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The study of facial expressions in mammals provided great advances in the identification of their emotions and then in the comprehension of their sentience. So far, this area of research has excluded birds. With a naturalist approach, we analysed facial blushing and feather displays in domestic fowl. Hens were filmed in situations contrasting in emotional valence and arousal level: situations known to indicate calm states (positive valence / low arousal), have rewarding effects (positive valence / high arousal) or induce fear-related behaviour (negative valence / high arousal). Head feather position as well as skin redness of comb, wattles, ear lobes and cheeks varied across these situations. Skin of all four areas was less red in situations with low arousal compared to situations with higher arousal. Furthermore, skin redness of the cheeks and ear lobes also varied depending on the valence of the situation: redness was higher in situations with negative valence compared to situations with positive valence. Feather position also varied with the situations. Feather fluffing was mostly observed in positively valenced situations, except when hens were eating. We conclude that hens have facial displays that reveal their emotions and that blushing is not exclusive to humans. This opens a promising way to explore the emotional lives of birds, which is a critical step when trying to improve poultry welfare.
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Pollos , Emociones , Expresión Facial , Plumas , Animales , Pollos/fisiología , Emociones/fisiología , Femenino , Conducta Animal/fisiología , Nivel de Alerta/fisiologíaRESUMEN
Recently, horses and other domestic mammals have been shown to perceive and react to human emotional signals, with most studies focusing on joy and anger. In this study, we tested whether horses can learn to identify human joyful and sad expressions against other emotions. We used a touchscreen-based automated device that presented pairs of human portraits and distributed pellets when the horse touched the rewarded face. Six horses were trained to touch the sad face and 5 the joyful face. By the end of training, horses' performances at the group level were significantly higher than chance level, with higher scores for horses trained with the sad face. At the individual level, evidence of task learning varied among horses, which could be explained by individual variations in horses' ability to identify different human facial expressions or attention issues during the tests. In a generalization test, we introduced portraits of different humans than those presented during training. Horses trained with the joyful face performed better than chance, demonstrating generalization. Conversely, horses trained with the sad face did not. Horses also showed differences in learning performance according to the non-rewarded emotion, providing insights into horses' cognitive processing of facial expressions.
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Emociones , Expresión Facial , Felicidad , Caballos/psicología , Animales , Humanos , Masculino , Emociones/fisiología , Femenino , Tristeza , Aprendizaje/fisiologíaRESUMEN
Magnetic resonance imaging (MRI) is a non-invasive technique that requires the participant to be completely motionless. To date, MRI in awake and unrestrained animals has only been achieved with humans and dogs. For other species, alternative techniques such as anesthesia, restraint and/or sedation have been necessary. Anatomical and functional MRI studies with sheep have only been conducted under general anesthesia. This ensures the absence of movement and allows relatively long MRI experiments but it removes the non-invasive nature of the MRI technique (i.e., IV injections, intubation). Anesthesia can also be detrimental to health, disrupt neurovascular coupling, and does not permit the study of higher-level cognition. Here, we present a proof-of-concept that sheep can be trained to perform a series of tasks, enabling them to voluntarily participate in MRI sessions without anesthesia or restraint. We describe a step-by-step training protocol based on positive reinforcement (food and praise) that could be used as a basis for future neuroimaging research in sheep. This protocol details the two successive phases required for sheep to successfully achieve MRI acquisitions of their brain. By providing structural brain MRI images from six out of ten sheep, we demonstrate the feasibility of our training protocol. This innovative training protocol paves the way for the possibility of conducting animal welfare-friendly functional MRI studies with sheep to investigate ovine cognition.
