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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 diferently to the videos of PDS and ADS: they were signifcantly more attentive and their heart rates increased signifcantly more during PDS than during ADS. We found no diference in the expressions of negative or positive emotional states during PDS and ADS videos. Thus, we confrm that horses’ perception of humans can be studied by means of video projections, and we conclude that PDS attracts attention and has an arousing efect in horses, with consequences on the use of PDS in daily interactions with them.
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Pet‑directed speech improves
horses’ attention toward humans
Plotine Jardat 1*, Ludovic Calandreau1, Vitor Ferreira1,2, Chloé Gouyet1, Céline Parias1,
Fabrice Reigner3 & Léa Lansade 1*
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 dierently
to the videos of PDS and ADS: they were signicantly more attentive and their heart rates increased
signicantly more during PDS than during ADS. We found no dierence in the expressions of negative
or positive emotional states during PDS and ADS videos. Thus, we conrm that horses’ perception of
humans can be studied by means of video projections, and we conclude that PDS attracts attention
and has an arousing eect in horses, with consequences on the use of PDS in daily interactions with
them.
In the past 20years, an increasing number of studies have explored the cognitive abilities of domestic mammals
toward humans, bringing to light sometimes unexpected sociocognitive skills1. For example, sheep recognize
individual human faces2, goats know when humans are attentive to them3, and dogs and cats recognize and
react to our emotions46. ese ndings enable us to improve human-animal interactions and animal welfare,
as we better understand how our actions and emotions aect domestic mammals. Horses also have excellent
sociocognitive skills toward humans. ey recognize our emotions through vocalizations, facial expressions and
odors711, they know whether we are attentive to them12 and what the intentions of our gestures are13. is may be
linked to proximity to humans since their domestication approximately 5500years ago14 and to the importance
of social interactions in this species15.
Horses are also sensitive to the way we talk to them, especially to a kind of speech used to speak to compan-
ion animals, called pet-directed speech (PDS). PDS resembles the type of speech used with infants (“baby-talk”,
“parentese” or “infant-directed speech”—IDS)16 and has similar characteristics, namely, a high and varying
pitch, wide pitch range, slow rate of speech, simple syntax and semantics and more repeated words, compared
to adult-directed speech (ADS)1621. Moreover, IDS is an emotional form of speech and a multimodal commu-
nication style16, which includes visual modalities such as facial expressions, particularly smiles. IDS and PDS
eects have been extensively studied in human infants and other animal species, such as primates and dogs. In
human infants, IDS is preferred to ADS22; it has an arousing eect and facilitates social interactions16. Infants
emotions are inuenced by IDS, with 5-month-old infants smiling more in response to approval expressed in
IDS than ADS23. In infant rhesus macaques, IDS has been shown to inuence long-term memory24. Moreover,
dogs looked longer at and preferred to spend time close to a loudspeaker or person broadcasting PDS rather
than ADS17,18, and they were more attentive when spoken to in PDS rather than ADS19. In horses, we showed in
a recent experiment that PDS induced a dierent way of interacting with an experimenter compared to ADS.
While being scratched on the withers, horses moved less, made more grooming attempts (i.e., mouth gestures
equivalent to those made when grooming a conspecic), and looked more at the experimenter when they talked
in PDS rather than ADS. Furthermore, in a pointing task in which the horses had to nd the location of a food
reward from cues given by the experimenter, horses that were talked to in PDS performed better than horses
that were talked to in ADS21.
In connection with the observations made in other species, we proposed several hypotheses to explain this
reaction of horses to PDS. First, PDS could attract horses’ attention and arouse them. Indeed, IDS is arousing
for infants16,25, and PDS attracts attention in dogs1719. is hypothesis could explain why horses looked more
OPEN
1CNRS, IFCE, INRAE, University of Tours, PRC, 37380 Nouzilly, France. 2Department of Physics, Chemistry and
Biology, IFM Biology, Linköping University, 581 83 15 Linköping, Sweden. 3UEPAO, INRAE, 37380 Nouzilly,
France. *email: plotine.jardat@gmail.com; lea.lansade@inrae.fr
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at the experimenter during grooming and their better performance in nding hidden food due to greater atten-
tion given to experimenter cues. Second, PDS could inuence the valence of emotions felt by horses. Indeed,
the positive emotions expressed through PDS could make horses react positively to this type of speech. In fact,
horses have been observed to relax in response to joyful intonations of humans10,11, and PDS could have similar
consequences, in the same way that IDS is known to trigger positive emotions in infants16,23. Moreover, in dogs
and infants, the preference for IDS or PDS over ADS also suggests a more positive emotional experience in
response to the former. us, in our rst study on PDS in horses, a more positive emotional state, linked to the
positive emotional charge of PDS, could have lead horses to make more grooming attempts (as in26). In addition,
it could have helped them follow the experimenter’s indications when pointing toward the food reward due to
the better cognitive performance that results from a more positive emotional state27,28.
e aim of this study was to determine whether horses would have dierent behavioral and physiological reac-
tions when presented with lms of humans speaking in PDS or ADS and to explore two nonexclusive hypotheses,
H1 and H2, that can explain horses’ sensitivity to PDS:
H1: PDS helps to attract horses’ attention and has an arousing eect on them.
