Ontogeny of Song Recognition in Birds

SYNOPSIS. This paper reviews song recognition in two congenericspecies of sparrow the swamp sparrow (Melospiza georgiana) andsong sparrow (Melospiza melodia). Data from psychophysical studiesof hearing, tutoring experiments with young birds, and fieldplayback studies with adult birds are considered together inorder to gain insight into the mechanisms of species recognitionthrough song development. In aggregate, the evidence suggestsa multi-stage process of song development consisting of an earlyperceptual preference for learning conspecific song, a sensorimotorphase of song development during which vocal output matchesan auditory memory as if through trial and error, and a finalphase of full song which functions in territorial defense andmate attraction.     

Neuroendocrine and behavioral implications of endocrine disrupting chemicals in quail

Studies in our laboratory have focused on endocrine, neuroendocrine, and behavioral components of reproduction in the Japanese quail. These studies considered various stages in the life cycle, including embryonic development, sexual maturation, adult reproductive function, and aging. A major focus of our research has been the role of neuroendocrine systems that appear to synchronize both endocrine and behavioral responses. These studies provide the basis for our more recent research on the impact of endocrine disrupting chemicals (EDCs) on reproductive function in the Japanese quail. These endocrine active chemicals include pesticides, herbicides, industrial products, and plant phytoestrogens. Many of these chemicals appear to mimic vertebrate steroids, often by interacting with steroid receptors. However, most EDCs have relatively weak biological activity compared to native steroid hormones. Therefore, it becomes important to understand the mode and mechanism of action of classes of these chemicals and sensitive stages in the life history of various species. Precocial birds, such as the Japanese quail, are likely to be sensitive to EDC effects during embryonic development, because sexual differentiation occurs during this period. Accordingly, adult quail may be less impacted by EDC exposure. Because there are a great many data available on normal development and reproductive function in this species, the Japanese quail provides an excellent model for examining the effects of EDCs. Thus, we have begun studies using a Japanese quail model system to study the effects of EDCs on reproductive endocrine and behavioral responses. In this review, we have two goals: first, to provide a summary of reproductive development and sexual differentiation in intact Japanese quail embryos, including ontogenetic patterns in steroid hormones in the embryonic and maturing quail. Second, we discuss some recent data from experiments in our laboratory in which EDCs have been tested in Japanese quail. The Japanese quail provides an excellent avian model for testing EDCs because this species has well-characterized reproductive endocrine and behavioral responses. Considerable research has been conducted in quail in which the effects of embryonic steroid exposure have been studied relative to reproductive behavior. Moreover, developmental processes have been studied extensively and include investigations of the reproductive axis, thyroid system, and stress and immune responses. We have conducted a number of studies, which have considered long-term neuroendocrine consequences as well as behavioral responses to steroids. Some of these studies have specifically tested the effects of embryonic steroid exposure on later reproductive function in a multigenerational context. A multigenerational exposure provides a basis for understanding potential exposure scenarios in the field. In addition, potential routes of exposure to EDCs for avian species are being considered, as well as differential effects due to stage of the life cycle at exposure to an EDC. The studies in our laboratory have used both diet and egg injection as modes of exposure for Japanese quail. In this way, birds were exposed to a specific dose of an EDC at a selected stage in development by injection. Alternatively, dietary exposure appears to be a primary route of exposure; therefore experimental exposure through the diet mimics potential field situations. Thus, experiments should consider a number of aspects of exposure when attempting to replicate field exposures to EDCs.     

Aging and Reproduction: Comparative Endocrinology of the Common Tern and Japanese Quail

SYNOPSIS. The endocrinology of reproductive aging in avian specieshas been described primarily in captive domestic birds, suchas the Japanese quail (Coturnix japonica), which show majorchanges in hormones and reproductive performance. To explorereproductive aging in longer-lived avian species, longitudinalstudies are being conducted on the Common Tern (Sterna hirundo)in which age-related changes in nesting patterns and clutchsize have been monitored. However, little information is availablerelevant to endocrine status of breeding pairs of Common Terns.This review summarizes information pertinent to the breedingbiology and endocrine status of the Common Tern during reproductiveaging and compares these findings to data available from theJapanese quail. Fundamental mechanisms in the process of agingin avian species may become apparent in the comparison of thesedata and data from field species.     

