Differences in the expression of cortex-wide neural dynamics are related to behavioral phenotype.

Behavior differs across individuals, ranging from typical to atypical phenotypes.1 Understanding how differences in behavior relate to differences in neural activity is critical for developing treatments of neuropsychiatric and neurodevelopmental disorders. One hypothesis is that differences in behavior reflect individual differences in the dynamics of how information flows through the brain. In support of this, the correlation of neural activity between brain areas, termed "functional connectivity," varies across individuals2 and is disrupted in autism,3 schizophrenia,4 and depression.5 However, the changes in neural activity that underlie altered behavior and functional connectivity remain unclear. Here, we show that individual differences in the expression of different patterns of cortical neural dynamics explain variability in both functional connectivity and behavior. Using mesoscale imaging, we recorded neural activity across the dorsal cortex of behaviorally "typical" and "atypical" mice. All mice shared the same recurring cortex-wide spatiotemporal motifs of neural activity, and these motifs explained the large majority of variance in cortical activity (>75%). However, individuals differed in how frequently different motifs were expressed. These differences in motif expression explained differences in functional connectivity and behavior across both typical and atypical mice. Our results suggest that differences in behavior and functional connectivity are due to changes in the processes that select which pattern of neural activity is expressed at each moment in time.

Sexual coordination in a whole-brain map of prairie vole pair bonding.

Sexual bonds are central to the social lives of many species, including humans, and monogamous prairie voles have become the predominant model for investigating such attachments. We developed an automated whole-brain mapping pipeline to identify brain circuits underlying pair-bonding behavior. We identified bonding-related c-Fos induction in 68 brain regions clustered in seven major brain-wide neuronal circuits. These circuits include known regulators of bonding, such as the bed nucleus of the stria terminalis, paraventricular hypothalamus, ventral pallidum, and prefrontal cortex. They also include brain regions previously unknown to shape bonding, such as ventromedial hypothalamus, medial preoptic area, and the medial amygdala, but that play essential roles in bonding-relevant processes, such as sexual behavior, social reward, and territorial aggression. Contrary to some hypotheses, we found that circuits active during mating and bonding were largely sexually monomorphic. Moreover, c-Fos induction across regions was strikingly consistent between members of a pair, with activity best predicted by rates of ejaculation. A novel cluster of regions centered in the amygdala remained coordinated after bonds had formed, suggesting novel substrates for bond maintenance. Our tools and results provide an unprecedented resource for elucidating the networks that translate sexual experience into an enduring bond.

Linguistic laws in biology.

Linguistic laws, the common statistical patterns of human language, have been investigated by quantitative linguists for nearly a century. Recently, biologists from a range of disciplines have started to explore the prevalence of these laws beyond language, finding patterns consistent with linguistic laws across multiple levels of biological organisation, from molecular (genomes, genes, and proteins) to organismal (animal behaviour) to ecological (populations and ecosystems). We propose a new conceptual framework for the study of linguistic laws in biology, comprising and integrating distinct levels of analysis, from description to prediction to theory building. Adopting this framework will provide critical new insights into the fundamental rules of organisation underpinning natural systems, unifying linguistic laws and core theory in biology.

Sexual coordination in a whole-brain map of prairie vole pair bonding.

Sexual bonds are central to the social lives of many species, including humans, and monogamous prairie voles have become the predominant model for investigating such attachments. We developed an automated whole-brain mapping pipeline to identify brain circuits underlying pair-bonding behavior. We identified bonding-related c-Fos induction in 68 brain regions clustered in seven major brain-wide neuronal circuits. These circuits include known regulators of bonding, such as the bed nucleus of the stria terminalis, paraventricular hypothalamus, ventral pallidum, and prefrontal cortex. They also include brain regions previously unknown to shape bonding, such as ventromedial hypothalamus, medial preoptic area and the medial amygdala, but that play essential roles in bonding-relevant processes, such as sexual behavior, social reward and territorial aggression. Contrary to some hypotheses, we found that circuits active during mating and bonding were largely sexually monomorphic. Moreover, c-Fos induction across regions was strikingly consistent between members of a pair, with activity best predicted by rates of ejaculation. A novel cluster of regions centered in the amygdala remained coordinated after bonds had formed, suggesting novel substrates for bond maintenance. Our tools and results provide an unprecedented resource for elucidating the networks that translate sexual experience into an enduring bond.

