Luke Remage-Healey's research while affiliated with University of Massachusetts Amherst and other places

Publications (83)

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The path of Andrew Bass, a first-generation scientist, toward fundamental discoveries in behavioral neuroendocrinologyBehavioral neuroendocrinology was serpentine and serendipitous, and marked by the advice and care from established mentors, as well as his career-long ability to combine discovery with mentoringMentoring those around him to thrive i...
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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...
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Sensory neurons parse millisecond-variant sound streams like birdsong and speech with exquisite precision. The auditory pallial cortex of vocal learners like humans and songbirds contains an unconventional neuromodulatory system: neuronal expression of the estrogen synthesis enzyme aromatase. Local forebrain neuroestrogens fluctuate when songbirds...
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Distinguishing between regular and irregular heartbeats, conversing with speakers of different accents, and tuning a guitar-all rely on some form of auditory learning. What drives these experience-dependent changes? A growing body of evidence suggests an important role for non-sensory influences, including reward, task engagement, and social or lin...
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This review explores the role of aromatase in the brain as illuminated by a set of conserved network-level connections identified in several vertebrate taxa. Aromatase-expressing neurons are neurochemically heterogeneous but the brain regions in which they are found are highly-conserved across the vertebrate lineage. During development, aromatase n...
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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...
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Estrogens support major brain functions including cognition, reproduction, neuroprotection, and sensory processing. Neuroestrogens are synthesized within some brain areas by the enzyme aromatase and can rapidly modulate local circuit functions, yet the cellular physiology and sensory‐response profiles of aromatase neurons are essentially unknown. I...
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Vocal learning species must form and extensively hone associations between sounds and social contingencies. In songbirds, dopamine signaling guides song motor-production, variability, and motivation, but it is unclear how dopamine regulates fundamental auditory associations for learning new sounds. We hypothesized that dopamine regulates learning i...
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In vertebrates, advanced cognitive abilities are typically associated with the telencephalic pallium. In mammals, the pallium is a layered mixture of excitatory and inhibitory neuronal populations with distinct molecular, physiological, and network phenotypes. This cortical architecture is proposed to support efficient, high-level information proce...
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Synopsis Goal-directed learning is a key contributor to evolutionary fitness in animals. The neural mechanisms that mediate learning often involve the neuromodulator dopamine. In higher order cortical regions, most of what is known about dopamine’s role is derived from brain regions involved in motivation and decision-making, while significantly le...
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Encoding of conspecific signals during development can reinforce species barriers as well as set the stage for learning and production of species‐typical vocalizations. In altricial songbirds, development of the auditory system is not complete at hatching, so it is unknown the degree to which recently hatched young can process auditory signals like...
Preprint
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In vertebrates, advanced cognitive abilities are associated with a highly developed telencephalic pallium. In mammals, the six-layered neocortex of the pallium is composed of excitatory neurons and inhibitory interneurons, organized across layers into microcircuits. These organizational principles are proposed to support efficient, high-level infor...
Preprint
Full-text available
Vocal learning species must form and extensively hone associations between sounds and social contingencies. In songbirds, dopamine signaling guides song motor-production, variability, and motivation, but it is unclear how dopamine regulates fundamental auditory associations for learning new sounds. We hypothesized that dopamine regulates learning i...
Chapter
This chapter explores the current understanding of the hormonal regulation of auditory function in songbirds by focusing on three themes. The first section is an overview of seasonal changes in the auditory pathway that are regulated by hormones. Next, the concept of the songbird brain as both a source and a target of neuromodulatory steroid hormon...
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Birdsong learning, like human speech, depends on the early memorization of auditory models, yet how initial auditory experiences are formed and consolidated is unclear. In songbirds, a putative cortical locus is the caudomedial nidopallium (NCM), and one mechanism to facilitate auditory consolidation is 17β-estradiol (E2), which is associated with...
Article
Decades of work have established the brain as a source of steroid hormones, termed ‘neurosteroids’. The neurosteroid neuroestradiol is produced in discrete brain areas and influences cognition, sensory processing, reproduction, neurotransmission, and disease. A prevailing research focus on neuroestradiol has essentially ignored whether its immediat...
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Animals continually assess their environment for cues associated with threats, competitors, allies, mates or prey, and experience is crucial for those associations. The auditory cortex is important for these computations to enable valence assignment and associative learning. The caudomedial nidopallium (NCM) is part of the songbird auditory associa...