Genetic Control of Acoustic Behavior in Crickets

Evidence is presented that acoustic behavior in field cricketsis under firm genetic control. The calling song of adult malesis highly stereotyped and species specific. Hybrids can be madeby crossing two species of Teleogryllus with dissimilar callingsongs. The calling songs of the hybrids are uniquely differentfrom that of either parental species, and in addition the songsof the two reciprocal hybrids are different from each other.Genetic control of song production is polygenic and multichromosomal;sex-linkage of some song determinants is also indicated. Femalephonoresponse to calling song was measured on a Y-maze. Speciesspecificity of phonoresponse was confirmed and in addition,hybrid females prefer hybrid song to either parental song. Thepossibility that calling song production in the male and itsreception in the female are genetically coupled is discussed.     

Development of cardiac rhythms in altricial avian embryos

Mean heart rate (MHR) was determined during incubation and in hatchlings of 14 altricial avian species to investigate (1) if there is a common developmental pattern of heart rate in altricial embryos and (2) if heart rate changes during incubation are correlated with changes in embryonic growth rate. On the basis of normalized incubation MHR increased approximately linearly in 12 of 14 species from as early as 30-40% of incubation to that of pipped embryos. The MHR of hatchlings was equal to or higher than that of pipped embryos in seven species. Passerine embryos and hatchlings maintained higher MHR in comparison to parrots of similar egg mass, which may reflect phylogenetic differences in development. Embryonic MHR increased at a higher rate while embryonic growth rates were highest during the first 40% of incubation in tit, budgerigar and crow embryos than during subsequent development when relative growth rates decreased. MHR became independent of yolk-free wet mass at a smaller fraction of hatchling mass in budgerigar and crow than in the tit, suggesting that MHR is more likely to increase continuously after 40% of incubation in small altricial species than larger species.     

Effects of learning on song preferences and Zenk expression in female songbirds

Male songbirds learn to produce their songs, and females attend to these songs during mate choice. The evidence that female song preferences are learned early in life, however, is mixed. Here we review studies that have found effects of early song learning on adult song preferences, and those that have not. In at least some species, early experience with song can modify adult song preferences. Whether this learning needs to occur during an early sensitive phase, akin to male imitative vocal learning, or not remains an open question. Studies of the neural bases for female song preferences highlight activity (as measured by immediate-early gene induction) in regions of the auditory forebrain as often, but not always, being associated with song preferences. Immediate-early gene induction in these regions, however, is not specific to songs experienced early in life. On the whole, inherited factors, early experience, and adult experience all appear to play a role in shaping female songbirds preferences for male songs.     

Neuroanatomical Correlates of Hormone Sensitive Behaviors in Frogs and Birds

In this paper I review some aspects of neural and endocrineinteractions in the control of reproductive behaviors of frogsand song birds. In Xenopus laevis, we have shown that castrationwill eliminate a male sex behavior, clasping, and that thisbehavior can be restored by the administration of exogenoustestosterone or dihydrotestosterone but not by estradiol. Thisdifference in hormone action is paralleled by differences inthe locations of androgen and estrogen concentrating cells inthe CNS of Xenopus. Certain brain regions contain autoradiographicallydemonstrable labelled cells only after the administration oftritiated testosterone; others only after estradiol injection.The possibility that label in a third group of nuclei, whichcontain radioactive steroid after either hormone, is due tometabolism of testosterone to estradiol is discussed. Studiesin other anuran species have demonstrated that regions of hormoneuptake are also involved in neural control of frog sex behavior.The song of oscine birds represents another hormone sensitivereproductive behavior whose neural control is probably inlluencedby the activity of hormone concentrating CNS cells. Some ofthe brain nuclei which comprise the efferent pathway for controlof song in the canary have been shown to concentrate tritiatedandrogen in autoradiographic studies on song birds. The uptakeof androgens by medullary motor neurons involved in the controlof reproductively important vocalizations is common to anuransand oscine song birds. Whether this feature of hormone actionon the CNS represents a special feature of the frog and birdbrain or whether the phenomenon may also be present in othervertebrate groups awaits further investigation.     

The evolution of immune defense and song complexity in birds

Abstract There are three main hypotheses that explain how the evolution of parasite virulence could be linked to the evolution of secondary sexual traits, such as bird song. First, as Hamilton and Zuk proposed a role for parasites in sexual selection, female preference for healthy males in heavily parasitized species may result in extravagant trait expression. Second, a reverse causal mechanism may act, if sexual selection affects the coevolutionary dynamics of host-parasite interactions per se by selecting for increased virulence. Third, the immuno-suppressive effects of ornamentation by testosterone or limited resources may lead to increased susceptibility to parasites in species with elaborate songs. Assuming a coevolutionary relationship between parasite virulence and host investment in immune defense we used measures of immune function and song complexity to test these hypotheses in a comparative study of passerine birds. Under the first two hypotheses we predicted avian song complexity to be positively related to immune defense among species, whereas this relationship was expected to be negative if immuno-suppression was at work. We found that adult T-cell mediated immune response and the relative size of the bursa of Fabricius were independently positively correlated with a measure of song complexity, even when potentially confounding variables were held constant. Nestling T-cell response was not related to song complexity, probably reflecting age-dependent selective pressures on host immune defense. Our results are consistent with the hypotheses that predict a positive relationship between song complexity and immune function, thus indicating a role for parasites in sexual selection. Different components of the immune system may have been independently involved in this process.     