H2: PDS inuences the valence of emotions felt by horses, making them more positive.
We used an innovative paradigm in which horses watched videos of humans that had been previously lmed
in the laboratory. Horses are known to react to projected lms of humans or conspecics, with an inuence
on their emotional state and behavior11,29. We showed 28 horses two-minute-long lms composed of four 30-s
sections, each consisting of a woman saying the same sentence four times in either PDS or ADS. To test our two
hypotheses, the propensity to be more attentive to PDS than ADS, relative to the total time spent being attentive
to the screen (hereaer called the attention index) was registered, and behavioral indicators of emotional valence
were observed. e time spent in an alert posture and signs of fear (number of defecations, number of times the
white of the eye was visible—called shows of sclera, number of neighs)30,31, which reect a negative emotional
state, were recorded. e time spent in a relaxed posture and the number of snorts32, which reect a positive
emotional state, were also quantied. e horses’ heart rates were also recorded as a possible marker of either
emotional valence8,11 or arousal33,34 (the two axes of the dimensional approach of emotional states in animals35,
where valence describes the variation between positive and negative experiences and arousal is dened as the
degree of “bodily activation, e.g. calm versus excited33,35).
According to H1, we expected horses to be attentive for a longer period of time during PDS than during ADS,
with a possible greater increase in heart rate during PDS due to increased arousal. According to H2, we expected
horses to show more signs of a positive emotional state (relaxed posture, snorts) during PDS than during ADS,
with a possible greater decrease in heart rate and fewer behavioral signs of a negative emotional state (e.g., alert
postures, neighs, defecations, shows of sclera) during the former.
Results
e attention index (measuring the propensity to be more attentive to PDS than ADS) was signicantly greater
than 0 (one-tailed Wilcoxon test, N = 28, V = 288, P = 0.027, Fig.1a), indicating that the horses were more atten-
tive to the videos when the human was speaking in PDS rather than ADS, relative to the total time spent being
attentive to the screen.
e time spent in an alert posture was not lower during PDS sections than during ADS sections (one-tailed
paired Wilcoxon test, N = 28, U = 61, P = 0.952; Fig.1b), and the time spent in a relaxed posture was not higher
during PDS sections than during ADS sections (one-tailed paired Wilcoxon test, N = 28, U = 175, P = 0.632;
Fig.1c). e proportions of horses that defecated, neighed and showed the sclera at least once during PDS were
not lower than those during ADS (one-tailed Z tests, P = 28, defecations: PDS 1/28, ADS 2/28, Z = 0.593, P = 0.500;
neighs: PDS 2/28, ADS 4/28, Z = 0.864, P = 0.333; shows of sclera: PDS 5/28, ADS 7/28, Z = 0.651, P = 0.372).
Furthermore, we did not observe any snorts during the tests.
e mean dierence in heart rate between the end and the beginning of the sections was signicantly higher
for PDS than ADS (two-tailed paired Wilcoxon test, N = 28, V = 96, P = 0.014, Fig.1d), and this variation was
dierent from 0 during both PDS and ADS sections (two-tailed Wilcoxon tests, N = 28; PDS: V = 294, P = 0.038;
ADS: V = 87, P = 0.007), indicating that horses’ heart rate increased during the PDS lm sections and decreased
during the ADS lm sections.
Discussion
In this experiment, horses had dierent behavioral and physiological reactions when presented with lms of
humans speaking in PDS or ADS. Horses were more attentive to PDS videos than ADS videos, and their heart
rates increased more during PDS than during ADS; however, they did not show fewer signs of a negative emo-
tional state or more signs of a positive emotional state during PDS than during ADS.
