Deprivation of direct adult contact during development affects social representation in a songbird.

Social cognition involves a wide array of skills that are built largely through interactions with conspecifics and therefore depend upon early social experience. Motivation for social stimuli is a key feature of social behavior and an operant conditioning task showed that isolated wild-caught adult starlings (Sturnus vulgaris) are highly motivated to access pictures of other starlings. Here, we show that hand-raised adult starlings maintained in groups of peers throughout development but without any contact with adult models were not or only poorly motivated to access pictures of conspecifics. Moreover, they did not prefer pictures of starlings to pictures of landscapes, unlike birds wild-caught as adults. These results raise questions about the role of social experience during development, particularly with adult models, in the development of social motivation and of social representation in general.

Experimental Tests for Measuring Individual Attentional Characteristics in Songbirds.

Attention is defined as the ability to process selectively one aspect of the environment over others and is at the core of all cognitive processes such as learning, memorization, and categorization. Thus, evaluating and comparing attentional characteristics between individuals and according to situations is an important aspect of cognitive studies. Recent studies showed the interest of analyzing spontaneous attention in standardized situations, but data are still scarce, especially for songbirds. The present study adapted three tests of attention (towards visual non-social, visual social, and auditory stimuli) as tools for future comparative research in the European starling (Sturnus vulgaris), a species that is well known to present individual variations in social learning or engagement. Our results reveal that attentional characteristics (glances versus gazes) vary according to the stimulus broadcasted: more gazes towards unusual visual stimuli and species-specific auditory stimuli and more glances towards species-specific visual stimuli and hetero-specific auditory stimuli. This study revealing individual variations shows that these tests constitute a very useful and easy-to-use tool for evaluating spontaneous individual attentional characteristics and their modulation by a variety of factors. Our results also indicate that attentional skills are not a uniform concept and depend upon the modality and the stimulus type.

When perceptual laterality vanishes with curiosity: A study in dolphins and starlings.

Sensory laterality is influenced by the individual's attentional state. There are variations in the way different individuals of a same species attend to stimuli. When confronted to novelty, some individuals are more explorative than others. Curiosity is composed of sensation and knowledge seeking in humans. In the present study, we hypothesized that more curious animals, i.e., showing more sensory exploration would be less lateralized than quietly attentive individuals, performing instead more gazing behaviours. In order to test this hypothesis and its possible generality, we performed two studies using two animal models (dolphins and starlings) and two modalities (visual and auditory) of presentation of species-specific and non-species-specific stimuli. Both dolphins and starlings presented more gazes for the species-specific stimuli and more exploratory components for the non-species-specific stimuli. Moreover, in both cases, the non-species-specific stimuli involved more lateralized responses whereas there was no or less clear laterality for the species-specific stimuli. The more exploratory dolphins and starlings also showed a decreased laterality: the more "curious" individuals showed no laterality. Further studies are needed on characterization of curiosity in relation to attention structure. The present study suggests that individual variations in sensory laterality may help disentangle the subtle differences between curiosity, attention and boldness.

Erratum: Catala, A., et al. Is There a Profile of Spontaneous Seizure-Alert Pet Dogs? A Survey of French People with Epilepsy. Animals 2020, 10, 254.

The authors wish to make the following corrections to this paper: [...].

EEG individual power profiles correlate with tension along spine in horses.

Assessing chronic pain is a challenge given its subjective dimension. In humans, resting state electroencephalography (EEG) is a promising tool although the results of various studies are contradictory. Spontaneous chronic pain is understudied in animals but could be of the highest interest for a comparative study. Riding horses show a very high prevalence of back disorders thought to be associated with chronic pain. Moreover, horses with known back problems show cognitive alterations, such as a lower attentional engagement. Therefore, we hypothesized that the individual EEG power profiles resting state (i.e. quiet standing) of different horses could reflect the state of their back, that we measured using static sEMG, a tool first promoted to assess lower back pain in human patients. Results show that 1) EEG profiles are highly stable at the intra-individual level, 2) horses with elevated back tension showed resting state EEG profiles characterized by more fast (beta and gamma) and less slow (theta and alpha) waves. The proportion of theta waves was particularly negatively correlated with muscular tension along the spine. Moreover, elevated back tension was positively correlated with the frequency of stereotypic behaviours (an "addictive- like" repetitive behavior) performed by the horses in their stall. Resting state quantitative EEG appears therefore as a very promising tool that may allow to assess individual subjective chronic pain experience, beyond more objective measures of tension. These results open new lines of research for a multi-species comparative approach and might reveal very important in the context of animal welfare.

