Lateralized behavior and cardiac activity of dogs in response to human emotional vocalizations

Siniscalchi, Marcello; d’Ingeo, Serenella; Fornelli, Serena; Quaranta, Angelo

doi:10.1038/s41598-017-18417-4

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Published: 08 January 2018

Lateralized behavior and cardiac activity of dogs in response to human emotional vocalizations

Marcello Siniscalchi¹,
Serenella d’Ingeo¹,
Serena Fornelli¹ &
…
Angelo Quaranta¹

Scientific Reports volume 8, Article number: 77 (2018) Cite this article

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Abstract

Over the recent years, the study of emotional functioning has become one of the central issues in dog cognition. Previous studies showed that dogs can recognize different emotions by looking at human faces and can correctly match the human emotional state with a vocalization having a negative emotional valence. However, to this day, little is known about how dogs perceive and process human non-verbal vocalizations having different emotional valence. The current research provides new insights into emotional functioning of the canine brain by studying dogs’ lateralized auditory functions (to provide a first insight into the valence dimension) matched with both behavior and physiological measures of arousal (to study the arousal dimension) in response to playbacks related to the Ekman’s six basic human emotions. Overall, our results indicate lateralized brain patterns for the processing of human emotional vocalizations, with the prevalent use of the right hemisphere in the analysis of vocalizations with a clear negative emotional valence (i.e. “fear” and “sadness”) and the prevalent use of the left hemisphere in the analysis of positive vocalization (“happiness”). Furthermore, both cardiac activity and behavior response support the hypothesis that dogs are sensitive to emotional cues of human vocalizations.

Introduction

Evolutionary and ontogenetic processes played a pivotal role in dogs’ ability to detect social information from human behavior, providing the basis for complex forms of interspecific social communication^1,2. There is a growing body of literature showing that dogs developed cognitive and social abilities in order to communicate with humans. Dogs are able to interpret human communicative gestures (e.g. the direction in which humans are facing or gazing), to detect his attentional states^3,4 and to recognize different emotions by looking at human faces ^5,6. Furthermore, recent studies reported that dogs discriminate human emotional faces from neutral ones^5,6, that they are able to distinguish between happy and angry emotional human faces expressions⁷ and between the happy and neutral expression of the owner⁸. Moreover, Albuquerque et al.⁹ reported a cross-modal capacity in dogs related to the integration of visual and auditory emotional cues. In particular, dogs can correctly match “happy” or “angry” human faces with a vocalization expressing the same emotional valence.

Regarding the auditory sensory domain, it has been reported that dogs recognize the different valences of positive (laughing) and negative (crying) emotional sounds, showing an increase of indicators for arousal and negative emotional states in response to negative emotional sounds compared to positive ones¹⁰. Nevertheless, further studies are required in order to set reliable behavior indicators for positive emotional states in dogs.

To date, evidence for dogs’ perception and processing of human vocalizations characterised by different emotional valence is scarce¹¹. Considering that it has been reported that the six basic emotions universally inferred from facial expressions¹² are cross-culturally recognized from vocal signals in humans¹³, our study aimed at investigating if dogs are able to recognize the six basic emotions expressed by human non-verbal vocalizations.

In order to investigate this issue, we used the head-orienting paradigm to evaluate the potential asymmetrical behavior responses of dogs to human emotional vocalizations. The head-orienting response is commonly used as a behavior method for studying lateralized attention to acoustic stimuli in mammals tested in unrestrained conditions¹⁴. It requires sounds to be played simultaneously from two speakers located symmetrically at the same distance from the tested animal’s head. In order to ensure the correct position of the animal, the experiment is usually run during its feeding behaviors, positioning a bowl containing food midway between the two speakers. Since the head turning is an unconditioned response, its direction indicates the advantage of the contralateral hemisphere in processing the acoustic stimulus (e.g. if the subject turns his head towards the speaker with the right ear leading, the acoustic input is processed primarily by the left hemisphere, or at least in the initial attention to the stimulus^14,15,16).

