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Liu, R. C.

Publications and source records attributed to Liu, R. C..

6 recordsLinked to original sources

Natural variation in the oxytocin receptor gene predicts social observation in female prairie voles

Genetic variation in the oxytocin receptor gene (Oxtr) has been linked to differences in brain OXTR expression and long-term social bonds, but whether it shapes the moment-to-moment dynamics of early social interactions is unclear. Here we examined how the intronic Oxtr single nucleotide polymorphism (SNP) NT213739 in female prairie voles (Microtus ochrogaster) shapes their dynamic social interactions with an opposite-sex conspecific. Leveraging a computational pipeline to analyze the movements of freely interacting voles, we found that C/C females, which expressed higher OXTR levels in the nucleus accumbens than T/T females, spent more time socially observing novel males from a distance, especially early in interactions. This genotype-phenotype relationship persisted in multiple contexts, including the social preference test. Thus, natural Oxtr variation biases social observation in females toward unfamiliar males before bonds form, consistent with models where accumbens OXTR enhances the salience of social cues. These findings show that SNPs can shape subtle behavioral dimensions in early social encounters, with important implications for the role of oxytocin in the study of social attachment.

neuroscience↗

Vocal recognition of partners by female prairie voles

Recognizing conspecifics is vitally important for differentiating kin, mates, offspring and social threats.1 Although often reliant upon chemical or visual cues, individual recognition across the animal kingdom is also facilitated by unique acoustic signatures in vocalizations.2-4 However, amongst the large Muroidea superfamily of rodents that encompasses laboratory species amenable to neurobiological studies, there is scant behavioral evidence for individual vocal recognition despite individual acoustic variation.5-10 Playback studies have found evidence for coarse communicative functions like mate attraction and territorial defense, but limited finer ability to discriminate known individuals vocalizations.11-17 Such a capacity would be adaptive for species that form lifelong pair bonds requiring partner identification across timescales, distances and sensory modalities, so to improve the chance of finding individual vocal recognition in a Muroid rodent, we investigated vocal communication in the prairie vole (Microtus ochrogaster) - one of the few socially monogamous mammals.18 We found that the ultrasonic vocalizations of adult prairie voles can communicate individual identity. Even though the vocalizations of individual males change after cohabitating with a female to form a bond, acoustic variation across individuals is greater than within an individual so that vocalizations of different males in a common context are identifiable above chance. Critically, females behaviorally discriminate their partners vocalizations over a strangers, even if emitted to another stimulus female. These results establish the acoustic and behavioral foundation for individual vocal recognition in prairie voles, where neurobiological tools19-22 enable future studies revealing its causal neural mechanisms. HighlightsO_LIMuroid rodents can display individual vocal recognition C_LIO_LIAdult prairie vole USVs are more variable across individuals than social experience C_LIO_LIIndividual vole identity can be decoded from their vocalizations C_LIO_LICarefully constructed protocol sustains voles interest in vocal playback C_LIO_LIFemale prairie voles behaviorally recognize their mates vocalizations C_LI

animal behavior and cognition↗

Instinct to insight: Neural correlates of ethological strategy learning

In ethological behaviors like parenting, animals innately follow stereotyped patterns of choices to decide between uncertain outcomes but can learn to modify their strategies to incorporate new information. For example, female mice in a T-maze instinctively use spatial-memory to search for pups where they last found them but can learn more efficient strategies employing pup-associated acoustic cues. We uncovered neural correlates for transitioning between these innate and learned strategies. Auditory cortex (ACx) was required during learning. ACx firing at the nest increased with learning and correlated with subsequent search speed but not outcome. Surprisingly, ACx suppression rather than facilitation during search was more prognostic of correct sound-cued outcomes - even before adopting a sound-cued strategy. Meanwhile medial prefrontal cortex encoded the last pup location, but this decayed as the spatial-memory strategy declined. Our results suggest a neural competition between a weakening spatial-memory and strengthening sound-cued neural representation to mediate strategy switches.

neuroscience↗

Social experience alters oxytocinergic modulation in the nucleus accumbens of female prairie voles