In line with other studies11,29, our results conrm that broadcasting preregistered videos is a valid methodol-
ogy to investigate horses’ perception of humans. A two-dimensional image accompanied by sound is sucient
to make horses react behaviorally and physiologically, with reactions comparable to those observed in response
to real-life corresponding stimuli (for example, in this study, the horses were more attentive during PDS, a
behavior comparable to the higher number of looks toward the experimenter during grooming accompanied
by PDS in our previous study21). Moreover, this method has the advantage of allowing the presentation to all the
animals of the same standardized stimuli of humans who are blind to the reactions of the subject. In addition,
compared to the broadcasting of sound alone, video projection enables the inclusion of facial expressions, an
intrinsic component of PDS16.
e main result of this study is that horses were more attentive when addressed via PDS than ADS, which
enables us to conclude that PDS can indeed attract horses’ attention. In addition, the heart rate of horses increased
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Figure1. Horses’ behavior and heart rate variations during PDS and ADS. Boxplots showing median, rst
and third quartiles;. Grey dot: individual results (N = 28); Red Plus symbol: mean. Wilcoxon tests, NS not
signicant. (a) Attention index: (APDS-AADS)/(APDS + AADS) with APDS the time spent being attentive to the screen
during PDS sections, and AADS during ADS sections. (b) Time spent in an alert posture when ADS or PDS was
projected (s). (c) Time spent in a relaxed posture when ADS or PDS was projected (s). (d) Mean dierence in
heart rate between the last ve and the rst ve seconds of the sections when ADS or PDS was projected (bpm).
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more during PDS than during ADS. In mammals, heart rate can uctuate with arousal state (in both positive33,34,36
and negative30,31,37 situations), suggesting that horses in the present study were more aroused during PDS than
ADS. us, PDS has an arousing eect on horses in addition to attracting their attention, as proposed in H1.
In the second hypothesis (H2, which does not exclude H1), we asked whether PDS inuences the valence
of emotions felt by horses. Our results show that the horses were not in a more positive or less negative emo-
tional state during PDS than during ADS. e time spent in a relaxed posture was not longer during PDS than
during ADS, and no snorts (an indicator of positive emotional state32) were observed during either PDS or
ADS. Moreover, the horses were not less alert and did not defecate, neigh or show the sclera less during PDS
than during ADS. us, we do not have sucient evidence to accept H2 and conclude that PDS inuences the
valence of emotions felt by horses and makes them more positive. However, in horses, contrary to other species
such as dogs in which a high or wagging tail indicates condence or friendliness38, few indicators of a positive
emotional state, other than a relaxed posture, snorts, or a facial expression described during the specic context
of grooming26,29,32, have been characterized, to our knowledge. Consequently, data are not in favor of H2; and
more observable behavioral indicators of positive emotional states are needed to investigate this question further.
Moreover, the tested horses expressed low levels of fear or stress, making it dicult to demonstrate a change
toward a less negative emotional state due to a possible oor eect.
Several explanations can be proposed to interpret horses’ increased attention and arousal in response to PDS
(H1). First, this eect could be due to the acoustic characteristics of PDS. Acoustic characteristics such as the
mean pitch, pitch variation, pitch range and rate of speech, can be referred to as prosody, while the type of words
used and their degree of repetition, along with syntax and semantics, can be referred to as content. In dogs, both
prosody and content are important factors in the preference for PDS over ADS. Indeed, this preference is only
revealed when the stimuli combine both factors as opposed to stimuli made either of PDS content spoken in
ADS prosody or ADS content spoken in PDS prosody17. In our study, the same sentence was used for the PDS
and ADS stimuli, so the content was stable but the prosody varied. It is possible that the dierences in prosody,
namely, a higher pitch and wider pitch range, could be more stimulating for horses than a more monotonous
voice (ADS), similar to the suggested arousing eect of high pitch frequency and variation in infants16. In addi-
tion, in the present study, the attention of horses was drawn more eciently by PDS, showing that in horses, for
constant content, a dierent prosody is sucient to promote greater attention (similar to the study by Jeannin
etal.19 in dogs). It would be interesting to present horses with stimuli of stable prosody with a variation in content
to determine if PDS content could also draw attention in this species.
Second, we can wonder whether the attention of horses was drawn more eciently by PDS because this type
of language enables them to better perceive our intention to communicate. Horses are known to perceive human
intentions13. Indeed, in a protocol similar to those classically used in primates (“unwilling versus unable” para-
digm)39, horses behaved dierently toward an experimenter when the latter was able but unwilling to give a treat
than when she was unable to do so (because the experimenter dropped the treat or a physical barrier prevented
it)13. IDS is known to communicate parents’ intentions, and in infants, it is thought to work as an ostensive cue,
alerting the child that communication is intended for them16. Dogs and cats have been shown to respond to
ostensive cues as well4042. erefore, it is possible that horses could be sensitive to ostensive cues and that PDS
could play this role. Hence, in this study, the greater attention and arousal of horses in response to PDS could
be explained by improved perception of the lmed women’s intention to interact due to this type of speech.
A third possibility is that horses’ attention and arousal were increased in response to PDS due to the emotions
conveyed by this type of speech. IDS is emotionally charged16, and in our study, the stimuli included emotional
indicators such as facial expressions (for example, smiles during PDS and more neutral expressions during ADS).