Prediction and detection of human epileptic seizures based on SIFT-MS chemometric data.

Although epilepsy is considered a public health issue, the burden imposed by the unpredictability of seizures is mainly borne by the patients. Predicting seizures based on electroencephalography has had mixed success, and the idiosyncratic character of epilepsy makes a single method of detection or prediction for all patients almost impossible. To address this problem, we demonstrate herein that epileptic seizures can not only be detected by global chemometric analysis of data from selected ion flow tube mass spectrometry but also that a simple mathematical model makes it possible to predict these seizures (by up to 4 h 37 min in advance with 92% and 75% of samples correctly classified in training and leave-one-out-cross-validation, respectively). These findings should stimulate the development of non-invasive applications (e.g., electronic nose) for different types of epilepsy and thereby decrease of the unpredictability of epileptic seizures.

Lateralization of social signal brain processing correlates with the degree of social integration in a songbird.

Group cohesion relies on the ability of its members to process social signals. Songbirds provide a unique model to investigate links between group functioning and brain processing of social acoustic signals. In the present study, we performed both behavioral observations of social relationships within a group of starlings and individual electrophysiological recordings of HVC neuronal activity during the broadcast of either familiar or unfamiliar individual songs. This allowed us to evaluate and compare preferred partnerships and individual electrophysiological profiles. The electrophysiological results revealed asymmetric neuronal activity in the HVC and higher responsiveness to familiar than to unfamiliar songs. However, most importantly, we found a correlation between strength of cerebral asymmetry and social integration in the group: the more preferred partners a bird had, the more its HVC neuronal activity was lateralized. Laterality is likely to give advantages in terms of survival. Our results suggest that these include social skill advantages. Better knowledge of links between social integration and lateralization of social signal processing should help understand why and how lateralization has evolved.

Is there a Profile of Spontaneous Seizure-Alert Pet Dogs? A Survey of French People with Epilepsy.

Despite controversies and the lack of research, dogs are empirically selected and trained to perform as service dogs, in relation to the dogs' and future owners' characteristics. We assessed the characteristics of both humans and dogs in an unbiased population (not selected or trained) of spontaneous seizure-alert by pet dogs and investigated whether we could replicate previous findings. We addressed a self-reporting questionnaire to French people with epilepsy. We analyzed the general characteristics of the humans and pet dogs and their behaviors that could alert their owner before a seizure. In addition, we used the Monash Canine Personality Questionnaire refined to evaluate pet dogs' personality through five different traits, and the Monash Dog-Owner Relationship scale to assess human-dog relationships. In line with previous reports, we found no particular factor, either pet-, people- or epilepsy-related that could be associated with the presence or absence of alert behaviors. Alert behaviors and circumstances were explored and three different alert patterns emerged. In terms of personality, seizure-alert pet dogs scored significantly higher than non-alerting dogs for the traits "Motivation" and "Training Focus" and lower for "Neuroticism". The owner-dog bond score was significantly higher for seizure-alert dogs than for non-alerting dogs.

Horses associate individual human voices with the valence of past interactions: a behavioural and electrophysiological study.

Brain lateralization is a phenomenon widely reported in the animal kingdom and sensory laterality has been shown to be an indicator of the appraisal of the stimulus valence by an individual. This can prove a useful tool to investigate how animals perceive intra- or hetero-specific signals. The human-animal relationship provides an interesting framework for testing the impact of the valence of interactions on emotional memories. In the present study, we tested whether horses could associate individual human voices with past positive or negative experiences. Both behavioural and electroencephalographic measures allowed examining laterality patterns in addition to the behavioural reactions. The results show that horses reacted to voices associated with past positive experiences with increased attention/arousal (gamma oscillations in the right hemisphere) and indicators of a positive emotional state (left hemisphere activation and ears held forward), and to those associated with past negative experiences with negative affective states (right hemisphere activation and ears held backwards). The responses were further influenced by the animals' management conditions (e.g. box or pasture). Overall, these results, associating brain and behaviour analysis, clearly demonstrate that horses' representation of human voices is modulated by the valence of prior horse-human interactions.

