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Flying animals have had to evolve robust and effective guidance strategies for dealing with habitat clutter. Birds and insects use optic flow expansion cues to sense and avoid obstacles, but orchid bees have also been shown to use brightness cues during gap negotiation. Such brightness cues might therefore be of general importance in structuring visually guided flight behaviours. To test the hypothesis that brightness cues also affect gap negotiation behaviours in birds, we presented captive zebra finches Taeniopygia guttata with a symmetric or asymmetric background brightness distribution on the other side of a tunnel. The background brightness conditions influenced both the birds' decision to enter the tunnel aperture, and their flight direction upon exit. Zebra finches were more likely to initiate flight through the tunnel if they could see a bright background through it; they were also more likely to fly to the bright side upon exiting. We found no evidence of the centring response that would be expected if optic flow cues were balanced bilaterally during gap negotiation. Instead, the birds entered the tunnel by targeting a clearance of approximately one wing length from its near edge. Brightness cues therefore affect how zebra finches structure their flight when negotiating gaps in enclosed environments.
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Sensory experience during development has lasting effects on perception and neural processing. Exposing animals to artificial stimuli early in life influences the tuning and functional organization of the auditory cortex, but less is known about how the rich acoustical environments experienced by vocal communicators affect the processing of complex vocalizations. Here, we show that in zebra finches (Taeniopygia guttata), a colonial-breeding songbird species, exposure to a naturalistic social-acoustical environment during development has a profound impact on cortical-level auditory responses to conspecific song. Compared to birds raised by pairs in acoustic isolation, birds raised in a breeding colony had higher average firing rates, selectivity, and discriminability, especially in the narrow-spiking, putatively inhibitory neurons of a higher-order auditory area, the caudomedial nidopallium (NCM). Neurons in colony-reared birds were also less correlated in their tuning and more efficient at encoding the spectrotemporal structure of conspecific song. These results suggest that the auditory cortex adapts to noisy, complex acoustical environments by strengthening inhibitory circuitry, functionally decoupling excitatory neurons while maintaining overall excitatory-inhibitory balance.
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Identifying key molecular pathways and genes involved in the response to urban pollutants is an important step in furthering our understanding of the impact of urbanisation on wildlife. The expansion of urban habitats and the associated human-introduced environmental changes are considered a global threat to the health and persistence of humans and wildlife. The present study experimentally investigates how short-term exposure to three urban-related pollutants -soot, artificial light at night (ALAN) and traffic noise-affects transcriptome-wide gene expression in livers from captive female zebra finches (Taeniopygia guttata). Compared to unexposed controls, 17, 52, and 28 genes were differentially expressed in soot, ALAN and noise-exposed birds, respectively. In soot-exposed birds, the enriched gene ontology (GO) terms were associated with a suppressed immune system such as interferon regulating genes (IRGs) and responses to external stimuli. For ALAN-exposed birds, enriched GO terms were instead based on downregulated genes associated with detoxification, redox, hormonal-, and metabolic processes. Noise exposure resulted in downregulation of genes associated with the GO terms: cellular responses to substances, catabolic and cytokine responses. Among the individually differentially expressed genes (DEGs), soot led to an increased expression of genes related to tumour progression. Likewise, ALAN revealed an upregulation of multiple genes linked to different cancer types. Both sensory pollutants (ALAN and noise) led to increased expression of genes linked to neuronal function. Interestingly, noise caused upregulation of genes associated with serotonin regulation and function (SLC6A4 and HTR7), which previous studies have shown to be under selection in urban birds. These outcomes indicate that short-term exposure to the three urban pollutants perturbate the liver transcriptome, but most often in different ways, which highlights future studies of multiple-stress exposure and their interactive effects, along with their long-term impacts for urban-dwelling wildlife.
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Perfilação da Expressão Gênica , Fígado , Transcriptoma , Animais , Fígado/metabolismo , Feminino , Ruído/efeitos adversos , Tentilhões/genética , Poluentes Ambientais , LuzRESUMO
Songbirds' vocal mastery is impressive, but to what extent is it a result of practice? Can they, based on experienced mismatch with a known target, plan the necessary changes to recover the target in a practice-free manner without intermittently singing? In adult zebra finches, we drive the pitch of a song syllable away from its stable (baseline) variant acquired from a tutor, then we withdraw reinforcement and subsequently deprive them of singing experience by muting or deafening. In this deprived state, birds do not recover their baseline song. However, they revert their songs toward the target by about 1 standard deviation of their recent practice, provided the sensory feedback during the latter signaled a pitch mismatch with the target. Thus, targeted vocal plasticity does not require immediate sensory experience, showing that zebra finches are capable of goal-directed vocal planning.
