Barney A Schlinger

University of California, Los Angeles | UCLA · Department of Integrative Biology and Physiology

Art Arnold is a leading figure in behavioral neuroendocrinology and the genetics of vertebrate sexual differentiation. This review provides a personal perspective on Arnold’s life and career, a lifetime filled with breakthrough biomedical discovery and dedicated scientific training and mentoring. His integrity, his devotion to family, and his deep...

The zebra finch (Taeniopygia guttata), a representative oscine songbird species, has been widely studied to investigate behavioral neuroscience, most notably the neurobiological basis of vocal learning, a rare trait shared in only a few animal groups including humans. In 2019, an updated zebra finch genome annotation (bTaeGut1_v1.p) was released fr...

Significance The process by which new complex traits evolve has been a persistent conundrum throughout the history of evolutionary inquiry. How multiple physiological changes at the organism level and genetic changes at the molecular level combine is still unclear for many traits. Here, we studied the displays of manakins, who beat their wings toge...

Songbirds have emerged as exceptional research subjects for helping us appreciate and understand estrogen synthesis and function in brain. In the context of recognizing the vertebrate-wide importance of brain aromatase expression, in this review we highlight where we believe studies of songbirds have provided clarification and conceptual insight. W...

Biologists have long been fascinated by the elaborate courtship displays performed by diverse organisms throughout the animal kingdom. The evolution of courtship behaviour often requires specializations of neural, sensory and motor systems. In addition, physically impressive displays may also require optimized metabolic, respiratory and cardiovascu...

A Correction to this paper has been published: https://doi.org/10.1038/s41586-021-03473-8.

Synopsis Gonadal hormones can activate performance of reproductive behavior in adult animals, but also organize sex-specific neural circuits developmentally. Few studies have examined the hormonal basis of sex differences in the performance of elaborate, physically complex, and energetic male courtship displays. Here we describe our studies over mo...

Regulation of glucocorticoids (GCs), important mediators of physiology and behavior at rest and during stress, is multi-faceted and dynamic. The 11ß hydroxysteroid dehydrogenases 11ß-HSD1 and 11ß-HSD2 catalyze the regeneration and inactivation of GCs, respectively, and provide peripheral and central control over GC actions in mammals. While these e...

Whole-genome sequencing projects are increasingly populating the tree of life and characterizing biodiversity1,2,3,4. Sparse taxon sampling has previously been proposed to confound phylogenetic inference5, and captures only a fraction of the genomic diversity. Here we report a substantial step towards the dense representation of avian phylogenetic...

Glucocorticoids (hereafter CORT) are well‐known as important regulators of behavior and cognition at basal levels and under stress. However, the precise mechanisms governing CORT action and functional outcomes of this action in the brain remain unclear, particularly in model systems other than rodents. Here we investigated the dynamics of CORT regu...

Glucocorticoids are commonly associated with responses to stress, but other important functions include homeostatic regulation, energy metabolism and tissue remodeling. At low circulating levels, glucocorticoids bind to high-affinity mineralocorticoid receptors (MR) to activate tissue repair and homeostasis (anabolic pathways), whereas at elevated...

Migratory birds, including Gambel’s white-crowned sparrows (Zonotrichia leucophrys gambelii), exhibit profound modifications of skeletal muscles prior to migration, notably hypertrophy of the pectoralis muscle required for powered flight. Muscle growth may be influenced by anabolic effects of androgens; however, prior to spring departure, circulati...

Vocal signals are important in territoriality and mate attraction across animal taxa. Vocalizations are particularly elaborate in some groups, such as songbirds, which learn their songs, but much remains to be known about the physiological mechanisms that produce variation, especially in vocalizations of nonlearners. We address the extent that andr...

The courtship behavior of some species of birds can be energetically demanding, but it is unknown if cardiovascular specializations enable such behaviors. While performing a highly acrobatic courtship dance, heart rate in male golden-collared manakins increases briefly to 1300 beats per minute, among the highest heart rates recorded in any bird or...

SBN Elsevier Lecture Investigation into mechanisms whereby hormones control behavior often starts with actions on central nervous system (CNS) motivation and motor systems and is followed by assessment of CNS drive of coordinated striated muscle contractions. Here we turn this perspective on its head by discussing ways in which hormones might first...

Glucocorticoid (GC) hormones act on the brain to regulate diverse functions, from behavior and homeostasis to the activity of the hypothalamic–pituitary–adrenal axis. Local regeneration and metabolism of GCs can occur in target tissues through the actions of the 11β-hydroxysteroid dehydrogenases [11 beta-hydroxysteroid dehydrogenase type 1 (11β-HSD...