Horses are known to recognize positive human emotions, particularly joyful facial expressions and voices, in
lms11, and they react to face pictures of dierent human emotions43. erefore, in this study, the perception of
the positive emotional charge of PDS could have attracted the horses’ attention and aroused them.
us, the arousing and attention-attracting eect of PDS could be explained by the acoustic characteristics
of PDS, better communication of intentions through this type of speech or attraction to the positive emotional
charge of PDS. ese three mechanisms could also be concomitant and function in a loop, with horses’ attention
being drawn in response to acoustic stimulation, which would lead them to perceive our emotions and com-
municative intention and, in turn, increase their attention and arousal.
Conclusion
In this study, we used an innovative setup in which horses watched and reacted to videos of women speaking in
PDS or ADS. e results conrm horses’ sensitivity to PDS21 and provide some explanation of the mechanisms
behind this phenomenon. We could not conrm that PDS inuences the valence of emotions felt by horses, but
it could be the case in other contexts (e.g., less pleasant situations). We showed that horses’ attention is drawn
by PDS more than it is by ADS and that horses appear to be aroused by PDS. is nding could be helpful for
horsemen and horsewomen, who could use this type of speech to attract horses’ attention and arouse them.
Methods
Ethics statement. Our experiment received a positive recommendation and was approved by the Val de
Loire Ethical Committee (CEEA VdL, Nouzilly, France, authorization number CE19—2021-1101-1). Animal
care and experimental treatments complied with the French and European guidelines for the housing and care of
animals used for scientic purposes (European Union Directive 2010/63/EU) and were performed under author-
ization and supervision of ocial veterinary services (agreement number F371752 delivered to the UEPAO ani-
mal facility by the veterinary service of the Département d’Indre et Loire, France). e animals lived in groups,
they were not food deprived during the experiment and did not undergo any invasive procedures. However, if a
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horse was too agitated during the test due to separation from its conspecics or if it reacted too strongly to the
videos (moved backward, turned around and tried to escape), it was removed from the experiment.
All methods were performed in accordance with relevant guidelines and regulations for direct human involve-
ment in the study. All the people participating in the study provided their informed consent.
Subjects. e study initially involved 32 Welsh mares aged 8.9 ± 2.4years (mean ± sd) reared at the Ani-
mal Physiology Experimental Unit PAO (UEPAO, https:// doi. org/ 10. 15454/1. 55738 963217 28955E12), INRAE.
e horses lived in groups in an indoor stall on straw with free access to an outdoor area and environmental
enrichments. Fresh straw was added daily and the stalls were cleaned extensively every one to three weeks. e
horses had free access to an outdoor paddock. Hay and water were available adlibitum. e whole protocol was
successfully implemented with 28 of these animals, which were considered in the nal statistical analysis (see
Habituation” and “Test” sections).
Stimuli. e stimuli consisted of 2-min-long lms composed of four 30-s sections. Each section consisted
of one of four women speaking the same sentence four times in either PDS or ADS (Table1). In each lm,
two women spoke in PDS and two others spoke in ADS. e order in which the types of speech appeared was
counterbalanced between the lms. e order in which the women appeared in the videos was counterbalanced
between horses. e type of speech (ADS or PDS) used by each woman in front of the horses was also counter-
balanced between horses (half of the horses saw two women speak in PDS and the other two women speak in
ADS, and vice versa for the other half).
e lms were recorded at the INRAE PRC lab. e four women were volunteers unknown to the horses.
ey were lmed saying the sentence « Oui mon beau, cest bien tu écoutes très bien. Allez ma lle, tu viens,
on y va, tu es la plus belle» (meaning «Yes my beauty, that’s good you’re listening very well. Come on girl, let’s
go, you’re the most pretty »), made of phrases they were likely to hear in their everyday life. ey were asked to
speak it either with a neutral tone (ADS) or with a tone that they would use in front of a baby or cute juvenile
animal (PDS), with the appropriate facial expressions for the type of speech used (smiling for PDS and neutral
for ADS—see Supplementary Fig.S1). In the end, we obtained eight sequences of the same content that diered
in prosody (four sequences of ADS and four of PDS). e sound amplitude was normalized so that the sound
level would be between 65 et 75dB from where the head of the horse stood for each sequence. e vocalizations
were analyzed using Praat V6.1.16 (Supplementary Fig.S1). e mean pitch and pitch range were calculated
for each woman. ese analyses showed that the mean pitch was higher and the pitch range was wider in the
PDS than in the ADS condition (mean pitch (Hz) PDS: 325[308;340], ADS: 239[217;254]; pitch range (Hz)
PDS: 405[387;408], ADS: 168[129;211]). A high pitch and wide pitch range are two characteristics of PDS1621.
