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1.  Individual differences in the motivation to communicate relate to levels of midbrain and striatal catecholamine markers in male European starlings 
Hormones and behavior  2011;60(5):10.1016/j.yhbeh.2011.08.001.
Individuals display dramatic differences in social communication even within similar social contexts. Across vertebrates dopaminergic projections from the ventral tegmental area (VTA) and midbrain central gray (GCt) strongly influence motivated, reward-directed behaviors. Norepinephrine is also rich in these areas and may alter dopamine neuronal activity. The present study was designed to provide insight into the roles of dopamine and norepinephrine in VTA and GCt and their efferent striatal target, song control region area X, in the regulation of individual differences in the motivation to sing. We used high pressure liquid chromatography with electrochemical detection to measure dopamine, norepinephrine and their metabolites in micropunched samples from VTA, GCt, and area X in male European starlings (Sturnus vulgaris). We categorized males as sexually motivated or non-sexually motivated based on individual differences in song produced in response to a female. Dopamine markers and norepinephrine in VTA and dopamine in area X correlated positively with sexually-motivated song. Norepinephrine in area X correlated negatively with non-sexually-motivated song. Dopamine in GCt correlated negatively with sexually-motivated song, and the metabolite DOPAC correlated positively with non-sexually-motivated song. Results highlight a role for evolutionarily conserved dopaminergic projections from VTA to striatum in the motivation to communicate and highlight novel patterns of catecholamine activity in area X, VTA, and GCt associated with individual differences in sexually-motivated and non-sexually-motivated communication. Correlations between dopamine and norepinephrine markers also suggest that norepinephrine may contribute to individual differences in communication by modifying dopamine neuronal activity in VTA and GCt.
doi:10.1016/j.yhbeh.2011.08.001
PMCID: PMC3827950  PMID: 21907203
dopamine; norepinephrine; communication; motivation; social context; courtship; song control system; social behavior; sexual behavior; songbird
2.  Song in the cold is ‘hot’: memory of and preference for sexual signals perceived under thermal challenge 
Biology Letters  2012;8(5):751-753.
The environmental conditions under which signals are perceived can affect receiver responses. Many songbird populations produce a song chorus at dawn, when, in cold habitats, they would experience thermal challenge. We recorded temperature and the song activity of Lincoln's sparrows (Melospiza lincolnii) on a high-elevation meadow, and determined that song behaviour is concentrated around the coldest time of the day, at dawn. We hypothesized that this is because male song in the cold is more attractive to females than song in the warm. To test this, we exposed laboratory-housed Lincoln's sparrow females to songs at 1°C and 16°C, which they naturally experience in the wild. Females spent 40 per cent more time close to the speaker during playback at 1°C than at 16°C. When tested at 16°C 1–2 days later, females biased their movement towards the speaker playing songs previously heard at 1°C over 16°C. Thus, female Lincoln's sparrows remembered and affiliated with songs they heard under thermal challenge, indicating that the thermal environment can affect the attractiveness of a sexual signal.
doi:10.1098/rsbl.2012.0481
PMCID: PMC3441005  PMID: 22809726
dawn chorus; temperature; Melospiza lincolnii; mate choice; songbird
3.  Annual variation in vocal performance and its relationship with bill morphology in Lincoln’s sparrows 
Animal behaviour  2009;77(3):663-671.
Morphology may affect behavioural performance through a direct, physical link or through indirect, secondary mechanisms. Although some evidence suggests that the bill morphology of songbirds directly constrains vocal performance, bill morphology may influence vocal performance through indirect mechanisms also, such as one in which morphology influences foraging and thus the ability to perform some types of vocal behaviour. This raises the possibility for ecologically induced variation in the relationship between morphology and behaviour. To investigate this, I used an information theoretic approach to examine the relationship between bill morphology and several measures of vocal performance in Lincoln’s sparrows (Melospiza lincolnii). I compared this relationship between two breeding seasons that differed markedly in ambient temperatures, phenology of habitat maturation, and food abundance. I found a strong curvilinear relationship between bill shape (height/width) and vocal performance in the seemingly less hospitable season but not in the other, leading to a difference between seasons in the population’s mean vocal performance. Currently, I do not know the cause of this annual variation. However, it could be due to the effects of bill shape on foraging and therefore on time budget, energy balance, or some other behavioural or physiological response that manifests mostly under difficult environmental conditions or, alternatively, to associations between male quality and both vocal performance and bill shape. Regardless of the cause, these results suggest the presence of an indirect, ecologically mediated link between morphology and behavioural performance, leading to annual variation in the prevailing environment of acoustic signals.
doi:10.1016/j.anbehav.2008.11.016
PMCID: PMC2673008  PMID: 20160859
annual variation; bill morphology; bird song; environmental change; Lincoln’s sparrow; Melospiza lincolnii; sexual selection; signal production; trill performance
4.  Song Competition Affects Monoamine Levels in Sensory and Motor Forebrain Regions of Male Lincoln's Sparrows (Melospiza lincolnii) 
PLoS ONE  2013;8(3):e59857.