The masculine reproductive phenotype varies significantly across vertebrates. As a result, biologists have long recognized that many of the mechanisms that support these phenotypes—particularly the androgenic system—is evolutionarily labile, and thus susceptible to the effects of selection for different traits. However, exactly how androgenic signa...

Age-related decrements in cognitive ability have been proposed to stem from deteriorating function of the hippocampus. Many birds are long lived, especially for their relatively small body mass and elevated metabolism, making them a unique model of resilience to aging. Nevertheless, little is known about avian age-related changes in cognition and h...

Many species perform elaborate physical displays to court mates and compete with rivals, but the biomechanical mechanisms underlying such behavior are poorly understood. Here we address this issue by studying the neuromuscular origins of display behavior in a small tropical passerine bird called the golden-collared manakin (Manacus vitellinus). Mal...

Sexual selection can drive the evolution of novel traits, including behaviours, that may arise in sex-specific patterns and be under sex-steroid hormone control. In some polygynous species, males actively manipulate their display environment, likely to influence female perception of male sexual traits. As a presumptive appetitive reproductive behav...

The prohormone, dehydroepiandrosterone (DHEA) circulates in vertebrate blood with the potential for actions on target tissues including the central nervous system (CNS). Many actions of DHEA require its conversion into more active products, some of which are catalyzed by the enzyme 3β-hydroxysteroid-dehydrogenase/isomerase (3β-HSD). Studies of bird...

Sexual dimorphism is common but evolutionarily labile in vertebrates. While it is well established that gonadal hormones exert considerable influence on the development and expression of sexual traits, studies of animals with exceptional sexually dimorphic neural or neuromuscular phenotypes are limited. We studied the extent to which androgen treat...

Birdsong is a complex learned behavior performed by the oscine passerine birds. Birds sing in reproductive and aggressive contexts, but there is a great diversity in song behavior across species, seasons, and sexes. Song learning and production are controlled by a specialized neural circuit, the song control system, that is unique to this group of...

Background: Through the actions of one or more isoforms of the enzyme 5α-reductase in many male reproductive tissues, circulating testosterone (T) undergoes metabolic conversion into 5α-dihydrotestosterone (DHT), which binds to and activates androgen receptors (AR) with greater potency than T. In birds, T is also subject to local inactivation into...

The morphology of the avian skeleton is often studied in the context of adaptations for powered flight. The effects of other evolutionary forces, such as sexual selection, on avian skeletal design are unclear, even though birds produce diverse behaviors that undoubtedly require a variety of osteological modifications. Here, we investigate this issu...

Recent studies demonstrate that rapid modulation of the estrogen synthetic enzyme aromatase, regulates hypothalamic (HYP) estrogen production and subsequent neurophysiology and reproductive behavior. In songbirds, in addition to expression in the HYP, aromatase is expressed at high levels in several brain regions notably in the hippocampus (HP) and...

Male Golden-collared manakins (Manacus vitellinus), small suboscine passeriform birds of Panamanian forests, communicate acoustically using a variety of nonvocal sonations. The most prominent sonations are single or multiple intense 'wingsnaps' with a dominant acoustic frequency around 5 kHz. Several hypotheses have been proposed addressing the sou...

Western scrub-jays are known for their highly discriminatory and flexible behaviors in a caching (food storing) context. However, it is unknown whether their cognitive abilities are restricted to a caching context. To explore this question, we tested scrub-jays in a non-caching context using the Aesop’s Fable paradigm, where a partially filled tube...

Male vertebrate social displays vary from physically simple to complex, with the latter involving exquisite motor command of the body and appendages. Studies of these displays have, in turn, provided substantial insight into neuro-motor mechanisms. The neotropical golden-collared manakin (Manacus vitellinus) has been used previously as a model to i...

Western scrub-jays are known for their highly discriminatory and flexible behaviors in a caching (food storing) context. However, it is unknown whether their cognitive abilities are restricted to a caching context. To explore this question, we tested scrub-jays in a non-caching context using the Aesop’s Fable paradigm, where a partially filled tube...

Western scrub-jays are known for their highly discriminatory and flexible behaviors in a caching (food storing) context. However, it is unknown whether their cognitive abilities are restricted to a caching context. To explore this question, we tested scrub-jays in a non-caching context using the Aesop’s Fable paradigm, where a partially filled tube...

Estrogens significantly impact spatial memory function in mammalian species. Songbirds express the estrogen synthetic enzyme aromatase at relatively high levels in the hippocampus and there is evidence from zebra finches that estrogens facilitate performance on spatial learning and/or memory tasks. It is unknown, however, whether estrogens influenc...

Coordinated courtship displays are a common feature of species forming long-term pair bonds. In lekking species, on the contrary, there are no stable pair bonds because partners meet only to copulate, and males indicate their quality and/or attractiveness to females by displaying morphological and behavioral traits. In some cases, females interact...