Early appearance of catecholaminergic neurons in the central nervous system of precocial and altricial avian species

Summary The early appearance of catecholaminergic neurons, as revealed by fluorescence histochemistry, has been determined in the central nervous system of quail, pheasant, and pigeon embryos. The first neuronal assemblies displaying specific fluorescence are the locus coeruleus and the nucleus subcoeruleus ventralis. Taking into account the differences in the length of the prehatching period of these three avian species, the first catecholamine-containing neurons appear earlier in the precocial quail and pheasant than in the altricial pigeon.Investigation supported by grants from the Italian National Research Council (CNR) No 83.02058.04 (R.G.) and No 83.00492.04 (G.C.P.).     

Developmental patterns of NMDAR expression within the song system do not recur during adult vocal plasticity in zebra finches

All songbirds learn to sing during postnatal development but then display species differences in the capacity to learn song in adulthood. While the mechanisms that regulate avian vocal plasticity are not well characterized, one contributing factor may be the composition of N-methyl-D-aspartate receptors (NMDAR). Previous studies of an anterior forebrain pathway implicated in vocal plasticity revealed significant regulation of NMDAR subunit expression during the developmental sensitive period for song learning. Much less is known about the developmental regulation of NMDAR subunit expression in regions that participate more directly in motor aspects of song behavior. We show here that an increase in NR2A subunit mRNA and a decrease in NR2B subunit mRNA within the vocal motor pathway accompany song learning in zebra finches; however, manipulations that can alter the timing of song learning did not alter the course of these developmental changes. We also tested whether adult deafening, a treatment that provokes vocal change in songbirds that normally sing a stable song throughout adulthood, would render NMDAR subunit expression more similar to that observed developmentally. We report that NR2A and NR2B mRNA levels did not change within the anterior forebrain or vocal motor pathways after adult deafening, even after substantial changes in song structure. These results indicate that vocal plasticity does not require "juvenile patterns" of NMDAR gene expression in the avian song system.     

Mode of development and interspecific avian brood parasitism

Avian interspecific brood parasites differ considerably in theircommitment to parasitism; 87 species are obligate brood parasites,whereas 35 species are known to be facultative brood parasites.This variation is strongly related to mode of development. Obligateparasitism is found almost exclusively in altricial species,whereas facultative interspecific parasitism is predominantin precocial birds. We propose that the association betweenmode of development and form of parasitism reflects a fundamentaldifference between altricial and precocial birds in the relativebenefits of emancipation from parental care after laying. Weargue that altricial brood parasites obtain such a large increasein realized fecundity by avoiding the costs of parental carethat obligate parasitism is favored over facultative parasitism.In contrast, precocial brood parasites gain relatively littlein terms of increased fecundity via obligate parasitism, andmuch of this increase could potentially be gained by facultativeparasitism. Thus, obligate interspecific brood parasitism willnot be favored in precocial birds. Three factors influence thisdifference between altricial and precocial species: (1) altricialbirds have relatively more energy and nutrients with which tolay additional eggs, (2) altricial birds can produce more eggsfor the same amount of energy and nutrients, and (3) altricialbirds realize a greater relative gain in fecundity for eachadditional egg laid. We suggest further that facultative interspecificparasitism in birds may originate simply through a carry overof intraspecific parasitism; 29 of 33 facultative interspecificparasites also parasitize conspecifics. Facultative parasitismof other species would provide a greater range of potentialhost nests and could be maintained as an evolutionarily stableend point by the same mechanisms that maintain intraspecificbrood parasitism. [Behav Ecol 1991;2:309–318]     

Age effect of deafening on stereotyped song maintenance in adult male bengalese finches Lonchura striata domestica

Birdsong is a complex learned vocal behavior that relies on auditory experience for development.However,it appears that among different species of close-ended songbirds,there are some variations in the necessity of auditory feedback for maintaining stereotyped adult song.In zebra finches,the deterioration of adult songs following deafness depends on the birds' age.It is unknown whether this age effect is a general rule in other avian species as well.Therefore,we chose Bengalese finches,whose songs show more...     