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Neuron-derived estrogens are synthesized by aromatase and act through membrane receptors to modulate neuronal physiology. In many systems, long-lasting hormone treatments can alter sensory-evoked neuronal activation. However, the significance of acute neuroestrogen production is less understood. Both sexes of zebra finches can synthesize estrogens...
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Rodent dorsal medial prefrontal cortex (mPFC), typically prelimbic cortex, is often described as promoting actions such as reward seeking, whereas ventral mPFC, typically infralimbic cortex, is thought to promote response inhibition. However, both dorsal and ventral mPFC are necessary for both expression and suppression of different behaviors, and...
Preprint
Full-text available
Birdsong, like human speech, is learned early in life by first memorizing an auditory model. Once memorized, birds compare their own burgeoning vocalizations to their auditory memory, and adjust their song to match the model. While much is known about this latter part of vocal learning, less is known about how initial auditory experiences are forme...
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Breast cancer patients using aromatase inhibitors (AIs) as an adjuvant therapy often report side effects including hot flashes, mood changes, and cognitive impairment. Despite long-term use in humans, little is known about the effects of continuous AI administration on the brain and cognition. We used a primate model of human cognitive aging, the c...
Article
Steroid hormones, such as estrogens, were once thought to be exclusively synthesized in the ovaries and enact transcriptional changes over the course of hours to days. However, estrogens are also locally synthesized within neural circuits, wherein they rapidly (within minutes) modulate a range of behaviors, including spatial cognition and communica...
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Estrogens affect cerebellar activity and cerebellar-based behaviors. Within the adult rodent cerebellum, the best-characterized action of estradiol is to enhance glutamatergic signaling. However, the mechanism(s) by which estradiol promotes glutamatergic neurotransmission remain unknown. Within the mouse cerebellum, we find that estrogen receptor a...
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Estradiol acts as a neuromodulator in brain regions important for cognition and sensory processing. Estradiol also shapes brain sex differences, but rarely have these concepts been considered simultaneously. In male and female songbirds, estradiol rapidly increases within the auditory forebrain during song exposure and enhances local auditory proce...
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This brief commentary reviews key steps in the history of endocrinology that have resulted in important conceptual shifts. Our understanding of the "Fast Effects of Steroids" has now made substantial progress, including the major concept that steroids act rapidly on a variety of physiological and behavioral responses, via mechanisms that are too fa...
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In humans and other animals, behavioural variation in learning has been associated with variation in neural features like morphology and myelination. By contrast, it is essentially unknown whether cognitive performance scales with electrophysiological properties of individual neurons. Birdsong learning offers a rich system to investigate this topic...
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Vocal learning occurs during an experience-dependent, age-limited critical period early in development. In songbirds, vocal learning begins when presinging birds acquire an auditory memory of their tutor’s song (sensory phase) followed by the onset of vocal production and refinement (sensorimotor phase). Hearing is necessary throughout the vocal le...
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Norepinephrine (NE) can dynamically modulate excitability and functional connectivity of neural circuits in response to changes in external and internal states. Regulation by NE has been demonstrated extensively in mammalian sensory cortices, but whether NE-dependent modulation in sensory cortex alters response properties in downstream sensorimotor...
Article
Species diversity in experimental neuroscience research provides a vital resource. Addressing contemporary questions using nontraditional model systems (i.e., studies of species other than rats or mice) have regularly led to serendipitous breakthroughs in this discipline. The “comparative” approach to neuroscience and neuroendocrinology harnesses t...
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A fast, neuromodulatory role for estrogen signaling has been reported in many regions of the vertebrate brain. Regional differences in the cellular distribution of aromatase (estrogen synthase) in several species suggest that mechanisms for neuroestrogen signaling differ between and within brain regions. A more comprehensive understanding of neuroe...
Chapter
The avian brain is both a target and a source of estrogens. The rapid effects of estrogens on avian social behavior have been studied extensively in both captive and free-living birds. Here we present accumulated evidence that brain estrogens regulate avian social behaviors. Fast changes in neuroestrogens occur during sexual behavior, aggression, a...
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Over the past two decades, the classical understanding of steroid action has been updated to include rapid, membrane-initiated, neurotransmitter-like functions. While steroids were known to function on very short time spans to induce physiological and behavioral changes, the mechanisms by which these changes occur are now becoming more clear. In av...
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The potent estrogen 17β-Estradiol (E2) plays a critical role in mediating hippocampal function, yet the precise mechanisms through which E2 enhances hippocampal memory remain unclear. In young adult female rodents, the beneficial effects of E2 on memory are generally attributed to ovarian-synthesized E2. However, E2 is also synthesized in the adult...
