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Accueil du site Neuro-PSI > Departments > Cognition & Behavior > Nicolas Mathevon Team

Sensory Neuro-Ethology (ENES Team)

Group leader : Nicolas Mathevon (University of Lyon/Saint-Étienne &
Institut universitaire de France)

Elucidating how environmental and social constraints shape the evolution of acoustic communication and the ability to produce vocalizations bearing complex information in both animals and humans is one of the most interesting challenges of modern science. We propose a comparative and experimental view to tackle this question, developing an alliance between research on wild animal behavior in the field and investigations in the laboratory. Our research goes along four axes : a phylogenetical axis with a comparative approach of communication systems throughout the vertebrate phylum (fish, crocodiles, birds and mammals) ; a trans-disciplinary axis by investigating processes at the brain level together with the behavioral level ; a social complexity axis focusing on one end on “simple” communication and social systems found in fish and crocodiles, and on the other end on complex or highly complex ones in birds, marine mammals and primates including Humans ; an applied axis where our bioacoustic approach is valued to assess the impacts of human activities on animals’ behavior and serves to develop wildlife management solutions that integrate the ethological dimension.

Our team includes 1 professor, 6 associate professors (all with a heavy teaching load), 1.5 technicians, post-docs and PhD students. We are ethologists, specialized in bioacoustics, and we use to work in close collaboration with neuroscientists on one hand (electrophysiologists, specialists in brain imaging) and behavioral ecologists on the other hand. Within Neuro-PSI, our team is under the main tutelage of two organizations : the university of St-Etienne and the CNRS.

Main research projects

Human baby’s non-verbal acoustic communication

Crying is a vital built-in survival mechanism for the Human baby. Yet, despite this, the information encoded in cries remains poorly understood, and the factors driving the perception of cries by adult listeners have not been thoroughly investigated. To provide a step change in our understanding of the nature and function of babies’ cries, we have started a long-term, multilevel (from behavior to brain), multidisciplinary investigation centered on the coding (production) and decoding (perception) of this communicative signal. A first aim of our project is to search for reliable correlations between cry structure, stress sources and stress levels. Using dedicated sound analysis tools to compare the structure of cries of healthy babies recorded in controlled conditions differing by the degree of elicited stress (bath, vaccinations), we have identified vocal ‘roughness’, a composite acoustic factor characterizing the level of aperiodicity of the cries, that differs between different levels of discomfort or pain. Besides, we showed that at the age of 3 months the cries of human babies support a well-defined individual signature that allow parents to reliably identify their baby. Remarkably, we showed that both mothers and fathers can reliably and equally recognize their baby from their cries, and that the only crucial factor affecting this ability is the amount of time spent by the parent with their own baby (results published in Nature Communications). Our results thus highlight the importance of exposure and learning in the development of this ability. In a third line of research we investigated the consequences of sex stereotypes on adults’ perception of babies’ cries. We found that the vocal dimorphism characterizing the voice of adult speakers (men are lower-pitched than women) is generalized by adult listeners to their perception of babies’ cries : low-pitched cries of 3-month old babies are more likely to be attributed to boys and high-pitched cries to girls by adult listeners, despite the absence of sex differences in pitch at this age. Moreover, we found that adult men rated relatively low-pitched cries as expressing more discomfort when presented as belonging to boys than when presented as belonging to girls. These initial results highlight the importance of further investigating the impact of sex stereotypes on adult assessment of babies’ cries, in order to better understand how cries mediate parent-baby communication.

Non-human mammals’ acoustic communication networks

Among animals living in social groups, individuals form communication networks essential to mediate their social interactions. The origin and maintenance of social group structure is thus a central topic in behavioral biology. Whereas one approach is to understand the processes that account for sociality over an evolutionary scale, our proximal approach aims at deciphering the mechanisms by which the social fabric is maintained over an individual lifetime scale. We explored this question by studying the vocal communication of three non-human primates known for their complex social relationships (mandrill, gorilla, and bonobo) and a marine mammal demonstrating one of the most competitive breeding systems, the northern elephant seal. Conversely to common belief, we found that mandrills and bonobos demonstrate some degree of vocal plasticity. We thus stressed that mandrills’ calls contain information about genetic relatedness and the degree of familiarity between JPEGindividuals, and that individuals can rely on these complex vocal signals alone to discriminate unknown kin from non-kin (results published in Nature Communications). We found a similar plasticity in bonobos and further showed that these apes demonstrate reliable vocal recognition of social partners, even if they have been separated for five years. Apart structural variations of signals, non-human primates can follow primitive forms of conversational rules, a result that we found when investigating vocal exchanges between gorillas. Besides, we demonstrated that northern elephant seal males routinely memorize and recognize the unique tempo and timbre of their rivals’ voices, and use this rhythmic information to individually identify competitors, which facilitates navigation within the social network of the reproductive colony (a result published in Current Biology).

