Estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal pattern generator

Estrogens rapidly regulate neuronal activity within seconds-to-minutes, yet it is unclear how estrogens interact with neural circuits to rapidly coordinate behavior. This study examines whether 17-beta-estradiol interacts with an opioidergic network to achieve rapid modulation of a vocal control circuit. Adult plainfin midshipman fish emit vocalizations that mainly differ in duration, and rhythmic activity of a hindbrain–spinal vocal pattern generator (VPG) directly establishes the temporal features of midshipman vocalizations. VPG activity is therefore predictive of natural calls, and ‘fictive calls’ can be elicited by electrical microstimulation of the VPG. Prior studies show that intramuscular estradiol injection rapidly (within 5 min) increases fictive call duration in midshipman. Here, we delivered opioid antagonists near the VPG prior to estradiol injection. Rapid estradiol actions on fictive calling were completely suppressed by the broad-spectrum opioid antagonist naloxone and the mu-opioid antagonist beta-funaltrexamine, but were unaffected by the kappa-opioid antagonist nor-binaltorphimine. Unexpectedly, prior to estradiol administration, all three opioid antagonists caused immediate, transient reductions in fictive call duration. Together, our results indicate that: (1) vocal activity is modulated by opioidergic networks, confirming hypotheses from birds and mammals, and (2) the rapid actions of estradiol on vocal patterning depend on interactions with a mu-opioid modulatory network

Estradiol Synthesis and Action at the Synapse: Evidence for “Synaptocrine” Signaling

Classically, the modulation of brain function and behavior by steroid hormones was linked exclusively to secretion by peripheral endocrine glands. Subsequently, steroid actions within the brain were shown dependent upon either synthesis and secretion by peripheral organs or by production within the CNS itself using peripheral sources of precursors. Discovery of the estrogen-synthetic enzyme aromatase in brain further bolstered the latter view and served as a catalyst for expanding concepts of neurosteroidogenesis. In parallel research, several steroids, including estradiol, were found to have rapid effects on neuronal excitability, partially explained by novel actions at neuronal membranes. Recent findings from multiple levels of analysis and labs necessitate an updated view on how steroids are delivered to neural circuits. There is now considerable evidence for expression of the aromatase enzyme within synaptic boutons in the vertebrate CNS. Furthermore, additional work now directly couples rapid regulation of neuroestrogen synthesis with neurophysiological and behavioral outcomes. In this review we summarize evidence for targeted and acute synaptic estrogen synthesis and perisynaptic estrogen actions in the CNS of songbirds. We evaluate these findings in the context of criteria associated with classic neuromodulatory signaling. We term this novel form of signaling “synaptocrine,” and discuss its implications

Socially-mediated arousal and contagion within domestic chick broods

Emotional contagion – an underpinning valenced feature of empathy – is made up of simpler, potentially dissociable social processes which can include socially-mediated arousal and behavioural/physiological contagion. Previous studies of emotional contagion have often conflated these processes rather than examining their independent contribution to empathic response. We measured socially-mediated arousal and contagion in 9-week old domestic chicks (n = 19 broods), who were unrelated but raised together from hatching. Pairs of observer chicks were exposed to two conditions in a counterbalanced order: air puff to conspecifics (AP) (during which an air puff was applied to three conspecifics at 30 s intervals) and control with noise of air puff (C) (during which the air puff was directed away from the apparatus at 30 s intervals). Behaviour and surface eye temperature of subjects and observers were measured throughout a 10-min pre-treatment and 10-min treatment period. Subjects and observers responded to AP with increased freezing, and reduced preening and ground pecking. Subjects and observers also showed reduced surface eye temperature - indicative of stress-induced hyperthermia. Subject-Observer behaviour was highly correlated within broods during both C and AP conditions, but with higher overall synchrony during AP. We demonstrate the co-occurrence of socially-mediated behavioural and physiological arousal and contagion; component features of emotional contagion

Neural expression and post-transcriptional dosage compensation of the steroid metabolic enzyme 17β-HSD type 4

<p>Abstract</p> <p>Background</p> <p>Steroids affect many tissues, including the brain. In the zebra finch, the estrogenic steroid estradiol (E₂) is especially effective at promoting growth of the neural circuit specialized for song. In this species, only the males sing and they have a much larger and more interconnected song circuit than females. Thus, it was surprising that the gene for 17β-hydroxysteroid dehydrogenase type 4 (HSD17B4), an enzyme that converts E₂to a less potent estrogen, had been mapped to the Z sex chromosome. As a consequence, it was likely that HSD17B4 was differentially expressed in males (ZZ) and females (ZW) because dosage compensation of Z chromosome genes is incomplete in birds. If a higher abundance of HSD17B4 mRNA in males than females was translated into functional enzyme in the brain, then contrary to expectation, males could produce less E₂in their brains than females.</p> <p>Results</p> <p>Here, we used molecular and biochemical techniques to confirm the HSD17B4 Z chromosome location in the zebra finch and to determine that HSD17B4 mRNA and activity were detectable in the early developing and adult brain. As expected, HSD17B4 mRNA expression levels were higher in males compared to females. This provides further evidence of the incomplete Z chromosome inactivation mechanisms in birds. We detected HSD17B4 mRNA in regions that suggested a role for this enzyme in the early organization and adult function of song nuclei. We did not, however, detect significant sex differences in HSD17B4 activity levels in the adult brain.</p> <p>Conclusions</p> <p>Our results demonstrate that the HSD17B4 gene is expressed and active in the zebra finch brain as an E₂metabolizing enzyme, but that dosage compensation of this Z-linked gene may occur via post-transcriptional mechanisms.</p

Rapid effects of estrogens on behavior: Environmental modulation and molecular mechanisms

