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Functional asymmetries, e.g. the preferential involvement of one brain hemisphere to process stimuli, may increase brain efficiency and the capacity to carry out tasks simultaneously. We investigated which hemisphere was primarily involved in processing acoustic stimuli in goats using a head-orienting paradigm. Three playbacks using goat vocalisations recorded in different contexts: food anticipation (positive), isolation (negative), food frustration (negative), as well as one playback involving dog barks (negative) were presented on the left and right sides of the test subjects simultaneously. The head-orienting response (left or right) and latency to resume feeding were recorded. The direction of the head-orientating response did not differ between the various playbacks. However, when the head-orienting response was tested against chance level, goats showed a right bias regardless of the stimuli presented. Goats responded more to dog barks than to food frustration calls, while responses to food anticipation and isolation calls were intermediate. In addition, the latency to resume feeding, an indicator of fear reaction, was not affected by the kind of vocalisation presented. These results provide evidence for asymmetries in goat vocal perception of emotional-linked conspecific and heterospecific calls. They also suggest involvement of the left brain hemisphere for processing acoustic stimuli, which might have been perceived as familiar and non-threatening.
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Perceptual lateralization of vocal stimuli
in goats
*, Christian NAWROTH
, Elodie F. BRIEFER
, and
Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of
London, Mile End Road, London E1 4NS, UK,
Institute of Behavioural Physiology, Leibniz Institute for Farm Animal
Biology, Dummerstorf, Germany,
Institute of Agricultural Sciences, ETH Zu¨rich, Universita¨tstrasse 2, 8092 Zu¨rich,
Switzerland, and
Department of Life Sciences, University of Roehampton, London SW15 4JD, UK
*Address correspondence to Luigi Baciadonna, E-mail:; and Alan G. McElligott;
Handling editor: Zhi-Yun Jia
Received on 23 July 2017; accepted on 9 March 2018
Functional asymmetries, for example, the preferential involvement of 1 brain hemisphere to process
stimuli, may increase brain efficiency and the capacity to carry out tasks simultaneously. We investi-
gated which hemisphere was primarily involved in processing acoustic stimuli in goats using a head-
orienting paradigm. Three playbacks using goat vocalizations recorded in different contexts: food
anticipation (positive), isolation (negative), food frustration (negative), as well as 1 playback involving
dog barks (negative) were presented on the left and right sides of the test subjects simultaneously.
The head-orienting response (left or right) and latency to resume feeding were recorded. The direc-
tion of the head-orienting response did not differ between the various playbacks. However, when the
head-orienting response was tested against chance level, goats showed a right bias regardless of
the stimuli presented. Goats responded more to dog barks than to food frustration calls, whereas re-
sponses to food anticipation and isolation calls were intermediate. In addition, the latency to resume
feeding, an indicator of fear reaction, was not affected by the kind of vocalization presented. These re-
sults provide evidence for asymmetries in goat vocal perception of emotional-linked conspecific and
heterospecific calls. They also suggest involvement of the left brain hemisphere for processing
acoustic stimuli, which might have been perceived as familiar and non-threatening.
Key words: auditory processing, brain asymmetry, emotions, lateralization, social cognition, vocal communication
Behavioral lateralization refers to how behaviors are performed pre-
dominantly using either the right or the left side of the body (Rogers
and Andrew 2002;Baruzzi et al. 2017). When an individual shows a
right or left preference, it indicates asymmetry at an individual level
(e.g., being left- or right-handed; Rogers and Andrew 2002). When
the majority of individuals show the same side preference, this sug-
gests asymmetry at the population level (Vallortigara and Rogers
2005). In humans, population-level asymmetries are represented by
the predominance of the left hemisphere in processing syntactic and
semantic information, and by the prevalence of the right hemisphere
in processing information about prosody, novelty, and emotional
content (Fitch et al. 1997;Friederici and Alter 2004).
The experimental procedure usually applied to test functional
auditory asymmetries in response to vocalizations of conspecifics and
heterospecifics is based on a major assumption (Teufel et al. 2007;
Siniscalchi et al. 2008). It is assumed that when a sound is perceived
simultaneously in both ears, the head orientation to either the left or
right side is an indicator of the side of the hemisphere that is primarily
involved in the response to the stimulus presented. There is strong evi-
dence that this is the case in humans; auditory input in humans is
CThe Author(s) 2018. Published by Oxford University Press on behalf of Editorial Office, Current Zoology. 67
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Current Zoology, 2019, 65(1), 67–74
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processed by the contralateral hemisphere when 2 auditory stimuli are
presented simultaneously from both sides (dichotic paradigm). The as-
sumption is also supported by the neuroanatomic evidence of the
contralateral connection of the auditory pathways in the mammalian
brain (Rogers and Andrew 2002;Ocklenburg et al. 2011).
In animals, brain lateralization seems to underline the different
response to conspecific versus heterospecific calls. Japanese ma-
caques Macaca fuscata, rhesus monkeys Macaca mulatta, California
sea lions Zalophus californianus and dogs Canis lupus familiaris dis-
played a left hemisphere asymmetry when processing calls from con-
specifics (Petersen et al. 1978; Heffner HE and Heffner RS 1984;
Hauser and Andersson 1994;Poremba et al. 2004;Bo¨ ye et al.
2005). By contrast, mouse lemurs Microcebus myoxinus and
Barbary macaques Macaca sylvanus showed no orientation prefer-
ences in response to conspecific or heterospecific vocalizations
(Scheumann and Zimmermann 2005;Teufel et al. 2007). Vervet
monkeys Cercopithecus aethiops displayed a right hemisphere asym-
metry for conspecific vocalizations regardless of their familiarity
with these vocalizations (Gil-da-Costa and Hauser 2006). Horses
Equus caballus showed a left hemisphere (right ear turn) processing
for calls emitted by a familiar neighbor (familiar horse housed in a
close field or stall), but no preference for group members (also famil-
iar) or strangers (Basile et al. 2009). The lack of consistency between
species regarding which hemisphere processes specific types of
acoustic stimuli shows that further investigations are needed to ex-
plore the mechanisms underlying the variation in the direction of
auditory asymmetry across species.