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Tentilhões , Objetivos , Vocalização Animal , Animais , Vocalização Animal/fisiologia , Tentilhões/fisiologia , MasculinoRESUMO
Background: Vocal learning is a rare, convergent trait that is fundamental to both human speech and birdsong. The Forkhead Box P2 (FoxP2) transcription factor appears necessary for both types of learned signals, as human mutations in FoxP2 result in speech deficits, and disrupting its expression in zebra finches impairs male-specific song learning. In juvenile and adult male finches, striatal FoxP2 mRNA and protein decline acutely within song-dedicated neurons during singing, indicating that its transcriptional targets are also behaviorally regulated. The identities of these targets in songbirds, and whether they differ across sex, development and/or behavioral conditions, are largely unknown. Results: Here we used chromatin immunoprecipitation followed by sequencing (ChIP-Seq) to identify genomic sites bound by FoxP2 in male and female, juvenile and adult, and singing and non-singing birds. Our results suggest robust FoxP2 binding concentrated in putative promoter regions of genes. The number of genes likely to be bound by FoxP2 varied across conditions, suggesting specialized roles of the candidate targets related to sex, age, and behavioral state. We validated these binding targets both bioinformatically, with comparisons to previous studies and biochemically, with immunohistochemistry using an antibody for a putative target gene. Gene ontology analyses revealed enrichment for human speech- and language-related functions in males only, consistent with the sexual dimorphism of song learning in this species. Fewer such targets were found in juveniles relative to adults, suggesting an expansion of this regulatory network with maturation. The fewest speech-related targets were found in the singing condition, consistent with the well-documented singing-driven down-regulation of FoxP2 in the songbird striatum. Conclusions: Overall, these data provide an initial catalog of the regulatory landscape of FoxP2 in an avian vocal learner, offering dozens of target genes for future study and providing insight into the molecular underpinnings of vocal learning.
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Developmental environmental stressors can have instructive effects on an organism's phenotype. This developmental plasticity can prepare organisms for potentially stressful future environments, circumventing detrimental effects on fitness. However, the physiological mechanisms underlying such adaptive plasticity are understudied, especially in vertebrates. We hypothesized that captive male zebra finches (Taeniopygia castanotis) exposed to a mild heat conditioning during development would acquire a persisting thermotolerance, and exhibit increased heat-shock protein (HSP) levels associated with a decrease in oxidative damage when exposed to a high-intensity stressor in adulthood. To test this, we exposed male finches to a prolonged mild heat conditioning (38°C) or control (22°C) treatment as juveniles. Then in a 2 × 2 factorial manner, these finches were exposed to a high heat stressor (42°C) or control (22°C) treatment as adults. Following the adult treatment, we collected testes and liver tissue and measured HSP70, HSP90, and HSP60 protein levels. In the testes, finches exhibited lower levels of HSP90 and HSP60 when exposed to the high heat stressor in adulthood if they were exposed to the mild heat conditioning as juveniles. In the liver, finches exposed to the high heat stressor in adulthood had reduced HSP90 and HSP60 levels, regardless of whether they were conditioned as juveniles. In some cases, elevated testes HSP60 levels were associated with increased liver oxidative damage and diminishment of a condition-dependent trait, indicating potential stress-induced tradeoffs. Our results indicate that a mild conditioning during development can have persisting effects on HSP expression and acquired thermotolerance.