Chapter
A growing body of literature points to the importance of estrogens in the development, maintenance, modulation, and protection of vertebrate audition. Birds, with their long history in endocrinological research, and their reliance on vocal communication for reproductive and social interactions, have proven to be particularly fruitful for such studi...
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The vertebrate central nervous system integrates cognition and behavior, and it also acts as both a source and target for steroid hormones like estrogens. Recent exploration of brain estrogen production in the context of learning and memory has revealed several common themes. First, across vertebrates, the enzyme that synthesizes estrogens is expre...
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The catecholamine norepinephrine plays a significant role in auditory processing. Most studies to date have examined the effects of norepinephrine on the neuronal response to relatively simple stimuli, such as tones and calls. It is less clear how norepinephrine shapes the detection of complex syntactical sounds, as well as the coding properties of...
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Estrogens shape brain circuits during development, and the capacity to synthesize estrogens locally has consequences for both sexual differentiation and the acute modulation of circuits during early learning. A recently-optimized method to detect and quantify fluctuations in brain estrogens in vivo provides a direct means to explore how brain estro...
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The actions of estrogens have been associated with brain differentiation and sexual dimorphism in a wide range of vertebrates. Here we consider the actions of brain-derived 'neuroestrogens' in the forebrain and the accompanying differences and similarities observed between males and females in a variety of species. We summarize recent evidence show...
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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...
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Neuromodulators rapidly alter activity of neural circuits and can therefore shape higher order functions, such as sensorimotor integration. Increasing evidence suggests that brain-derived estrogens, such as 17-β-estradiol, can act rapidly to modulate sensory processing. However, less is known about how rapid estrogen signaling can impact downstream...
Article
Neurons communicate primarily via action potentials that transmit information on the timescale of milliseconds. Neurons also integrate information via alterations in gene transcription and protein translation that are sustained for hours to days after initiation. Positioned between these two signaling timescales are the minute-by-minute actions of...
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It is now clear that estrogens are not just circulating reproductive hormones, but that they also have neurotransmitter-like properties in a wide range of brain circuits. The view of estrogens as intrinsic neuromodulators that shape behavior has been bolstered by a series of recent developments from multiple vertebrate model systems. Here, we revie...
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This chapter explores recent evidence that estrogen production and action within acoustic communication circuits occurs rapidly, at the time scale of neuromodulation (seconds to minutes). The chapter traces historical roots of this relatively new idea, and summarizes insights from comparative studies of vocalizing fish and avian species, which have...
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Although estrogens are widely considered circulating "sex steroid hormones" typically associated with female reproduction, recent evidence suggests that estrogens can act as local modulators of brain circuits in both males and females. The functional implications of this newly characterized estrogen signaling system have begun to emerge. This essay...
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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...
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The activity of sensory circuits is shaped by neuromodulators, which can have downstream consequences for both sensorimotor integration and behavioral output. Recent evidence indicates that brain-derived estrogens ("neuroestrogens") can act as local circuit modulators in the songbird auditory forebrain. Specifically, neuroestrogens fluctuate in the...
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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...
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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....
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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...
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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...
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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...
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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...
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Higher cognitive function depends on accurate detection and processing of subtle features of sensory stimuli. Such precise computations require neural circuits to be modulated over rapid timescales, yet this modulation is poorly understood. Brain-derived steroids (neurosteroids) can act as fast signaling molecules in the vertebrate central nervous...
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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 vocaliza...
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The forebrain circuits involved in singing and audition (the 'song system') in songbirds exhibit a remarkable capacity to synthesize and respond to steroid hormones. This review considers how local brain steroid production impacts the development, sexual differentiation, and activity of song system circuitry. The songbird forebrain contains all of...
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Concepts of brain-steroid signaling have traditionally placed emphasis on the gonads and adrenals as the source of steroids, the strict dichotomy of early developmental ("organizational") and mature ("activational") effects, and a relatively slow mechanism of signaling through intranuclear receptors. Continuing research shows that these concepts ar...
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The enzyme aromatase, which converts androgens into oestrogens, is expressed throughout the brain in zebra finches. Aromatase is enzymatically active in both cell bodies and synaptic terminals of neurones of the songbird brain, particularly within the forebrain motor and auditory networks. Aromatisation within synaptic terminals could thus provide...
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Neurosteroids are powerful modulators of brain function and behavior, yet their dynamics in the brain have remained elusive. Using in vivo microdialysis in male zebra finches, we found that local estradiol levels increased rapidly in the forebrain during social interactions with females. Furthermore, when males were exposed to other males' songs, l...