Sex steroids influence a diversity of neural and behavioral endpoints in birds, including some that have little to do with reproduction per se. Recent advances in neurochemistry and molecular biology further indicate that the avian brain comprises a network of unique sex steroid microenvironments. Factors involved in steroid synthesis and metabolis...

Superior physical competence is vital to the adaptive behavioural routines of many animals, particularly those that engage in elaborate sociosexual displays. How such traits evolve across species remains unclear.Recent work suggests that activation of sex steroid receptors in neuromuscular systems is necessary for the fine motor skills needed to ex...

This protocol describes a method for the in vivo measurement of steroid hormones in brain circuits of the zebra finch. A guide cannula is surgically implanted into the skull, microdilysate is collected through a microdialysis probe that is inserted into the cannula, and steroid concentrations in the microdialysate are determined using the enzyme-li...

Males of many animal species perform specialized courtship behaviors to gain copulations with females. Identifying physiological and anatomical specializations underlying performance of these behaviors helps clarify mechanisms through which sexual selection promotes the evolution of elaborate courtship. Our knowledge about neuromuscular specializat...

Sex steroids control vertebrate behavior by modulating neural circuits specialized for sex steroid sensitivity. In birds, receptors for androgens (AR) and estrogens (ERα) show conserved expression in neural circuits controlling copulatory and vocal behaviors. Male golden-collared manakins have become a model for evaluating hormonal control of compl...

The adrenal hormone corticosterone (CORT) acts on brain to mediate physiology and behavior. In songbirds, behavioral effects of CORT vary across species, environmental conditions, and life history stage with several mechanisms proposed to account for these divergent results. Although blood CORT levels are well characterized, few studies measure COR...

Androgenic activation of intracellular androgen receptors (AR) influences avian vocal production, though this has largely been investigated at the level of the brain. We investigated the influence of predominantly peripheral AR on vocal output in wild Golden-collared Manakins (Manacus vitellinus). In this suboscine species, males court females by p...

In lek mating systems, females choose mates through indicators of quality, which males may exhibit by their performance of courtship displays. In temperate regions, displaying seasons are brief (one to two months), whereas in the tropics courtship seasons may be prolonged. Moreover, in temperate-breeding animals lekking behaviour can be energetical...

Androgenic hormones regulate many aspects of animal social behavior, including the elaborate display routines on which many species rely for advertisement and competition. One way that this might occur is through peripheral effects of androgens, particularly on skeletal muscles that control complex movements and postures of the body and its limbs....

Understanding how complex organisms function as integrated units that constantly interact with their environment is a long-standing challenge in biology. To address this challenge, organismal biology reveals general organizing principles of physiological systems and behavior—in particular, in complex multicellular animals. Organismal biology also f...

The processes of adaptation and speciation are expected to shape genomic variation within and between diverging species. Here we analyze genomic heterogeneity of genetic differentiation and introgression in a hybrid zone between two bird species (Manacus candei and M. vitellinus) using 59 100 SNPs, a whole genome assembly, and Bayesian models. Meas...

Abstract The males of the Golden-collared manakin (Manacus vitellinus), a passerine bird of the Neotropical region, perform elaborate courtship displays that are among the most spectacular in the animal kingdom. During a 7-mo long breeding season, male manakins aggregate in leks of up to 12 individuals, and each male clears a small ‘court’ on the f...

Avian studies have played a pivotal role in our appreciation of the importance of brain aromatization, the mechanics of neuroestrogen production, and the roles of neuroestrogens in organization of the vertebrate brain and the activation of diverse behaviors. Studies across bird species have also unveiled complexity in the cellular and subcellular d...

Estradiol is known to impact cognitive function including spatial learning and memory, with studies focused largely on rodent models. Estrogens can be produced peripherally or centrally as neuroestrogens, and the specific role for neuroestrogens in memory processes remains unresolved. Many songbirds possess remarkable spatial memory capabilities an...

Circulating androgens in adult reproductively active male vertebrates influence a diversity of organ systems and thus are considered costly. Recently, we obtained evidence that androgen receptors (AR) are expressed in several skeletal muscles of three passeriform birds, the golden-collared manakin (Manacus vitellinus), zebra finch (Taenopygia gutta...

This chapter reviews the contribution of avian studies towards our understanding of the constitutive provision of estrogens within the brain. The chapter first summarizes numerous studies describing the distribution of aromatase across diverse avian taxa. Then this chapter focuses on the novel finding, that of the expression, sexual dimorphism, and...

Steroid hormones synthesized in the brain, known as neurosteroids, influence neuroplasticity and behavior, including learning and memory, as well as recovery from neural injury. In particular, estradiol has been identified as a neurosteroid affecting neuronal plasticity and thus may play a role in learning and memory. Neuroestrogens are produced fr...