Emotional content could account for the variation observed be-
tween species in auditory asymmetries. Historically, 2 main theories
of brain lateralization have been proposed for the cortical lateraliza-
tion of emotional processing (Demaree et al. 2005). The “right-
hemisphere model” proposes right hemisphere dominance for ex-
pression and perception of emotionally loaded signals, regardless of
valence. By contrast, the “valence model,” suggests a dominance of
the right hemisphere in processing negative emotions and a domin-
ance of the left hemisphere in processing positive emotions (Tucker
1981;Silberman and Weingartner 1986;Ehrlichman 1987;
Demaree et al. 2005). In dogs, a left hemisphere preference has been
observed when processing different types of vocalizations from a
conspecific and a right hemisphere preference (head turning to the
left side) when processing thunderstorm sounds (Siniscalchi et al.
2008). In addition, a right hemisphere preference was linked with
conspecific calls produced in a context eliciting intense arousal, like
isolation and play (Siniscalchi et al. 2008). The involvement of the
right side of the brain for processing emotional signals was also con-
firmed by later research showing a left turning bias in response to
the visual presentation of threatening (silhouette of snake) and
alarming (silhouette of cat) stimuli (Siniscalchi et al. 2010), and also
in response to broadcasted dog barks (Reinholz-Trojan et al. 2012).
This left turning bias was claimed to result from the emotional con-
tent of the barks used, which were recorded when an unknown dog
appeared (Reinholz-Trojan et al. 2012;Andics et al. 2017). Dogs
also exhibit a right hemisphere asymmetry (left head-orienting bias)
in response to a meaningless human voice (phonemic components
removed) with positive intonation (Ratcliffe and Reby 2014). In
addition, fMRI in dogs found a left hemisphere bias for processing
human and dog sounds with positive valence (Andics et al. 2014,
2016, 2017;Andics 2017;Reinholz-Trojan et al. 2012). These find-
ings indicate that both the familiarity with the stimulus, whether it
is produced by a conspecific or heterospecific, and its emotional
arousal and valence, could interact to affect lateralized behavioral
responses in non-univocal ways.
Goats display different behavioral, neural, and physiological reac-
tions to situations inducing positive (i.e., food anticipation) and nega-
tive emotions (i.e., isolation or food frustration, in which food was
inaccessible; Gygax et al. 2013;Briefer et al. 2015). When goats were
expected to receive food reward after 3 days of habituation and when
they experienced food frustration, they had high physiological and be-
havioral activation compared with a control and isolation situation,
and also high activation in the prefrontal cortex (Gygax et al. 2013;
Briefer et al. 2015). Bilateral prefrontal cortex activation was found
in the negative condition, whereas in the positive situation, the activa-
tion was mainly revealed in the left hemisphere (Gygax et al. 2013).
This suggests that situations that elicit positive emotions preferentially
engaged one side of the brain (i.e., left hemisphere). Remarkably, goat
vocalizations also vary according to the emotional arousal and va-
lence experienced by the animals (Briefer et al. 2015). However, to
date, hemispheric lateralization in goats in response to emotional
vocalizations from conspecifics, and how this compares to processing
heterospecific vocalizations, remains to be investigated.
Potential auditory processing asymmetries in goats were investi-
gated in this study. A head-orienting paradigm was used to examine
perceptual asymmetry in response to playbacks of conspecifics emit-
ted under positive high arousal (food anticipation), negative low
arousal (isolation) and negative high arousal (food frustration) emo-
tional states, and to dog barks (i.e., stimuli potentially perceived as
negative). According to previous findings (Petersen et al. 1978;
Hauser and Andersson 1994;Siniscalchi et al. 2008), it was pre-
dicted that goats would turn their heads toward the right (left hemi-
sphere processing) in response to conspecific calls, and to the left in
response to dog barks (right hemisphere processing). Alternatively,
if the right hemisphere processes only high arousal sounds (“right-
hemisphere model”; Demaree et al. 2005), we would expect a right
hemisphere bias to process food anticipation calls, food frustration
calls, and dog barks, because they are all produced under high
arousal and likely elicit high arousal in receivers (Briefer et al.
2015). A right hemisphere (left side) bias for processing all tested
acoustic stimuli could also be expected, because this hemisphere is
involved in processing novel stimuli and/or stimuli with emotional
content. Finally, according to the “valence model” (Demaree et al.
2005), we would expect the right hemisphere to process negative
sounds (dog barks, food frustration, and isolation calls), and the left
hemisphere to process positive sounds (food anticipation calls).
Materials and Methods
Subjects and management conditions
The study was carried out at a goat sanctuary (Buttercups Sanctuary
for Goats,; Kent, UK). Employees
and volunteers at the sanctuary provided routine care for the ani-
mals (120 animals housed at the time of testing), and therefore the
goats were fully habituated to human presence and handling (Briefer
et al. 2015). During the day, goats were released together into 1 or 2
large fields where shelters are provided. During the night, goats
were kept indoors either in individual or shared pens (average
size ¼3.5 m
) with straw bedding. Goats had ad libitum access to
hay, grass, and water, and were also fed with a commercial concen-
trate in quantities that vary according to their size, health, and age.
