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Baragli, P., Scopa, C., Maglieri, V., & Palagi, E. (2021). If horses had toes: demonstrating mirror self recognition at group level in Equus caballus. Anim. Cogn., .
Abstract: Mirror self-recognition (MSR), investigated in primates and recently in non-primate species, is considered a measure of self-awareness. Nowadays, the only reliable test for investigating MSR potential skills consists in the untrained response to a visual body mark detected using a reflective surface. Here, we report the first evidence of MSR at group level in horses, by facing the weaknesses of methodology present in a previous pilot study. Fourteen horses were used in a 4-phases mirror test (covered mirror, open mirror, invisible mark, visible colored mark). After engaging in a series of contingency behaviors (looking behind the mirror, peek-a-boo, head and tongue movements), our horses used the mirror surface to guide their movements towards their colored cheeks, thus showing that they can recognize themselves in a mirror. The analysis at the group level, which 'marks' a turning point in the analytical technique of MSR exploration in non-primate species, showed that horses spent a longer time in scratching their faces when marked with the visible mark compared to the non-visible mark. This finding indicates that horses did not see the non-visible mark and that they did not touch their own face guided by the tactile sensation, suggesting the presence of MSR in horses. Although a heated debate on the binary versus gradualist model in the MSR interpretation exists, recent empirical pieces of evidence, including ours, indicate that MSR is not an all-or-nothing phenomenon that appeared once in phylogeny and that a convergent evolution mechanism can be at the basis of its presence in phylogenetically distant taxa.
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Scopa, C., Greco, A., Contalbrigo, L., Fratini, E., Lanatà, A., Scilingo, E. P., et al. (2020). Inside the Interaction: Contact With Familiar Humans Modulates Heart Rate Variability in Horses. Frontiers in Veterinary Science, 7, 998.
Abstract: A human-animal relationship can be developed through subsequent interactions, affected by the positive or negative emotional valence of the proceeding one. Horses implement a process of categorization to classify humans with whom they interact as positive, negative, or neutral stimuli by evaluating the kind of approach and the nature of the contact. In these terms, human-animal interactions are emotionally charged events, eliciting specific emotional states in both subjects involved. Although the human-horse relationship has been mainly investigated through behavioral analysis, physiological indicators are needed for a more objective assessment of the emotional responses. Heart rate variability (HRV) is a commonly used autonomic nervous system (ANS) correlate estimating the sympathovagal balance as a psychophysiological marker of emotion regulation in horses. We have assumed that long-term positive relationships with humans may have a positive and immediate impact on the emotional arousal of the horse, detectable, via ANS activity, during the interaction. We analyzed horses' heartbeat dynamics during their interaction with either familiar or unfamiliar handlers, applying a standardized experimental protocol consisting of three different conditions shifting from the absence of interaction to physical contact. The ANS signals were monitored through an innovative non-invasive wearable system, not interfering with the unconscious emotional response of the animal. We demonstrated that horses appeared to feel more relaxed while physically interacting (e.g., grooming on the right side) with some familiar handlers compared to the same task performed by someone unfamiliar. The shift of the sympathovagal balance toward a vagal predominance suggests that the horses experienced a decrease in stress response as a function not only of the handler's familiarity but also of the type of interaction they are experiencing. These results constitute the objective evidence of horses' capacity to individually recognize a familiar person, adding the crucial role of familiarity with the handler as a paramount component of human-animal interaction. Our rigorous methodological approach may provide a significant contribution to various fields such as animal welfare while further investigating the emotional side of the human-animal relationships.
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Vitale, V., Balocchi, R., Varanini, M., Sgorbini, M., Macerata, A., Sighieri, C., et al. (2013). The effects of restriction of movement on the reliability of heart rate variability measurements in the horse (Equus caballus). J. Vet. Behav., 8(5), 400–403.
Abstract: Analysis of heart rate variability (HRV) is a noninvasive approach for investigating the sympathovagal balance of the autonomic nervous system. In recent years, HRV has been increasingly evaluated in animal research. In horses, it has been suggested that basal resting conditions can be achieved by restraining them. The aim of this study was to verify how restriction of movement influences HRV i2n horses. Ten healthy standardbred mares were used to measure the electrocardiographic signal under 2 conditions: free to move in the stall and restrained in the stock. Results indicate that the restriction of movement is associated with increased nervous system sympathetic activity not consistent with resting conditions.