Dogs demonstrate the existence of an epileptic seizure odour in humans.

Although different studies have shown that diseases such as breast or lung cancer are associated with specific bodily odours, no study has yet tested the possibility that epileptic seizures may be reflected in an olfactory profile, probably because there is a large variety of seizure types. The question is whether a "seizure-odour", that would be transversal to individuals and types of seizures, exists. This would be a pre requisite for potential anticipation, either by electronic systems (e.g., e-noses) or trained dogs. The aim of the present study therefore was to test whether trained dogs, as demonstrated for cancer or diabetes, may discriminate a general epileptic seizure odor (different from body odours of the same person in other contexts and common to different persons). The results were very clear: all dogs discriminated the seizure odour. The sensitivity and specificity obtained were amongst the highest shown up to now for discrimination of diseases. This constitutes a first proof that, despite the variety of seizures and individual odours, seizures are associated with olfactory characteristics. These results open a large field of research on the odour signature of seizures. Further studies will aim to look at potential applications in terms of anticipation of seizures.

Dog alerting and/or responding to epileptic seizures: A scoping review.

Recently, there has been a rising interest in service dogs for people with epilepsy. Dogs have been reported as being sensitive to epileptic episodes in their owners, alerting before and/or responding during or after a seizure, with or without specific training. The purpose of this review is to present a comprehensive overview of the scientific research on seizure-alert/response dogs for people with epilepsy. We aimed to identify the existing scientific literature on the topic, describe the characteristics of seizure-alert/response dogs, and evaluate the state of the evidence base and outcomes. Out of 28 studies published in peer-reviewed journals dealing with this topic, only 5 (one prospective study and four self-reported questionnaires) qualified for inclusion according to PRISMA guidelines. Reported times of alert before seizure varied widely among dogs (with a range from 10 seconds to 5 hours) but seemed to be reliable (accuracy from ≥70% to 85% according to owner reports). Alerting behaviors were generally described as attention-getting. The alert applied to many seizure types. Dogs mentioned as being seizure-alert dogs varied in size and breed. Training methods differed between service animal programs, partially relying on hypothesized cues used by dogs (e.g., variations in behavior, scent, heart rate). Most studies indicated an increase in quality of life and a reduction in the seizure frequency when living with a dog demonstrating seizure-related behavior. However, the level of methodological rigor was generally poor. In conclusion, scientific data are still too scarce and preliminary to reach any definitive conclusion regarding the success of dogs in alerting for an impending seizure, the cues on which this ability may be based, the best type of dog, and associated training. While these preliminary data suggest that this is a promising topic, further research is needed.

An Ambulatory Electroencephalography System for Freely Moving Horses: An Innovating Approach.

Electroencephalography (EEG) that has been extensively studied in humans presents also a large interest for studies on animal brain processes. However, since the quality of the recordings is altered by muscular activity, most EEG recordings on animals are obtained using invasive methods with deeply implanted electrodes. This requires anesthesia and can thus only be used in laboratory or clinical settings. As EEG is a very useful tool both for detecting brain alterations due to diseases or accidents and to evaluate the arousal and attentional state of the animal, it seemed crucial to develop a tool that would make such recordings possible in the horse's home environment, with a freely moving horse. Such a tool should neither be invasive nor cause discomforts to the horse as the usual other practice which consists, after shaving the zone, in gluing the electrodes to the skin. To fulfill these requirements, we developed a novel EEG headset adapted to the horse's head that allows an easy and fast positioning of the electrodes and that can be used in the home environment on a freely moving horse. In this study, we show that this EEG headset allows to obtain reliable recordings, and we propose an original evaluation of an animal's "EEG profile" that allows comparisons between individuals and situations. This EEG headset opens new possibilities of investigation on horse cognition, and it can also become a useful tool for veterinarians to evaluate cerebral disorders or check the anesthesia level during a surgery.