Specifically, in dogs a striking left head-orienting bias was observed in response to thunderstorm playbacks, confirming the right hemisphere advantage in attending to threatening and alarming stimuli¹⁷. On the contrary, conspecific vocalizations elicited a significant head-turning bias to the right (left hemisphere advantage). The specialization of the left hemisphere in processing the vocalizations of familiar conspecifics has been also reported for other animal models, such as nonhuman primates^18,19, horses²⁰, cats²¹, and sea lions²². Nevertheless, recent studies employing the orienting paradigm in other species found an inconsistent pattern of the head-turning response to conspecific calls. For instance, Vervet monkeys showed a right hemisphere dominant activity²³ while no bias was found for Barbary macaques²⁴. Moreover, a sex-specific asymmetries was shown for mouse lemurs, in particular male individuals displayed a left hemisphere bias in response to conspecific vocalizations with negative emotional valence¹⁶. This contradictory pattern might be due to a different phylogenetic distribution of hemispheric specialization and lateralization in closely related species²⁵ or to the different emotional valence of the message conveyed. Furthermore, within the canine species, it has been reported that the left hemisphere involvement in attending to conspecific vocalizations depends on the characteristics of the sound, for example on the temporal acoustic features of the calls²⁶. When dogs were presented with the reversed versions of specific vocalizations of play, disturbance and isolation, they showed a shift in their head-orienting behavior from a right-ear orienting bias (normal call versions) to a left-ear orienting bias (play calls) or to no asymmetry (disturbance and isolation calls²⁶). In addition, recent studies describe a right hemisphere dominant activity to process conspecific vocalizations when they elicit intense emotions^17,27.

Dogs show also an asymmetric head-turning behavior in response to human vocalizations. They displayed a significant bias to turn the head with the right ear leading (left hemisphere activity) when presented with a familiar spoken command in which the salience of meaningful phonemic (segmental) cues was artificially increased; on the other hand, they showed a significant head-turning behavior to the left side (right hemisphere dominant activity) in response to commands with artificially increased salience of intonational or speaker-related (suprasegmental) vocal cues²⁸. Nevertheless, the more recent results of Andics et al.^29,30 showed the opposite pattern of the hemispheres activity. Using the fMRI technique, they found a right hemisphere advantage in processing meaningful words and a left hemispheric bias for distinguishing intonationally marked words.

Overall, although these experiments showed lateralized auditory functions in the canine brain and provide insights into mechanisms of interspecific vocal perception, it remains unclear how dogs perceive and process the six basic emotions expressed by human non-verbal vocalizations. One of the possible methods employed to assess brain emotional functioning in the animal kingdom consists in observing and analyzing physiological (e.g. cardiac activity) and behavior responses to specific stimuli in experimental conditions that resemble as much as possible the natural ones³¹. Regarding the physiological response, there is now scientific evidence that cardiac activity could be considered a valid indicator to predict different emotional states in dogs^32,33,34,35.

As to the behavior response, a recent study scored dogs’ behaviors in order to investigate emotional contagion to conspecific and human emotional sounds¹⁰. Although results indicate that for both canine and human sounds dogs express more stress behaviors after hearing sounds with a negative emotional valence, further studies are required to determine valid and reliable behavior indicators for positively valenced sounds¹⁰.

The study of behavior lateralization has the potential to provide new insights into animal emotional processing³⁶. An increasing body of evidence shows common lateralized neural patterns for emotional processing across all vertebrate classes, with specialization of the right hemisphere for processing withdrawal and negative emotions (e.g. fear and aggression) and a dominant role of the left hemisphere for processing positive emotions and approach^37,38. Thus, external manifestation of hemispheric dominance (e.g. head-turning behavior) matched with both behavior and physiological responses could represent useful tools for understanding the valence of an emotion perceived by an animal during a particular situation, facilitating the categorization of the emotion along with valence and arousal dimensions^39,40,41. In the light of this evidence, the aim of the present work was to investigate dogs’ emotional responses to human non-verbal emotional vocalizations by measuring subjects’ head-turning bias (valence dimension) and the related behavior and cardiac activities (arousal dimension).

