Biology subjects

Woolley, S. C.

Publications and source records attributed to Woolley, S. C..

9 recordsLinked to original sources

bioRxiv2026

Emergence of social recognition in auditory and integrative circuits during pair bonding

Social relationships profoundly shape the perception of communication signals. In animals that form long-term social bonds, sensory cues such as vocalizations, scent, or physical appearance, and rewarding mating experiences can become associated with a bonded mate. While this natural process has hallmarks of some forms of associative learning, little is known about where or how these experiences shape neural circuits over the course of pair bonding. We used whole-brain BOLD fMRI in female songbirds to explore experience-dependent changes in neural activity in response to male songs. Pair bonding experiences drove changes in activation in response to the partners song within secondary auditory areas as well as two regulatory hubs that receive sensory input and connect to circuits that generate behavioral responses. In contrast, mere exposure to the vocal interactions of a neighboring pair did not result in changes in response to the neighbors song within the same areas, suggesting that pair bonding uniquely impacts auditory responses to familiar songs in select sensory and integrative circuits. Moreover, within the areas that showed increased activation for the partners song over the course of pair bonding, we observed diminished activation in response to the partners song after blocking D1 dopamine receptors, indicating a potential role for dopamine in the expression or maintenance of preference for the partners song. Eavesdropping females had changes in neural activation in response to the familiar song in a different suite of brain regions that were not affected by dopamine manipulation. Our data identify a potential circuit in which concurrent activation of sensory, reward, and regulatory hubs integrates multisensory information from social interactions and leads to the emergence of acoustic preferences and formation of long-lasting social bonds.

neuroscience↗

bioRxiv2026

Zebra finch females flexibly communicate with each other and with AI-driven acoustic interaction models

Vocal interactions are fundamental for social functioning across animals, including humans. The diverse rules underlying these exchanges remain largely unknown, and emerging AI technologies offer promising avenues for investigation. We used computational tools to collect and analyze >1,000 hours of vocal interactions between female zebra finches and discovered that their interactions were characterized by correlated call production and structure, rapid acoustic modulation, and response selectivity. To test these interaction rules, we developed a generative audio large language model (ZF-AIM Acoustic Interaction Model) that engaged in real-time vocal exchanges with birds. When birds interacted with ZF-AIM, their vocal production and flexibility recapitulated key naturalistic features, which did not happen with non-interactive playbacks. Targeted ablations of ZF-AIM revealed that call timing and structure differentially contribute to natural vocal interactions. Using these AI-animal interactions, we demonstrate how AI can be leveraged to reveal fundamental rules underlying animal communication.

animal behavior and cognition↗

bioRxiv2026

Motor learning and adaptation in bird flight

Birds are capable of performing elaborate flight maneuvers in variable environmental conditions. While flight is an adaptable and skilled motor behavior, we know surprisingly little about how birds master this ability. Across species, skilled motor behaviors show practice-related changes or improvements in performance and understanding which features of a motor behavior change with learning can lend insight into the constraints, flexibility, and optimization of motor behavior. Here, we combined high-speed video recordings and pose-tracking software to analyze the kinematics of thousands of flights in zebra finches over multiple days of flight training and over different distances. Small birds, such as the zebra finch, use an intermittent flap-bounding flight style that alternates between flapping phases and flexed-wing bounding phases. We found that birds increase their flight speed and the time spent bounding and reduce variability in the bound position over ten days of flight performance. These motor changes to flight show savings, as performance is maintained even after two months without flight experience. Moreover, these same parameters are adjusted when birds fly longer distances, indicating that they may be key to flight flexibility. We built kinematic models to determine what features birds might be optimizing toward with learning and found that the data was best fit by a model simultaneously optimizing for minimum energy and flight duration. Taken together, our data highlight that flap-bounding flight shows hallmarks of skilled motor learning and lend new insight into the function of bounds.

animal behavior and cognition↗

bioRxiv2025

Rearing condition affects behavioral response to cross-modal expectancy violation paradigm in zebra finches

Interacting in a multimodal world, including recognizing other individuals across multiple sensory modalities, is important for animals who rely on social relationships for survival. Social and sensory experiences shape how multisensory information is processed and integrated; however, we have less understanding of how multimodal recognition may be modulated by early sensory experience in a single modality. Zebra finches are gregarious songbirds that form lifelong pair-bonds with a single partner whom they recognize acoustically and visually. However, it is unknown to what extent multisensory signals might interact to enable recognition or whether this is affected by auditory exposure during development. In this paper, we tested females for responses to audio and visual stimuli from their mate or a stranger in a digital cross-modal expectancy violation paradigm. Using automated pose tracking, we determined that, like many species, zebra finches react differently when the stimuli are congruent versus incongruent. However, while birds reared in a colony setting and birds reared without exposure to adult song both detected audiovisual congruency, the degree of behaviors exhibited differed between the rearing conditions. Thus, multisensory integration appears to be important for females to identify their mates, but differences in developmental environment influence how recognition is behaviorally expressed.

