Content uploaded by Christian Nawroth
Author content
All content in this area was uploaded by Christian Nawroth on Mar 04, 2019
Content may be subject to copyright.
Available via license: CC BY-NC 4.0
Content may be subject to copyright.
Article
Perceptual lateralization of vocal stimuli
in goats
Luigi BACIADONNA
a,
*, Christian NAWROTH
a,b
, Elodie F. BRIEFER
c
, and
Alan G. MCELLIGOTT
a,d,
*
a
Biological and Experimental Psychology, School of Biological and Chemical Sciences, Queen Mary University of
London, Mile End Road, London E1 4NS, UK,
b
Institute of Behavioural Physiology, Leibniz Institute for Farm Animal
Biology, Dummerstorf, Germany,
c
Institute of Agricultural Sciences, ETH Zu¨rich, Universita¨tstrasse 2, 8092 Zu¨rich,
Switzerland, and
d
Department of Life Sciences, University of Roehampton, London SW15 4JD, UK
*Address correspondence to Luigi Baciadonna, E-mail: luigi.baciadonna@gmail.com; and Alan G. McElligott;
E-mail: alan.mcelligott@roehampton.ac.uk.
Handling editor: Zhi-Yun Jia
Received on 23 July 2017; accepted on 9 March 2018
Abstract
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
V
CThe Author(s) 2018. Published by Oxford University Press on behalf of Editorial Office, Current Zoology. 67
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/),
which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact
journals.permissions@oup.com
Current Zoology, 2019, 65(1), 67–74
doi: 10.1093/cz/zoy022
Advance Access Publication Date: 16 March 2018
Article
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
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, http://www.buttercups.org.uk; 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
2
) 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
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
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 sounddog.com), 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.
2017).
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
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
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
above.
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
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
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.
Results
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 (z¼3.36, 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
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
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
17
¼2.15,
P¼0.046) compared with chance level (i.e., 0.50). Goats thus
showed a general right bias in their head-orienting responses.
Discussion
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
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
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.
Acknowledgments
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.
buttercups.org.uk) 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.
References
Andics A, 2017. Erratum for the report “Neural mechanisms for lexical pro-
cessing in dogs” by A. Andics, A. Ga´bor, M. Ga´csi, T. Farago´ , D. Szabo´, A.
Miklo´ si. Science 356:eaan3276.
Andics A, Ga´ csi M, Farago´ T, Kis A, Miklo´ si A, 2014. Report voice-sensitive
regions in the dog and human brain are revealed by comparative fMRI. Curr
Biol 24:574–578.
Andics A, Ga´ bor A, Ga´ csi M, Farago´ T, Szabo´ D et al., 2016. Neural mechan-
isms for lexical processing in dogs. Science 353:1030–1032.
Andics A, Ga´ csi M, Farago´ T, Kis A, Miklo´ si A, 2017. Corrections
voice-sensitive regions in the dog and human brain are revealed by compara-
tive fMRI. Curr Biol 27:1248–1249.
Association for the Study of Animal Behaviour, 2016. Guidelines for the treat-
ment of animals in behavioural research and teaching. Anim Behav 111:
I–IX.
Baruzzi C, Nawroth C, McElligott AG, Baciadonna L, 2017. Motor asym-
metry in goats during a stepping task. Laterality, doi:
10.1080/1357650X.2017.1417993.
Basile M, Boivin S, Boutin A, Blois-Heulin C, Hausberger M et al., 2009.
Socially dependent auditory laterality in domestic horses Equus caballus.
Anim Cogn 12:611–619.
Beausoleil NJ, Stafford KJ, Mellor DJ, 2005. Sheep show more aversion to a
dog than to a human in an arena test. Appl Anim Behav Sci 91:219–232.
Boersma P, Weenink D, 2009. Praat: doing phonetics by computer [cited 2018
February 24]. Available from: http://www.praat.org/.
Bo¨yeM, Gu¨ntu¨ rku¨ n O, Vauclair J, 2005. Right ear advantage for conspecific
calls in adults and subadults, but not infants, California sea lions Zalophus
californianus: hemispheric specialization for communication? Eur J
Neurosci 21:1727–1732.
Briefer EF, 2018. Vocal contagion of emotions in non-human animals. Proc R
Soc B 285:20172783.
Briefer E, McElligott AG, 2011a. Mutual mother-offspring vocal recognition
in an ungulate hider species Capra hircus.Anim Cogn 14:585–598.
Briefer E, McElligott AG, 2011b. Indicators of age, body size and sex in goat
kid calls revealed using the source-filter theory. Appl Anim Behav Sci 133:
175–185.
Briefer EF, McElligott AG, 2012. Social effects on vocal ontogeny in an ungu-
late, the goat Capra hircus.Anim Behav 83:991–1000.
Briefer EF, Tettamanti F, McElligott AG, 2015. Emotions in goats: mapping
physiological, behavioural and vocal profiles. Anim Behav 99:131–143.
Craig AD, 2005. Forebrain emotional asymmetry: a neuroanatomical basis?
Trends Cogn Sci 9:566–571.
de Waal FBM, 2008. Putting the altruism back into altruism: the evolution of
empathy. Annu Rev Psychol 59:279–300.
Baciadonna et al. Acoustic laterality in goats 73
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
Demaree HA, Everhart DE, Youngstrom EA, Harrison DW, 2005. Brain lat-
eralization of emotional processing: historical roots and a future incorporat-
ing “dominance.” Behav Cogn Neurosci Rev 4:3–20.
Ehrlichman H, 1987. Hemispheric asymmetry and positive-negative affect. In:
Ottoson D, editor. Duality and Unity of the Brain. Boston (MA): Springer
US, 194–206.