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Cultural and genetic inheritance combine to enable rapid changes in trait expression, but their relative importance in determining trait expression across generations is not clear. Birdsong is a socially learned cognitive trait that is subject to both cultural and genetic inheritance, as well as being affected by early developmental conditions. We sought to test whether early-life conditions in one generation can affect song acquisition in the next generation. We exposed one generation (F1) of nestlings to elevated corticosterone (CORT) levels, allowed them to breed freely as adults, and quantified their son's (F2) ability to copy the song of their social father. We also quantified the neurogenetic response to song playback through immediate early gene (IEG) expression in the auditory forebrain. F2 males with only one corticosterone-treated parent copied their social father's song less accurately than males with two control parents. Expression of ARC in caudomedial nidopallium (NCM) correlated with father-son song similarity, and patterns of expression levels of several IEGs in caudomedial mesopallium (CMM) in response to father song playback differed between control F2 sons and those with a CORT-treated father only. This is the first study to demonstrate that developmental conditions can affect social learning and neurogenetic responses in a subsequent generation.
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Corticosterona , Aprendizagem , Vocalização Animal , Animais , Vocalização Animal/fisiologia , Masculino , Aprendizagem/fisiologia , Corticosterona/metabolismo , Feminino , Tentilhões/fisiologia , Prosencéfalo/metabolismo , Prosencéfalo/fisiologia , Genes PrecocesRESUMO
AbstractDevelopmental plasticity allows organisms to increase the fit between their phenotype and their early-life environment. The extent to which such plasticity also enhances adult fitness is not well understood, however, particularly when early-life and adult environments differ substantially. Using a cross-factorial design that manipulated diet at two life stages, we examined predictions of major hypotheses-silver spoon, environmental matching, and thrifty phenotype-concerning the joint impacts of early-life and adult diets on adult morphology/display traits, survival, and reproductive allocation. Overall, results aligned with the silver spoon hypothesis, which makes several predictions based on the premise that development in poor-quality environments constrains adult performance. Males reared and bred on a low-protein diet had lower adult survivorship than other male treatment groups; females' survivorship was higher than males' and not impacted by early diet. Measures of allocation to reproduction primarily reflected breeding diet, but where natal diet impacted reproduction, results supported the silver spoon. Both sexes showed reduced expression of display traits when reared on a low-protein diet. Results accord with other studies in supporting the relevance of the silver spoon hypothesis to birds and point to significant ramifications of sex differences in early-life viability selection on the applicability/strength of silver spoon effects.
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Tentilhões , Reprodução , Animais , Masculino , Feminino , Tentilhões/fisiologia , Longevidade , Dieta/veterinária , Fenótipo , Dieta com Restrição de ProteínasRESUMO
Injury, tumors, ischemia, and lesions in the cerebellum show the involvement of this region in human speech. The association of the cerebellum with learned birdsong has only been identified recently. Cerebellar dysfunction in young songbirds causes learning disabilities, but its role in adult songbirds has not been established. The aim of this study was to investigate the role of the deep cerebellar nuclei (DCN) in adult birdsong. We created bilateral excitotoxic lesions in the DCN of adult male zebra finches (Taeniopygia guttata) and recorded their songs for up to 4 months. Using magnetic resonance imaging (MRI) and immunohistochemistry, we validated the lesion efficacy. We found that the song duration significantly increased from 14 weeks post-op; the increase in duration was caused by a greater number of introductory notes as well as a greater number of syllables sung after the introductory notes. On the other hand, the motif duration decreased from 8 weeks after DCN lesions were induced, which was due to faster singing of syllables, not changes in inter-syllable interval length. DCN lesions also caused a decrease in the fundamental frequency of syllables. In summary, we showed that DCN lesions influence the temporal and acoustic features of birdsong. These results suggest that the cerebellum influences singing in adult songbirds.
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Tentilhões , Aves Canoras , Animais , Masculino , Cerebelo/diagnóstico por imagem , Comunicação , Aprendizagem , Vocalização AnimalRESUMO
In recent years, the impact of prenatal sound on development, notably for programming individual phenotypes for postnatal conditions, has increasingly been revealed. However, the mechanisms through which sound affects physiology and development remain mostly unexplored. Here, I gather evidence from neurobiology, developmental biology, cellular biology and bioacoustics to identify the most plausible modes of action of sound on developing embryos. First, revealing often-unsuspected plasticity, I discuss how prenatal sound may shape auditory system development and determine individuals' later capacity to receive acoustic information. I also consider the impact of hormones, including thyroid hormones, glucocorticoids and androgen, on auditory plasticity. Second, I review what is known about sound transduction to other - non-auditory - brain regions, and its potential to input on classical developmental programming pathways. Namely, the auditory pathway has direct anatomical and functional connectivity to the hippocampus, amygdala and/or hypothalamus, in mammals, birds and anurans. Sound can thus trigger both immediate and delayed responses in these limbic regions, which are specific to the acoustic stimulus and its biological relevance. Third, beyond the brain, I briefly consider the possibility for sound to directly affect cellular functioning, based on evidence in earless organisms (e.g. plants) and cell cultures. Together, the multi-disciplinary evidence gathered here shows that the brain is wired to allow multiple physiological and developmental effects of sound. Overall, there are many unexplored, but possible, pathways for sound to impact even primitive or immature organisms. Throughout, I identify the most promising research avenues for unravelling the processes of acoustic developmental programming.