Results

Head-orienting response

Friedman’s ANOVA revealed that there was no effect of acoustic stimulus on the % of response (χ2 (5) = 6,782, P = 0.237); average %: anger (83.3%); fear (80.0%); disgust (93.3%); sadness (76.6%); surprise (90.0%) and happiness (93.3%).

Results for the head-orienting response are shown in Fig. 1. A significant main effect of playbacks was observed (F(5,99) = 5.766, P = 0.000; GLMM analysis): pairwise comparisons revealed that this main effect was due to “happiness” vocalization being significantly different from other sounds (“happiness” vs. “fear”, “anger” and “sadness” (P = 0.000); “happiness” vs. “disgust” (P = 0.009) and “surprise” (P = 0.026); Fisher’s LSD). In addition, the analysis revealed that for “fear” and “sadness” call types, dogs consistently turned their head with the left ear leading (“fear”: Z = 140.000, P = 0.039; “sadness”: Z = 102.000, P = 0.046; One-Sample Wilcoxon Signed Ranks Test) (see Fig. 1). A very similar trend was observed for “anger” vocalization even if not statistically significant (Z = 221.000, P = 0.072). On the other hand, a significant right bias in the head turning response was found when dogs attended to playbacks of “happiness” (Z = 46.000, P = 0.003). No statistical significant biases were found for both “disgust” and “surprise” stimuli (P > 0.05, One-Sample Wilcoxon Signed Ranks Test). On investigating possible methodological confounding factors, a binomial GLMM analysis revealed that the direction of head orienting response turns was not significantly influenced by vocalization gender (F(1,99) = 0.102, P = 0.750) and playback order (F(6,93) = 0.705, P = 0.646). In addition no effects of sex (F(1,99) = 0.306, P = 0.581), age (F(1,99) = 0.000, P = 0.998) and temperament questionnaire scores were observed (P > 0.05 for all queries of the questionnaire, see Table 1).

Table 1 Questionnaire queries. Effects of questionnaire queries on “Orienting Response”, “HV”, “LV”, “AUC”, “AAC” and “Stress” variables (df1 = 1; df2 = 136; GLMM analysis).

Full size table

Reactivity and latency to resume feeding

The cumulative incidences of reactivity and latency to resume feeding during playbacks’ presentations are presented in Fig. 2(A,B). As for reactivity, mixed effects Cox regression revealed that subjects hearing “anger” playbacks had a higher probability to react than after attending, respectively, playbacks of happiness (β(SE) = 0.93(0.37); [Exp(β) = 0.39; 95%-CI = 0.19;0.81]; P = 0.012), “disgust” (β(SE) = 1.16(0.43); [Exp(β) = 0.31; 95%-CI = 0.13;0.74]; P = 0.008) and “sadness” (β(SE) = 1.13(0.39); [Exp(β) = 0.32; 95%-CI = 0.15;0.69]; P = 0.004) see Fig. 2(A–C). The probability to react to the stimuli was increased in male subjects with respect to females (β(SE) = 0.52(0.24); [Exp(β) = 0.59; 95%-CI = 0.37;0.95]; P = 0.031) while it was decreased as age increased (B(SE) = −0.1(0.047); [Exp(β) = 0.90; 95%-CI = 0.82;0.99]; P = 0.033). A primary effect of the first playback has been observed since the probability to react was increased if the sound was presented after respectively “anger” (β(SE) = 0.69(0.34); [Exp(β) = 1.99; 95%-CI = 1.03;3.85]; P = 0.041) and “surprise” acoustic stimuli (β(SE) = 0.77(0.37); [Exp(β) = 2.17; 95%-CI = 1.04;4.5]; P = 0.038); on the other hand, the probability to react was lower if the sound was presented after “sadness” stimulus (β(SE) = −1.51(0.54); [Exp(β) = 0.22; 95%-CI = 0.07;0.63]; P = 0.005). Finally, there were effects of stress behaviors and query scales, since the probability to react to playbacks increased with increasing scores of stress behaviors during the test (β(SE) = 0.25(0.08); [Exp(β) = 1.28; 95%-CI = 1.08;1.51]; P = 0.003) and increasing scores of excitability in the query (β(SE) = 0.07(0.03); [Exp(β) = 0.39; 95%-CI = 1.00;1.14]; P = 0.048). Finally, the probability to react to vocalizations sounds decreased with increasing scores of “stranger aggression” in the query (β(SE) = −0.06(0.02); [Exp(β) = 0.94; 95%-CI = 0.89;0.99]; P = 0.019).