In total, 18 adult goats (9 females and 9 castrated males) of different
breeds and ages (age range: 2–16 years old) housed at the sanctuary
68 Current Zoology, 2019, Vol. 65, No. 1
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for at least 1 year were randomly selected and tested from
September to October 2016.
Playback test
Sound recordings
The goat vocalizations used in the playback test were obtained from a
previous study (Briefer et al. 2015) at the same location. Vocalizations
were recorded at distances of 3–5 m from the focal animal using a
Sennheiser MKH-70 directional microphone (frequency response
50–20, 000 Hz, max SPL 124 dB at 1 kHz) connected to a Marantz
PMD-660 numeric recorder (sampling rate: 44.1 kHz with amplitude
resolution of 16 bits in WAV format), and were then edited and
rescaled to the same maximum amplitude using PRAAT software
(Boersma and Weenink 2009). The vocalizations for the playback test
were recorded during 3 different contexts: 1) food anticipation (posi-
tive, high arousal), in which the animals, tested in pairs in 2 adjacent
pens, learned to anticipate a food reward after 3 days of training (1 ses-
sion per day to the situation), and were recorded on the 4th day when
the experimenter approached them with the food; 2) food frustration
(negative, high arousal), in which only 1 of 2 goats tested in adjacent
pens received food from the experimenter (duration: 4 min); 3) isola-
tion (negative, low arousal), in which goats were left alone for 5 min in
an outdoor isolated pen, after 3 days of habituation (1 exposition per
day to the situation; Briefer et al. 2015). The arousal and valence of the
situations during which the calls were recorded were validated using
physiological and behavioral indicators of emotions. The arousal was
established based on the heart rate elicited by the various situations
and revealed that the food anticipation and food frustration triggered
emotions of similar high arousal, whereas the isolation situation trig-
gered emotions of low arousal that did not differ from the control situ-
ation (by pair, undisturbed, with hay in the feeders). Analyses revealed
that the high arousal situations (food anticipation and food frustra-
tion), compared with the low arousal ones (isolation and control),
were also associated with lower heart-rate variability, higher respir-
ation rate, more movements, more calls, more time spent with ears
pointing forward and less time with ears on the side. In the positive
situation (food anticipation), compared with the neutral (control) and
negative situations (isolation and food frustration), goats had their ears
oriented backward less often and spent more time with their tails up
(Briefer et al. 2015). These indicators of positive situations are similar
to those found in other studies (e.g., Reimert et al. 2013,2015). The
detailed acoustic vocal parameter analysis identified 6 acoustic param-
eters affected by the arousal. F0 contour over time and energy quartile
increased with arousal, whereas the 1st formant decreased. F0 vari-
ation within the call was influenced by valence and decreased from
negative to positive valence (for more details see Briefer et al. 2015). In
addition, a 4th kind of vocalization (heterospecific) was played back:
dog barks (obtained from, with a sampling rate of
44.1 kHz and amplitude resolution of 16 bits in WAV format.
The audio stimuli used in the playback test consisted of one sin-
gle vocalization each (mean duration: 0.74 60.12 s). In total, 4
treatments were prepared: food anticipation, food frustration, isola-
tion, and dog bark (Figure 1). For each treatment, 3 unique stimuli,
produced by 3 different individuals (for both goats and dogs) were
selected to reduce pseudoreplication (Waller et al. 2013). The goat
calls used were recorded in 2011 at the same location. The calls se-
lected belonged to goats that did not share a pen with the subjects
during the night, or to goats that were no longer at the sanctuary at
the time of testing. Therefore, we expected all goat calls used in our
experiment to be equally familiar for the subjects (Pitcher et al.
Test procedure
Figure 2 illustrates the experimental setup (7 m 5 m), which was
placed in the usual daytime range of the goats. A feeding bowl filled
with a mixture of dry pasta and hay and familiar to the goats was
fixed in the center, on the opposite side of the entrance of the arena.
Each vocalization was broadcasted from 2 Mackie Thump TH-12A
loudspeakers (LOUD Technologies Inc., Woodinville, WA; fre-
quency response: 57–20 kHz 63 dB) connected to an active box to
boost the sound (Active Box DI-100 Fame) and an Mp4 player
(Technika MP111), at approximately natural amplitude commonly
used in previous studies (Briefer and McElligott 2011a,
80.08 60.90 dB measured at 2 m using an ASL-8851 sound level
meter). Both speakers were set at the same, constant volume. The
speakers were positioned at equal distance (2 m) from the right and
left side of the bowl, and were aligned to it. In addition, the speakers
were concealed using camouflage netting.
Each subject received 3 sessions, with 1 session being administered
per day. Each session consisted of 8 consecutive trials, that is, 2 repeti-
tions of each treatment (same stimulus was repeated within the session
but changed across the sessions), adding up to 6 repetitions per treat-
ment over the 3 sessions. The order in which the treatments were tested
within each session was counterbalanced between subjects and ses-
sions. As soon as the goat started to feed from the bowl, 1 of 4 treat-
ment vocalizations was played from the 2 speakers simultaneously.
The minimum time between each playback trial was 10 s. The max-
imum time to resume feeding (i.e., the subject moved the head inside
the bucket) was set at 30 s (average time to resume feeding after the off-
set of the playback: 3.70 60.21 s). Playbacks were initiated only if the
test subject’s body was positioned orthogonally to the speakers. In
cases where the subject was in an incorrect position, a 2nd experi-
menter adjusted the body position of the goat before the next trial
started. During the test, this 2nd experimenter was standing still, be-
hind the goat, close to the gate inside the testing arena (Figure 2).