animal behavior and cognition↗

bioRxiv2025

Humans share acoustic preferences with other animals

Many animals produce sounds during courtship and receivers prefer some sounds over others. Shared ancestry and convergent evolution may generate similarities in preference across species and could underlie Darwins conjecture that some animals "have nearly the same taste for the beautiful as we have". Here, we show that humans share acoustic preferences with a wide range of animals, that the strength of human preferences correlates with that in other animals, and that human responses are quicker when in agreement with animals. Furthermore, we found greatest agreement in preference for adorned, evolutionarily ancestral, and lower frequency sounds. Humans music listening experience was associated with preferences. These results are consistent with theories arguing that biases in sensory and cognitive processing sculpt acoustic preferences and confirm Darwins century-old hunch about the conservation of aesthetics in nature.

animal behavior and cognition↗

bioRxiv2024

Early auditory and adult mating experiences interact with singer identity to shape neural responses to song in female zebra finches

Social and sensory experiences across the lifespan can shape social interactions, however, experience-dependent plasticity is widely studied within discrete life stages. In the socially monogamous zebra finch, in which females use learned vocal signals to identify individuals and form long-lasting pair bonds, developmental exposure to song is key for females to show species-typical song perception and preferences. While adult mating experience can still lead to pair-bonding and song preference learning even in birds with limited previous song exposure ("song-naive"), whether similarities in adult behavioral plasticity between normally-reared and song-naive females reflect convergent patterns of neural activity is unknown. We investigated this using expression of a marker of neural activity and plasticity (phosphorylated S6) in mated normally-reared and song-naive females in response to song from either their mate, a neighbor, or an unfamiliar male. We found that, in portions of a secondary auditory region (the caudomedial nidopallium NCM) and in dopaminergic neurons of the caudal ventral tegmental area, hearing the mates song significantly increased pS6 expression in females from both rearing conditions. In contrast, within other NCM subregions, song-identity drove different patterns of pS6 expression depending on the rearing condition. These data suggest that developmental experiences can have long-lasting impacts on the neural signatures of behaviors acquired in adulthood and that socially-driven behavioral plasticity in adults may arise through both shared and divergent neural circuits depending on an individuals developmental experiences.

neuroscience↗

bioRxiv2023

Sex Differences in Human Music Perception are Negligible

Since Darwin1, researchers have proposed that human musicality evolved in a reproductive context in which males produce music to signal their mate quality to females. Sexually selected traits involve tradeoffs in the costs of high-quality signal production and high-fidelity signal detection2, leading to observable sexual dimorphisms across many species3,4. If musicality is a sexually selected trait in humans, males and females should then differ in their music perception ability, music production ability, or both. The evidence for this possibility is unclear, because previous reports of sex differences in human auditory perception are restricted in scope and inconsistent in direction5-15. Here, we report a test of music processing ability in 360,009 men and 194,291 women from 208 countries. In contrast to other non-musical human traits16-19, and in contrast to music-related traits in non-human animals20-23, we found no consistent advantage for either sex. The sex differences we did observe were negligible (Cohens d range: 0.009-0.111) and Bayesian analyses indicated evidence in favor of the null hypothesis of no sex difference in general musical ability (Bayes Factor = 0.6). These results suggest that it is unlikely that music evolved in the context of sexual selection.

animal behavior and cognition↗

bioRxiv2023

Social experiences shape song preference learning independent of developmental exposure to song

Communication governs the formation and maintenance of social relationships. The interpretation of communication signals depends not only on the signals content, but also on a receivers individual experience. Experiences throughout life may interact to affect behavioral plasticity, such that a lack of developmental sensory exposure could constrain adult learning, while salient adult social experiences could remedy developmental deficits. We investigated how experiences impact the formation and direction of female auditory preferences in the zebra finch. Zebra finches form long-lasting pair bonds and females learn preferences for their mates vocalizations. We found that after two weeks of cohabitation with a male, females formed pair-bonds and learned to prefer their mates song regardless of whether they were reared with ("normally-reared") or without ("song-naive") developmental exposure to song. In contrast, females that heard but did not physically interact with a male did not prefer his song. Moreover, even following mating, song-naive females failed to show species-typical preferences for courtship song, hinting that mating is insufficient to ameliorate broader deficits in sensory processing that arise during development. Thus, courtship and mating interactions, but not acoustic-only interactions, strongly influence preference learning regardless of rearing experience, and may dynamically drive auditory plasticity for recognition and preference.

animal behavior and cognition↗

bioRxiv2019

Dopamine in the songbird auditory cortex shapes auditory preference

In vocal communication, vocal signals can provide listeners with information and also elicit motivated responses. Auditory cortical and mesolimbic reward circuits are often considered to have distinct roles in these processes, with auditory cortical circuits responsible for detecting and discriminating sounds and mesolimbic circuits ascribing salience and modulating preference for those sounds. Here, we investigated whether dopamine within auditory cortical circuits themselves can shape the incentive salience of a vocal signal. Using female zebra finches, who show natural preferences for vocal signals produced by males ( songs), we found that pairing passive song playback with pharmacological manipulations of dopamine in the secondary auditory cortex drives changes to song preferences. Plasticity of song preferences by dopamine lasted for at least one week and was not influenced by norepinephrine manipulations. These data suggest that dopamine acting directly in sensory processing areas can shape the incentive salience of communication signals.

neuroscience↗