As for the latency to resume feeding, mixed effects Cox regression revealed that dogs hearing “anger” had smaller probability to resume feeding than when they were hearing respectively “happiness” (β(SE) = −1.30(0.33); [Exp(β) = 3.70; 95%-CI = 1.91;7.15]; P = 0.000), “fear” (β(SE) = −0.73(0.32); [Exp(β) = 2.07; 95%-CI = 1.10;3.90]; P = 0.023), “disgust” (β(SE) = −1.28(0.34); [Exp(β) = 3.59; 95%-CI = 1.84;7.05]; P = 0.000) and “sadness” (β(SE) = −1.15(0.35); [Exp(β) = 3.16; 95%-CI = 1.58;6.33]; P = 0.001) (see Fig. 2B–D). The probability to resume feeding after hearing the sounds decreased as age increased (β(SE) = −0.08(0.04); [Exp(β) = 0.91; 95%-CI = 0.85;0.98]; P = 0.024). As expected, there were effects of stress behaviors and query scales, since the probability to resume feeding decreased with increasing scores of stress behaviors during the test (β(SE) = −0.28(0.08); [Exp(β) = 0.75; 95%-CI = 0.64;0.88]; P = 0.001) and increasing scores of respectively trainability (β(SE) = −0.06(0.03); [Exp(β) = 0.94; 95%-CI = 0.88;0.99]; P = 0.042), excitability (β(SE) = −0.05(0.02); [Exp(β) = 0.94; 95%-CI = 0.90;0.99]; P = 0.040) and pain sensitivity (β(SE) = −0.11(0.04); [Exp(β) = 0.89; 95%-CI = 0.81;0.98]; P = 0.019) in the query.

Cardiac activity

Results for cardiac activity are shown in Fig. 3. The highest (HV) and lowest values (LV) of the Heart Rate (HR) response to different playbacks were analyzed. Moreover, the area delimited by the HR curve and the HR basal average (baseline) was computed for each dog and the Area Under Curve (above baseline and under curve, AUC) and the Area Above Curve (under baseline and above curve, AAC) were then obtained. No statistically significant differences were observed between acoustic stimuli regarding higher heart rate values (GLMM analysis): emotional category: (F(5,131) = 1.449, P = 0.211; see Fig. 3A); playback order (F(6,131) = 0.966, P = 0.451); vocalization gender (F(1,131) = 0.419, P = 0.518); sex (F(1,131) = 0.023, P = 0.881); age (F(1,131) = 3.431, P = 0.066;) and questionnaire scales (P > 0.05 for all queries of the questionnaire, see Table 1).

Regarding lower heart rate values (see Fig. 3A), a statistically significant effect of age was observed F(1,131) = 6.701, P = 0.011; GLMM analysis), showing that adult subjects have higher rate to have lower LV values after attending to emotional playbacks (β(SE) = −2.44(0.94); [95%-CI = −4.30; −0.57]). In addition, the analysis revealed that subjects with higher scores for both “owner aggression” (β(SE) = 6.97(2.02); [95%-CI = 2.97;10.98]; P = 0.001) and “separation related behaviors” (β(SE) = 1.46(0.58); [95%-CI = 0.31;2.61]; P = 0.013) queries had lower values of LV after hearing emotional vocalizations (see Table 1). No other statistically significant effects were observed regarding lower heart values: emotion category (F(5,131) = 0.796 P = 0.554; GLMM analysis); vocalization gender (F(1,131) = 0.136, P = 0.712); playback order (F(6,131) = 0.960, P = 0.493); sex (F(1,131) = 1.379, P = 0.242); questionnaire scales (P > 0.05 for all others queries of the questionnaire, see Table 1).