All trials were video recorded using a digital video camera placed
behind the subject (Sony HDR-CX190E). The head-orienting re-
sponses of goats toward the speakers were recorded, from the time
the sound started to 30 s after. Four possible responses were con-
sidered and scored: head oriented right (head toward the right side
when the body of the goat was orthogonal to the speaker), head ori-
ented left (head toward the left side when the body of the goat was
orthogonal to the speaker), head up (no turning to either the left or
right sides and head raised toward the horizon from the initial pos-
ition), and no response (i.e., the subject did not move its head within
30 s from the start of the sound). The latency to resume feeding
from the bowl (measure of fear reaction) was scored directly during
the testing. The maximum time to resume feeding was set at 30 s
after the offset of the sound. If the subject did not resume feeding
within the 30 s time window, they were gently moved toward the
bucket and all goats tested continued feeding.
Statistical analyses
In order to determine if the strength of the responses differed be-
tween treatments, we tested the effect of the sound treatment on the
proportion of head movement response and on the time to resume
feeding. The proportion of head movement response was treated as
a binary choice (head oriented right, head oriented left or head
up ¼1, and no response ¼0) and was analyzed with a generalized
mixed-effects model (GLMM) fit with binomial family distribution
and logit link function (GLMM; glmer function, lme4 library;
Pinheiro 2000) in R v.3.2.2 (R Core 2013). The time to resume feed-
ing was analyzed with a linear mixed-effects model (LMM) fit with
Baciadonna et al. Acoustic laterality in goats 69
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Gaussian family distribution and identity link function (lmer func-
tion, lme4 library). Both models included the treatment (Food
Anticipation, Isolation, Food Frustration, and Dog) and the order of
presentations of stimuli for each treatment over the 3 sessions as
fixed factors. Including the presentation order allowed us to control
for any potential habituation effect over the 3 sessions. The session
nested within the identity of the goats was included as a random fac-
tor to control for repeated measurements.
We also analyzed the effect of the treatment on the head-
orienting response of the goats. Head orientation was treated as a
binary choice variable (head oriented right ¼1, head oriented
left ¼0, head up and no response ¼NA) and was analyzed using
a GLMM fit with binomial family distribution and logit link
function (glmer function). This model included the same fixed ef-
fects (treatment and presentation order) and random effect struc-
ture (session nested within goat identity) as the models described
For all models (GLMM and LMM), we checked the residuals
of the models graphically for normal distribution and homoscedas-
ticity (simulateResiduals function, DHARMa library). In order to
Figure 1. Examples of calls used in the experiment. Oscillograms (above) and spectrograms (below) of (A) goat food anticipation call, (B) goat isolation call, (C)
goat food frustration call and (D) dog bark used in the playback experiment.
70 Current Zoology, 2019, Vol. 65, No. 1
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meet the model assumptions, the latency to resume feeding was
log-transformed. P-values (PBmodcomp function, pbkrtest library)
were calculated using parametric bootstrap methods (1,000 boot-
strap samples). To this aim, models were fitted with maximum like-
lihood. P-values calculated with parametric bootstrap tests give the
fraction of simulated likelihood ratio test (LRT) statistic values that
are larger or equal to the observed LRT value. This test is more ad-
equate than the raw LRT because it does not rely on large-sample
asymptotic analysis and correctly takes the random-effects structure
into account (Halekoh and Højsgaard 2014). When a significant
treatment effect was detected, we carried out Tukey post hoc tests
for 2-by-2 comparison (glht function, multcomp library in R).
In addition, we investigated whether the head-orienting response
showed a deviation from chance level. This was done by comparing
the average head-orienting response for each goat (ranging from 0
to 0.5 for a left bias, and from 0.5 to 1 for a right bias) to a hypo-
thetic mean of 0.5 (absence of laterality) using a 1-sample t-test. The
average head-orienting response was logit-transformed beforehand
in order to approximate a normal distribution.
Proportion of head movement responses and latency to
resume feeding
The kind of vocalization presented during the playback (food antici-
pation, food frustration, isolation, and dog bark) affected the pro-
portion of head movement responses of the goats (GLMM: n¼432
trials, 18 goats; P¼0.005; Figure 3). Post hoc comparisons revealed
that goats moved their heads more often after dog barks compared
with food frustration calls (z¼3.36, P¼0.005; Figure 3). The
other 2-by-2 comparisons were not significant (P0.11). An effect
of the order of stimulus presentation was also found (P¼0.001;
Figure 4), with goats gradually habituated to the vocalizations dur-
ing the 6 presentations.
The time to resume feeding was affected neither by the treat-
ments (LMM: n¼267 trials, 18 goats; v2
3¼1:13, P¼0.89;
Figure 5) nor by the presentation order (P¼0.43). Overall, this sug-
gests that goats were more alert when hearing dog barks compared
with food frustration calls, and that they habituated to the sound
treatments during the 6 trials.
Head-orienting response and head-orienting bias
The head-orienting response was not affected by the kind of vocal-
izations presented (GLMM: n¼149 trials, 18 goats; P¼0.26;
Figure 6). This parameter was also not affected by the order of
stimulus presentations (P¼0.29), suggesting that the direction of
the head-orienting response did not differ between treatments.
Figure 2. Experimental enclosure. The experimental apparatus (7 m 5m)
consisted of a door that allowed access to a central arena. A familiar feeding
bowl was fixed at the center of the opposite side of the arena. The speakers
were positioned at a distance of 2 m from the right and left side of the bowl
and were aligned to it. X indicates the position of Experimenter 2.
Figure 3. Proportion of head movement responses for each of the 4 treat-
ments (mean and 0.025 and 0.975 quantiles). The vocalizations presented dur-
ing the playback (Food Anticipation, Isolation, Food Frustration, and Dog)
affected the response pattern of the goats (P¼0.005). Post hoc comparisons
revealed that goats responded less when a food frustration compared with
dog call was presented (**P<0.01).