Experimental set‑up. e experiment was performed in a large stall (3.5 × 4.5m). e lms were projected
on a white 2 × 2.5m screen, so that the projected faces were approximately the size of a real person’s face (Fig.2).
e sound was broadcast by a speaker placed above the screen (approximately 70dB, from where the head of
the horse was located). For safety reasons, an assistant stayed with the horse (to ensure that it did not panic or
get entangled in the ropes) but never interacted with the horse during the tests, remaining still and looking nei-
ther at the screen nor the horse, with the head down. e horses were free to look at the screen or not. Whether
the assistant was standing on the le or the right of the horse was counterbalanced between the horses and
the conditions. e experiment was lmed by two cameras in front of the horse (Fig.2). An overview camera
allowed the experimenter to follow the running of the experiment from outside the stall and control the projec-
tion accordingly. e horses were equipped with a heart monitor system composed of an external captor and a
watch giving real-time values of heart rate and recording these values (Polar Equine RS800CX Science, Polar Oy,
Finland). e external captor was composed of two electrodes placed on the withers and behind the front leg on
the le, aer clipping the hair and applying some ultrasound gel. e recordings started just before the start of
the habituation phase, a signal was given to the camera at that moment to allow for synchronisation between the
records and the proceedings of the test.
Schedule. e experimental sessions were performed in the aernoon. On day 1, each horse went through
a habituation session. If the habituation criterion was met (see below), the horse proceeded to the test session
immediately on the same day; otherwise, a new habituation session with the same criterion was scheduled for the
following day. All but one horses met the criterion on day 1 and proceeded to the test session on the same day.
One horse did not reach the criterion on day 1 or day 2 and was excluded from the experiment.
Table 1. Example composition of a stimulus lm. A lm lasted two minutes and was divided in four sections.
During each section a same sentence was repeated four times. e orders of the types of speech, along with
which type of speech each woman was using for each horse, were counterbalanced.
Section 1 2 3 4
Wom an A B C D
Type of speech ADS PDS ADS PDS
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Habituation. e horse was led to the middle of the stall facing the screen. Two loose ropes were attached,
the assistant took his place, and the habituation phase began. Scenes of nature accompanied by bird songs were
projected while the assistant monitored the horse’s heart rate on the Polar watch. In this phase, the assistant
could reposition the horse if it was facing the door opposite the screen. Once the horse was calm (not neighing,
pulling on the ropes with his head, nor trying to turn around or leave) and its heart rate had remained below
100bpm for two consecutive minutes, the test phase began immediately. If this criterion was not met aer ve
minutes, the session ended, and a new session was scheduled for the following day.
Test. Immediately aer the horse met the criterion, a lm presenting the four women speaking in PDS and
ADS (see “Stimuli” section above) was projected. e conditions were the same as during habituation, but the
assistant did not intervene, unless the horse’s level of stress was too high. is occurred three times, and the
horses in question had to be excluded from the study (one horse behaved dangerously and two were agitated and
tried to escape). At the end of the test, the horse was led directly back to its stall.
Behavioral and physiological analysis. Videos of the tests were watched on a standard media player
(http:// www. video lan. org/) by the same coder without sound, so that the coder was blind to the condition (the
screen was not visible in the videos). e start and end times or times of occurrence of the behaviors were noted.
e time the horse spent being attentive to the lm (facing the screen with both ears oriented forward) was
quantied. Signs of negative emotions were also recorded: defecations, the number of times the white of an eye
was visible (shows of sclera), and neighs (based on a second viewing with the sound on) were counted, and the
time the horse spent in an alert posture (neck held high with both ears oriented forward, regardless of the gaze
direction) was quantied. Signs of positive emotions were also recorded: the time the horse spent in a relaxed
posture (neck held low or medium, eyes weakly or moderately open, regardless of the gaze direction) was quan-
tied, and the number of snorts (dened as a voluntary expulsion of air through the nostrils that make them
vibrate and results in a pulsed sound32) was counted. A second coder reanalyzed 20% of the videos to assess the
interobserver reliability of the times spent being attentive to the video, in a relaxed posture or in an alert posture.
Interclass Correlation Coecients (ICC) were calculated, showing good to excellent reliabilities for the three
variables44 (ICC estimates and 95% condence intervals: time spent being attentive to the screen 0.93[0.85,0.97],
time spent in a relaxed posture 0.93[0.84,0.97], time spent in an alert posture 0.94[0.87,0.97]).
e time spent being attentive to the screen was highly variable between horses (from 6 to 80s over the
120-s test). To take this variation into account, for each horse, we calculated an attention index measuring the
propensity to be more attentive to PDS than ADS relative to the total time spent being attentive to the screen.
is index was dened as (APDS-AADS)/(APDS + AADS), where APDS is the time spent being attentive to the screen
during PDS sections and AADS is the time spent being attentive during ADS sections (see4). is index varied
from -1 to 1, with a negative value indicating that a horse was more attentive during ADS than PDS, and a posi-
tive value indicating the opposite.