A significant main effect of playbacks was observed in the overall increase of the heart rate values compared to the baseline (see Fig. 3B, AUC) (i.e. the area above baseline and under curve (F(5,131) = 4.242, P = 0.001) after controlling for the effect of playback order (F(6,131) = 1.485, P = 0.188) and vocalization gender (F(1,131) = 1.586, P = 0.210) (GLMM analysis): pairwise comparisons revealed that the AUC values were higher for “anger” stimulus than for the other emotional vocalizations: “anger” vs. “sadness” (P = 0.000); “anger” vs. “happiness” (P = 0.001); “anger” vs. “fear” (P = 0.002); “anger” vs. “surprise” (P = 0.017) and “anger” vs. “disgust” (P = 0.049). In addition, the analysis revealed that “disgust” stimulus induced higher AUC values than “sadness” (P = 0.008). No effects of sex (F(1,131) = 0.096, P = 0.757) and age (F(1,131) = 1.761, P = 0.187) were found. As to the questionnaire, the analysis revealed a statistically significant effect of query 6 indicating that the higher the scores for “attachment or attention-seeking behaviors”, the more likely dogs had lower AUC values after attending vocalizations (β(SE) = −52.877(26.104); [95%-CI = −104.518;−1.235]; P = 0.045); on the other hand, subjects with higher scores for “non-social fear” (β(SE) = 75.632(31.393; [95%-CI = 13.529;137.736]; P = 0.017) and “trainability” (β (SE) = 72.847(34.963); [95%-CI = 3.681;142.013]; P = 0.038) had higher AUC values after hearing emotional playbacks. No other statistically significant effects were found (P > 0.05 for all the remaining queries of the questionnaire, see Table 1).

Regarding the overall decrease of the heart rate values compared to the baseline (i.e. the area under baseline and above curve, AAC), the GLMM analysis revealed that the higher the scores for trainability, the more likely dogs had lower AAC values (β(SE) = −27.611(10.678); [95%-CI = −48.736; −6.487]; P = 0.011) (see Table 1).

No other statistical significant effects were observed in AAC values: emotional category (F(5,131) = 0.304, P = 0.910; GLM analysis) (Fig. 3B); vocalization gender (F(1,131) = 0.006, P = 0.941); playback order (F(6,131) = 0.928, P = 0.477); sex (F(1,131) = 0.806, P = 0.371); age (1,131) = 0.237, P = 0.627) and query scales (P > 0.05 for all the rest queries of the questionnaire, see Table 1).

Behavior score

As to behavioral score, analysis of the stressed behavioral category revealed that there was a significant difference between acoustic stimuli (F(5,131) = 10.851, P = 0.000; GLMM analysis, see Fig. 4) after controlling for the effect of both playback order (F(6,131) = 0.840, P = 0.541), vocalization gender (F(1,131) = 2.128, P = 0.147) and age (F(1,131) = 0.420, P = 0.518). A statistically significant effect of sex was observed (F(1,131) = 4.994, P = 0.027) indicating that male subjects have lower rate compared to females to display lower rate to display stress behaviors after attending to emotional playbacks (β(SE) = −0.44(0.19); [95%-CI = −0.82; −0.05]; P = 0.027). Post hoc pairwise comparisons revealed that dogs showed more stress-related behavior when they attended to “anger” and “fear” playbacks than to the others sounds, (“anger” “vs. “surprise” and “disgust” (P = 0.000); “anger” vs. “sadness” (P = 0.001); “anger” vs. “happiness” (P = 0.004); “fear” vs. “disgust” and “surprise” (P = 0.000); “fear” vs. “sadness” (P = 0.002); “fear” vs. “happiness” (P = 0.004); Fisher’s LSD). In addition stressed behavioral score was higher for “happiness” than “disgust” (P = 0.006). Finally, pairwise comparisons revealed higher stress behavioral scores while hearing the playbacks of “sadness” than “disgust” (P = 0.026) (see Fig. 4). Significant positive relationships were found between stress levels and queries 1 (β(SE) = 0.05(0.02); [95%-CI = 0.01;0.09]; P = 0.007) and 4 (β(SE) = 0.05(0.04); [95%-CI = 0.00;0.10]; P = 0.045; GLMM analysis) of temperament questionnaire scores indicating that the stronger the “aggressiveness to strangers” and “non social fear”, the more likely dogs have higher stress levels when attending to playbacks sounds (see Table 1).