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Historically, most studies of vertebrate central pattern generators (CPGs) have focused on mechanisms for locomotion and respiration. Here, we highlight new results for ectothermic vertebrates, namely teleost fish and amphibians, showing how androgenic steroids can influence the temporal patterning of CPGs for social vocalization. Investigations of...
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Divergent steroid hormone profiles can shape the development of male versus female neural phenotypes, but whether they also determine differences in the short-term, neurophysiological patterning of behavior is unknown. We now show that steroid hormone-specific modulation of a vocal pattern generator (VPG) diverges between reproductive morphs in a t...
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The plainfin midshipman fish, Porichthys notatus, is a well-established neuroethological model system that has provided insights into neural and endocrine mechanisms of vocal-acoustic communication that are shared by teleost fishes and tetrapods, including birds and mammals. The reproductive success of midshipman fish is intricately linked to the p...
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The long-term transcriptional actions of steroids that shape neuronal morphology and the probability of behavioral expression are well established. More recently, attention has been focused on the role of rapid (minute-by-minute) steroid actions on neuronal mechanisms of reproductive behavior. In this review, we first consider the rapid actions of...
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The passive listening hypothesis proposes that dolphins and whales detect acoustic signals emitted by prey, including sound-producing (soniferous) fishes. Previous work showed that bottlenose dolphins (Tursiops truncatus) behaviorally orient toward the sounds of prey, including the advertisement calls of male Gulf toadfish (Opsanus beta). In additi...
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Across vertebrates, androgens are rapidly elevated within minutes in response to aggressive or reproductive stimuli, yet it is unclear what the causal relationship is between fast androgen elevation and the ongoing (minute-by-minute) expression of behavior. This study tested the hypothesis that rapid increases in plasma steroid levels induce simila...
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It is well known that plasma androgens are rapidly released in response to aggressive or sexual stimuli in a broad array of vertebrates. However, experimental work on behavioral functions of rapid androgen elevation is rare. A combination of field-based behavioral experiments and lab-based neuroendocrinological approaches is beginning to show how s...
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Vocal control systems have been identified in all major groups of jawed vertebrates. Although steroid hormones are instrumental in the long-term development and maintenance of neural structures underlying vocalization, it is unknown whether steroids rapidly modulate the neural activity of vocal motor systems. The midshipman fish generates advertise...
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The adaptive value of social affiliation has been well established. It is unclear, however, what endogenous mechanisms may mediate affiliative behavior. The Australian zebra finch (Taeniopygia guttata) breeds colonially and adults maintain lifelong pair bonds that may be disrupted in the wild due to high mortality rates. Many of its natural, social...
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Captive starlings (Sturnus vulgaris) undergoing a prebasic molt were given exogenous insulin (INS) and corticosterone (CORT), to determine how these counterregulatory hormones would affect glucose and triglyceride concentrations during stress. Experiments were conducted at both morning (11:00) and night (23:00) to monitor daily variation in these r...
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Captive European starlings (Sturnus vulgaris) were exposed to the stress of handling and restraint while corticosterone, glucose, and triglyceride concentrations were monitored in blood plasma. In saline-injected controls, basal samples were taken within 3 min of disturbance with subsequent samples taken at 40, 70, and 150 min. This was repeated at...
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Captive starlings were used to examine daily and seasonal changes in basal and stress-induced corticosterone levels. Birds were bled at 4 times during the daily cycle and during three different simulated seasons: under a short-day photoperiod (mimicking winter), under a long-day photoperiod (mimicking summer), and while undergoing a prebasic molt....
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We investigated the seasonal and daily variation in plasma glucose levels in response to stress in captive wild starlings. Starlings were captured from the wild during the winter, held on short days (11L:13D, mimicking winter), and then shifted to long days (19L:5D, mimicking summer). Birds were maintained on long days until they began a prebasic m...

Citations

... By regulating the androgen/estrogen ratio, aromatase modulates various biological processes and contributes to sexspecific behavioral responses. Our current understanding of how aromatase-positive neurons are connected into brain networks was recently reviewed (Spool et al. 2021). Here, we summarize the current evidence to better understand whether and how aromatase, from the OE and OB, contribute to this network, possibly by modulation of olfactory sensitivity. ...