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Acústica , Som , Humanos , Animais , Feminino , Gravidez , Tonsila do Cerebelo , Anuros , Vias Auditivas , MamíferosRESUMO
The development of individuality during learned behavior is a common trait observed across animal species; however, the underlying biological mechanisms remain understood. Similar to human speech, songbirds develop individually unique songs with species-specific traits through vocal learning. In this study, we investigate the developmental and molecular mechanisms underlying individuality in vocal learning by utilizing F1 hybrid songbirds (Taeniopygia guttata cross with Taeniopygia bichenovii), taking an integrating approach combining experimentally controlled systematic song tutoring, unbiased discriminant analysis of song features, and single-cell transcriptomics. When tutoring with songs from both parental species, F1 hybrid individuals exhibit evident diversity in their acquired songs. Approximately 30% of F1 hybrids selectively learn either song of the two parental species, while others develop merged songs that combine traits from both species. Vocal acoustic biases during vocal babbling initially appear as individual differences in songs among F1 juveniles and are maintained through the sensitive period of song vocal learning. These vocal acoustic biases emerge independently of the initial auditory experience of hearing the biological father's and passive tutored songs. We identify individual differences in transcriptional signatures in a subset of cell types, including the glutamatergic neurons projecting from the cortical vocal output nucleus to the hypoglossal nuclei, which are associated with variations of vocal acoustic features. These findings suggest that a genetically predisposed vocal motor bias serves as the initial origin of individual variation in vocal learning, influencing learning constraints and preferences.
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Individualidade , Aves Canoras , Animais , Humanos , Predisposição Genética para Doença , Fala , Acústica , ViésRESUMO
Zebra finches are a model animal used in the study of audition. They are adept at recognizing zebra finch songs, and the neural pathway involved in song recognition is well studied. Here, this example is used to illustrate the estimation of mutual information between stimuli and responses using a Kozachenko-Leonenko estimator. The challenge in calculating mutual information for spike trains is that there are no obvious coordinates for the data. The Kozachenko-Leonenko estimator does not require coordinates; it relies only on the distance between data points. In the case of bird songs, estimating the mutual information demonstrates that the information content of spiking does not diminish as the song progresses.
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Humans readily recognize familiar rhythmic patterns, such as isochrony (equal timing between events) across a wide range of rates. This reflects a facility with perceiving the relative timing of events, not just absolute interval durations. Several lines of evidence suggest this ability is supported by precise temporal predictions arising from forebrain auditory-motor interactions. We have shown previously that male zebra finches, Taeniopygia guttata, which possess specialized auditory-motor networks and communicate with rhythmically patterned sequences, share our ability to flexibly recognize isochrony across rates. To test the hypothesis that flexible rhythm pattern perception is linked to vocal learning, we ask whether female zebra finches, which do not learn to sing, can also recognize global temporal patterns. We find that females can flexibly recognize isochrony across a wide range of rates but perform slightly worse than males on average. These findings are consistent with recent work showing that while females have reduced forebrain song regions, the overall network connectivity of vocal premotor regions is similar to males and may support predictions of upcoming events. Comparative studies of male and female songbirds thus offer an opportunity to study how individual differences in auditory-motor connectivity influence perception of relative timing, a hallmark of human music perception.