Figure 4. Proportion of head movement response over the 6 repetitions of the
stimuli (mean 0.025 and 0.975 quantiles). Goats gradually habituated to the
vocalizations during the 6 presentations of each treatment (P¼0.001).
Baciadonna et al. Acoustic laterality in goats 71
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The 1-sample t-test performed on all treatments combined re-
vealed a significant deviation of head-orienting response toward the
right side (mean [95% confidence interval] head-orienting re-
sponse ¼0.74 [0.50, 0.89]); 1-sample t-test: feeding, t
P¼0.046) compared with chance level (i.e., 0.50). Goats thus
showed a general right bias in their head-orienting responses.
Auditory asymmetries were investigated in goats in response to vo-
calizations of conspecifics produced in situations eliciting positive
high arousal (food anticipation) or negative low and high arousal
emotions (isolation and food frustration, respectively), as well as
dog barks. The direction of the head-orienting response did not dif-
fer between treatments. However, goats showed a general right bias
toward the presented acoustic stimuli. These results suggest the in-
volvement of the left hemisphere in response to both conspecific and
heterospecific acoustic stimuli in this species. Brain asymmetries
provide neural advantages and a general increase in brain efficiency,
and therefore have been selected and favored over the course of evo-
lution (Rogers et al. 2004;Vallortigara 2007). However, brain
asymmetry direction (e.g., left or right side) could vary across spe-
cies due to genetics or environmental constraints (Rogers et al.
2004;Gil-da-Costa and Hauser 2006;Vallortigara 2007;
Ocklenburg et al. 2011). For example, head rotation in vertebrate
embryos is determined by several genes (e.g., Nodal, Lefty;Schier
2003). Furthermore, steroid hormones can reduce the degree of vis-
ual lateralization in chicks leaving the direction of lateralization un-
altered (Rogers and Deng 2005).
Goats showed a head-orienting response to the right side when
conspecific vocalizations were played back regardless of the context
on which the calls were recorded. Our findings could thus be in line
with the general interpretation that the left hemisphere (right side
bias) is specialized to process vocalizations that are familiar and/or
positive/non-threatening (Craig 2005;Demaree et al. 2005).
However, these findings have not been replicated consistently in re-
sponse to vocalizations of conspecifics in species such as Vervet
monkeys and dogs (Gil-da-Costa and Hauser 2006;Siniscalchi et al.
2008;Ratcliffe and Reby 2014). Vervet monkeys show a left ori-
enting response (i.e., right hemisphere asymmetry) when processing
conspecifics calls, but no side bias for heterospecific calls (Gil-da-
Costa and Hauser 2006). In dogs, the vocalizations emitted from
conspecifics are normally processed by the left hemisphere, whereas
the right hemisphere seems to be involved in processing auditory
cues eliciting intense emotions, for example, a thunderstorm
(Siniscalchi et al. 2008). In horses, a right head-orienting bias (i.e.,
left hemisphere asymmetry) is associated with a non-group member
(i.e., neighbors or strangers, thus the bias is affected by level of fa-
miliarity; Basile et al. 2009). In contrast to the head-orienting re-
sponse, the ears-orienting response is biased to the right side for of
familiar neighbor individuals, and to the left side for calls of stran-
gers (Basile et al. 2009). In addition, a positive correlation between
the right head-ears orienting response is associated with hearing a
known whinny (familiar neighbor and group member; Basile et al.
2009). Conclusions on which hemisphere is involved (left vs. right
direction across species) in specific stimuli processing are difficult to
draw because factors such as ontogeny, genetics or environmental
constraints interact to generate varying patterns of hemispheric pref-
erence (Vallortigara and Rogers 2005;Ocklenburg et al. 2011).
According to the “right-hemisphere model,” a left head-orienting
response to calls eliciting high arousal would have been expected.
Indeed, the use of the right hemisphere has been linked with the ex-
pression of intense emotions (Quaranta et al. 2007;Siniscalchi et al.
2008;Ratcliffe and Reby 2014). By contrast, according to the “va-
lence model,” we would expect the right hemisphere to process nega-
tive sounds (isolation, food frustration calls, and dog barks) and the
left hemisphere to process positive sounds (food anticipation calls).
The vocalizations used in our experiment have been analyzed previ-
ously and were shown to be associated with different patterns of be-
havioral and physiological responses in the caller (Briefer et al. 2015).
Figure 5. Time to resume feeding (log-transformed) for each treatment (mean
0.025 and 0.975 quantiles). The latency to resume feeding(s) was not affected
by the kind of vocalizations presented (Food Anticipation, Isolation, Food
Frustration, and Dog; P¼0.89).
Figure 6. Head-orienting response toward the various vocalizations pre-
sented during the playbacks (mean 0.025 and 0.975 quantiles). The head-ori-
enting response was not affected by the kind of vocalizations presented
(P¼0.26). Values from 0 to 0.5 indicate a left bias, whereas values from 0.5 to
1 indicate a right bias.