Finally, tail-wagging behavior was observed during five occasions and 3 of these occurred after “surprise” and 2 after “happiness” sounds. In addition, after “surprise” playbacks dogs approached the speakers 2 times (given the low frequency of these observed behaviors, statistical analysis was not performed).

Discussion

Previous studies have reported that dogs’ olfactory system works in an asymmetrical way to decode different emotions conveyed by human odors³². Our results demonstrate that this asymmetry is also manifested in the auditory sensory domain since dogs showed an asymmetrical head-orienting response to the playbacks of different human non-verbal emotional vocalizations. In particular, they turned the head with their left ear leading in response to “fear” and “sadness” human vocalizations. Given that in the head-orienting paradigm the head-turning direction indicates an advantage of the contralateral hemisphere in processing sounds¹⁴, the left head turning in response to “fear” and “sadness” vocalizations here reported suggests the prevalent activation of the right hemisphere. This finding is consistent with the general hypothesis of the right hemisphere dominant role in the analysis of intense emotional stimuli (e.g. horse^42,43,44; dog⁴⁵). Other evidences come from studies on cats, showing that, using the same head-orienting paradigm, they turned the head with their left ear leading in response to dogs’ “disturbance” and “isolation” vocalizations²¹.

Furthermore, dogs’ right hemisphere activation to process stimuli of negative emotional valence has also been reported by studies on motor functions (e.g. tail wagging behavior, see Siniscalchi et al.³⁵) and on sensory domains (e.g. vision⁴⁶; olfaction⁴⁷). Specifically, a bias to the left side (right hemisphere) in the head-turning response has been observed when dogs were presented with visual alarming stimuli (i.e. black silhouette of a snake and of a cat displaying an agonistic aversive posture⁴⁶) and a right nostril preferential use (right hemisphere) to investigate conspecific “isolation” odours³². Our data from the arousal dimension indicate that although both “sadness” and “fear” vocalizations are processed mainly by the right hemisphere, after hearing “sadness” playbacks dogs were less stressed than after hearing “fear” (see scattergrams, Fig. 5). The latter could be explained by the fact that despite both “fear” and “sadness” vocalizations are characterized by negative valence, they can differ on the functional and communicative level. In some individuals, “sadness” vocalizations could be clearly an approach evoking call while “fear” vocalizations could produce a different reaction in the receiver (approach/withdrawal) depending on the social context in which it is produced and perceived. However, considering the communicative function of these vocalizations, it could be hypothesized that the “fear” ones may elicit stronger reactions in the listener, explaining the higher arousal and stress behaviors registered in response to this vocalization. Moreover, in the light of recent findings^48,49, the higher arousal and stressed behaviors showed by dogs after hearing “fear” vocalizations, which is a higher-arousal emotion compared to “sadness”, suggest the occurrence of a cross-species emotional contagion between human and dogs. Nevertheless, further investigations are needed to address this issue.

As Fig. 3 shows, there was a clear tendency for dogs to turn their head to the left side in response to “anger” playbacks, but it didn’t reach statistical significance. Previous studies hypothesized that dogs perceive the “anger” emotion to have a negative emotional valence⁵⁰. It has been recently reported indeed that dogs showed a left gaze bias while looking at human negative facial expressions (angry faces), suggesting the right hemisphere involvement in processing the emotional message conveyed⁵¹. Furthermore, dogs looked preferentially at the lower face region of unfamiliar humans showing a negative expression (“sadness” and “angry”), avoiding consequently an eye contact with a potential threatening stimulus⁵⁰. The high emotional valence attributed to the anger emotion is also attested by the longer time employed to correctly associate a reward to a human angry face rather than a happy one⁷. One possible explanation for the weaker left orienting bias observed in response to the “anger” vocalizations with respect to “fear” and “sadness”, is that these sounds displayed an acoustic feature resembling the one of canine “threatening growls” (harsh, low frequency call). Although the emotional valence of this canine vocalization is similar to the “anger” one (most likely eliciting a right hemisphere activity), overall, a specialization of the left hemisphere for processing conspecific vocalizations has been observed¹⁷. In addition, fMRI studies identified two auditory regions in the dog brain, one bilaterally located and the other one in the left dorsal auditory cortex, both responding selectively to conspecific sounds⁵². Hence, it cannot be entirely ruled out the possibility that some subjects might have misinterpreted the “anger” vocalizations, categorizing them as a conspecific call. As a consequence, this phenomenon might have produced a sort of left hemisphere “interference” in processing the sound. On the other hand, as results for the head orienting response to “anger” sounds were marginally significant, it would be interesting to test this condition in future studies using a larger sample of dogs in order to verify if the lack of statistical significance is only a question of statistical power.