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Encéfalo , Imagen por Resonancia Magnética , Vigilia , Imagen por Resonancia Magnética/métodos , Animales , Encéfalo/diagnóstico por imagen , Encéfalo/fisiología , Ovinos , Vigilia/fisiología , Femenino , Neuroimagen/métodos , Refuerzo en PsicologíaRESUMEN
Communication of emotions plays a key role in intraspecific social interactions and likely in interspecific interactions. Several studies have shown that animals perceive human joy and anger, but few studies have examined other human emotions, such as sadness. In this study, we conducted a cross-modal experiment, in which we showed 28 horses two soundless videos simultaneously, one showing a sad, and one a joyful human face. These were accompanied by either a sad or joyful voice. The number of horses whose first look to the video that was incongruent with the voice was longer than their first look to the congruent video was higher than chance, suggesting that horses could form cross-modal representations of human joy and sadness. Moreover, horses were more attentive to the videos of joy and looked at them for longer, more frequently, and more rapidly than the videos of sadness. Their heart rates tended to increase when they heard joy and to decrease when they heard sadness. These results show that horses are able to discriminate facial and vocal expressions of joy and sadness and may form cross-modal representations of these emotions; they also are more attracted to joyful faces than to sad faces and seem to be more aroused by a joyful voice than a sad voice. Further studies are needed to better understand how horses perceive the range of human emotions, and we propose that future experiments include neutral stimuli as well as emotions with different arousal levels but a same valence.
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Tristeza , Voz , Humanos , Caballos , Animales , Expresión Facial , Emociones/fisiología , FelicidadRESUMEN
Several studies have shown that horses have the ability to cross-modally recognize humans by associating their voice with their physical appearance. However, it remains unclear whether horses are able to differentiate humans according to different criteria, such as the fact that they are women or men. Horses might recognize some human characteristics, such as sex, and use these characteristics to classify them into different categories. The aim of this study was to explore whether domesticated horses are able to cross-modally recognize women and men according to visual and auditory cues, using a preferential looking paradigm. We simultaneously presented two videos of women and men's faces, while playing a recording of a human voice belonging to one of these two categories through a loudspeaker. The results showed that the horses looked significantly more towards the congruent video than towards the incongruent video, suggesting that they are able to associate women's voices with women's faces and men's voices with men's faces. Further investigation is necessary to determine the mechanism underlying this recognition, as it might be interesting to determine which characteristics horses use to categorize humans. These results suggest a novel perspective that could allow us to better understand how horses perceive humans.
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Voz , Masculino , Humanos , Femenino , Caballos , Animales , Señales (Psicología) , Reconocimiento en PsicologíaRESUMEN
Animals are widely believed to sense human emotions through smell. Chemoreception is the most primitive and ubiquitous sense, and brain regions responsible for processing smells are among the oldest structures in mammalian evolution. Thus, chemosignals might be involved in interspecies communication. The communication of emotions is essential for social interactions, but very few studies have clearly shown that animals can sense human emotions through smell. We used a habituation-discrimination protocol to test whether horses can discriminate between human odors produced while feeling fear vs. joy. Horses were presented with sweat odors of humans who reported feeling fear or joy while watching a horror movie or a comedy, respectively. A first odor was presented twice in successive trials (habituation), and then, the same odor and a novel odor were presented simultaneously (discrimination). The two odors were from the same human in the fear or joy condition; the experimenter and the observer were blinded to the condition. Horses sniffed the novel odor longer than the repeated odor, indicating they discriminated between human odors produced in fear and joy contexts. Moreover, differences in habituation speed and asymmetric nostril use according to odor suggest differences in the emotional processing of the two odors.
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Habituación Psicofisiológica , Odorantes , Humanos , Caballos , Animales , Olor Corporal , Miedo , Olfato , MamíferosRESUMEN
BACKGROUND: The impact of very early castration of foals has not yet been studied despite the many positive effects observed in dogs and cats. OBJECTIVES: The objective of the study was to compare castration at 3 days and 18 months and assess their subsequent morphological and behavioural development. STUDY DESIGN: This was a randomised, blinded clinical study. METHODS: Twenty-two Welsh ponies underwent either early (3-day old, EC group, n = 11) or traditional (18-month old, TC group, n = 11) castration. Animals were followed up to 3 years of age. All ponies were castrated using a primary closure technique under general anaesthesia. Weight and morphometric measurements were monitored monthly from birth until 8 months of age in both groups. Then, measurements were taken every 3 months until 2 years of age and then every 6 months until 3 years of age. Temperament tests were performed on all animals when they were 1- and 3-years old. RESULTS: No differences were observed between the EC and TC groups in terms of physical development from birth until 40 months of age or in terms of temperament and behaviour at either 1 or 3 years of age. MAIN LIMITATIONS: The study included only one breed (Welsh ponies) and only 22 animals that were castrated before 2 years of age, precluding comparison with castration performed at older ages. CONCLUSIONS: We demonstrate that early castration at 3 days does not interfere with morphological or behavioural development.