Male animals often change their behavior in response to the level of competition for mates. Male Lincoln's sparrows (Melospiza lincolnii) modulate their competitive singing over the period of a week as a function of the level of challenge associated with competitors' songs. Differences in song challenge and associated shifts in competitive state should be accompanied by neural changes, potentially in regions that regulate perception and song production. The monoamines mediate neural plasticity in response to environmental cues to achieve shifts in behavioral state. Therefore, using high pressure liquid chromatography with electrochemical detection, we compared levels of monoamines and their metabolites from male Lincoln's sparrows exposed to songs categorized as more or less challenging. We compared levels of norepinephrine and its principal metabolite in two perceptual regions of the auditory telencephalon, the caudomedial nidopallium and the caudomedial mesopallium (CMM), because this chemical is implicated in modulating auditory sensitivity to song. We also measured the levels of dopamine and its principal metabolite in two song control nuclei, area X and the robust nucleus of the arcopallium (RA), because dopamine is implicated in regulating song output. We measured the levels of serotonin and its principal metabolite in all four brain regions because this monoamine is implicated in perception and behavioral output and is found throughout the avian forebrain. After controlling for recent singing, we found that males exposed to more challenging song had higher levels of norepinephrine metabolite in the CMM and lower levels of serotonin in the RA. Collectively, these findings are consistent with norepinephrine in perceptual brain regions and serotonin in song control regions contributing to neuroplasticity that underlies socially-induced changes in behavioral state.
doi:10.1371/journal.pone.0059857
PMCID: PMC3608548  PMID: 23555809
5.  Estradiol-dependent Modulation of Serotonergic Markers in Auditory Areas of a Seasonally Breeding Songbird 
Behavioral Neuroscience  2011;126(1):110-122.
Because no organism lives in an unchanging environment, sensory processes must remain plastic so that in any context, they emphasize the most relevant signals. As the behavioral relevance of sociosexual signals changes along with reproductive state, the perception of those signals is altered by reproductive hormones such as estradiol (E2). We showed previously that in white-throated sparrows, immediate early gene responses in the auditory pathway of females are selective for conspecific male song only when plasma E2 is elevated to breeding-typical levels. In this study, we looked for evidence that E2-dependent modulation of auditory responses is mediated by serotonergic systems. In female nonbreeding white-throated sparrows treated with E2, the density of fibers immunoreactive for serotonin transporter innervating the auditory midbrain and rostral auditory forebrain increased compared with controls. E2 treatment also increased the concentration of the serotonin metabolite 5-HIAA in the caudomedial mesopallium of the auditory forebrain. In a second experiment, females exposed to 30 min of conspecific male song had higher levels of 5-HIAA in the caudomedial nidopallium of the auditory forebrain than birds not exposed to song. Overall, we show that in this seasonal breeder, (1) serotonergic fibers innervate auditory areas; (2) the density of those fibers is higher in females with breeding-typical levels of E2 than in nonbreeding, untreated females; and (3) serotonin is released in the auditory forebrain within minutes in response to conspecific vocalizations. Our results are consistent with the hypothesis that E2 acts via serotonin systems to alter auditory processing.