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Parvalbumin (PV) neurons play an integral role in regulating neural dynamics and plasticity. Therefore, understanding the factors that regulate PV expression is important for revealing modulators of brain function. While the contribution of PV neurons to neural processes has been studied in mammals, relatively little is known about PV function in non-mammalian species, and discerning similarities in the regulation of PV across species can provide insight into evolutionary conservation in the role of PV neurons. Here we investigated factors that affect the abundance of PV in PV neurons in sensory and motor circuits of songbirds and rodents. In particular, we examined the degree to which perineuronal nets (PNNs), extracellular matrices that preferentially surround PV neurons, modulate PV abundance as well as how the relationship between PV and PNN expression differs across brain areas and species and changes over development. We generally found that cortical PV neurons that are surrounded by PNNs (PV+PNN neurons) are more enriched with PV than PV neurons without PNNs (PV-PNN neurons) across both rodents and songbirds. Interestingly, the relationship between PV and PNN expression in the vocal portion of the basal ganglia of songbirds (Area X) differed from that in other areas, with PV+PNN neurons having lower PV expression compared to PV-PNN neurons. These relationships remained consistent across development in vocal motor circuits of the songbird brain. Finally, we discovered a causal contribution of PNNs to PV expression in songbirds because degradation of PNNs led to a diminution of PV expression in PV neurons. These findings in reveal a conserved relationship between PV and PNN expression in sensory and motor cortices and across songbirds and rodents and suggest that PV neurons could modulate plasticity and neural dynamics in similar ways across songbirds and rodents.
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Bilaterally organized brain regions are often simultaneously active in both humans1,2,3 and animal models,4,5,6,7,8,9 but the extent to which the temporal progression of internally generated dynamics is coordinated across hemispheres and how this coordination changes with brain state remain poorly understood. To address these issues, we investigated the zebra finch courtship song (duration: 0.5-1.0 s), a highly stereotyped complex behavior10,11 produced by a set of bilaterally organized nuclei.12,13,14 Unilateral lesions to these structures can eliminate or degrade singing,13,15,16,17 indicating that both hemispheres are required for song production.18 Additionally, previous work demonstrated broadly coherent and symmetric bilateral premotor signals during song.9 To precisely track the temporal evolution of activity in each hemisphere, we recorded bilaterally in the song production pathway. We targeted the robust nucleus of the arcopallium (RA) in the zebra finch, where population activity reflects the moment-to-moment progression of the courtship song during awake vocalizations19,20,21,22,23,24 and sleep, where song-related network dynamics reemerge in "replay" events.24,25 We found that activity in the left and right RA is synchronized within a fraction of a millisecond throughout song. In stark contrast, the two hemispheres displayed largely independent replay activity during sleep, despite shared interhemispheric arousal levels. These findings demonstrate that the degree of bilateral coordination in the zebra finch song system is dynamically modulated by behavioral state.
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Tentilhões , Vocalização Animal , Animais , Humanos , EncéfaloRESUMO
Mercury is a widespread pollutant of increasing global concern that exhibits a broad range of deleterious effects on organisms, including birds. Because the developing brain is well-known to be particularly vulnerable to the neurotoxic insults of mercury, many studies have focused on developmental effects such as on the embryonic brain and resulting behavioral impairment in adults. It is not well understood how the timing of exposure, for example exclusively in ovo versus throughout life, influences the impact of mercury. Using dietary exposure to environmentally relevant methylmercury concentrations, we examined the role that timing and duration of exposure play on spatial learning and memory in a model songbird species, the domesticated zebra finch (Taeniopygia guttata castanotis). We hypothesized that developmental exposure was both necessary and sufficient to disrupt spatial memory in adult finches. We documented profound disruption of memory for locations of hidden food at two spatial scales, cage- and room-sized enclosures, but found that both developmental and ongoing adult exposure were required to exhibit this behavioral impairment. Methylmercury-exposed birds made more mistakes before mastering the spatial task, because they revisited unrewarded locations repeatedly even after discovering the rewarded location. Contrary to our prediction, hippocampal volume was not affected in birds exposed to methylmercury over their lifetimes. The disruption of spatial cognition that we detected is severe and would likely have implications for survival and reproduction in wild birds; however, it appears that individuals that disperse or migrate from a contaminated site might recover later in life if no longer exposed to the toxicant.