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Enfermedades de los Gatos , Enfermedades de los Perros , Enfermedades de los Caballos , Masculino , Caballos , Animales , Perros , Gatos , Orquiectomía/veterinariaRESUMEN
Recently, research on domestic mammals' sociocognitive skills toward humans has been prolific, allowing us to better understand the human-animal relationship. For example, horses have been shown to distinguish human beings on the basis of photographs and voices and to have cross-modal mental representations of individual humans and human emotions. This leads to questions such as the extent to which horses can differentiate human attributes such as age. Here, we tested whether horses discriminate human adults from children. In a cross-modal paradigm, we presented 31 female horses with two simultaneous muted videos of a child and an adult saying the same neutral sentence, accompanied by the sound of an adult's or child's voice speaking the sentence. The horses looked significantly longer at the videos that were incongruent with the heard voice than at the congruent videos. We conclude that horses can match adults' and children's faces and voices cross-modally. Moreover, their heart rates increased during children's vocalizations but not during adults'. This suggests that in addition to having mental representations of adults and children, horses have a stronger emotional response to children's voices than adults' voices.
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Emociones , Voz , Humanos , Femenino , Caballos , Animales , Audición , Sonido , Interacción Humano-Animal , MamíferosRESUMEN
Under natural conditions, foals stop nursing from their dam at approximately-9 months old, but their bond persists until 1.5-2.5â¯years of age. In contrast, in horse breeding, foals are generally artificially weaned and totally separated from their dam at 5-7â¯months. However, it is not known whether the bond between the dam and her foal is maintained after artificial weaning. The aim of this study was (1) to assess whether foals still recognise and prefer their dam over other familiar mares several months after weaning and (2) to evaluate whether the preference for the dam is more pronounced in fillies or colts. Fifteen fillies and 19 colts were weaned at the age of 7 months old (complete separation from the mother). At the age of one year (i.e., 5 months after the separation), they underwent a test evaluating their preference for their dam or a familiar mare from their natal group. Significantly more foals first approached their dam; they also sniffed and tended to look more often at her. This finding indicates that artificially weaned horses remember and still exhibit a preference for their dam, suggesting that the bond persists even after 5 months of separation. Moreover, fillies exhibited a stronger preference for both mares than colts: they looked at them more frequently, sniffed them for a longer duration and spent more time in proximity to both mares than colts. This suggests that fillies generally have an even stronger attachment to their dam as well as to other mares from their natal group. This study calls into question the practice of artificial weaning at 5-7â¯months of age.
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Destete , Animales , Femenino , Caballos , MasculinoRESUMEN
In a recent experiment, we showed that horses are sensitive to pet-directed speech (PDS), a kind of speech used to talk to companion animals that is characterized by high pitch and wide pitch variations. When talked to in PDS rather than adult-directed speech (ADS), horses reacted more favorably during grooming and in a pointing task. However, the mechanism behind their response remains unclear: does PDS draw horses' attention and arouse them, or does it make their emotional state more positive? In this study, we used an innovative paradigm in which female horses watched videos of humans speaking in PDS or ADS to better understand this phenomenon. Horses reacted differently to the videos of PDS and ADS: they were significantly more attentive and their heart rates increased significantly more during PDS than during ADS. We found no difference in the expressions of negative or positive emotional states during PDS and ADS videos. Thus, we confirm that horses' perception of humans can be studied by means of video projections, and we conclude that PDS attracts attention and has an arousing effect in horses, with consequences on the use of PDS in daily interactions with them.