doi:10.1037/a0025586
PMCID: PMC3266998  PMID: 21942431
5-HT; 5-HIAA; estradiol; serotonin transporter (SERT); songbird
6.  Estradiol-dependent Catecholaminergic Innervation of Auditory Areas in a Seasonally Breeding Songbird 
A growing body of evidence suggests that gonadal steroids such as estradiol (E2) alter neural responses not only in brain regions associated with reproductive behavior, but also in sensory areas. Because catecholamine systems are involved in sensory processing and selective attention, and because they are sensitive to E2 in many species, they may mediate the neural effects of E2 in sensory areas. Here, we tested the effects of E2 on catecholaminergic innervation, synthesis, and activity in the auditory system of white-throated sparrows, a seasonally breeding songbird in which E2 promotes selective auditory responses to song. Non-breeding females with regressed ovaries were held on a winter-like photoperiod and implanted with silastic capsules containing either no hormone or E2. In one hemisphere of the brain, we used immunohistochemistry to quantify fibers immunoreactive for tyrosine hydroxylase or dopamine beta-hydroxylase in the auditory forebrain, thalamus, and midbrain. E2 treatment increased catecholaminergic innervation in the same areas of the auditory system in which E2 promotes selectivity for song. In the contralateral hemisphere, we quantified dopamine, norepinephrine and their metabolites in tissue punches using HPLC. Norepinephrine increased in the auditory forebrain, but not the midbrain, after E2 treatment. We found evidence of interhemispheric differences, both in immunoreactivity and catecholamine content did not depend on E2 treatment. Overall, our results show that increases in plasma E2 typical of the breeding season enhance catecholaminergic innervation and synthesis in some parts of the auditory system, raising the possibility that catecholamines play a role in E2-dependent auditory plasticity in songbirds.
doi:10.1111/j.1460-9568.2011.07751.x
PMCID: PMC3148281  PMID: 21714815
dopamine; dopamine beta-hydroxylase; norepinephrine; tyrosine hydroxylase; white-throated sparrow
7.  Rapid Effects of Hearing Song on Catecholaminergic Activity in the Songbird Auditory Pathway 
PLoS ONE  2012;7(6):e39388.
Catecholaminergic (CA) neurons innervate sensory areas and affect the processing of sensory signals. For example, in birds, CA fibers innervate the auditory pathway at each level, including the midbrain, thalamus, and forebrain. We have shown previously that in female European starlings, CA activity in the auditory forebrain can be enhanced by exposure to attractive male song for one week. It is not known, however, whether hearing song can initiate that activity more rapidly. Here, we exposed estrogen-primed, female white-throated sparrows to conspecific male song and looked for evidence of rapid synthesis of catecholamines in auditory areas. In one hemisphere of the brain, we used immunohistochemistry to detect the phosphorylation of tyrosine hydroxylase (TH), a rate-limiting enzyme in the CA synthetic pathway. We found that immunoreactivity for TH phosphorylated at serine 40 increased dramatically in the auditory forebrain, but not the auditory thalamus and midbrain, after 15 min of song exposure. In the other hemisphere, we used high pressure liquid chromatography to measure catecholamines and their metabolites. We found that two dopamine metabolites, dihydroxyphenylacetic acid and homovanillic acid, increased in the auditory forebrain but not the auditory midbrain after 30 min of exposure to conspecific song. Our results are consistent with the hypothesis that exposure to a behaviorally relevant auditory stimulus rapidly induces CA activity, which may play a role in auditory responses.
doi:10.1371/journal.pone.0039388
PMCID: PMC3378548  PMID: 22724011
8.  Song environment affects singing effort and vasotocin immunoreactivity in the forebrain of male Lincoln’s sparrows 
Hormones and behavior  2010;58(3):544-553.
Male songbirds often establish territories and attract mates by singing, and some song features can reflect the singer’s condition or quality. The quality of the song environment can change, so male songbirds should benefit from assessing the competitiveness of the song environment and appropriately adjusting their own singing behavior and the neural substrates by which song is controlled. In a wide range of taxa social modulation of behavior is partly mediated by the arginine vasopressin or vasotocin (AVP/AVT) systems. To examine the modulation of singing behavior in response to the quality of the song environment we compared the song output of laboratory-housed male Lincoln’s sparrows (Melospiza lincolnii) exposed to one week of chronic playback of songs categorized as either high or low quality, based on song length, complexity and trill performance. To explore the neural basis of any facultative shifts in behavior, we also quantified the subjects’ AVT immunoreactivity (AVT-IR) in three forebrain regions that regulate socio-sexual behavior: the medial bed nucleus of the stria terminalis (BSTm), the lateral septum (LS) and the preoptic area. We found that high quality songs increased singing effort and reduced AVT-IR in the BSTm and LS, relative to low quality songs. The effect of the quality of the song environment on both singing effort and forebrain AVT-IR raises the hypothesis that AVT within these brain regions plays a role in the modulation of behavior in response to competition that individual males may assess from the prevailing song environment.
doi:10.1016/j.yhbeh.2010.04.002
PMCID: PMC2916047  PMID: 20399213
arginine vasotocin (AVT); bird song; competition; sexual selection; social behavior network
10.  Female Lincoln's sparrows modulate their behavior in response to variation in male song quality 
Behavioral Ecology  2010;21(3):562-569.