72 Current Zoology, 2019, Vol. 65, No. 1
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However, the behavioral and physiological reactions on hearing these
vocalizations and whether a conspecific is able to discriminate be-
tween calls with different valence and arousal have not been tested
yet. Therefore, it is not known if the calls produced under high
arousal (food anticipation and food frustration) also elicit high
arousal emotions in receivers, and if the calls produced under positive
emotional state (food anticipation) also elicited positive emotions in
receivers (and vice versa for negative calls). State matching between
producer and receiver of a signal is termed emotional contagion, and
is predicted to be widespread in the animal kingdom (de Waal 2008;
Briefer 2018). Such information would have been beneficial to disen-
tangle the results predicted according to the “right-hemisphere mod-
el” and “the valence model” of brain asymmetries. If emotional
contagion indeed had occurred in our study, according to the “right-
hemisphere model,” we would have expected an involvement of the
right hemisphere to process food anticipation and food frustration
calls (i.e., high-arousal calls). By contrast, according to the “valence
model,” we would have expected an involvement of the right hemi-
sphere to process food frustration and, isolation calls and possibly
dog barks (i.e., negative calls), and an involvement of the left hemi-
sphere to process food anticipation calls (i.e., positive calls). The lack
of positive calls of low arousal in this study represents a methodo-
logical limitation that has to be taken into account when considering
the involvement of the right hemisphere and the valence model of
brain asymmetries. Recent evidence has shown that contact calls in
goats convey information about size, sex, age, and individuality
(Briefer and McElligott 2011b, 2012;Pitcher et al. 2017), but the abil-
ity to extract emotional information from vocalizations had not been
experimentally tested yet. Overall, our study suggests that the spon-
taneous response in the head-orienting paradigm might be under the
control of the left hemisphere (Basile et al. 2009;Ghazanfar and
Hauser 1999;Siniscalchi et al. 2008,2010).
Our results do not confirm the hypothesis of a left head-
orienting response (i.e., right hemisphere asymmetry) toward hetero-
specific calls or calls eliciting intense emotions (dog barks). Dogs are
potential predators of small ruminants and hearing a dog barking
from a close distance may induce a fear reaction and a more atten-
tive response (Beausoleil et al. 2005). Although goats were more
alert when hearing dog barks than conspecific food frustration calls,
responses to dog barks did not differ from those to conspecific food
anticipation and isolation calls. In addition, the time to resume feed-
ing (a measure of fear), in our study did not differ between dog
barks and the vocalizations of conspecifics. This suggests that goats
at our study site may have been habituated to dog barks and that
they did not perceive dog barks as a serious threat.
To summarize, goats showed a general head-orienting bias to the
right side, providing evidence for perceptual lateralization of both
conspecific and heterospecific acoustic stimuli, which might have
been perceived as familiar and non-threatening. The overall findings
of the study suggest that the head responses are potentially mediated
by general acoustic features rather than specific information con-
veyed (Teufel et al. 2007). The results also indicate the need to con-
trol for the characteristics of the stimuli employed, such as degree of
familiarity, emotional valence, and arousal, and the importance to
use appropriate controls (e.g., non-biological sound) in order to dis-
entangle the involvement of each brain hemisphere.
The authors are grateful to Carolina Baruzzi, Monica Padilla de la Torre,
Caroline Spence, Luca Tommasi and Claudia Wascher for helpful comments
on the manuscript. They also thank Bob Hitch, Gower McCarthy, Samantha
Taylor, and all the volunteers at Buttercups Sanctuary for Goats (http://www. for their excellent help and free access to the animals
Conflict of Interest
The authors declare that they have no conflicts of interest.
Ethical Note
Animal care and all experimental procedures were conducted in accordance
with the Association for the Study of Animal Behaviour guidelines
(Association for the Study of Animal Behaviour, 2016). The study was
approved by the Animal Welfare and Ethical Review Board of Queen Mary
University of London (002/2016AWERBqmul). The tests were non-invasive
and behaviors indicating stress (e.g., vocalizations and strong reaction to the
sounds) were monitored throughout the exposure to the playbacks. If any
signs of distress had occurred, the procedure would have been stopped and
the subject removed. None of the goats were removed from the experiment.
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74 Current Zoology, 2019, Vol. 65, No. 1
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... As a precursor for human language, conspecific vocalizations have been found to be processed with left hemispheric dominance in several species (reviewed in [185]). However, such studies are still rare, and findings from auditory laterality experiments in goats [168] and horses [100,125] do not provide support for this pattern. Therefore, more research is needed to better understand the auditory processing of conspecific vocalizations. ...
... Even though humans are not conspecifics, horses are in frequent contact with humans, so laughter may have positive emotional relevance for horses [27]. Finally, several other studies have failed to find any lateralized emotional processing [69,116,163,168]. Thus, lateralized emotional processing needs to be further studied in ungulate livestock to better understand emotional processing, but new findings in positive social interactions already provide a good start, since they have the potential to challenge the emotional valence hypothesis. ...
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... One model is the right hemisphere hypothesis, in which the right hemisphere is generally dominant in processing all types of emotions; the other model is the valence specificity hypothesis, which emphasizes left hemisphere dominance when processing positive emotions and right hemisphere dominance when processing negative emotions [18,19]. Furthermore, valence hypotheses have been developed for different patterns including a sex valence specificity hypothesis, an approach-withdrawal hypothesis, and the emotional-type hypothesis [20][21][22][23][24]. Several studies have supported the right hemisphere hypothesis [25][26][27] and additional evidence of the valence hypothesis has been obtained [28][29][30][31][32], while there has also been some evidence that did not support the two hypotheses [22][23][24]. Behavioral and neurophysiological characteristics of cerebral lateralization have been identified using emotional valence, sound function, age, and sex [21,33,34]. ...
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Functional lateralization in the auditory system has been widely studied. Accordingly, behavioral laterality responses affected by acoustic stimuli have been observed in many vertebrate species. In this study, we assessed giant pandas’ behavioral responses to different acoustic stimuli in order to examine cerebral lateralization. We concluded that adult giant pandas showed a left-hemisphere bias in response to positive acoustic stimuli. Furthermore, we found the specific valence of cerebral lateralization for different categories of acoustic stimuli, of which some were relevant to the lateralization while others were not relevant. Our findings support an evolutionary strategy that giant pandas process auditory signals similar to other mammals.
... All the animals were used to being handled and many of them had participated in previous experiments (e.g. [40,41]). ...