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Atención , Habla , Animales , Atención/fisiología , Emociones , Femenino , Aseo Animal , Caballos , Humanos , VigiliaRESUMEN
Chronic stress and the gut microbiota appear to comprise a feed-forward loop, which contributes to the development of depressive disorders. Evidence suggests that memory can also be impaired by either chronic stress or microbiota imbalance. However, it remains to be established whether these could be a part of an integrated loop model and be responsible for memory impairments. To shed light on this, we used a two-pronged approach in Japanese quail: first stress-induced alterations in gut microbiota were characterized, then we tested whether this altered microbiota could affect brain and memory function when transferred to a germ-free host. The cecal microbiota of chronically stressed quails was found to be significantly different from that of unstressed individuals with lower α and ß diversities and increased Bacteroidetes abundance largely represented by the Alistipes genus, a well-known stress target in rodents and humans. The transfer of this altered microbiota into germ-free quails decreased their spatial and cue-based memory abilities as previously demonstrated in the stressed donors. The recipients also displayed increased anxiety-like behavior, reduced basal plasma corticosterone levels and differential gene expression in the brain. Furthermore, cecal microbiota transfer from a chronically stressed individual was sufficient to mimic the adverse impact of chronic stress on memory in recipient hosts and this action may be related to the Alistipes genus. Our results provide evidence of a feed-forward loop system linking the microbiota-gut-brain axis to stress and memory function and suggest that maintaining a healthy microbiota could help alleviate memory impairments linked to chronic stress.
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Microbioma Gastrointestinal , Microbiota , Animales , Ansiedad/metabolismo , Corticosterona , Coturnix , Trastornos de la MemoriaRESUMEN
Chronic stress profoundly affects forms of declarative memory, such as spatial memory, while it may spare non-declarative memory, such as cue-based memory. It is known, however, that the effects of chronic stress on memory systems may vary according to the level of training of an individual was submitted. Here, we investigated, in birds, how chronic stress impact spatial and cue-based memories according to training level. For that, control and chronically stressed Japanese quail were trained in a task that could be solved using spatial and cue-based memory and tested for their memory performance after 5 and 15 training days (initial training and overtraining, respectively) and following an emotional challenge (exposure to an open field). Our results showed that, compared to control quail, chronic stress impacted negatively spatial memory performances in stressed birds after initial training, but these differences were lowered after overtraining. Control birds seemed to shift from spatial to cue-based memory to solve the task across overtraining. However, an emotional challenge before testing reinstated the negative impact of chronic stress on spatial memory performances between the groups, revealing that chronic stress/overtraining did not eliminate the spatial memory and differences caused by stressors can reemerge depending on the individual's immediate psychological state. Contrary to spatial memory, cue-based memory was not affected in chronically stressed birds compared to control birds in any test occasion, confirming its resistance against the negative effects of chronic stress. Altogether these findings reveal a dynamic dialogue between stress, training level, and memory systems in birds.
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Conducta Animal/fisiología , Señales (Psicología) , Práctica Psicológica , Desempeño Psicomotor/fisiología , Memoria Espacial/fisiología , Estrés Psicológico/fisiopatología , Animales , Coturnix , MasculinoRESUMEN
Pet-directed speech (PDS) is a type of speech humans spontaneously use with their companion animals. It is very similar to speech commonly used when talking to babies. A survey on social media showed that 92.7% of the respondents used PDS with their horse, but only 44.4% thought that their horse was sensitive to it, and the others did not know or doubted its efficacy. We, therefore, decided to test the impact of PDS on two tasks. During a grooming task that consisted of the experimenter scratching the horse with their hand, the horses (n = 20) carried out significantly more mutual grooming gestures toward the experimenter, looked at the person more, and moved less when spoken to with PDS than with Adult-directed speech (ADS). During a pointing task in which the experimenter pointed at the location of a reward with their finger, horses who had been spoken to with PDS (n = 10) found the food significantly more often than chance, which was not the case when horses were spoken to with ADS (n = 10). These results thus indicate that horses, like certain non-human primates and dogs are sensitive to PDS. PDS could thus foster communication between people and horses during everyday interactions.