Heart rate data were extracted from the Polar recordings. A visual correction was applied to eliminate arti-
factual beats (as recommended in45). e dierence in heart rate (beats per minute—bpm) between the last ve
and rst ve seconds of each section was calculated. en, for each horse, the mean of this dierence over the
two sections of each type (PDS or ADS) was calculated.
Figure2. Schematic representation of the experimental setup.
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www.nature.com/scientificreports/
Statistical analyses. Due to the exclusion of one horse during habituation and three horses during the
tests, the statistical analysis considered 28 animals. All statistical analyses were performed using R 4.0.3 (R Core
Team, 2013). Due to the small sample size (N = 28), nonparametric tests were used. e signicance threshold
was xed at α = 0.05.
To test whether the attention index was greater than 0 (H1), which would indicate that the horses spent a
longer period of time being attentive to the screen during PDS than during ADS sections, we used a one-tailed
paired Wilcoxon test. To test whether the horses spent more time in a relaxed posture and less time in an alert
posture during PDS than during ADS (H2), we used one-tailed paired Wilcoxon tests. Defecations, neighs
and shows of the sclera were expressed by less than 30% of the horses, so the corresponding observations were
transformed into binary data. We used one-tailed Z tests to determine whether the proportions of horses that
expressed each of these behaviors during PDS were smaller than those during ADS (H2). Finally, we tested
whether the mean dierence in heart rate over PDS sections was greater (H1) or smaller (H2) than that over
ADS sections using a two-tailed paired Wilcoxon test, and we tested whether the heart rate variation of horses
over each type of section was dierent from 0 using two two-tailed Wilcoxon tests.
Ethical approval. is study was reported in accordance with ARRIVE guidelines.
Data availability
e datasets generated and analyzed during the current study are available in the INRAE data repository from
the following link: https:// doi. org/ 10. 15454/ T9DW8Y.
Received: 4 October 2021; Accepted: 17 February 2022
References
1. Jardat, P. & Lansade, L. Cognition and the human–animal relationship: a review of the sociocognitive skills of domestic mammals
toward humans. Anim. Cogn. https:// doi. org/ 10. 1007/ s10071- 021- 01557-6 (2021).
2. Knolle, F., Goncalves, R. P. & Jennifer Morton, A. Sheep recognize familiar and unfamiliar human faces from two-dimensional
images. R. Soc. Open Sci. 4, 171228 (2017).
3. Nawroth, C. & McElligott, A. G. Human head orientation and eye visibility as indicators of attention for goats (Capra hircus). PeerJ
5, e3073 (2017).
4. Albuquerque, N. et al. Dogs recognize dog and human emotions. Biol. Lett. 12, 20150883 (2016).
5. Albuquerque, N., Guo, K., Wilkinson, A., Resende, B. & Mills, D. S. Mouth-licking by dogs as a response to emotional stimuli.
Behav. Processes 146, 42–45 (2018).
6. Quaranta, A., D’ingeo, S., Amoruso, R. & Siniscalchi, M. Emotion recognition in cats. Animals 10, 1107 (2020).
7. Sabiniewicz, A., Tarnowska, K., Świątek, R., Sorokowski, P. & Laska, M. Olfactory-based interspecic recognition of human emo-
tions: Horses (Equus ferus caballus) can recognize fear and happiness body odour from humans (Homo sapiens). Appl. Anim.
Behav. Sci. 230, 105072 (2020).
8. Smith, A. V., Proops, L., Grounds, K., Wathan, J. & McComb, K. Functionally relevant responses to human facial expressions of
emotion in the domestic horse (Equus caballus). Biol. Lett. 12, 20150907 (2016).
9. Smith, A. V. et al. Domestic horses (Equus caballus) discriminate between negative and positive human nonverbal vocalisations.
Sci. Rep. 8, 13052 (2018).
10. Nakamura, K., Takimoto-Inose, A. & Hasegawa, T. Cross-modal perception of human emotion in domestic horses (Equus cabal-
lus). Sci. Rep. 8, 8660 (2018).
11. Trösch, M. et al. Horses categorize human emotions cross-modally based on facial expression and non-verbal vocalizations. Animals
9, 862 (2019).
12. Sankey, C., Henry, S., André, N., Richard-Yris, M. A. & Hausberger, M. Do horses have a concept of person? PLoS One 6, e18331
(2011).