Androgen Regulation of Avian Premigratory Hyperphagia and Fattening: From Eco-Physiology to Neuroendocrinology

In many high latitude-breeding avian species, reproductive andwintering seasons are separated by migratory periods that involvedramatic physiological and behavioral adjustments such as hyperphagiaand fat deposition. The endocrine mechanisms responsible forthese adjustments have been extensively studied, yet remainonly partly understood. The currently available informationindicates that food consumption and/or fattening can be experimentallymodulated by multiple hormones including testosterone, prolactin,glucocorticoids, and opioids. These hormones may control migratoryfunctions through mutual interactions rather than independently.Little is known, however, concerning the nature of these interactionsand their relative importance in the control of annual cyclesin natural conditions. This paper focuses on the role of gonadalandrogens in the control of migratory functions, and it summarizesthe information which is available on the physiological andbehavioral interactions between these androgens and other hormones.     

Memory in the making: localized brain activation related to song learning in young songbirds

Songbird males learn to sing their songs from an adult ‘tutor’ early in life, much like human infants learn to speak. Similar to humans, in the songbird brain there are separate neural substrates for vocal production and for auditory memory. In adult songbirds, the caudal pallium, the avian equivalent of the auditory association cortex, has been proposed to contain the neural substrate of tutor song memory, while the song system is involved in song production as well as sensorimotor learning. If this hypothesis is correct, there should be neuronal activation in the caudal pallium, and not in the song system, while the young bird is hearing the tutor song. We found increased song-induced molecular neuronal activation, measured as the expression of an immediate early gene, in the caudal pallium of juvenile zebra finch males that were in the process of learning to sing their songs. No such activation was found in the song system. Molecular neuronal activation was significantly greater in response to tutor song than to novel song or silence in the medial part of the caudomedial nidopallium (NCM). In the caudomedial mesopallium, there was significantly greater molecular neuronal activation in response to tutor song than to silence. In addition, in the NCM there was a significant positive correlation between spontaneous molecular neuronal activation and the strength of song learning during sleep. These results suggest that the caudal pallium contains the neural substrate for tutor song memory, which is activated during sleep when the young bird is in the process of learning its song. The findings provide insight into the formation of auditory memories that guide vocal production learning, a process fundamental for human speech acquisition.     

Adult bengalese finches (Lonchura striata var. domestica) require real-time auditory feedback to produce normal song syntax

Songbirds develop their songs by imitating songs of adults. For song learning to proceed normally, the bird's hearing must remain intact throughout the song development process. In many species, song learning takes place during one period early in life, and no more new song elements are learned thereafter. In these so-called close-ended learners, it has long been assumed that once song development is complete, audition is no longer necessary to maintain the motor patterns of full song. However, many of these close-ended learners maintain plasticity in overall song organization; the number and the sequence of song elements included in a song of an individual vary from one utterance to another, although no new song elements are added or lost in adulthood. It is conceivable that these species rely on continued auditory feedback to produce normal song syntax. The Bengalese finch is a close-ended learner that produces considerably variable songs as an adult. In the present study, we found that Bengalese finches require real-time auditory feedback for motor control even after song learning is complete; deafening adult finches resulted in development of abnormal song syntax in as little as 5 days. We also found that there was considerable individual variation in the degree of song deterioration after deafening. The neural mechanisms underlying adult song production in different species of songbirds may be more diverse than has been traditionally considered. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 343–356, 1997     

Influences of weather on reproductive function in male Song sparrows, Melospiza melodia

The avian reproductive cycle is integrated and timed by a variety of environmental factors that include day length, availability of food, nest sites, presence of a mate, etc. However, reproduction can be delayed or disrupted by inclement weather and, until recently, the endocrine responses of avian species to storms were entirely unknown. This communication describes changes in endocrine state in free-living male Song sparrows, Melospiza melodia, during gonadal recrudescence after a severe winter, and in response to storms in early spring and summer. Both the severe winter weather and an early spring snow storm delayed testicular development, and depressed circulating levels of testosterone. The sparrows did not appear to be stressed, however, since body mass and fat deposits were higher than in birds sampled during the previous spring after a less severe winter.
A second storm occurred in late May and early June when Song sparrows were feeding young. Curiously, plasma levels of testosterone were not affected, but the sparrows did appear to be stressed since there was a significant decline in body mass, and a marked increase in circulating levels of corticosterone. These data suggest that the effects of inclement weather on reproductive function can vary in relation to the stage in the reproductive cycle when the storm strikes, and that the endocrine mechanisms underlying acclimatization to severe meteorological conditions are also different.     