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Gestos , Habla , Comunicación Animal , Animales , Perros , Emociones , Aseo Animal , Caballos , HumanosRESUMEN
Recent studies have demonstrated that horses can recognize humans based simply on visual information. However, none of these studies have investigated whether this involves the recognition of the face itself, or simply identifying people from non-complex external clues, such as hair color. To go beyond this we wanted to know whether certain features of the face were indispensable for this recognition (e.g., colors, hair or eyes). The 11 horses in this study had previously learned to identify four unfamiliar faces (portrait view and in color) presented repeatedly on a screen. We thus assessed whether they were able to identify these same faces spontaneously when they were presented in four other conditions: profile view, black and white, eyes hidden, changed hairstyle. The horses' performances remained higher than chance level for all the conditions. In a choice test under real conditions, they then approached the people whose face they had learned more often than unknown people. In conclusion, when considering all the individuals studied, no single facial element that we tested appears to be essential for recognition, suggesting holistic processing in face recognition. That means horses do not base their recognition solely on an easy clue such as hair color. They can also link faces from photographs with people in real life, indicating that horses do not process images of faces as simple abstract shapes.
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Chronic stress is a strong modulator of cognitive processes, such as learning and memory. There is, however, great within-individual variation in how an animal perceives and reacts to stressors. These differences in coping with stress modulate the development of stress-induced memory alterations. The present study investigated whether and how chronic stress and individual emotionality interrelate and influence memory performances and brain neurogenesis in birds. For that, we used two lines of Japanese quail (Coturnix japonica) with divergent emotionality levels. Highly (E+) and less (E-) emotional quail were submitted to chronic unpredictable stress (CUS) for 3 weeks and trained in a spatial task and a discrimination task, a form of cue-based memory. E + and E- birds were also used to assess the impact of CUS and emotionality on neurogenesis within the hippocampus and the striatum. CUS negatively impacted spatial memory, and cell proliferation, and survival in the hippocampus. High emotionality was associated with a decreased hippocampal neurogenesis. CUS improved discrimination performances and favored the differentiation of newborn cells into mature neurons in the striatum, specifically in E+ birds. Our results provide evidence that CUS consequences on memory and neural plasticity depends both on the memory system and individual differences in behavior.
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Cuerpo Estriado/fisiología , Emociones/fisiología , Hipocampo/fisiología , Memoria/fisiología , Neurogénesis/fisiología , Estrés Psicológico/fisiopatología , Animales , Proliferación Celular/fisiología , Coturnix , Señales (Psicología) , Masculino , Aprendizaje por Laberinto/fisiología , Conducta Espacial/fisiologíaRESUMEN
Horses are capable of identifying individual conspecifics based on olfactory, auditory or visual cues. However, this raises the questions of their ability to recognize human beings and on the basis of what cues. This study investigated whether horses could differentiate between a familiar and unfamiliar human from photographs of faces. Eleven horses were trained on a discrimination task using a computer-controlled screen, on which two photographs were presented simultaneously (32 trials/session): touching one was rewarded (S+) and the other not (S-). In the training phase, the S+ faces were of four unfamiliar people which gradually became familiar over the trials. The S- faces were novel for each trial. After the training phase, the faces of the horses' keepers were presented opposite novel faces to test whether the horses could identify the former spontaneously. A reward was given whichever face was touched to avoid any possible learning effect. Horses touched the faces of keepers significantly more than chance, whether it was their current keeper or one they had not seen for six months (t = 3.65; p < 0.004 and t = 6.24; p < 0.0001). Overall, these results show that horses have advanced human face-recognition abilities and a long-term memory of those human faces.
