Evolving nonapeptide mechanisms of gregariousness and social diversity in birds.

In most vertebrate species, the production of vasotocin (VT; non-mammals) and vasopressin (VP; mammals) in the medial bed nucleus of the stria terminalis (BSTm) waxes and wanes with seasonal reproductive state; however, opportunistically breeding species might need to maintain high levels of this behaviorally relevant neuropeptide year-round in anticipation of unpredictable breeding opportunities. We here provide support for this hypothesis and demonstrate that these neurons are instead regulated ‘cryptically’ via hormonal regulation of their activity levels, which may be rapidly modified to adjust VT signaling. First, we show that combined treatment of male and female zebra finches (Estrildidae: Taeniopygia guttata) with the androgen receptor antagonist flutamide and the aromatase inhibitor 1,4,6-androstatriene-3,17-dione does not alter the expression of VT immunoreactivity within the BSTm; however, both hormonal treatment and social housing environment (same-sex versus mixed-sex) alter VT colocalization with the immediate early gene product Fos (a proxy marker of neural activation) in the BSTm. In a second experiment, manipulations of estradiol (E2) levels with the aromatase inhibitor letrozole (LET) or subcutaneous E2 implants failed to alter colocalization, suggesting that the colocalization effects in experiment 1 were solely androgenic. LET treatment also did not affect VT immunoreactivity in a manner reversible by E2 treatment. Finally, comparisons of VT immunoreactivity in breeding and nonbreeding individuals of several estrildid species demonstrate that year-round stability of VT immunoreactivity is found only in highly opportunistic species, and is therefore not essential to the maintenance of long-term pair bonds, which are ubiquitous in the Estrildidae.

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Cryptic Regulation of Vasotocin Neuronal Activity but Not Anatomy by Sex Steroids and Social Stimuli in Opportunistic Desert Finches

In order to study the effect of the temporal synergism of neural oscillations on reproductive regulation and the response of RFamide-related peptide-3 (RFRP-3; a mammalian ortholog of avian gonadotropin-inhibitory hormone), expression of immunoreactive RFRP-3 in the neurons of the dorsomedial nucleus of the hypothalamus was monitored in sexually immature and mature laboratory mice (study I). In study II, the effects of serotonin and dopamine precursors (5-hydroxytryptophan and L-dihydroxyphenylalanine; injected daily, 8 or 12 h apart, for 13 days in 3-week-old mice) on testicular activity and immunoreactive RFRP-3 neurons were studied until 24 days after treatment. Results indicate high levels of expression of immunoreactive RFRP-3 in the sexually immature and 8-hour mice (simulating gonadal suppression), while a low level was noted in mature and 12-hour mice (simulating gonadal stimulation). These findings not only suggest the modulation of gonadal development in mice (during the course of puberty attainment) by changing the temporal phase relation of serotonergic and dopaminergic oscillations (as in some seasonally breeding species), but also demonstrate an inverse correlation of RFRP-3 neurons and gonadal activity in both control and experimental conditions.

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Temporal phase relation of circadian neural oscillations alters RFamide-related peptide-3 and testicular function in the mouse.

Correlation of nitric oxide (NO) activity and gonadal function in Japanese quail, Coturnix coturnix japonica following temporal phase relation of serotonergic and dopaminergic oscillations

Reproductive performance of many avian species, including Japanese quail, is reported to be modulated by specific temporal phase relation of serotonergic and dopaminergic oscillations. Accordingly, it has been shown that the serotonin precursor 5-HTP and the dopamine precursor l-DOPA given 8 h apart induce gonadal suppression and given 12 h apart lead to gonadal stimulation, while other temporal relationships were found to be ineffective. In the present study, we investigated the effects of 8- and 12-h phase relation of neural oscillations on testicular responses including expression of GnRH-I, GnIH, pro-apoptotic proteins (p53 and Bax), inactive and active executioner caspase-3, and the uncleaved DNA repair enzyme PARP-1. Testicular volume and mass decreased significantly in 8-h quail and increased in 12-h quail compared with controls. Expression of ir -GnIH, p53, Bax and active-caspase-3 increased and that of GnRH-I, pro-caspase-3 and uncleaved PARP-1 decreased in 8-h quail compared with controls. A TUNEL assay also confirmed testicular regression in these quail. Testes of 12-h quail exhibited significantly increased expression of GnRH-I, pro-caspase-3 and uncleaved PARP-1 compared with the control group. Our findings suggest that differential response of avian testes to 8- and 12-h phase relation of serotonergic and dopaminergic neural oscillations may be attributed to autocrine/paracrine action of GnIH expression, which is upregulated in regressed testes, leading to apoptotic changes, and downregulated in developed testes, causing apoptotic inhibition. It is concluded that specific phase relation of neural oscillations may modulate the local testicular GnRH-GnIH system and alter the apoptotic mechanism in quail testes. Moreover, these findings highlight the physiological effects of time-dependent drug delivery, including the specific time intervals between two drugs.

Apoptosis-mediated testicular alteration in Japanese quail (Coturnix coturnix japonica) in response to temporal phase relation of serotonergic and dopaminergic oscillations

The present study was designed to examine the role of circadian organization in the control of seasonality in the seasonally breeding spotted munia, Lonchura punctulata, which does not utilize photoperiod to time its reproduction under natural day-length conditions.



Daily injections of L-dihydroxyphenylalanine (L-DOPA, precursor of dopamine) given 12 hr and 8 hr after administration of 5-hydroxytryptophan (5-HTP, precursor of serotonin) alter the gonadal and body-weight responses of the spotted munia, when it is maintained under short-day conditions (LD 6:18). The 12-hr interval was stimulatory and the 8-hr interval was inhibitory for both gonadal and body-weight responses while other intervals (0, 4, and 16 hr) had no effect. A 20-hr interval was stimulatory only for gonadal growth and had no effect on body weight.



These findings support the suggestion that the endogenous seasonal mechanism is determined by circadian organization (i.e., by changes in the phase relationships of two neural oscillations and their many other circadian expressions). The results also indicate that interaction between these two systems does not produce any pharmacological effect but actually affects the seasonality of the birds, as indicated by the different gonadal and metabolic conditions that followed differently timed daily injections of drugs that influence serotonergic and dopaminergic activities. Furthermore, the mechanism of regulation of seasonality seems to be similar in species that do and do not utilize day length as the primary regulator with which to time their seasonal reproductive and metabolic cycles.

Timed daily injections of neurotransmitter precursors alter the gonad and body weights of spotted munia, Lonchura punctulata, maintained under short daily photoperiods

C. M. Chaturvedi

Papers

Timed daily injections of neurotransmitter precursors alter the gonad and body weights of spotted munia, Lonchura punctulata, maintained under short daily photoperiods