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... Additionally, in a related experiment, it was found that domestic pigs exhibited behavioral and cardiac responses when they heard a distress call from another pig [73]. In a more recent study, goats showed a head-orienting response to the right side whenever they heard calls from other goats, indicating that they use parts of their left hemisphere brain actively to associate with non-threatening vocal signals [74]. These studies give us enough clues into how important vocal signals and emotional states are interconnected. ...
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... This suggests that brain processing of auditory stimuli and the associated emotional valence differs between these species, that distraction and anaesthesia certainly do not represent the same level of attention alteration, or that there is another common process that may explain these discrepancies. Overall, all EEG studies converge to indicate a LH bias for positive and RH bias for negative emotional states in human studies including when processing speech, as also shown in most animal studies using visual stimuli (i.e., [58,[60][61][62][63][64]). Animal behavioural studies on auditory perception are not as clear-cut: dogs turn more the head towards the left (RH) when hearing a thunderstorm noise or human voices with a negative valence [65,66], as do Campbell's for conspecific calls with a negative valence [31] but mouse lemurs turn more the head towards the right (LH) for the same type of stimulus [33]. ...
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... These results strongly support the notion that the vocal domain in group-living animals, such as goats, could be a potential way of emotion transmission. Moreover, playback experiments in goats indicated that subjects exposed to emotional-linked calls (food anticipation, food frustration, and isolation) from conspecifics preferentially showed a lateralized head-turning response to the right side (43). This right side headturning bias suggests the involvement of the left hemisphere for processing calls conveying emotional contents (44,45). ...
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Emotions can be defined as an individual’s affective reaction to an external and/or internal event that, in turn, generates a simultaneous cascade of behavioural, physiological, and cognitive changes. Those changes that can be perceived by conspecifics have the potential to also affect other’s emotional states, a process labelled as “emotional contagion”. Especially in the case of gregarious species, such as livestock, emotional contagion can have an impact on the whole group by, for instance, improving group coordination and strengthening social bonds. We noticed that the current trend of research on emotions in livestock, i.e. investigating affective states as a tool to assess and improve animal welfare, appears to be unbalanced. A majority of studies focuses on the individual rather than the social component of emotions. In this paper, we highlight current limitations in the latter line of research and suggest a stronger emphasis on the mechanisms of how emotions in livestock are transmitted and shared, which could serve as a promising tool to synergistically enhance the welfare of all individuals within a group.
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The study of emotional functioning is of crucial importance for improving the welfare of domestic animals. The investigation of animal emotions is mainly based on the outcomes of affective states, specifically animal behaviour, physiology and cognition. The cognitive component of emotions includes the processes regulating the affective states in animals, which are lateralized in the animal kingdom. Functional asymmetries in emotional processing, indeed, have been widely reported in both vertebrates and invertebrates. To date, the study of animal emotions through the evaluation of cerebral lateralization has been mainly performed through the analysis of lateralized behaviours, which indirectly reflect the prevalent activation of the right or the left hemisphere. In particular, the asymmetric processing of different environmental stimuli through the different senses as well as the lateralized motor patterns have been associated with different aspects of animal emotions. In this review, we present a comprehensive overview of the behavioural asymmetries for the sensory and motor functions related to emotional functioning of domestic animals. Our final aim is to support the use of laterality as a tool to evaluate animal emotional processing, and therefore, their welfare.
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Brain lateralization is a phenomenon widely reported in the animal kingdom and sensory laterality has been shown to be an indicator of the appraisal of the stimulus valence by an individual. This can prove a useful tool to investigate how animals perceive intra- or hetero-specific signals. The human-animal relationship provides an interesting framework for testing the impact of the valence of interactions on emotional memories. In the present study, we tested whether horses could associate individual human voices with past positive or negative experiences. Both behavioural and electroencephalographic measures allowed examining laterality patterns in addition to the behavioural reactions. The results show that horses reacted to voices associated with past positive experiences with increased attention/arousal (gamma oscillations in the right hemisphere) and indicators of a positive emotional state (left hemisphere activation and ears held forward), and to those associated with past negative experiences with negative affective states (right hemisphere activation and ears held backwards). The responses were further influenced by the animals’ management conditions (e.g. box or pasture). Overall, these results, associating brain and behaviour analysis, clearly demonstrate that horses’ representation of human voices is modulated by the valence of prior horse-human interactions.
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Behavioural lateralization consists of perceptual and motor lateralization and provides adaptive advantages such as a general increase in brain efficiency. Motor laterality refers to the preferred use of either left or right limbs or organs to perform a specific task. We investigated motor laterality in goats (Capra hircus), using the First-stepping Task. During this task, the first foreleg used to step off a board after standing with both forelimbs was recorded. Subjects varied individually in their expression of motor lateralization with 36.6% of subjects showing individual-level asymmetries. However, goats as a group did not show a preference for a specific foreleg or lateralization in general. Our results support the hypothesis that the need to coordinate behaviour among conspecifics might be important for determining the presence of lateralization at the population level. We suggest that future research investigates how social complexity might affect population-level asymmetries, and whether stimuli with high emotional valence impact on lateralization presence and level (i.e., individual or population).
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When identifying other individuals, animals may match current cues with stored information about that individual from the same sensory modality. Animals may also be able to combine current information with previously acquired information from other sensory modalities, indicating that they possess complex cognitive templates of individuals that are independent of modality. We investigated whether goats (Capra hircus) possess cross-modal representations (auditory–visual) of conspecifics. We presented subjects with recorded conspecific calls broadcast equidistant between two individuals, one of which was the caller. We found that, when presented with a stablemate and another herd member, goats looked towards the caller sooner and for longer than the non-caller, regardless of caller identity. By contrast, when choosing between two herd members, other than their stablemate, goats did not show a preference to look towards the caller. Goats show cross-modal recognition of close social partners, but not of less familiar herd members. Goats may employ inferential reasoning when identifying conspecifics, potentially facilitating individual identification based on incomplete information. Understanding the prevalence of cross-modal recognition and the degree to which different sensory modalities are integrated provides insight into how animals learn about other individuals, and the evolution of animal communication.