Sexually reproducing organisms should mate with the highest quality individuals that they can. When female songbirds choose a mate, they are thought to use several aspects of male song that reflect his quality. Under resource-limited environmental conditions, male Lincoln's sparrows (Melospiza lincolnii) vary among one another in several aspects of song quality, including song length, song complexity, and trill performance. In a 2-pronged approach, we tested whether variation in song quality of male Lincoln's sparrows influences the behavior of females that are in a reproductive-like state. Over two trials, we exposed females to songs from the high and low ends of the distribution of naturally occurring song quality variation and found a higher level of behavioral activity in females exposed to high-quality songs, especially when they had first been exposed to low-quality songs. We also examined female phonotaxis toward antiphonally played songs with experimentally elevated and reduced trill performance and found that females moved preferentially toward the songs with elevated trill performance. Contrary to most studies investigating the behavioral responses of wild, female songbirds to variation in male song, we obtained our results without administering exogenous estradiol, which can artificially perturb the female's physiology. Our results demonstrate that the behavior of female Lincoln's sparrows is modulated by the quality of male songs to which they are exposed and that trill performance plays a significant role in this behavioral modulation. Furthermore, as the order of song quality presentation matters, it appears that recent song experience also influences female behavior.
doi:10.1093/beheco/arq022
PMCID: PMC2854529  PMID: 22476505
bird song; mate choice; Melospiza lincolnii; phonotaxis; sexual selection; song playback; trill performance; vocal performance
11.  Plasticity in Singing Effort and its Relationship with Monoamine Metabolism in the Songbird Telencephalon 
Developmental neurobiology  2010;70(1):41-57.
Factors intrinsic or extrinsic to individuals, such as their quality or the quality of competition in their social environment, can influence their communication signalling effort. We hypothesized that telencephalic monoamine secretion mediates the effects of a male’s own quality and quality of his social environment on his sexual signalling effort. The duration of a male European starling’s (Sturnus vulgaris) principal sexual signal, his song, positively correlates with several aspects of his quality, including his reproductive success, immunocompetence, and ability to attract mates. Therefore, the length of songs to which he is exposed reflects, in part, the quality of competition in his social environment. We manipulated the quality of the competitive environment by exposing male starlings to long or short songs for one week. We measured the length of songs produced by experimental males to gauge their quality, counted the number of songs they produced to gauge singing effort, and quantified telencephalic monoamine metabolism using HPLC. Singing effort increased with the length of the males’ own songs and with the length of songs to which we exposed them. Norepinephrine metabolism in Area X of the song control system was negatively correlated with the subjects’ mean song length and singing effort. Serotonin metabolism in the caudomedial mesopallium of the auditory telencephalon increased with the length of songs to which we exposed the subjects and with their singing effort. This raises the hypothesis that serotonin and norepinephrine secretion in the telencephalon help mediate the effects of extrinsic and intrinsic factors on signalling effort.
doi:10.1002/dneu.20752
PMCID: PMC2905645  PMID: 19899137
bird song; monoamines; neuroplasticity; norepinephrine; serotonin
12.  Independent effects of song quality and experience with photostimulation on expression of the immediate, early gene ZENK (EGR-1) in the auditory telencephalon of female European starlings 
Developmental neurobiology  2009;69(6):339-349.
Age influences behavioral decisions such as reproductive timing and effort. In photoperiodic species, such age effects may be mediated, in part, by the individual's age-accrued experience with photostimulation. In female European starlings (Sturnus vulgaris) that do not differ in age, experimental manipulation of photostimulation experience (photoexperience) affects hypothalamic, pituitary, and gonadal activity associated with reproductive development. Does photoexperience also affect activity in forebrain regions involved in processing a social cue, the song of males, which can influence mate choice and reproductive timing in females? Female starlings prefer long songs over short songs in a mate-choice context, and, like that in other songbird species, their auditory telencephalon plays a major role in processing these signals. We manipulated the photoexperience of female starlings, photostimulated them, briefly exposed them to either long or short songs, and quantified the expression of the immediate-early gene ZENK (EGR-1) in the caudomedial nidopallium as a measure of activity in the auditory telencephalon. Using an information theoretic approach, we found higher ZENK immunoreactivity in females with prior photostimulation experience than in females experiencing photostimulation for the first time. We also found that long songs elicited greater ZENK immunoreactivity than short song did. We did not find an effect of the interaction between photoexperience and song length, suggesting that photoexperience does not affect forebrain ZENK-responsiveness to song quality. Thus, photoexperience affects activity in an area of the forebrain that processes social signals, an effect that we hypothesize mediates, in part, the effects of age on reproductive decisions in photoperiodic songbirds.