Regarding the “happiness” vocalization”, a clear right bias in the head-orienting response (left hemisphere advantage) was observed. Previous studies have reported a left-hemisphere specialization for approach behavior⁵³. Specifically in dogs, a left-brain activation was indirectly observed throughout asymmetric tail wagging movements to the right side in response to stimuli that could be expected to elicit approach tendencies, such as seeing the owner¹¹. Thus, the involvement of the left hemisphere in the analysis of “happiness” vocalizations suggests that dogs perceived this sound as an expression of a positive emotional state that could elicit approaching behaviors, having a central role in the beginning and maintaining the dog-human interaction (note that tail wagging behaviors were observed during “happiness” playbacks). This evidence is supported by recent fMRI studies indicating a left bias for more positive human sounds⁵² and an increase of functional connectivity in the left hemisphere in response to positive rewarding speech compared to neutral one²⁹.

Overall, results from latency to resume feeding, cardiac activity and stress levels suggested that hearing “happiness” vocalization induced, as expected, low arousal levels with respect to hearing “fear” and “anger” but not “sadness”. The latter suggests that relying solely on the arousal dimension would not make it clear to distinguish between the emotions conveyed by sadness and happiness vocalizations (see scattergrams, Fig. 5). In dogs, this hypothesis is supported by recent findings that indicate that parasympathetic deactivation (i.e. arousal increasing) is associated with a more positive emotional state elicited by different positive stimuli (food or social rewards³³).

Regarding “surprise” and “disgust” vocalizations, we found no biases in dogs’ head-turning response. This result may suggest that the dogs perceived these sounds to be less distinguishable than the others in terms of both emotional valence and degree of familiarity. In particular, concerning the “disgust” vocalizations, our results fit in with the hypothesis of Turcsàn et al.⁸ about the ambiguous valence that this emotion could have for dogs. In everyday life, different objects or situations eliciting a “disgust” emotion in the owner could be attractive for the dog (e.g. feaces) or, on the contrary, could be associated with a negative outcome (e.g. scolding). Thus, dogs’ behavior responses (approaching or withdrawal) and the emotional valence attributed (negative or positive) could be strictly dependent on the individual experiences. Regarding surprise, evidence from human studies reported that this emotion could be perceived as both positive and negative, depending on the goal conduciveness of the surprising event⁵⁴ (note that in our experiments, during hearing surprise sounds, although the arousal levels were similar to those observed in response to sadness, tail wagging behavior and approaching behaviors to the speaker were observed). More interestingly, recent cognitive and psychophysiological studies indicate the possibility that surprise may be a (mildly) negative emotion⁵⁵. The latter would be very similar to the slight left orienting (but not statistically significant) bias (right-hemisphere activation) observed here in dogs.

Overall, our results provide evidences about the existence of an emotional modulation of the dog brain to process basic human non-verbal emotional vocalizations. In particular, results from our experiments have shown that dogs process human emotional vocalizations in an asymmetrical way, predominantly using the right hemisphere in response to vocalizations with a clear negative emotional valence (i.e. “fear” and “sadness”) and the left hemisphere in response to “happiness” playbacks. In addition, both cardiac activity and behavior response support the hypothesis that dogs are sensitive to emotional cues of human vocalizations, indicating that coupling the use of valence and arousal dimensions is a useful tool to deeply investigate brain emotional functioning in the animal kingdom.