Estradiol can modulate neural activity and behavior via both genomic and nongenomic mechanisms. Environmental cues have a major impact on the relative importance of these signaling pathways with significant consequences for behavior. First we consider how photoperiod modulates nongenomic estrogen signaling on behavior. Intriguingly, short days permit rapid effects of estrogens on aggression in both rodents and song sparrows. This highlights the importance of considering photoperiod as a variable in laboratory research. Next we review evidence for rapid effects of estradiol on ecologically-relevant behaviors including aggression, copulation, communication, and learning. We also address the impact of endocrine disruptors on estrogen signaling, such as those found in corncob bedding used in rodent research. Finally, we examine the biochemical mechanisms that may mediate rapid estrogen action on behavior in males and females. A common theme across these topics is that the effects of estrogens on social behaviors vary across different environmental conditions

Supplemental Information 1: Raw data: Plasma metabolite concentrations, moult stage, and timing of capture for young common snipe migrating through central Poland

Moult of feathers entails considerable physiological and energetic costs to an avian organism. Even under favourable feeding conditions, endogenous body stores and energy reserves of moulting birds are usually severely depleted. Thus, most species of birds separate moult from other energy-demanding activities, such as migration or reproduction. Common snipe Gallinago gallinago is an exception, as during the first autumn migration many young snipe initiate the post-juvenile moult, which includes replacement of body feathers, lesser and median wing coverts, tertials, and rectrices. Here, we evaluated moult-related changes in blood plasma biochemistry of the common snipe during a period of serious trade-off in energy allocation between moult and migration. For this purpose, concentrations of basic metabolites in plasma were evaluated in more than 500 young snipe migrating through Central Europe. We found significant changes in the plasma concentrations of total protein, triglyceride and glucose over the course of moult, while the concentrations of uric acid and albumin did not change. Total protein concentration increased significantly in the initial stage of moult, probably as a result of increased production of keratin, but it decreased to the pre-moult level at the advanced stage of moult. Plasma triglyceride concentration decreased during the period of tertial and rectrice moult, which reflected depletion of endogenous fat reserves. By contrast, glucose concentration increased steadily during the course of moult, which could be caused by increased catabolism of triglycerides (via gluconeogenesis) or, alternatively, due to increased glucocorticoids as a stress response. Our results suggest that physiological changes associated with moult may be considered important determinants of the low pace of migration typical of the common snipe

Steroid Concentrations in Plasma, Whole Blood and Brain: Effects of Saline Perfusion to Remove Blood Contamination from Brain

The brain and other organs locally synthesize steroids. Local synthesis is suggested when steroid levels are higher in tissue than in the circulation. However, measurement of both circulating and tissue steroid levels are subject to methodological considerations. For example, plasma samples are commonly used to estimate circulating steroid levels in whole blood, but steroid levels in plasma and whole blood could differ. In addition, tissue steroid measurements might be affected by blood contamination, which can be addressed experimentally by using saline perfusion to remove blood. In Study 1, we measured corticosterone and testosterone (T) levels in zebra finch (Taeniopygia guttata) plasma, whole blood, and red blood cells (RBC). We also compared corticosterone in plasma, whole blood, and RBC at baseline and after 60 min restraint stress. In Study 2, we quantified corticosterone, dehydroepiandrosterone (DHEA), T, and 17β-estradiol (E2) levels in the brains of sham-perfused or saline-perfused subjects. In Study 1, corticosterone and T concentrations were highest in plasma, significantly lower in whole blood, and lowest in RBC. In Study 2, saline perfusion unexpectedly increased corticosterone levels in the rostral telencephalon but not other regions. In contrast, saline perfusion decreased DHEA levels in caudal telencephalon and diencephalon. Saline perfusion also increased E2 levels in caudal telencephalon. In summary, when comparing local and systemic steroid levels, the inclusion of whole blood samples should prove useful. Moreover, blood contamination has little or no effect on measurement of brain steroid levels, suggesting that saline perfusion is not necessary prior to brain collection. Indeed, saline perfusion itself may elevate and lower steroid concentrations in a rapid, region-specific manner

Detection of low-frequency tones and whale predator sounds by the American sand lance Ammodytes americanus

Author Posting. © The Author(s), 2012. This is the author's version of the work. It is posted here by permission of John Wiley & Sons for personal use, not for redistribution. The definitive version was published in Journal of Fish Biology 81 (2012): 1646-1664, doi:10.1111/j.1095-8649.2012.03423.x.Auditory evoked potentials (AEPs) were used to measure the hearing range and auditory sensitivity of the American sand lance Ammodytes americanus. Responses to amplitude modulated tone pips indicated that the hearing range extended from 50 to 400 Hz. Sound pressure thresholds were lowest between 200 and 400 Hz. Particle acceleration thresholds showed an improved sensitivity notch at 200 Hz but not substantial differences between frequencies and only a slight improvement in hearing abilities at lower frequencies. The hearing range was similar to Pacific sand lance A. personatus and variations between species may be due to differences in threshold evaluation methods. AEPs were also recorded in response to pulsed sounds simulating humpback whale Megaptera novaeangliae foraging vocalizations termed ‘megapclicks’. Responses were generated with pulses containing significant energy below 400 Hz. No responses were recorded using pulses with peak energy above 400 Hz. These results show that A. americanus can detect the particle motion component of low frequency tones and pulse sounds, including those similar to the low frequency components of megapclicks. Ammodytes americanus hearing may be used to detect environmental cues and the pulsed signals of mysticete predators.We also thank the Mountlake Research Fund, the Provost’s Fund for Senior Thesis Research and the Horton Elmer Fund, all of which provided the support for this study through Princeton University. A. Mooney was supported through a Woods Hole Postdoctoral Scholar award and the Andrew W. Mellon Fund for Innovative Research.2014-09-0