Social relationships are dynamic and evolve with shared and personal experiences. Whether the functional role of social neuromodulators also evolves with experience to shape the trajectory of relationships is unknown. We utilized pair bonding in the socially monogamous prairie voles as an example of socio-sexual experience that dramatically alters behaviors displayed toward other individuals. We investigated oxytocin-dependent modulation of excitatory synaptic transmission in the nucleus accumbens as a function of pair bonding status. We found that an oxytocin receptor agonist decreases the amplitude of spontaneous Excitatory Postsynaptic Currents (EPSCs) in sexually naive virgin, but not pair-bonded, female voles, while it increases the amplitude of electrically evoked EPSCs in paired voles, but not in virgins. This oxytocin-dependent potentiation of synaptic transmission relies on the de novo coupling between oxytocin receptor signaling and endocannabinoid CB1 receptor signaling in pair bonded voles. Blocking CB1 receptors after pair bond formation increases the occurrence of a specific form of social rejection - defensive upright response - that is displayed towards the partner but not towards a novel individual. Altogether, our results demonstrate that oxytocins action in the nucleus accumbens is changed through social experience in a way that regulates the trajectory of social interactions as the relationship with the partner unfolds, potentially promoting the maintenance of a pair bond by inhibiting aggressive responses. These results provide a mechanism by which social experience and context shift oxytocinergic signaling to impact neural and behavioral responses to social cues.

neuroscience↗

Becoming a better parent: mice learn sounds that improve a stereotyped maternal behavior

While mothering is often instinctive and stereotyped in species-specific ways, evolution can favor genetically "open" behavior programs that allow experience to shape infant care. Among experience-dependent maternal behavioral mechanisms, sensory learning about infants has been hard to isolate from motivational changes arising from sensitization with infants. We developed a paradigm where sensory learning of an infant-associated cue improves a stereotypical maternal behavior in female mice. Mice instinctively employed a spatial memory-based strategy when engaged repetitively in a pup search and retrieval task. However, by playing a sound from a T-maze arm to signal where a pup will be delivered for retrieval, mice learned within 7 days and retained for at least 2 weeks the ability to use this specific cue to guide a more efficient search strategy. The motivation to retrieve pups also increased, but that alone did not sufficiently explain the shift in search strategy. Bilaterally silencing auditory cortical activity significantly impaired the new strategy without changing the motivation to retrieve pups. Finally, motherhood as compared to infant-care experience alone accelerated how quickly the new sensory-based strategy was acquired, suggesting a role for the maternal hormonal state. By rigorously establishing that newly formed sensory associations can improve the performance of a natural maternal behavior, this work facilitates future studies into the neurochemical and circuit mechanisms that mediate novel sensory learning in the maternal context, as well as more learning-based mechanisms of parental behavior in rodents.

neuroscience↗

Experience-dependent coding of frequency-modulated trajectories by offsets in auditory cortex

Frequency modulations are an inherent feature of many behaviorally relevant sounds, including vocalizations and music. Changing trajectories in a sounds frequency often conveys meaningful information, which can be used to differentiate sound categories, as in the case of intonations in tonal languages. However, it is not clear what features of the neural responses in what parts of the auditory cortical pathway might be more important for conveying information about behaviorally relevant frequency modulations, and how these responses change with experience. Here we uncover tuning to subtle variations in frequency trajectories in mouse auditory cortex. Surprisingly, we found that auditory cortical responses could be modulated by variations in a pure tone trajectory as small as 1/24th of an octave. Offset spiking accounted for a significant portion of tuned responses to subtle frequency modulation. Offset responses that were present in the adult A2, but not those in Core auditory cortex, were plastic in a way that enhanced the representation of an acquired behaviorally relevant sound category, which we illustrate with the maternal mouse paradigm for natural communication sound learning. By using this ethologically inspired sound-feature tuning paradigm to drive auditory responses in higher-order neurons, our results demonstrate that auditory cortex can track much finer frequency modulations than previously appreciated, which allows A2 offset responses in particular to attune to the pitch trajectories that distinguish behaviorally relevant, natural sound categories.

neuroscience↗