Males of the Golden-collared Manakin (Manacus vitellinus) perform elaborate courtship displays that are among the most spectacular in the animal kingdom. During an extended breeding season, male manakins aggregate in leks, where each male clears a small court on the forest floor to perform his displays. These behaviours are driven by sexual selecti...

Testosterone (T) regulates many traits related to fitness, including aggression. However, individual variation in aggressiveness does not always relate to circulating T, suggesting that behavioural variation may be more closely related to neural sensitivity to steroids, though this issue remains unresolved. To assess the relative importance of circ...

Sex steroids affect the motivation to court mates, but less is known about how they influence motor movements associated with courtship behavior. Steroidal control of motor function may be especially important for species in which courtship requires superior strength, stamina, and neuromuscular coordination. Here we use the golden-collared manakin...

Male Golden‐collared Manakins Manacus vitellinus perform an elaborate courtship display composed of acrobatic jumps between saplings delimiting a court on the forest floor. Males rehearse their displays for hours until they are executed with amazing precision and speed. Here we investigated the plasticity of the display by examining whether males m...

Recent evidence shows that brain-derived steroids such as estrogens ("neuroestrogens") are controlled in a manner very similar to traditional neurotransmitters. The advent of in vivo microdialysis for steroids in songbirds has provided new information about the spatial and temporal dynamics of neuroestrogen changes in a region of the auditory corte...

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....

Accuracy in quantifying brain-derived steroid hormones ("neurosteroids") has become increasingly important for understanding the modulation of neuronal activity, development, and physiology. Relative to other neuroactive compounds and classical neurotransmitters, steroids pose particular challenges with regard to isolation and analysis, owing to th...

Within the CNS of vertebrates, estrogens can directly modulate neural circuits that govern a wide range of behaviors, including feeding, spatial navigation, reproduction, and auditory processing. The rapid actions of estrogens in brain (seconds to minutes) have become well established, but it is unclear how estrogens are synthesized and released wi...

Male golden-collared manakins (Manacus vitellinus) perform a high-speed acrobatic courtship display punctuated by loud 'snaps' produced by the wings. Females join males on display courts to select individuals for copulation; females follow displaying males but do not perform acrobatics or make wing snaps. Sexually dimorphic courtship displays such...

Sex steroids have long been recognized for their dramatic impact on brain and behavior, including rapid modulation of membrane excitability. It is a widely held perception that these molecules are largely derived from peripheral sources and lack the spatial and temporal specificity ascribed to classical neuromodulatory systems. Neuromodulatory syst...

The long-held dogma that the brain is a target of steroids produced by peripheral organs has delayed the widespread acceptance of the functional importance of neurosteroidogenesis. Comparative studies have been vital for establishing the key actions of gonadal and adrenal hormones on brain and behaviour. No doubt, studies across diverse phyla will...

Sexual selection was proposed by Darwin to explain the evolution of male sexual traits such as ornaments and elaborate courtship displays. Empirical and theoretical studies have traditionally focused on ornaments; the reasons for the evolution of elaborate, acrobatic courtship displays remain unclear. We addressed the hypothesis that females choose...

Sex steroids assist adult neural tissue in the protection from and repair of damage resulting from neural injury; some steroids may be synthesized in the brain. Songbirds are especially useful models to explore steroidal neuroprotection and repair. First, the full suite of cholesterol transporters and steroidogenic enzymes are expressed in the zebr...

Neurogenesis in the adult songbird brain occurs along the ventricular zone (VZ), a specialized cell layer surrounding the lateral ventricles. To examine the acute effects of sex steroids on VZ cell proliferation, male and female adult zebra finch brain slices containing the VZ were exposed to 5-bromo-2'-deoxyuridine-5'-monophosphate (BrdU) in vitro...

The enzyme 11betaHSD2 inactivates glucocorticoids by synthesizing metabolites that bind poorly to mineralocorticoid and glucocorticoid receptors. Oscine songbirds (Passeriformes) are important models for investigating stress hormone effects on brain and behavior but nothing is known about 11betaHSD2 activity in the songbird brain. We measured 11bet...

In male song sparrows (Melospiza melodia), territorial challenges during the breeding season can rapidly increase circulating levels of testosterone (T). During the non-breeding season, male song sparrows are highly aggressive, but the gonads are regressed and plasma T levels are non-detectable and unaffected by territorial challenges. The pro-horm...

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...

Spectacular athleticism is a conspicuous feature of many animal courtship displays yet surprisingly little is known about androgen dependence of skeletal muscles underlying these displays. Testosterone (T) acts through androgen receptors (ARs) to stimulate muscular male Golden-collared manakins of Panama to perform a remarkably athletic courtship d...