Temporal synergism of corticosterone and prolactin controlling fat storage in the white-throated sparrow, Zonotrichia albicollis

doi:10.1016/0016-6480(71)90141-9

General and Comparative Endocrinology

Volume 17, Issue 2, October 1971, Pages 311-318

https://doi.org/10.1016/0016-6480(71)90141-9 Get rights and content

Abstract

Increases in body fat were induced by daily injections of corticosterone. However, the time of injection is of critical importance. Injections given 6 hr after the onset of a daily photoperiod of 6 hr caused fat increases, whereas injections at 12 or 18 hr after “dawn” were ineffective. In addition to fat increases, injections at 6 hr after “dawn” also induced nocturnal locomotor activity in the white-throated sparrow, a nocturnal migrant. Nocturnal activity was absent in the untreated birds as well as in those receiving corticosterone at 12 or 18 hr after “dawn.” Apparently, the daily variations in responses to corticosterone depend on the circadian release of endogenous pituitary prolactin. In birds kept on continuous light, it was discovered that a temporal synergism of injected corticosterone and injected prolactin can regulate the level of fat stores. Daily injections of prolactin at 4 or 12 hr after corticosterone produced high levels of obesity in lean photorefractory birds after 5 days. Injections at 8 or 20 hr after corticosterone depressed fat stores, and injections at 0 or 16 hr after the adrenal steroid produced intermediate levels of fat. It is concluded that seasonal levels of fat stores are the cumulative results of daily changes that are regulated by a temporal synergism of corticosterone and prolactin.

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Cited by (48)