Early life conditions that impact song learning in male zebra finches also impact neural and behavioral responses to song in females

Early life stressors can impair song in songbirds by negatively impacting brain development and subsequent learning. Even in species in which only males sing, early life stressors might also impact female behavior and its underlying neural mechanisms, but fewer studies have examined this possibility. We manipulated brood size in zebra finches to simultaneously examine the effects of developmental stress on male song learning and female behavioral and neural response to song. Although adult male HVC volume was unaffected, we found that males from larger broods imitated tutor song less accurately. In females, early condition did not affect the direction of song preference: all females preferred tutor song over unfamiliar song in an operant test. However, treatment did affect the magnitude of behavioral response to song: females from larger broods responded less during song preference trials. This difference in activity level did not reflect boldness per se, as a separate measure of this trait did not differ with brood size. Additionally, in females we found a treatment effect on expression of the immediate early gene ZENK in response to tutor song in brain regions involved in song perception (dNCM) and social motivation (LSc.vl, BSTm, TnA), but not in a region implicated in song memory (CMM). These results are consistent with the hypothesis that developmental stressors that impair song learning in male zebra finches also influence perceptual and/or motivational processes in females. However, our results suggest that the learning of tutor song by females is robust to disturbance by developmental stress. © 2018 Wiley Periodicals, Inc. Develop Neurobiol, 2018     

Song tutoring triggers CaMKII phosphorylation within a specialized portion of the avian basal ganglia

In several songbird species, a specialized anterior forebrain pathway (AFP) that includes part of the avian basal ganglia has been implicated specifically in song learning. To further elucidate cellular mechanisms and circuitry involved in vocal learning, we used quantitative immunoblot analysis to determine if early song tutoring promotes within the AFP phosphorylation of calcium/calmodulin-dependent kinase II (CaMKII), a multifunctional kinase whose phosphorylation at threonine 286 is critical for many forms of neural plasticity and behavioral learning. We report that in young male zebra finches likely to have begun the process of song acquisition, brief tutoring by a familiar conspecific adult promotes a dramatic increase in levels of phosphorylated CaMKII (pCaMKII) in Area X, the striatal/pallidal component of the AFP. In contrast, pCaMKII levels in this region were not elevated if 1) the tutor did not sing, 2) the tutor sang but was visually isolated from the pupil, or 3) the tutor was an unfamiliar adult. In young males that had not previously heard any conspecific song, first exposure to a song tutor produced a more modest, but significant rise in pCaMKII levels. Young females (who do not develop song behavior) did not exhibit any effect of tutoring on pCaMKII levels in that portion of the basal ganglia that corresponds to Area X in males. These data are consistent with the hypothesis that Area X participates in encoding and/or attaching reward value to a representation of tutor song that is accessed later to guide motor learning.     

Hatching late in the season requires flexibility in the timing of song learning

Most songbirds learn their songs from adult tutors, who can be their father or other male conspecifics. However, the variables that control song learning in a natural social context are largely unknown. We investigated whether the time of hatching of male domesticated canaries has an impact on their song development and on the neuroendocrine parameters of the song control system. Average age difference between early- and late-hatched males was 50 days with a maximum of 90 days. Song activity of adult tutor males decreased significantly during the breeding season. While early-hatched males were exposed to tutor songs for on average the first 99 days, late-hatched peers heard adult song only during the first 48 days of life. Remarkably, although hatching late in the season negatively affected body condition, no differences between both groups of males were found in song characteristics either in autumn or in the following spring. Similarly, hatching date had no effect on song nucleus size and circulating testosterone levels. Our data suggest that late-hatched males must have undergone accelerated song development. Furthermore, the limited tutor song exposure did not affect adult song organization and song performance.     

Neuronal Organization of Mammalian Stellate Ganglion in Postnatal Ontogenesis

The paper considers the problem of peculiarities of maturation of the stellate ganglion nerve elements in mammals of different species. This process differs in precocious and altricial animals. It has been shown that in spite of some individual peculiarities, the neurons, fibers, and conducting pathways in altricial animals are not, on the whole, completely formed morphologically and functionally. In the course of postnatal ontogenesis, not only an increase of cell sizes and development of dendrite tree, but also reorganization of nerve connections with target organ occur. The postnatal ontogenesis is also accompanied by an increase of the excitation transmission rate along the fibers and by their myelination. The asymmetry of the right and left stellate ganglia (SG) by their sizes and functional peculiarities, which exists in adult animals appears as soon as at early stages of postnatal development. The neural elements of precocious animals are changed to a lesser extent in postnatal ontogenesis and are, in many aspects, similar to those of adult organisms as early as at birth.