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Guidi, A., Lanata, A., Valenza, G., Scilingo, E. P., & Baragli, P. (2017). Validation of smart textile electrodes for electrocardiogram monitoring in free-moving horses. J. Vet. Behav., 17, 19–23.
Abstract: This article focuses on the validation of smart textile electrodes used to acquire electrocardiogram (ECG) signals in horses in a comfortable and robust manner. The performance of smart textile electrodes is compared with standard Ag/AgCl electrodes in terms of the percentage of motion artifacts (MAs, the noise that results from the movement of electrodes against the skin) and signal quality. Seven healthy Standardbred mares were equipped with 2 identical electronic systems for the simultaneous collection of ECGs. One system was equipped with smart textile electrodes, whereas the second was equipped with standard Ag/AgCl electrodes. Each horse was then monitored individually in a stall for 1 hour, without any movement constraints. The ECGs were visually examined by an expert who blindly labeled the ECG segments that had been corrupted by MAs. Finally, the percentage of MAs (MA%) was computed as the number of samples of the corrupted segments over the whole length of the signal. The total MA% was found to be lower for the smart textiles than for the Ag/AgCl electrodes. Consistent results were also obtained by investigating MAs over time. These results suggest that smart textile electrodes are more reliable when recording artifact-free ECGs in horses at rest. Thus, improving the acquisition of important physiological information related to the activity of the autonomic nervous system, such as heart rate variability, could help to provide reliable information on the mood and state of arousal of horses.
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Baragli, P., Vitale, V., Paoletti, E., Mengoli, M., & Sighieri, C. (2011). Encoding the Object Position for Assessment of Short Term Spatial Memory in Horses (Equus caballus). International Journal of Comparative Psychology, 24(3).
Abstract: In this study, the detour problem was combined with the classic delayed-response task to investigate equine short-term spatial memory. Test subjects were eight female horses, divided into two groups (A and B) of four subjects each. The motivating object was made to move and disappear behind one oftwo identical obstacles in a two-point-choice apparatus. After a 10 s (Group A) or 30 s (Group B) delay the animal was released to seek the object. Both groups made more correct (14.8 ± 1.3 forGroup A and 13.5 ± 3.1 for Group B, mean ± SD) than incorrect choices (5.3 ± 1.3 for Group A and6.5 ± 3.1 for Group B, mean ± SD) and the performance of each group was significantly above chance level (z = 4.14, p = 0.000, for Group A and z = 3.02, p = 0.002, for Group B). Therefore, tested animals were able to recover the object by approaching the correct obstacle after 10 s or 30 s delays, showing that they had encoded and recovered from memory the existence of the target object and its location.
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Baragli, P., Paoletti, E., Vitale, V., & Sighieri, C. (2011). Looking in the correct location for a hidden object: brief note about the memory of donkeys (Equus asinus). Ethology Ecology & Evolution, 23(2), 187–192.
Abstract: In recent years, considerable literature has been published on cognition in horses; however, much less is known about the cognitive abilities of domestic donkey (Equus asinus). This study aimed to expand our knowledge of donkey cognition by assessing their short-term memory capacity. We employed a detour problem combined with the classic delayed-response task, which has been extensively used to compare working memory duration in a variety of different species. A two-point choice apparatus was used to investigate location recall and search behaviour for a food target, after a short delay following its disappearance. Four donkeys completed the task with a 10 sec delay, while four others were tested with a 30 sec delay. Overall, each group performed above chance level on the test, showing that subjects had successfully encoded, maintained, and retrieved the existence and location of the target despite the loss of visual contact.
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Lanata, A., Guidi, A., Valenza, G., Baragli, P., & Scilingo, E. P. (2017). The Role of Nonlinear Coupling in Human-Horse Interaction: a Preliminary Study. In 2016 38th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC).
Abstract: This study focuses on the analysis of humanhorse
dynamic interaction using cardiovascular information
exclusively. Specifically, the Information Theoretic Learning
(ITL) approach has been applied to a Human-Horse Interaction
paradigm, therefore accounting for the nonlinear information
of the heart-heart interplay between humans and horses.