Individual differences in social attachment: A multi-disciplinary perspective.

Social behavior varies across both individuals and species. Research to explain this variation falls under the purview of multiple disciplines, each with its own theoretical and empirical traditions. Integration of these disciplinary traditions is key to developing a holistic perspective. Here, we review research on the biology of social attachment, a phenomena in which individuals develop strong affective connections to one another. We provide a historical overview of research on social attachment from psychological, ethological and neurobiological perspectives. As a case study, we describe work on pair-bonding in prairie voles, a socially monogamous rodent. This specific topic takes advantage of many biological perspectives and techniques to explain social bonds. Lastly, we conclude with an overview of multi-dimensional conceptual frameworks that can be used to explain social phenomena, and we propose a new framework for research on individual variation in attachment behavior. These conceptual frameworks originate from philosophy, physics, ethology, cognitive science and neuroscience. The application and synthesis of such frameworks offers a rich opportunity to advance understanding of social behavior and its mechanisms.

Linguistic laws in biology.

Linguistic laws, the common statistical patterns of human language, have been investigated by quantitative linguists for nearly a century. Recently, biologists from a range of disciplines have started to explore the prevalence of these laws beyond language, finding patterns consistent with linguistic laws across multiple levels of biological organisation, from molecular (genomes, genes, and proteins) to organismal (animal behaviour) to ecological (populations and ecosystems). We propose a new conceptual framework for the study of linguistic laws in biology, comprising and integrating distinct levels of analysis, from description to prediction to theory building. Adopting this framework will provide critical new insights into the fundamental rules of organisation underpinning natural systems, unifying linguistic laws and core theory in biology.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

A Neuroscientist's Guide to the Vole.

Prairie voles have emerged as an important rodent model for understanding the neuroscience of social behavior. Prairie voles are well known for their capacity for pair bonding and alloparental care. These behavioral phenomena overlap with human social behavior but are not commonly observed in traditional rodent models. In this article, we highlight the many benefits of using prairie voles in neuroscience research. We begin by describing the advantages of using diverse and non-traditional study models. We then focus on social behaviors, including pair bonding, alloparental care, and peer interactions, that have brought voles to the forefront of social neuroscience. We describe many additional features of prairie vole biology and behavior that provide researchers with opportunities to address an array of research questions. We also survey neuroethological methods that have been used with prairie voles, from classic to modern techniques. Finally, we conclude with a discussion of other vole species, particularly meadow voles, and their own unique advantages for neuroscience studies. This article provides a foundation for researchers who are new to working with voles, as well as for experienced neuroscientists who want to expand their research scope. © 2021 Wiley Periodicals LLC.

Vocal and locomotor coordination develops in association with the autonomic nervous system.

In adult animals, movement and vocalizations are coordinated, sometimes facilitating, and at other times inhibiting, each other. What is missing is how these different domains of motor control become coordinated over the course of development. We investigated how postural-locomotor behaviors may influence vocal development, and the role played by physiological arousal during their interactions. Using infant marmoset monkeys, we densely sampled vocal, postural and locomotor behaviors and estimated arousal fluctuations from electrocardiographic measures of heart rate. We found that vocalizations matured sooner than postural and locomotor skills, and that vocal-locomotor coordination improved with age and during elevated arousal levels. These results suggest that postural-locomotor maturity is not required for vocal development to occur, and that infants gradually improve coordination between vocalizations and body movement through a process that may be facilitated by arousal level changes.

Divergent acoustic properties of gelada and baboon vocalizations and their implications for the evolution of human speech.