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Conducta Animal/fisiología , Señales (Psicología) , Reconocimiento Facial/fisiología , Caballos/fisiología , Memoria/fisiología , Animales , Femenino , Humanos , Estimulación Luminosa/métodos , FotograbarRESUMEN
Animals can indirectly gather meaningful information about other individuals by eavesdropping on their third-party interactions. In particular, eavesdropping can be used to indirectly attribute a negative or positive valence to an individual and to adjust one's future behavior towards that individual. Few studies have focused on this ability in nonhuman animals, especially in nonprimate species. Here, we investigated this ability for the first time in domestic horses (Equus caballus) by projecting videos of positive and negative interactions between an unknown human experimenter (a "positive" experimenter or a "negative" experimenter) and an actor horse. The horses reacted emotionally while watching the videos, expressing behavioral (facial expressions and contact-seeking behavior) and physiological (heart rate) cues of positive emotions while watching the positive video and of negative emotions while watching the negative video. This result shows that the horses perceived the content of the videos and suggests an emotional contagion between the actor horse and the subjects. After the videos were projected, the horses took a choice test, facing the positive and negative experimenters in real life. The horses successfully used the interactions seen in the videos to discriminate between the experimenters. They touched the negative experimenter significantly more, which seems counterintuitive but can be interpreted as an appeasement attempt, based on the existing literature. This result suggests that horses can indirectly attribute a valence to a human experimenter by eavesdropping on a previous third-party interaction with a conspecific.
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Emociones , Expresión Facial , Animales , Señales (Psicología) , Caballos , HumanosRESUMEN
Over the last few years, an increasing number of studies have aimed to gain more insight into the field of animal emotions. In particular, it is of interest to determine whether animals can cross-modally categorize the emotions of others. For domestic animals that share a close relationship with humans, we might wonder whether this cross-modal recognition of emotions extends to humans, as well. In this study, we tested whether horses could recognize human emotions and attribute the emotional valence of visual (facial expression) and vocal (non-verbal vocalization) stimuli to the same perceptual category. Two animated pictures of different facial expressions (anger and joy) were simultaneously presented to the horses, while a speaker played an emotional human non-verbal vocalization matching one of the two facial expressions. Horses looked at the picture that was incongruent with the vocalization more, probably because they were intrigued by the paradoxical combination. Moreover, horses reacted in accordance with the valence of the vocalization, both behaviorally and physiologically (heart rate). These results show that horses can cross-modally recognize human emotions and react emotionally to the emotional states of humans, assessed by non-verbal vocalizations.
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Horses are mainly housed in individual boxes. This housing system is reported to be highly detrimental with regard to welfare and could trigger the expression of four behavioural indicators of a compromised welfare state: stereotypies, aggressiveness toward humans, unresponsiveness to the environment, and stress-related behaviours. The aim of this study was to identify housing and management factors that could alleviate the detrimental effects of individual boxes on welfare. A total of 187 horses were observed over 50 days by scan sampling. The impact of 12 factors was investigated on the expression of the four behavioural indicators in three different analyses. The results show that the majority of factors tested did not influence the expression of the behavioural indicators. Only three (straw bedding, a window opening onto the external environment, and a reduced quantity of concentrated feed) would have beneficial, although limited, effects. Furthermore, the longer the horses spent in individual boxes, the more likely they were to express unresponsiveness to the environment. To preserve the welfare of horses, it seems necessary to allow free exercise, interactions with conspecifics, and fibre consumption as often as possible, to ensure the satisfaction of the species' behavioural and physiological needs.
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Inferring what others witnessed provides important benefits in social contexts, but evidence remains scarce in nonhuman animals. We investigated this ability in domestic horses by testing whether they could discriminate between two experimenters who differed in what they previously witnessed and decide whom to solicit when confronted with an unreachable food source based on that information. First, horses saw food being hidden in a closed bucket (impossible for them to open) in the presence of two experimenters who behaved identically but differed in their attention to the baiting process (the "witness" experimenter faced the bucket, the "non-witness" faced away). Horses were then let free with both experimenters, and their interest towards each (gaze and touch) was measured. They gazed at and touched the witness significantly more than the non-witness (nâ¯=â¯15, gaze: pâ¯=â¯0.004; touch: pâ¯=â¯0.003). These results might suggest that horses inferred the attentional state of the experimenters during the baiting process and used this information to adapt their later behavior. Although further study would be necessary to conclude, our study provides new insight into attentional state attribution in horses and might hint to the existence of precursors of a Theory of Mind in horses.