... In addition, 5α-DHP, 5α-DHDOC, 5α-DHB, 5α-DHADIONE, and 5α-DHT can be reduced, respectively, to 3β5α-THP, 3β5α-THDOC, 3β5α-THB, 3β5α-THA, and 3β5α-THT by the 3β-hydroxysteroid oxidoreductase. Testosterone can also be converted to 17β-estradiol via local aromatization in the brain (20). Biosynthesis of steroid hormones and their precursors and metabolites, referred to as steroidogenesis, is a complex and fine-tuned process. ...
... First, a pharmacological approach shows that song-driven induction of immediate-early gene expression in NCM neurons is dependent on aromatase activity to a similar extent in males and females (Krentzel et al., 2020). Second, an immunocytochemical approach examining the expression of aromatase coupled with the immediate-early gene egr-1 showed that aromatase neurons are similar in abundance, as well as equivalently responsive to song in the NCM of adult males and females (de Bournonville et al., 2021a). Furthermore, in vitro whole-cell recordings from aromatase neurons of the rodent MeA showed that their intrinsic excitability, including passive and active membrane properties, was indistinguishable between adult males and females ( Fig. 3A; Billing et al., 2020;de Bournonville et al., 2021a). ...
... Furthermore, in juvenile zebra finches, song tutoring increased VTA activation . We have recently established a causal relationship between local dopaminergic manipulations and NCM plasticity and learning mechanisms (Macedo-lima et al. 2020). Yet, whether and how dopamine from VTA (or other nuclei) is involved in auditory learning is unclear. ...
... Most prominently, the optic tectum and neighboring tegmental nuclei show modulation in the gamma range during attention (Goddard et al., 2012;Neuenschwander and Varela, 1993;Sridharan et al., 2011;Sridharan and Knudsen, 2015). Gamma band modulations were further reported in the avian forebrain during birdsong (Brown et al., 2021;Lewandowski and Schmidt, 2011;Spool et al., 2021), and in the avian hippocampal formation in vitro (Dheerendra et al., 2018) and during sleep (van der Meij et al., 2020). However, these observations cannot answer the question of whether oscillations underlie higher cognition since they were either made in the neatly layered optic tectum, were tightly linked to motor behavior, or occurred in sleeping birds. ...
... The increase of ACh levels in F rats suggests that a short-term fructose enriched diet may disrupt cholinergic signaling and predispose adolescents to altered states, such as anxiety disorders and depression, also corroborated by BDNF and dopamine reduction. The observed decrease of dopamine, which regulates different brain functions such as reinforcement processing, motivation, and attention [85], might be ascribed to both the corresponding enhanced MAO activity and the reduced amounts of tyrosine and tyramine. In agreement with our findings, previous studies have reported that HFCS can impair dopamine function in the absence of weight gain or increased fat consumption [10]. ...
... Later, mainly in zebra finches, the neural responses were compared across ages to investigate how such neural selectivity develops. Consistent with the sensitivity to ownspecies song at a behavioral level, electrophysiological recordings (Stripling et al., 2001;Schroeder and Remage-Healey, 2021) and immunohistochemical assay (Stripling et al., 2001;Wade, 2003, Bailey andWade, 2005) showed that some neurons in the NCM selectively respond to conspecific song over heterospecific song either at a single-cell level or at a population level. These results indicated that the selectivity is already present at the age of 20 days post hatch, which is said to be the beginning of the sensory learning in this species (Roper and Zann, 2006). ...
... For example, neural and behavioral responses to vocal signals have been shown to differ in breeding versus nonbreeding individuals (Adreani et al., 2020;Maney & Pinaud, 2011). Moreover, local application of estrogen alters the activity of song-responsive neurons in the secondary auditory cortex (Caras & Remage-Healey, 2016;Remage-Healey et al., 2010;Remage-Healey, 2020), suggesting that physiological changes caused by breeding influence the perceptual processing of auditory signals. ...
... Extracellular single-unit recording was performed in vivo in awake-restrained birds as in previous studies (Miller-Sims & Bottjer, 2014;Schneider & Woolley, 2013;Vahaba et al., 2020). Subjects were brought into an anechoic chamber and fixed to a stereotaxic apparatus (Herb Adams Engineering) on an air table at a 45° head angle. ...
... Studies from the same lab have not been able to replicate results using an immunoassay for measurement of 17b -E 2 in zebra finch brain microdialysate, which might be because of changes in the commercial immunoassay (C. de Bournonville et al., 2020). Further, when 17b -E 2 was measured in the same sample by both LC-MS/MS and immunoassay in quail brain microdialysate, LC-MS/ MS detected far lower 17b -E 2 concentrations than the immunoassay (M.P. de Bournonville et al., 2021), suggesting antibody cross-reactivity. ...