Human speech has many complex spectral and temporal features traditionally thought to be absent in the vocalizations of other primates. Recent explorations of the vocal capabilities of non-human primates are challenging this view. Here, we continue this trend by exploring the spectro-temporal properties of gelada (Theropithecus gelada) vocalizations. First, we made cross-species comparisons of geladas, chacma baboons, and human vowel space area. We found that adult male and female gelada exhaled grunts-a call type shared with baboons-have formant profiles that overlap more with human vowel space than do baboon grunts. These gelada grunts also contained more modulation of fundamental and formant frequencies than did baboon grunts. Second, we compared formant profiles and modulation of exhaled grunts to the derived call types (those not shared with baboons) produced by gelada males. These derived calls contained divergent formant profiles, and a subset of them, notably wobbles and vocalized yawns, were more modulated than grunts. Third, we investigated the rhythmic patterns of wobbles, a call type shown previously to contain cycles that match the 3-8 Hz tempo of speech. We use a larger dataset to show that the wobble rhythm overlaps more with speech rhythm than previously thought. We also found that variation in cycle duration depends on the production modality; specifically, exhaled wobbles were produced at a slower tempo than inhaled wobbles. Moreover, the variability in cycle duration within wobbles aligns with a linguistic property known as 'Menzerath's law' in that there was a negative association between cycle duration and wobble size (i.e. the number of cycles). Taken together, our results add to growing evidence that non-human primates are anatomically capable of producing modulated sounds. Our results also support and expand on current hypotheses of speech evolution, including the 'neural hypothesis' and the 'bimodal speech rhythm hypothesis'.

Gelada vocal sequences follow Menzerath's linguistic law.

Identifying universal principles underpinning diverse natural systems is a key goal of the life sciences. A powerful approach in addressing this goal has been to test whether patterns consistent with linguistic laws are found in nonhuman animals. Menzerath's law is a linguistic law that states that, the larger the construct, the smaller the size of its constituents. Here, to our knowledge, we present the first evidence that Menzerath's law holds in the vocal communication of a nonhuman species. We show that, in vocal sequences of wild male geladas (Theropithecus gelada), construct size (sequence size in number of calls) is negatively correlated with constituent size (duration of calls). Call duration does not vary significantly with position in the sequence, but call sequence composition does change with sequence size and most call types are abbreviated in larger sequences. We also find that intercall intervals follow the same relationship with sequence size as do calls. Finally, we provide formal mathematical support for the idea that Menzerath's law reflects compression-the principle of minimizing the expected length of a code. Our findings suggest that a common principle underpins human and gelada vocal communication, highlighting the value of exploring the applicability of linguistic laws in vocal systems outside the realm of language.

Vocal complexity influences female responses to gelada male calls.

Extensive research indicates that inter-sexual selection drives the evolution of complex vocal communication in birds, but parallel lines of evidence are almost entirely absent in mammals. This dearth of evidence, particularly among primates, limits our understanding of the link between sociality and vocal complexity. Here, we use a playback experiment to quantify how wild female geladas (Theropithecus gelada) respond to three call types that are 'derived' (i.e., unique to geladas) and made by males during various affiliative contexts. These derived calls appeared to be highly salient and preferable to females: they looked longer towards and spent more time in proximity to playbacks of male vocal sequences containing one of the derived calls than to sequences containing only common and less elaborate 'grunt' calls. Our results provide the first experimental evidence for vocal elaboration as a male-specific strategy to maintain social bonds with females in non-human primates.

Acoustic sequences in non-human animals: a tutorial review and prospectus.

Animal acoustic communication often takes the form of complex sequences, made up of multiple distinct acoustic units. Apart from the well-known example of birdsong, other animals such as insects, amphibians, and mammals (including bats, rodents, primates, and cetaceans) also generate complex acoustic sequences. Occasionally, such as with birdsong, the adaptive role of these sequences seems clear (e.g. mate attraction and territorial defence). More often however, researchers have only begun to characterise - let alone understand - the significance and meaning of acoustic sequences. Hypotheses abound, but there is little agreement as to how sequences should be defined and analysed. Our review aims to outline suitable methods for testing these hypotheses, and to describe the major limitations to our current and near-future knowledge on questions of acoustic sequences. This review and prospectus is the result of a collaborative effort between 43 scientists from the fields of animal behaviour, ecology and evolution, signal processing, machine learning, quantitative linguistics, and information theory, who gathered for a 2013 workshop entitled, 'Analysing vocal sequences in animals'. Our goal is to present not just a review of the state of the art, but to propose a methodological framework that summarises what we suggest are the best practices for research in this field, across taxa and across disciplines. We also provide a tutorial-style introduction to some of the most promising algorithmic approaches for analysing sequences. We divide our review into three sections: identifying the distinct units of an acoustic sequence, describing the different ways that information can be contained within a sequence, and analysing the structure of that sequence. Each of these sections is further subdivided to address the key questions and approaches in that area. We propose a uniform, systematic, and comprehensive approach to studying sequences, with the goal of clarifying research terms used in different fields, and facilitating collaboration and comparative studies. Allowing greater interdisciplinary collaboration will facilitate the investigation of many important questions in the evolution of communication and sociality.