Heartbeat dynamics was gathered from humans and horses
during three experimental conditions: absence of interaction,
visual-olfactory interaction, and brooming. Cross Information
Potential, Cross Correntropy, and Correntropy Coefficient were
computed to quantitatively estimate nonlinear coupling in a
group of eleven subjects and one horse. Results showed a
statistical significant difference on all of the three interaction
phases. Furthermore, a Support Vector Machine classifier
recognized the three conditions with an accuracy of 90:9%.
These preliminary and encouraging results suggest that ITL
analysis provides viable metrics for the quantitative evaluation
of human-horse interaction.
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Baragli, P., Demuru, E., Scopa, C., & Palagi, E. (2017). Are horses capable of mirror self-recognition? A pilot study. Plos One, 12(5), e0176717.
Abstract: Mirror Self-Recognition (MSR) unveils complex cognitive, social and emotional skills and it has been found only in humans and few other species, such as great apes, dolphins, elephants and magpies. In this pilot study, we tested if horses show the capacity of MSR. Four subjects living socially under naturalistic conditions were selected for the experiment. We adopted the classical mark test, which consists in placing a coloured mark on an out-of-view body part, visible only through mirror inspection. If the animal considers the image as its own, it will use its reflection to detect the mark and will try to explore it. We enhanced the classical paradigm by introducing a double-check control. Only in the presence of the reflecting surface, animals performed tactile and olfactory exploration of the mirror and looked behind it. These behaviors suggest that subjects were trying to associate multiple sensory cues (visual, tactile and olfactory) to the image in the mirror. The lack of correspondence between the collected stimuli in front of the mirror and the response to the colored mark lead us to affirm that horses are able to perceive that the reflected image is incongruent when compared with the memorized information of a real horse. However, without replication of data, the self-directed behavior towards the colored marks showed by our horses cannot be sufficient per se to affirm that horses are capable of self-recognition.
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Baragli, P., Demuru, E., & Palagi, E. (2015). Mirror on the wall, who is the horsest of our all? Self-recognition in Equus caballus. In Proceedings of the 3. International Equine Science Meeting.
Abstract: Mirror Self-Recognition (MSR) is an extremely rare capacity in the animal kingdom that reveals the emergence of complex cognitive capacities (de Waal 2008). So far, MSR has been reported only in humans, chimpanzees (Gallup, 1970), bottlenose dolphins (Reiss and Marino, 2001) and Asian elephants (Plotnik et al, 2006), all species characterized by a highly developed cognition. There is growing evidence that domestic horses posses high cognitive abilities, such as cross-modal individual recognition (Proops et al, 2009), triadic post-conflict reunion to maintain social homeostasis (Cozzi et al, 2010), complex communicative systems (Whatan and McComb, 2014), flexibility in problem-solving (Lovrovich et al, 2015), and long-term memory (Hanggi and Ingersoll, 2009). All these capacities make horses a good candidate to test the ability of MSR in a domestic species. Through a classical MSR experimental paradigm (de Waal 2008) we tested eight horses living in social groups under semi-natural conditions (from the Italian Horse Protection rescue centre). Animals showing MSR typically go through four stages (Plotnik et al, 2006): (i) social response, (ii) physical mirror inspection (e.g., looking behind the mirror), (iii) repetitive mirror-testing behaviour (i.e., the beginning of mirror understanding), and (iv) self-directed behaviour (i.e., recognition of the mirror image as self). The final stage, known as the “mark-test”, is verified when a subject spontaneously uses the mirror to check for a coloured artificial mark on its own body which it cannot perceive otherwise. The horses underwent a three-phase “mark-test”: 1) with sham mark (transparent ultrasound water gel) positioned on both side at jaw level, 2) mark (yellow eye shadow mixed with ultrasound water gel) positioned on left side of jaw (with sham mark on the right), 3) mark (yellow eye shadow mixed with ultrasound water gel) positioned on right side of jaw (with sham mark on the left)
The mirror was one 0.5-cm-thick piece of 140x220-cm plexiglass glue on wood. Each test lasted one hour, horses were tested once a day, in consecutive days and at the same time. Our preliminary result on 1 horse shows some changes in self-directed behaviours which can be attributed to presence of the coloured mark. Firstly, the presence of the coloured mark significantly increased the frequency of scratching on both sides of the muzzle (p < 0.0001). The most intriguing result (p < 0.0001) comes from the comparison of the scratching rates directed towards the coloured mark side (N = 41) and the sham mark side (N = 23). Under the control condition (i.e. sham mark on both sides) no statistical difference was found for the scratching rates directed to the muzzle sides (dx N = 8; sx N = 5). Although further analyses are needed to confirm these preliminary results, our finding opens new scenarios about the evolution of Mirror Self-Recognition. The capacity of horses to recognize themselves in a mirror may be the outcome of an evolutionary convergence process driven by the cognitive pressures imposed by a complex social system and maintained despite thousands years of domestication.