doi:10.1002/dneu.20707
PMCID: PMC2872984  PMID: 19224564
age and aging; Akaike Information Criterion (AIC); birdsong; experience; photoperiodism
13.  Ovulation Order Mediates a Trade-Off between Pre-Hatching and Post-Hatching Viability in an Altricial Bird 
PLoS ONE  2008;3(3):e1785.
Simultaneously dependent siblings often compete for parentally provided resources. This competition may lead to mortality, the probability of which may be a function, in part, of the individual offspring's production order. In birds, serial ovulation followed by hatching asynchrony of simultaneous dependents leads to differences in post-hatching survival that largely depend on ovulation (laying) order. This has led to the widespread assumption that early-laid eggs are of greater value and therefore should possess different maternally manipulated characteristics than later-laid eggs. However, this perspective ignores the potential effect of laying order on pre-hatching viability, an effect which some studies suggest should offset the effect of laying order on post-hatching viability. I examined the relationship between laying order and hatching and fledging probability in wild, free-living Lincoln's sparrows (Melospiza lincolnii). In broods with complete hatching success, first-laid and therefore first-hatched offspring had the highest probability of fledging, and fledging probability declined with increasing laying order. However, first-laid eggs were less likely than later-laid eggs to hatch. This effect of laying order on pre-hatching viability seemed to offset that on post-hatching viability, and, consistently, maternal investment in egg size varied little if at all with respect to laying order. These results suggest that ovulation order mediates a trade-off between pre-hatching and post-hatching viability and should encourage a re-evaluation of the solitary role post-embryonic survival often plays when researchers make assumptions about the value of propagules based on the order in which they are produced.
doi:10.1371/journal.pone.0001785
PMCID: PMC2262150  PMID: 18335056
14.  Economy of mate attraction in the Cassin's finch 
Biology Letters  2005;1(1):34-37.
Mate attraction can be costly. Thus, individuals should modulate it according to its probable benefits. Specifically, individuals should modulate mate-attraction efforts based on their need for, the probability of attracting, and the reproductive competence of prospective mates. We tested these predictions by monitoring song output in laboratory-housed male Cassin's finches (Carpodacus cassinii) before, during and after brief female exposure following variable periods of isolation from females. We inferred individual reproductive competence from the product of season and reproductive schedule, the latter estimated from moult progress. Males produced little song in the presence of a female but robustly elevated song output in response to female loss. However, mere absence of a female did not elevate song output in males unaccustomed to female proximity. Furthermore, song output in response to female loss increased with her reproductive competence. We suggest that individuals modulate mate-attraction effort based on the benefits such efforts are likely to yield.
doi:10.1098/rsbl.2004.0257
PMCID: PMC1629057  PMID: 17148122
bird song; courtship; reproductive decisions; moult; reproductive schedule; seasonal breeding
15.  Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. 
Mate-choice decisions can be experience dependent, but we know little about how the brain processes stimuli that release such decisions. Female European starlings (Sturnus vulgaris) prefer males with long-bout songs over males with short-bout songs, and show higher expression of the immediate early gene (IEG) ZENK in the auditory forebrain when exposed to long-bout songs than when exposed to short-bout songs. We exposed female starlings to a short-day photoperiod for one of three durations and then, on an increased photophase, exposed them to one week of long-bout or short-bout song experience. We then examined their IEG response to novel long-bout versus novel short-bout songs by quantifying ZENK protein in two song-processing areas: the caudo-medial hyperstriatum ventrale and the caudo-medial neostriatum. ZENK expression in both areas increased with tenure on short-day photoperiods, suggesting that short days sensitize females to song. The ZENK response bias toward long-bout songs was greater in females with long-bout experience than in females with short-bout experience, indicating that the forebrain response bias toward a preferred trait depends on recent experience with that category of trait. This surprising level of neuroplasticity is immediately relevant to the natural history and fitness of the organism, and may underlie a mechanism for optimizing mate-choice criteria amidst locally variable distributions of secondary sexual characteristics.
doi:10.1098/rspb.2002.2180
PMCID: PMC1691185  PMID: 12495492

Results 1-15 (15)