13. Trösch, M., Bertin, E., Calandreau, L., Nowak, R. & Lansade, L. Unwilling or willing but unable: can horses interpret human actions
as goal directed?. Anim. Cogn. 23, 1035–1040 (2020).
14. Warmuth, V. et al. Reconstructing the origin and spread of horse domestication in the Eurasian steppe. Proc. Natl. Acad. Sci. 109,
8202–8206 (2012).
15. VanDierendonck, M. C. & Goodwin, D. Social contact in horses: implications for human-horse interactions. in e human-animal
relationship. Forever and a day (eds. de Jonge, F. H. & van den Bos, R.) 65–81 (Royal van Gorcum, 2005).
16. Saint-Georges, C. et al. Motherese in Interaction: At the Cross-Road of Emotion and Cognition? (A Systematic Review). PLoS
ONE 8, 78103 (2013).
17. Benjamin, A. & Slocombe, K. ‘Who’s a good boy?!’ Dogs prefer naturalistic dog-directed speech. Anim. Cogn. 21, 353–364 (2018).
18. Ben-Aderet, T., Gallego-Abenza, M., Reby, D. & Mathevon, N. Dog-directed speech: Why do we use it and do dogs pay attention
to it?. Proc. R. Soc. B Biol. Sci. 284, 20162429 (2017).
19. Jeannin, S., Gilbert, C., Amy, M. & Leboucher, G. Pet-directed speech draws adult dogs’ attention more eciently than Adult-
directed speech. Sci. Rep. 7, 4980 (2017).
20. Lesch, R. et al. Talking to dogs: Companion animal-directed speech in a stress test. Animals 9, 417 (2019).
21. Lansade, L. et al. Horses are sensitive to baby talk : Pet-directed speech facilitates communication with humans in a pointing task
and during grooming. Anim. Cogn. 5, 999–1006 (2021).
22. Schachner, A. & Hannon, E. E. Infant-Directed Speech Drives Social Preferences in 5-Month-Old Infants. Dev. Psychol. 47, 19–25
(2011).
23. Fernald, A. Approval and Disapproval: Infant Responsiveness to Vocal Aect in Familiar and Unfamiliar Languages. Child Dev.
64, 657–674 (1993).
24. Slonecker, E. M., Simpson, E. A., Suomi, S. J. & Paukner, A. Who’s my little monkey? Eects of infant-directed speech on visual
retention in infant rhesus macaques. Dev. Sci. 21, 12519 (2018).
25. Kaplan, P. S., Goldstein, M. H., Huckeby, E. R. & Cooper, R. P. Habituation, sensitization, and infants’ responses to motherse speech.
Dev. Psychobiol. 28, 45–57 (1995).
26. Lansade, L. et al. Facial expression and oxytocin as possible markers of positive emotions in horses. Sci. Rep. 8, 14680 (2018).
27. Hausberger, M. et al. Mutual interactions between cognition and welfare: e horse as an animal model. Neurosci. Biobehav. Rev.
107, 540–559 (2019).
Content courtesy of Springer Nature, terms of use apply. Rights reserved
8
Vol:.(1234567890)
Scientic Reports | (2022) 12:4297 | https://doi.org/10.1038/s41598-022-08109-z
www.nature.com/scientificreports/
28. Fortin, M. et al. Emotional state and personality inuence cognitive exibility in horses (Equus caballus). J. Comp. Psychol. 132,
130–140 (2018).
29. Trösch, M. et al. Horses feel emotions when they watch positive and negative horse–human interactions in a video and transpose
what they saw to real life. Anim. Cogn. 23, 643–653 (2020).
30. Forkman, B., Boissy, A., Meunier-Salaün, M. C., Canali, E. & Jones, R. B. A critical review of fear tests used on cattle, pigs, sheep,
poultry and horses. Physiol. Behav. 92, 340–374 (2007).
31. Lansade, L., Bouissou, M. F. & Erhard, H. W. Fearfulness in horses: A temperament trait stable across time and situations. Appl.
Anim. Behav. Sci. 115, 182–200 (2008).
32. Stomp, M. et al. An unexpected acoustic indicator of positive emotions in horses. PLoS One 13, e0197898 (2018).
33. Briefer, E. F. et al. Segregation of information about emotional arousal and valence in horse whinnies. Sci. Rep. 5, 9989 (2015).
34. Briefer, E. F., Tettamanti, F. & McElligott, A. G. Emotions in goats: Mapping physiological, behavioural and vocal proles. Anim.
Behav. 99, 131–143 (2015).
35. Mendl, M., Burman, O. H. P. & Paul, E. S. An integrative and functional framework for the study of animal emotion and mood.
in Proceedings of the Royal Society B: Biological Sciences vol. 277 2895–2904 (Royal Society, 2010).