Keywords:
Domestic horse · Mark test · Socio-cognitive skills · Self-awareness
References
De Waal FBM (2008) The thief in the mirror. PloS Biol 6(8):e201
Gallup GG Jr (1970) Chimpanzees: Self-recognition. Science 167: 86-87.
Reiss D, Marino L (2001). Mirror self-recognition in the bottlenose dolphin: A case of cognitive convergence. Proc Natl Acad Sci U S A 98:5937-5942.
Plotnik J, de Waal FBM, Reiss D (2006) Self-recognition in an Asian elephant. Proc Natl Acad Sci U S A 103: 17053-17057.
Proops L, McComb K, Reby D. (2009) Cross-modal individual recognition in domestic horses (Equus caballus). Proc Nat Acad Sci USA;106:947-951.
Cozzi A, Sighieri C, Gazzano A, Nicol CJ, Baragli P. Post-conflict friendly reunion in a permanent group of horses (Equus caballus). Behav Process 2010;85:185-190.
Wathan J, McComb K. The eyes and ears are visual indicators of attention in domestic horses. Curr Biol 2014;24(15): R677-R679.
Lovrovich P, Sighieri C, Baragli P (2015) Following human-given cues or not? Horses (Equus caballus) get smarter and change strategy in a delayed three choice task. Appl Anim Behav Sci, in press.
Hanggi EB, Ingersoll JF. (2009) Long-term memory for categories and concepts in horses (Equus caballus). Anim Cogn; 12:451-462.
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Lovrovich, P., Sighieri, C., & Baragli, P. (2015). Following human-given cues or not? Horses (Equus caballus) get smarter and change strategy in a delayed three choice task. Appl. Anim. Behav. Sci., 166, 80–88.
Abstract: Highlights
�Horses remember the location of food hidden by the experimenter after a delay.
�They understand the communicative meaning of a human positioned close to the target.
�The same horses are capable of changing their decision-making strategy.
�They are able to shift from accuracy inferred from human given cues to speed.
�Horses can use human cues or not depending on time, cost, experience and reward.
Abstract
To date, horses have seemed capable of using human local enhancement cues only when the experimenter remains close to the reward, since they fail to understand the communicative meaning of the human as momentary local enhancement cue (when the human is not present at the moment of the animal's choice). This study was designed to analyse the ability of horses to understand, remember and use human-given cues in a delayed (10 s) three-choice task. Twelve horses (experimental group) had to find a piece of carrot hidden under one of three overturned buckets after seeing the experimenter hide it. The results were then compared with those of a control group (twelve horses) that had to find the carrot using only the sense of smell or random attempts. At the beginning, the experimental horses made more correct choices at the first attempt, although they took more time to find the carrot. Later the same horses were less accurate but found the carrot in less time. This suggests that the value of the proximal momentary local enhancement cues became less critical. It seemed, in fact, that the experimental and control group had aligned their behaviour as the trials proceeded. Despite this similarity, in the second half of the trials, the experimental group tended to first approach the bucket where they had found the carrot in the immediately preceding trial. Our findings indicate that horses are capable of remembering the location of food hidden by the experimenter after a delay, by using the human positioned close to the target as valuable information. The same horses are also capable of changing their decision-making strategy by shifting from the accuracy inferred from human given cues to speed. Therefore, horses are able to decide whether or not to use human given-cues, depending on a speed-accuracy trade-off.
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