Interactive effect of light colours and temporal synergism of circadian neural oscillations in reproductive regulation of Japanese quail
2016, Journal of Photochemistry and Photobiology B: Biology
Citation Excerpt :
According to this regulatory factor it is logical that temporal phase relations of different circadian hormonal or neural oscillations vary seasonally because circadian activities of different hormones/neurotransmitters do vary with different seasons and physiological conditions [29,49,53,54]. Hence experimentally it was possible to simulate specific seasonal breeding condition by duplicating the specific phase relation of two neural/hormonal oscillations [14,39–41,52,53,55]. Based on this assumption, six different temporal phase relation of serotonergic and dopaminergic oscillations were induced by administering the serotonin precursor 5-hydroxytryptophan (5-HTP) and dopamine precursor l-dihydroxyphenylalanine (l-DOPA) at intervals of 0, 4, 8, 12, 16 and 20 hrs establishing 0-h, 4-h, 8-h, 12-h, 16-h and 20-h phase relation between the two neural oscillations.
Avian literature reports the modulation of ‘photoperiodic gonadal responses’ by the temporal phase relation of serotonergic and dopaminergic oscillations in Japanese quail. But, the modulation of ‘light colour responses’ by the temporal synergism of neural oscillations is not yet known. Hence the present study was designed to investigate the interaction of the light colour (blue, red) and the phase relation of neural oscillations in the reproductive regulation of Japanese quail. Three week old male Japanese quail were divided into two groups and maintained under a long day length condition (16 L:8D) and were exposed to a 30 lux intensity of blue LED (light emitting diode) (B LED) and a red LED light (R LED). At the age of 15.5 weeks, quail of one subgroup of B LED were injected with serotonin precursor (5-HTP) and dopamine precursor (l-DOPA) 12 hrs apart (B LED + 12-hr) and those of the R LED group were injected with the same drugs (5 mg/100 g body weight over a period of thirteen days) but 8 hrs apart (R LED + 8-hr). The remaining subgroups of both the light colour groups (B LED & R LED) received normal saline twice daily and served as controls. Cloacal gland volume was recorded weekly until 35.5 weeks of age when the study was terminated and reproductive parameters (testicular volume, GSI, seminiferous tubule diameter and plasma testosterone) were assessed.
Results indicate that the 8-hr temporal phase relation of neural oscillations suppresses reproductive activity even during the photosensitive phase of the red light exposed quail (R LED + 8-hr) compare to the R LED controls. On the other hand, the 12-hr temporal phase relation stimulates the gonadal development of the B LED + 12-hr quail compared to the B LED controls which after completing one cycle entered into a regressive phase and remained sexually quiescent. These experiments suggest that the temporal phase relations of circadian neural oscillations, in addition to modulating the classical photoperiodic responses, may also modulate the gonadal responses to blue (suppressive) and red (stimulatory) light. These studies led us to conclude that the temporal phase relation of serotonergic and dopaminergic oscillations is not only an important regulator of avian reproduction but may also override the classical effects of light colours in Japanese quail.
Interaction of specific temporal phase relations of circadian neural oscillations and long term photoperiodic responses in Japanese quail, Coturnix coturnix japonica
2015, General and Comparative Endocrinology
Citation Excerpt :
On the other hand, the LD 8-h + 8-h group showed smaller semniferous tubule diameters with an overall inactive condition (Fig. 9). Numerous of studies regarding the effect of photoperiod/photoperiodic time measurement and the temporal phase relation of circadian neural oscillations have been reported by several workers (Farner and Follett, 1966; Kumar, 1997; Meier and Martin, 1971; Chaturvedi and Yadav, 2013). However, the synergistic/combined effect of these two factors on gonadal responses was unknown.
Specific temporal phase relations of neural oscillations are reported to regulate gonadal activity in many avian species but their interaction with photo-sexual response are still unclear. Hence in the present study, 3 week old Japanese quail maintained in short days (experiment 1) received normal saline (SD control) or serotonin precursor 5-HTP and dopamine precursor l-DOPA injections at the interval of 12 h (SD 12-h) for 13 days. At 37 week of age, one subgroup of SD 12-h received these drugs at the interval of 8-h (SD 12-h + 8-h). In the second experiment, 3 week old quail were injected with 5-HTP and l-DOPA 8 h apart (LD 8-h) and then maintained under long days. At the age of 37 weeks, one subgroup of these LD quail was retreated with 5-HTP and l-DOPA at the interval of 8 h (LD 8-h + 8-h). Cloacal gland volume was monitored weekly up to 45 weeks of age in both experiments and other reproductive parameters were monitored at 23 and 45 week of age.
These results indicate that 12-h phase relation of neurotransmitter precursors not only initiates early onset of scotorefractoriness i.e., full development of gonad even under short-day length but maintains it continuously (a long lasting effect) unlike control and the 8-h relation dissipates it, making the quail scotosensitive. On the other hand, the 8-h phase relation suppresses the gonado-stimulatory effect of long days but this effect is transitory. Thus the 12-h phase relation is gonado-stimulatory under short day conditions and the 8-h relation is gonado-inhibitory even under long days, inducing scotorefractoriness and photorefractoriness, respectively, it is suggested that effects of specific temporal phase relation of circadian neural oscillations similar to photoperiodic effects, are not only mediated by HPG axis but may also modulate the classical photoperiodic responses of Japanese quail.
Adipose Tissue and Lipid Metabolism
2015, Sturkie's Avian Physiology: Sixth Edition
Adipose tissue is the most variable carcass component and has traditionally been considered a rather inert storage tissue for energy in the form of lipids. Most of the fat in chickens is located in adipose depots, which are all late maturing. At the cellular level, preadipocyte differentiation and proliferation are under the control of multiple hormones and transcription factors. The growth of fat tissue is initially due to hyperplasia followed by hypertrophy of the mature adipocytes. The amount of fat deposited is controlled by numerous hormones and depends on genetic and nutritional factors.
Dietary fat is transported as portomicrons to the liver, which is also the primary site of the de novo lipogenesis. The newly formed very-low-density lipoproteins (VLDLs) are distributed by the blood to the rest of the body. Lipoprotein lipase is a key enzyme in the further processing of these lipoproteins at the level of various tissues, in particular the lipoprotein metabolism in laying hens. All egg yolk lipids are synthesized mainly by the liver and transported to the ovary in special yolk-targeted VLDL (VLDLy) with an unusual apoprotein (apo) composition (only apoB and apoVLDLII).
Recent research has, however, revealed that adipose tissue must now be regarded as a dynamic tissue, which secretes a considerable number of adipokines and hence plays a role in a multitude of bodily processes.
Contributions of endocrinology to the migration life history of birds
2012, General and Comparative Endocrinology
Citation Excerpt :
In conjunction with exogenous corticosterone, prolactin was also found to induce migratory activity (but note possible pharmacological doses; (Meier and Martin, 1971). Interestingly, the time of injection was important in achieving these effects and it has been hypothesized that the phase relationship between prolactin and corticosterone underlie changes in migratory activity (Dusseau and Meier, 1971; Meier and Martin, 1971). In contrast with these findings, endogenous prolactin levels correlated well with photoperiod but not with development of migratory condition in European quail and administration of exogenous prolactin caused an increase in food intake rates regardless of the time of administration (Boswell et al., 1995).
Migration is a key life cycle stage in nearly 2000 species of birds and is a greatly appreciated phenomenon in both cultural and academic arenas. Despite a long research tradition concerning many aspects of migration, investigations of hormonal contributions to migratory physiology and behavior are more limited and represent a comparatively young research field. We review advances in our understanding of the hormonal mechanisms of migration with particular emphasis on the sub-stages of the migration life history: development, departure, flight and arrival. These sub-stages vary widely in their behavioral, ecological and physiological contexts and, as such, should be given appropriate individual consideration.
Role of prolactin in obesity: Extending the hypothesis
2009, Medical Hypotheses
Correlation of nitric oxide (NO) activity and gonadal function in Japanese quail, Coturnix coturnix japonica following temporal phase relation of serotonergic and dopaminergic oscillations
2008, Animal Reproduction Science
Nitric oxide (NO), a highly reactive and short-lived radical, is considered to be an important trigger molecule for several physiological mechanisms including gonadotrophin releasing hormone (GnRH) secretion in mammals, although there is no such information in avian literature. On the other hand, specific temporal phase relation of circadian neural (serotonergic and dopaminergic) oscillations is reported to modulate reproductive activity in many avian species including Japanese quail. The present study was undertaken to investigate the correlation of NO activity and gonadal function of Japanese quail. In experiment I, the effect of serotonin and dopamine precursors, (5-hydroxytryptophan (5-HTP) and l-dihydroxyphenyalanine (l-DOPA) respectively; 5 mg per 100 g body weight) administered at intervals of 8 or 12 h over a period of 13 days, was studied on reproductive responses and NO activity. Measurements of body weight, cloacal gland size, testosterone concentration, spermatogenesis, nitrite–nitrate concentration in plasma, hypothalamus and testes, and NADPH-diaphorase (NADPH-d) activity in testes were made on the 2nd, 3rd, 6th and 11th days of treatment and 2nd and 30th day post-treatment. In experiment II, quail were divided into five groups including the control. One experimental group received 13 daily injections of 5-HTP and l-DOPA at intervals of 8 h along with 0.1 ml of normal saline administered orally (8-hr + Veh), while another group of 8-hr quail received NO donor (sodium nitroprusside (SNP), 5 mg per 100 g body weight) orally (8-hr + SNP). The third experimental group received 5-HTP and l-DOPA at intervals of 12 h along with normal saline (12-hr + Veh), while the fourth group of quail along with 5-HTP and l-DOPA at intervals of 12 h also received the NOS inhibitor (N-nitro-l-arginine methyl ester, l-NAME, 25 μg per 100 g body weight) intraperitoneally (12-hr + l-NAME) for 13 days. This experiment was terminated after 21 days of the treatment.
Results indicate that 5-HTP and l-DOPA administered 8 h apart (8-hr) suppressed but if given 12 h apart (12-hr) stimulated the reproductive system and NO activity compared to the control. These effects were apparent on the 6th day of injections and were maintained 30 days following the termination of the treatment. A significant decrease in nitrite and nitrate concentration and NADPH-d activity in reproductively inhibited 8-hr group and an increase in reproductively stimulated 12-hr quail was also evident. In contrast, these activities were stimulated in 8-hr + SNP quail and were suppressed in 12-hr + l-NAME group quail. It is concluded that activity of the reproductive system and NO activity waxes and wanes simultaneously in Japanese quail. Moreover, experimental modulation of gonadal activity (following changes in the phase relation of serotonergic and dopaminergic activity) or NO activity (following the administration of NO modulator or inhibitor) affects each other maintaining a parallel relation between the two systems. Further, it is interesting to note that the gonado-stimulatory effect of SNP overpowers the gonado-inhibitory effects of the 8-hr time interval and inhibitory effects of l-NAME mask the stimulatory effects of 12-hr temporal relation of 5-HTP and l-DOPA administration. These findings strongly suggest that reproductive effects may be induced via changes in NO activity, however the exact mechanism by which NO drives gonadal axis needs to be ascertained.