Acoustic communication and pair-bonding in birds

The benefits of communication during cooperative behaviors are generally assumed, but how communication and cooperation influence each other remains understudied. The monogamous pair bond in birds is a cooperative partnership on several aspects. Partners work as a team during parental care and may synchronize activities such as foraging or resource defence. The coordination of behaviors between mates is thus a central aspect of the biology of the monogamous pair bond and may rely on pair acoustic communication, which is surprisingly little understood. Focusing on the zebra finch as a study species and using a multidisciplinary approach involving bioacoustics, behavioural biology, ecology, physiology and in-vivo electrophysiology, we investigated how acoustic communication participates in pair bond formation, maintenance and success, what are the emerging properties of the pair bond for communication at the level of the social group, and what are the physiological and neurobiological consequences of pair bonding on individual auditory perception and acoustic communication. We showed that bird mates use call exchanges at the nest to organize bi-parental care and adapt this calling behaviour to maintain its efficiency during periods of increased background noise31. We also found that vocal exchanges help maintaining the pair-bond in diverse situations : when visual contact is lost, partners increase the temporal coordination of their calls ; in a group, birds preferentially call directly after their partner. We further demonstrated that social context impacts brain activity and vocal behaviour. Thus, social isolation of male zebra finches modifies not only call rate in response to female calls, but also the acoustic structure of evoked calls. Remarkably, we demonstrated that the stress-induced calls of males provoke both behavioral changes and an increase in corticosterone levels in their female partner, providing the first evidence for physiological resonance and emotional contagion in a songbird species.

Information coding in the vocalizations of crocodiles

The acoustic signals of crocodilians play a major role in the first stages of life. Specifically, parental care is the rule in all crocodilians and relies strongly on acoustic interactions between mothers (sometimes fathers) and their young. In addition to guarding the nest, females help hatchlings to go out of the eggs, guard them against potential predators, and occasionally move the pod to new nursery areas. Our team has been investigating the communication processes that coordinate mother’s and juveniles’ behaviors since a decade. These recent years, we found embedded information about the emitter’s size in juvenile calls, and experimentally demonstrated that Nile crocodile mothers breeding in the wild are less receptive to the calls of larger juveniles. Using synthetized sounds, we further showed that female’s reaction depends on call pitch, an important cue bearing size information. Besides, we investigated how crocodiles deal with decisional conflicts emerging from concurrent stimuli from different sensory channels. We found that inputs from one sensory modality (e.g. audition) may modulate the perception and behavioral reaction to another (e.g. olfaction). This cross-sensory modulation may contribute to decision making in the wild.

Multi-modal communication in fish

Communication is essential during social interactions including animal conflicts and it is often a complex process involving multiple sensory channels or modalities. How different sensory modalities interplay during agonistic interactions remains largely unknown in fish. To tackle this question we studied the behavioral responses to both the composite multimodal signal and each unimodal component. We found that acoustic signals alone do not elicit agonistic behavioral response in our model, the cichlid fish Metriaclima zebra. Conversely, the visual perception of a competitor is sufficient to trigger males’ aggressiveness. However, sound stimuli modulate the intensity of aggressive response.

Auditory scene analysis by a songbird

One of the most complex tasks performed by sensory systems is "scene analysis" : the interpretation of complex signals as behaviorally relevant objects. The study of this problem, universal to species and sensory modalities, is particularly challenging in audition, where sounds from various sources and localizations, degraded by propagation through the environment, sum to form a single acoustical signal. We studied how the individual signature coded in the zebra finch long distance contact call degrades with propagation, and how the zebra finch brain integrates individual and distance information. We demonstrated that the individual signature of zebra finches’ calls is very resistant to propagation-induced degradation, and that the most individualized acoustic parameters depend on distance. Using operant conditioning experiments, we showed that female birds are experts at discriminating between the degraded vocal signatures of two males, and that they can improve their ability substantially if they can train over increasing distances. Finally, we showed that this impressive discrimination ability also occurs at the neural level : we found a population of neurons in the avian auditory forebrain that discriminate individual voices with various degrees of propagation-induced degradation without prior familiarization or training (result published in the Journal of Neuroscience). The finding of such a high-level auditory processing, in the primary auditory cortex, opens a new range of investigations, at the interface of neural processing and behavior.

Multi-scale effects of acoustic stressors in aquatic environments

This research strand explores how acoustic pollution modulates animal behavior and between-species interactions. Individual responses to noise are well documented but we still do not know how they translate to higher integration levels and affect species coexistence and community stability. Moreover, while the effects of noise have been largely scrutinized in terrestrial and marine organisms, our knowledge remains scarce on fresh waters. We are currently characterizing the spatio-temporal features of anthropogenic noise in freshwater habitats (lakes) and test, under controlled conditions, the behavioral (organism level) and functional (interaction level) responses.

Acoustic monitoring of wildlife

Bioacoustics is an emergent and important tool used for monitoring animal populations and our team is more and more solicited by national and regional parks, as well as other organizations in charge of wildlife management (e.g. Office de la Chasse et de la Faune Sauvage). Considering that one of our missions as a public research team is to ensure the transfer of scientific knowledge, we have started to developing strong links with these organisms. These last years, our main project has revolved around the acoustic monitoring of populations of rock ptarmigans Lagopus muta (an endangered bird species) in the French Alps and the Pyreneans. With the aim of calibrating a census method using bioacoustic automatic recorders, we firstly assessed the individual variability of males’ calls, identifying acoustic features that allow a reliable discrimination between individuals. We then set up a triangulation method that takes into account the peculiar sound transmission constraints of mountainous areas. Beside its applied facet, this line of research brings first-hand data on acoustic communication networks in birds.




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