Derived vocalizations of geladas (Theropithecus gelada) and the evolution of vocal complexity in primates.

Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2-12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with 'their' females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.

An experimental study of behavioural coping strategies in free-ranging female Barbary macaques (Macaca sylvanus).

A fundamental goal of stress research is to understand how individuals cope with challenges. Studies on a range of vertebrate species suggest that three groups of behaviour--affiliative, aggressive and self-directed behaviours--serve as coping strategies. To date, experimental studies of coping behaviour have tended to be conducted in captive conditions; the limited number of studies in free-ranging or wild settings have been observational in nature. We investigated coping behaviours in free-ranging female Barbary macaques (Macaca sylvanus) at Trentham Monkey Forest, UK, using an experimental playback approach to quantify subjects' responses to mildly aversive threat-grunts. Compared to silent control trials, playbacks of threat-grunts increased aggressive behaviours and one of the two self-directed behaviours examined (self-scratching). No such differences were seen for self-grooming, or for any affiliative behaviour. Elevations in the rate of one measure of aggression, lunging, were positively related to an average measure of adrenocortical activity (median faecal glucocorticoid metabolite levels over the study period). Evidence from females in a variety of Old World monkey species, including Barbary macaques, indicates that affiliative behaviours have an important role in coping with stressful events in the medium to longer term. Our results suggest that, in the short term, female Barbary macaques may use aggressive rather than affiliative behaviours in response to mild stress. These findings highlight the importance of considering how coping mechanisms may vary over time after a stressor, and how coping mechanisms relate to adrenocortical activity. Playback approaches like ours provide a powerful, flexible tool to explore issues such as this in free-ranging and wild animal populations.

Flibanserin and 8-OH-DPAT implicate serotonin in association between female marmoset monkey sexual behavior and changes in pair-bond quality.

INTRODUCTION: Psychopathological origins of personally distressing, hypoactive sexual desire disorder (HSDD) in women are unknown, but are generally attributed to an inhibitory neural regulator, serotonin (5-HT). Flibanserin, a 5-HT(1A) agonist and 5-HT(2A) antagonist, shows promise as a treatment for HSDD. AIM: To test the hypothesis that female marmoset sexual behavior is enhanced by flibanserin and diminished by 8-OH-DPAT, in order to evaluate the efficacy of serotonergic modulation of female sexual behavior in a pairmate social setting comparable to humans. METHODS: Sexual and social behavior were examined in eight female marmoset monkeys receiving daily flibanserin (15 mg/kg), 8-OH-DPAT (0.1 mg/kg), or corresponding vehicle for 15-16 weeks in a counterbalanced, within-subject design, while housed in long-term, stable male-female pairs. MAIN OUTCOME MEASURES: Marmoset pairmate interactions, including sexual and social behavior, were scored during weeks 5-6 of daily flibanserin, 8-OH-DPAT or vehicle treatment. 24-hour pharmacokinetic profiles of the drugs and their metabolites, as well as drug-induced acute symptoms of the 5-HT behavioral syndrome were also assessed. RESULTS: Two-way analysis of variance reveals that flibanserin-treated females attract more male sexual interest (P=0.020) and trigger increased grooming (P=0.001) between partners. In contrast, 8-OH-DPAT-treated females show increased rejection of male sexual advances (P=0.024), a tendency for decreased male sexual interest (P=0.080), and increased aggression with their male pairmates (P=0.049). CONCLUSIONS: While 8-OH-DPAT-treated female marmosets display decreased sexual receptivity and increased aggressive interactions with their male pairmates, flibanserin-treated female marmosets demonstrate increased affiliative behavior with their male pairmates. Such pro-affiliation attributes may underlie flibanserin's effectiveness in treating HSDD in women.