36. Siniscalchi, M., D’Ingeo, S. & Quaranta, A. Orienting asymmetries and physiological reactivity in dogs’ response to human emo-
tional faces. Learn. Behav. 46, 574–585 (2018).
37. Munsters, C. C. B. M., Visser, K. E. K., van den Broek, J. & Sloet van Oldruitenborgh-Oosterbaan, M. M. e inuence of chal-
lenging objects and horse-rider matching on heart rate, heart rate variability and behavioural score in riding horses. Vet. J . 192,
75–80 (2012).
38. Siniscalchi, M., D’Ingeo, S., Minunno, M. & Quaranta, A. Communication in dogs. Animals 8, 131 (2018).
39. Call, J., Hare, B., Carpenter, M. & Tomasello, M. ‘Unwilling’ versus ‘unable’: Chimpanzees’ understanding of human intentional
action. Dev. Sci. 7, 488–498 (2004).
40. Kaminski, J., Schulz, L. & Tomasello, M. How dogs know when communication is intended for them. Dev. Sci. 15, 222–232 (2012).
41. Pongrácz, P., Szapu, J. S. & Faragó, T. Cats (Felis silvestris catus) read human gaze for referential information. Intelligence 74, 43–52
(2019).
42. Pongrácz, P. & Onofer, D. L. Cats show an unexpected pattern of response to human ostensive cues in a series of A-not-B error
tests. Anim. Cogn. 23, 681–689 (2020).
43. Proops, L., Grounds, K., Smith, A. V. & McComb, K. Animals remember previous facial expressions that specic humans have
exhibited. Curr. Biol. 28, 1428-1432.e4 (2018).
44. Koo, T. K. & Li, M. Y. A guideline of selecting and reporting intraclass correlation coecients for reliability research. J. Chiropr.
Med. 15, 155–163 (2016).
45. von Borell, E. et al. Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare
in farm animals—A review. Physiol. Behav. 92, 293–316 (2007).
Acknowledgements
We would like to thank the sta from the UEPAO (Unité Expérimentale de Physiologie Animale de l’Orfrasière)
for technical help; Springer Nature Authors Services for English language and text ow editing; Estel Blasi for
drawing Fig.2; the volunteers who were lmed to make up the stimuli of this experiment; Karine Reynaud for
allowing us to use her pictures for Fig.S1; and Aline Bertin for helping to draw Fig.S1 spectrograms. IFCE
(French Horse and Riding Institute) funded this experiment. is funding source had no role in the study design,
data collection and analysis, or preparation and submission of the manuscript.
Author contributions
All authors devised the protocol. P.J., C.G., C.P., F.R., L.L. implemented the protocol. P.J., C.G., L.L. coded the
videos and analyzed the data from heart rate monitoring and behavior coding. P.J., L.C., V.F., C.G. and L.L.
revised the analysis and report.
Funding
is article was funded by IFCE, 32 000809-Cognition Equine.
Competing interests
e authors declare no competing interests.
Additional information
Supplementary Information e online version contains supplementary material available at https:// doi. org/
10. 1038/ s41598- 022- 08109-z.
Correspondence and requests for materials should be addressed to P.J.orL.L.
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... We measured the horses' heart rates as a potential indicator of change in arousal or emotional valence felt by the horses (Jardat et al. 2022). Indeed, a rise in heart rate has been observed in horses in response to human voices expressing anger (Trösch et al. 2019a) or using pet-directed speech (Jardat et al. 2022), in fearful or stressful situations (Lansade et al. 2008;Munsters et al. 2012), and in a positively arousing situation (Briefer et al. 2015a). ...
... We measured the horses' heart rates as a potential indicator of change in arousal or emotional valence felt by the horses (Jardat et al. 2022). Indeed, a rise in heart rate has been observed in horses in response to human voices expressing anger (Trösch et al. 2019a) or using pet-directed speech (Jardat et al. 2022), in fearful or stressful situations (Lansade et al. 2008;Munsters et al. 2012), and in a positively arousing situation (Briefer et al. 2015a). Similar reactions have been observed in other mammals (Forkman et al. 2007), with for example dogs' heart rates fluctuating in response to different human facial expressions (Siniscalchi et al. 2018), and goats' heart rates increasing in a positively arousing situation (Briefer et al. 2015b). ...
... This is in line with previous findings, suggesting that some species react differently to children than to adults: dolphins and dogs seem to interact differently with these two age groups (Brensing and Linke 2003;Wanser et al. 2020Wanser et al. , 2021). An increase in heart rate can indicate either increased arousal or a change in the valence of emotions felt by horses (Jardat et al. 2022), and several hypotheses can explain such reactions to children's voices. First, the horses may have reacted to the novelty of this type of voice. ...
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