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Tentilhões , Mercúrio , Compostos de Metilmercúrio , Humanos , Adulto , Animais , Mercúrio/toxicidade , Compostos de Metilmercúrio/toxicidade , Cognição , EncéfaloRESUMO
The vocal control nucleus HVC in songbirds has emerged as a widespread model system to study adult brain plasticity in response to changes in the hormonal and social environment. I review here studies completed in my laboratory during the last decade that concern two aspects of this plasticity: changes in aggregations of extracellular matrix components surrounding the soma of inhibitory parvalbumin-positive neurons called perineuronal nets (PNN) and the production/incorporation of new neurons. Both features are modulated by the season, age, sex and endocrine status of the birds in correlation with changes in song structure and stability. Causal studies have also investigated the role of PNN and of new neurons in the control of song. Dissolving PNN with chondroitinase sulfate, a specific enzyme applied directly on HVC or depletion of new neurons by focalized X-ray irradiation both affected song structure but the amplitude of changes was limited and deserves further investigations.
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Aves Canoras , Vocalização Animal , Animais , Vocalização Animal/fisiologia , Aves Canoras/fisiologia , Neurônios , Plasticidade Neuronal/fisiologia , Neurogênese/fisiologia , Matriz ExtracelularRESUMO
The acoustic environment an animal experiences early in life shapes the structure and function of its auditory system. This process of experience-dependent development is thought to be primarily orchestrated by potentiation and depression of synapses, but plasticity of intrinsic voltage dynamics may also contribute. Here, we show that in juvenile male and female zebra finches, neurons in a cortical-level auditory area, the caudal mesopallium (CM), can rapidly change their firing dynamics. This plasticity was only observed in birds that were reared in a complex acoustic and social environment, which also caused increased expression of the low-threshold potassium channel Kv1.1 in the plasma membrane and endoplasmic reticulum (ER). Intrinsic plasticity depended on activity, was reversed by blocking low-threshold potassium currents, and was prevented by blocking intracellular calcium signaling. Taken together, these results suggest that Kv1.1 is rapidly mobilized to the plasma membrane by activity-dependent elevation of intracellular calcium. This produces a shift in the excitability and temporal integration of CM neurons that may be permissive for auditory learning in complex acoustic environments during a crucial period for the development of vocal perception and production.SIGNIFICANCE STATEMENT Neurons can change not only the strength of their connections to other neurons, but also how they integrate synaptic currents to produce patterns of action potentials. In contrast to synaptic plasticity, the mechanisms and functional roles of intrinisic plasticity remain poorly understood. We found that neurons in the zebra finch auditory cortex can rapidly shift their spiking dynamics within a few minutes in response to intracellular stimulation. This plasticity involves increased conductance of a low-threshold potassium current associated with the Kv1.1 channel, but it only occurs in birds reared in a rich acoustic environment. Thus, auditory experience regulates a mechanism of neural plasticity that allows neurons to rapidly adapt their firing dynamics to stimulation.
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Córtex Auditivo , Tentilhões , Animais , Masculino , Feminino , Córtex Auditivo/fisiologia , Tentilhões/fisiologia , Neurônios/fisiologia , Potenciais de Ação , Potássio , Vocalização Animal/fisiologia , Estimulação Acústica , Plasticidade Neuronal/fisiologia , Percepção Auditiva/fisiologiaRESUMO
Individuals show consistent between-individual behavioural variation when they interact with conspecifics or heterospecifics. Such patterns might underlie emergent group-specific behavioural patterns and between-group behavioural differences. However, little is known about (i) how social and non-social drivers (external drivers) shape group-level social structures and (ii) whether animal groups show consistent between-group differences in social structure after accounting for external drivers. We used automated tracking to quantify daily social interactions and association networks in 12 colonies of zebra finches (Taeniopygia guttata). We quantified the effects of five external drivers (group size, group composition, ecological factors, physical environments and methodological differences) on daily interaction and association networks and tested whether colonies expressed consistent differences in day-to-day network structure after controlling for these drivers. Overall, we found that external drivers contribute significantly to network structure. However, even after accounting for the contribution of external drivers, there remained significant support for consistent between-group differences in both interaction (repeatability R: up to 0.493) and association (repeatability R: up to 0.736) network structures. Our study demonstrates how group-level differences in social behaviour can be partitioned into different drivers of variation, with consistent contributions from both social and non-social factors.