Fitch RH, Miller S, Tallal P, 1997. Neurobiology of speech perception. Annu
Rev Neurosci 20:331–353.
Friederici AD, Alter K, 2004. Lateralization of auditory language functions: a
dynamic dual pathway model. Brain Lang 89:267–276.
Ghazanfar AA, Hauser MD, 1999. The neuroethology of primate vocal com-
munication: substrates for the evolution of speech. Trends Cogn Sci 3:
377–384.
Gil-da-Costa R, Hauser MD, 2006. Vervet monkeys and humans show brain
asymmetries for processing conspecific vocalizations, but with opposite pat-
terns of laterality. Proc R Soc B 273:2313–2318.
Gygax L, Reefmann N, Wolf M, Langbein J, 2013. Prefrontal cortex activity,
sympatho-vagal reaction and behaviour distinguish between situations of
feed reward and frustration in dwarf goats. Behav Brain Res 239:104–114.
Hauser MD, Andersson K, 1994. Left hemisphere dominance for processing
vocalizations in adult, but not infant, rhesus monkeys: field experiments.
Proc Natl Acad Sci USA 91:3946–3948.
Heffner HE, Heffner RS, 1984. Temporal lobe lesions and perception of
species-specific vocalizations by macaques. Science 226:75–76.
Halekoh U, Højsgaard S, 2014. A Kenward-Roger approximation and para-
metric bootstrap methods for tests in linear mixed models the R package
pbkrtest. J Stat Softw 59:1–32.
Ocklenburg S, Stro¨ ckens F, Gu¨ntu¨ rku¨ n O, 2011. Lateralisation of conspecific
vocalisation in non-human vertebrates. Laterality 18:1–31.
Petersen MR, Beecher MD, Zoloth SR, Moody DB, Stebbins WC, 1978.
Neural lateralization of species-specific vocalizations by Japanese macaques
Macaca fuscata.Science 202:324–327.
Pitcher BJ, Briefer EF, Baciadonna L, Mcelligott AG, 2017. Cross-modal rec-
ognition of familiar conspecifics in goats. R Soc Open Sci 4:160346.
Poremba A, Malloy M, Saunders RC, Carson RE, Herscovitch P et al., 2004.
Species-specific calls evoke asymmetric activity in the monkey’s temporal
poles. Nature 427:448–451.
Quaranta A, Siniscalchi M, Vallortigara G, 2007. Asymmetric tail-wagging re-
sponses by dogs to different emotive stimuli. Curr Biol 17:R199–R201.
Ratcliffe VF, Reby D, 2014. Orienting asymmetries in dogs’ responses to differ-
ent communicatory components of human speech. CurrBiol 24:2908–2912.
Reimert I, Bolhuis JE, Kemp B, Rodenburg TB, 2013. Indicators of positive and
negative emotions and emotional contagion in pigs. Physiol Behav 109:42–50.
Reimert I, Bolhuis JE, Kemp B, Rodenburg BT, 2015. Emotions on the loose:
emotionalcontagion and the role of oxytocin inpigs. Anim Cogn 18:517–532.
Reinholz-Trojan A, Włodarczyk E, Trojan M, Kulcz NA, Stefa´ NJ, 2012.
Hemispheric specialization in domestic dogs Canis familiaris for processing
different types of acoustic stimuli. Behav Processes 91:202–205.
Rogers L, Andrew R, 2002. Comparative Vertebrate Lateralization.
Cambridge (UK): Cambridge University Press.
Rogers LJ, Deng C, 2005. Corticosterone treatment of the chick embryo af-
fects light-stimulated development of the thalamofugal visual pathway.
Behav Brain Res 159:63–71.
Rogers LJ, Zucca P, Vallortigara G, 2004. Advantages of having a lateralized
brain. Proc R Soc B 271:S420–S422.
Scheumann M, Zimmermann E, 2005. Do mouse lemurs show asymmetries in
handedness and the perception of communication calls? Primate Rep 72:84–85.
Schier AF, 2003. Nodal Signaling in vertebrate development. Annu Rev Cell
Dev Biol 19:589–621.
Silberman EK, Weingartner H, 1986. Hemispheric lateralization of functions
related to emotion. Brain Cogn 5:322–353.
Siniscalchi M, Quaranta A, Rogers LJ, 2008. Hemispheric specialization in
dogs for processing different acoustic stimuli. PLoS ONE 3:e3349.
Siniscalchi M, Sasso R, Pepe AM, Vallortigara G, Quaranta A, 2010. Dogs
turn left to emotional stimuli. Behav Brain Res 208:516–521.
Teufel C, Hammerschmidt K, Fischer J, 2007. Lack of orienting asymmetries
in Barbary macaques: implications for studies of lateralized auditory pro-
cessing. Anim Behav 73:249–255.
Tucker DM, 1981. Lateral brain function, emotion, and conceptualization.
Psychol Bull 89:19–46.
Vallortigara G, 2007. The evolutionary psychology of left and right: costs and
benefits of lateralization. Dev Psychobiol 48:832–840.
Vallortigara G, Rogers LJ, 2005. Survival with an asymmetrical brain: advantages
and disadvantages of cerebral lateralization. Behav Brain Sci 28:575–589.
Waller BM, Warmelink L, Liebal K, Micheletta J, Slocombe KE, 2013.
Pseudoreplication: a widespread problem in primate communication re-
search. Anim Behav 86:483–488.
74 Current Zoology, 2019, Vol. 65, No. 1
Downloaded from https://academic.oup.com/cz/article-abstract/65/1/67/4939480 by guest on 04 March 2019