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During speech processing, human listeners can separately analyze lexical and intonational cues to arrive at a unified representation of communicative content. The evolution of this capacity can be best investigated by comparative studies. Using functional magnetic resonance imaging, we explored whether and how dog brains segregate and integrate lexical and intonational information. We found a left-hemisphere bias for processing meaningful words, independently of intonation; a right auditory brain region for distinguishing intonationally marked and unmarked words; and increased activity in primary reward regions only when both lexical and intonational information were consistent with praise. Neural mechanisms to separately analyze and integrate word meaning and intonation in dogs suggest that this capacity can evolve in the absence of language.
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We studied emotional contagion, a simple form of empathy, and the role of oxytocin herein in pigs. Two training pigs per pen (n = 16 pens) were subjected to a positive treatment (pairwise access to a large compartment filled with peat, straw and some chocolate raisins) and a negative treatment (social isolation in a small compartment) in a test room using a within-subjects design. Thereafter, two naive pen mates joined the training pigs in the test room, but were not given access to the treatments. This allowed testing for emotional contagion. Subsequently, the naive pigs, serving as their own controls, were given 24 IU of oxytocin or a placebo intranasally 30 min before accompanying the training pigs, which were exposed to either the negative or positive treatment, to the test room. Behavioral differences found between the positive and negative treatments (e.g., play and “tail wagging” vs. standing alert, urinating, defecating and ears backward) show that the treatments induced a positive and negative emotional state in the training pigs, respectively. Changes in behaviors of the training pigs with and without naive pigs present (e.g., in ears backwards) and of the naive pigs with and without training pigs present (e.g., in standing alert) indicated that emotional contagion occurred, especially during the negative treatment. Oxytocin did not seem to affect the behavior of the treated naive pigs, but did affect behaviors (e.g., defecating) of the training pigs which had not received oxytocin. This suggests a role for oxytocin in pig communication, which merits further research. Electronic supplementary material The online version of this article (doi:10.1007/s10071-014-0820-6) contains supplementary material, which is available to authorized users.
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When testing for reduction of the mean value structure in linear mixed models, it is common to use an asymptotic χ 2 test; for example that minus twice the maximized log– likelihood has an approximate χ 2 distribution under the hypothesis. Such tests can, how-ever, be very poor for small and moderate sample sizes. The pbkrtest package implements two alternatives to such approximate χ 2 –tests: The package implements a Kenward–Roger approximation for performing F –tests for reduction of the mean structure and also para-metric bootstrap methods for achieving the same goal. In addition to describing the methods and aspects of their implementation, the paper also contains several examples and comparison of the various methods.
Communicating emotions to conspecifics (emotion expression) allows the regulation of social interactions (e.g. approach and avoidance). Moreover, when emotions are transmitted from one individual to the next, leading to state matching (emotional contagion), information transfer and coordination between group members are facilitated. Despite the high potential for vocalizations to influence the affective state of surrounding individuals, vocal contagion of emotions has been largely unexplored in non-human animals. In this paper, I review the evidence for discrimination of vocal expression of emotions, which is a necessary step for emotional contagion to occur. I then describe possible proximate mechanisms underlying vocal contagion of emotions, propose criteria to assess this phenomenon and review the existing evidence. The literature so far shows that non-human animals are able to discriminate and be affected by conspecific and also potentially heterospecific (e.g. human) vocal expression of emotions. Since humans heavily rely on vocalizations to communicate (speech), I suggest that studying vocal contagion of emotions in non-human animals can lead to a better understanding of the evolution of emotional contagion and empathy.
For more than a century, functional asymmetry of the human brain was considered a matter of the lateralization of cognitive processes. Yet today most investigators would probably agree that emotional and affective processes, as well as cognitive processes, are lateralized in the brain. The inclusion of affect within the domain of cerebral laterality represents one of the most important and far-reaching consequences of the large body of research in functional brain asymmetry that has developed during the past two decades. Nevertheless, despite the evidence from many studies using a variety of laterality paradigms that affective processes are in some way lateralized, there remain major controversies as to the nature of emotional laterality. Most important, there continue to be fundamental disagreements as to exactly what is lateralized where.
It is well established that in human speech perception the left hemisphere (LH) of the brain is specialized for processing intelligible phonemic (segmental) content (e.g., [1–3]), whereas the right hemisphere (RH) is more sensitive to pro-sodic (suprasegmental) cues [4, 5]. Despite evidence that a range of mammal species show LH specialization when pro-cessing conspecific vocalizations [6], the presence of hemi-spheric biases in domesticated animals' responses to the communicative components of human speech has never been investigated. Human speech is familiar and relevant to domestic dogs (Canis familiaris), who are known to perceive both segmental phonemic cues [7–10] and supra-segmental speaker-related [11, 12] and emotional [13] proso-dic cues. Using the head-orienting paradigm, we presented dogs with manipulated speech and tones differing in segmental or suprasegmental content and recorded their orienting responses. We found that dogs showed a sig-nificant LH bias when presented with a familiar spoken command in which the salience of meaningful phonemic (segmental) cues was artificially increased but a significant RH bias in response to commands in which the salience of intonational or speaker-related (suprasegmental) vocal cues was increased. Our results provide insights into mech-anisms of interspecific vocal perception in a domesticated mammal and suggest that dogs may share ancestral or convergent hemispheric specializations for processing the different functional communicative components of speech with human listeners. Results and Discussion