A three-dimensional digital atlas of the starling brain.

Because of their sophisticated vocal behaviour, their social nature, their high plasticity and their robustness, starlings have become an important model species that is widely used in studies of neuroethology of song production and perception. Since magnetic resonance imaging (MRI) represents an increasingly relevant tool for comparative neuroscience, a 3D MRI-based atlas of the starling brain becomes essential. Using multiple imaging protocols we delineated several sensory systems as well as the song control system. This starling brain atlas can easily be used to determine the stereotactic location of identified neural structures at any angle of the head. Additionally, the atlas is useful to find the optimal angle of sectioning for slice experiments, stereotactic injections and electrophysiological recordings. The starling brain atlas is freely available for the scientific community.

Social visual contact, a primary "drive" for social animals?

Social animals are always searching for conspecifics, thereby expressing a genuine "social need". This need is illustrated by the fact that social isolation can induce isolation syndromes that can be attenuated by devices such as mirrors. Social contacts appear to be so vital for social animals that they may be ready to work to obtain social stimulations. We used operant conditioning to investigate the possibility to use visual contact (through pictures of conspecifics) as a primary reinforcer. Isolated European starlings (Sturnus vulgaris) were offered the choice of seeing either social images (i.e. pictures of conspecifics) or non-social images (i.e. pictures of landscapes or pictures of monkeys) by triggering sensors. In contrast with most studies, our subjects were presented still pictures of conspecifics and not videos. Moreover, these pictures were used as primary reinforcers and thus were not paired with food. Our data show that starlings were ready to work and to use the apparatus (i.e. sensors) to see pictures in the absence of any other reward. Moreover, they actively and significantly preferred pictures of conspecifics to pictures of inanimate objects (landscapes) or of heterospecifics (monkeys). This suggests that 2D pictures with a social overtone can be used as primary reinforcers for isolated social birds.

Assessing video presentations as environmental enrichment for laboratory birds.

The aim of the present study was to investigate the effects of video presentations of natural landscapes on European starlings' (Sturnus vulgaris) stereotypic behaviours (SBs) and other abnormal repetitive behaviours (ARBs) and to evaluate the impact of past experience by comparing wild-caught and hand-reared starlings' reactions. Ten wild-caught and five hand-reared starlings were presented 1-hour videos of landscapes twice a day for five successive days, while a control group of eight wild-caught and four hand-reared starlings was presented a grey screen for the same amount of time. The analysis of the starlings' behaviour revealed that the video presentations of landscapes appeared to have a positive but limited and experience-dependent effect on starlings' SBs and other ARBs compared to the controls. Indeed, whereas video presentations seemed to modulate high rates of SBs and ARBs, they did not appear to be enriching enough to prevent the emergence or the development of SBs and ARBs in an impoverished environment. They even appeared to promote a particular type of SB (somersaulting) that is thought to be linked to escape motivation. The fact that this effect was observed in hand-reared starlings suggests that videos of landscapes could elicit motivation to escape even in birds that never experienced outdoor life. These results highlight the importance of investigating stereotypic behaviour both quantitatively and qualitatively in order to provide crucial clues on animal welfare.

Seasonal female brain plasticity in processing social vs. sexual vocal signals.

While cerebral plasticity has been extensively studied and demonstrated - during ontogenetic development, few studies have considered adult plasticity in different social contexts using relevant social communication signals. Communication requires adaptability throughout the life of an individual, especially in species for which breeding periods (when intersexual signaling prevails) are interspersed with more 'social' (non-sexual) periods when intrasexual bonding prevails. In songbirds, structure or frequency of songs or song elements may convey different information depending on the season. This is the case in the European starling, where some song structures characterize social bonds between females while other song structures are more characteristic of male courtship. We hypothesized that the female perceptual system may have adapted to these changes in song structure and function according to season, and we tested for potential seasonal brain plasticity. Electrophysiological recordings from adult female starlings during playback of song elements with different functions showed clear seasonal (breeding/non-breeding) changes in neuronal responses in the primary auditory area. The proportion of responsive sites was higher in response to social (non-sexual) songs during the non-reproductive season, and higher in response to sexual songs during the reproductive season.