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^☆: Supported by a National Science Foundation grant, GB-20913.

²: Recipient of a Public Health Service Research Career Development Award, GM-17,898.

³: National Science Foundation Predoctoral Fellow.

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General and Comparative Endocrinology

Abstract

References (15)

Diurnal and seasonal variations of plasma adrenal steroid hormone in the White-throated Sparrow, Zonotrichia albicollis

Gen. Comp. Endocrinol

Annual stimulus for migration in birds

Animal Behavior

Diurnal variations of metabolic responses to prolactin in lower vertebrates

Gen. Comp. Endocrinol

Diurnal variations of the fattening response to prolactin in the White-throated Sparrow, Zonotrichia albicollis

Gen. Comp. Endocrinol

A possible endocrine basis for premigratory fattening in the White-crowned Sparrow, Zonotrichia leucophrys gambelii (Nuttall)

Gen. Comp. Endocrinol

A possible endocrine basis for migratory behavior in the White-crowned Sparrow, Zonotrichia leucophrys gambelii (Nuttall)

Anim. Behav

Seasonal variations in the diurnal rhythm of pituitary prolactin content in the White-throated Sparrow, Zonotrichia albicollis

Gen. Comp. Endocrinol

Cited by (48)

Interactive effect of light colours and temporal synergism of circadian neural oscillations in reproductive regulation of Japanese quail

Interaction of specific temporal phase relations of circadian neural oscillations and long term photoperiodic responses in Japanese quail, Coturnix coturnix japonica

Adipose Tissue and Lipid Metabolism

Contributions of endocrinology to the migration life history of birds

Role of prolactin in obesity: Extending the hypothesis

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

Temporal synergism of corticosterone and prolactin controlling fat storage in the white-throated sparrow, Zonotrichia albicollis☆

Abstract

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Gen. Comp. Endocrinol