Schematic model of the mechanism of seasonal reproduction in birds. Seasonal breeding birds detect environmental signals, such as light, temperature, water, and food availability, predator pressure, etc. to time reproduction. Their reproductive activity is also shaped by social interactions with the conspecifics, in terms of sound, sight, contact, etc. Hypothalamic neurons in the bran integrate external and internal signals, and regulate reproduction by releasing neurohormones at the median eminence (ME) to regulate the pituitary hormone secretion. The anterior pituitary gland synthesizes and releases gonadotropins (LH, FSH), and gonadotropins act on the gonads to stimulate gametogenesis and sex steroid secretion. Sex steroids induce secondary sexual characteristics of the organism. A hypothalamic neuropeptide, GnRH1, activates reproduction by stimulating gonadotropin synthesis and release via its receptor (GnRH-R) expressed on the gonadotropes. Another hypothalamic neuropeptide, GnIH, may inhibit gonadotropin synthesis and release directly by acting on the pituitary or indirectly by decreasing the activity of GnRH1 neurons via its receptor (GnIH-R) expressed on the gonadotropes and GnRH neurons. GnRH2 neurons may stimulate reproductive behavior, and GnIH may inhibit reproductive behavior by inhibiting GnRH2 neurons. GnRH and GnIH neurons in the hypothalamus and their receptors in the pituitary are also regulated by internal signals, such as testosterone (T), estradiol (E2), and progesterone (P4). It is hypothesized that locally produced triiodothyronine (T₃) from thyroxine (T₄) by the action of type 2 iodothyronine deiodinase (DIO2) at the mediobasal hypothalamus stimulates the release of GnRH1. The function of GnRH1 neurons is also regulated by transcription of the GnRH gene. Because melatonin, a nocturnal hormone, stimulates the synthesis and release of GnIH in birds, GnIH may regulate daily rhythm of gonadotropin secretion. GnIH may also temporally suppress gonadotropin secretion when environmental or social condition is unfavorable.