How social experience shapes song representation in the brain of starlings.

Birdsong, like speech, is a learned behaviour whose critical function is to communicate with others and whose development critically depends on social influences. Song learning is a complex phenomenon that involves not only the development of species-specific vocalisations, but also the development of the ability to organise these vocalisations and to use them in an appropriate context. Although the fact that interactions with adult experienced models are essential for song production to develop properly has been well established, far less is known about song perception and processing. The fact that songbirds learn to vocalise and to use their vocalisations selectively through interactions with adults questions whether such interactions are also required for songbirds to perceive and process their vocalisations selectively and whether social interactions may shape song perception and processing as they shape song production. In order to address these questions, our team uses an original neuroethological approach to study the neural bases of song behaviour in a highly social songbird species: the European starlings. We provide here a synthesis of the results we have obtained using this approach over the last decade. Our results show that direct social experience with adult experienced models not only shapes song behaviour but also shapes these songbirds' brains and their ability to perceive and to process acoustic signals whose communicative value, as well as their acoustic structure, have to be learned.

Experience with adults shapes multisensory representation of social familiarity in the brain of a songbird.

Social animals learn to perceive their social environment, and their social skills and preferences are thought to emerge from greater exposure to and hence familiarity with some social signals rather than others. Familiarity appears to be tightly linked to multisensory integration. The ability to differentiate and categorize familiar and unfamiliar individuals and to build a multisensory representation of known individuals emerges from successive social interactions, in particular with adult, experienced models. In different species, adults have been shown to shape the social behavior of young by promoting selective attention to multisensory cues. The question of what representation of known conspecifics adult-deprived animals may build therefore arises. Here we show that starlings raised with no experience with adults fail to develop a multisensory representation of familiar and unfamiliar starlings. Electrophysiological recordings of neuronal activity throughout the primary auditory area of these birds, while they were exposed to audio-only or audiovisual familiar and unfamiliar cues, showed that visual stimuli did, as in wild-caught starlings, modulate auditory responses but that, unlike what was observed in wild-caught birds, this modulation was not influenced by familiarity. Thus, adult-deprived starlings seem to fail to discriminate between familiar and unfamiliar individuals. This suggests that adults may shape multisensory representation of known individuals in the brain, possibly by focusing the young's attention on relevant, multisensory cues. Multisensory stimulation by experienced, adult models may thus be ubiquitously important for the development of social skills (and of the neural properties underlying such skills) in a variety of species.

No need to Talk, I Know You: Familiarity Influences Early Multisensory Integration in a Songbird's Brain.

It is well known that visual information can affect auditory perception, as in the famous "McGurk effect," but little is known concerning the processes involved. To address this issue, we used the best-developed animal model to study language-related processes in the brain: songbirds. European starlings were exposed to audiovisual compared to auditory-only playback of conspecific songs, while electrophysiological recordings were made in their primary auditory area (Field L). The results show that the audiovisual condition modulated the auditory responses. Enhancement and suppression were both observed, depending on the stimulus familiarity. Seeing a familiar bird led to suppressed auditory responses while seeing an unfamiliar bird led to response enhancement, suggesting that unisensory perception may be enough if the stimulus is familiar while redundancy may be required for unfamiliar items. This is to our knowledge the first evidence that multisensory integration may occur in a low-level, putatively unisensory area of a non-mammalian vertebrate brain, and also that familiarity of the stimuli may influence modulation of auditory responses by vision.

Neural correlates of experience-induced deficits in learned vocal communication.

Songbirds are one of the few vertebrate groups (including humans) that evolved the ability to learn vocalizations. During song learning, social interactions with adult models are crucial and young songbirds raised without direct contacts with adults typically produce abnormal songs showing phonological and syntactical deficits. This raises the question of what functional representation of their vocalizations such deprived animals develop. Here we show that young starlings that we raised without any direct contact with adults not only failed to differentiate starlings' typical song classes in their vocalizations but also failed to develop differential neural responses to these songs. These deficits appear to be linked to a failure to acquire songs' functions and may provide a model for abnormal development of communicative skills, including speech.