Dog and human neural sensitivity to voicelikeness: A comparative fMRI study.

Voice-sensitivity in the auditory cortex of a range of mammals has been proposed to be determined primarily by tuning to conspecific auditory stimuli, but recent human findings indicate a role for a more general tuning to voicelikeness. Vocal emotional valence, a central characteristic of vocalisations, has been linked to the same basic acoustic parameters across species. Comparative neuroimaging revealed that during voice perception, such acoustic parameters modulate emotional valence-sensitivity in auditory cortical regions in both family dogs and humans. To explore the role of voicelikeness in auditory emotional valence-sensitivity across species, here we constructed artificial emotional sounds in two sound categories: voice-like vs. sine-wave sounds, parametrically modulating two main acoustic parameters, f0 and call length. We hypothesised that if mammalian auditory systems are characterised by a general tuning to voicelikeness, voice-like sounds will be processed preferentially, and acoustic parameters for voice-like sounds will be processed differently than for sine-wave sounds - both in dogs and humans. We found cortical areas in both species that responded stronger to voice-like than to sine-wave stimuli, while there were no regions responding stronger to sine-wave sounds in either species. Additionally, we found that in bilateral primary and emotional valence-sensitive auditory regions of both species, the processing of voice-like and sine-wave sounds are modulated by f0 in opposite ways. These results reveal functional similarities between evolutionarily distant mammals for processing voicelikeness and its effect on processing basic acoustic cues of vocal emotions.

Speech naturalness detection and language representation in the dog brain.

Family dogs are exposed to a continuous flow of human speech throughout their lives. However, the extent of their abilities in speech perception is unknown. Here, we used functional magnetic resonance imaging (fMRI) to test speech detection and language representation in the dog brain. Dogs (n = 18) listened to natural speech and scrambled speech in a familiar and an unfamiliar language. Speech scrambling distorts auditory regularities specific to speech and to a given language, but keeps spectral voice cues intact. We hypothesized that if dogs can extract auditory regularities of speech, and of a familiar language, then there will be distinct patterns of brain activity for natural speech vs. scrambled speech, and also for familiar vs. unfamiliar language. Using multivoxel pattern analysis (MVPA) we found that bilateral auditory cortical regions represented natural speech and scrambled speech differently; with a better classifier performance in longer-headed dogs in a right auditory region. This neural capacity for speech detection was not based on preferential processing for speech but rather on sensitivity to sound naturalness. Furthermore, in case of natural speech, distinct activity patterns were found for the two languages in the secondary auditory cortex and in the precruciate gyrus; with a greater difference in responses to the familiar and unfamiliar languages in older dogs, indicating a role for the amount of language exposure. No regions represented differently the scrambled versions of the two languages, suggesting that the activity difference between languages in natural speech reflected sensitivity to language-specific regularities rather than to spectral voice cues. These findings suggest that separate cortical regions support speech naturalness detection and language representation in the dog brain.

The acoustic bases of human voice identity processing in dogs.

Speech carries identity-diagnostic acoustic cues that help individuals recognize each other during vocal-social interactions. In humans, fundamental frequency, formant dispersion and harmonics-to-noise ratio serve as characteristics along which speakers can be reliably separated. The ability to infer a speaker's identity is also adaptive for members of other species (like companion animals) for whom humans (as owners) are relevant. The acoustic bases of speaker recognition in non-humans are unknown. Here, we tested whether dogs can recognize their owner's voice and whether they rely on the same acoustic parameters for such recognition as humans use to discriminate speakers. Stimuli were pre-recorded sentences spoken by the owner and control persons, played through loudspeakers placed behind two non-transparent screens (with each screen hiding a person). We investigated the association between acoustic distance of speakers (examined along several dimensions relevant in intraspecific voice identification) and dogs' behavior. Dogs chose their owner's voice more often than that of control persons', suggesting that they can identify it. Choosing success and time spent looking in the direction of the owner's voice were positively associated, showing that looking time is an index of the ease of choice. Acoustic distance of speakers in mean fundamental frequency and jitter were positively associated with looking time, indicating that the shorter the acoustic distance between speakers with regard to these parameters, the harder the decision. So, dogs use these cues to discriminate their owner's voice from unfamiliar voices. These findings reveal that dogs use some but probably not all acoustic parameters that humans use to identify speakers. Although dogs can detect fine changes in speech, their perceptual system may not be fully attuned to identity-diagnostic cues in the human voice.

Comparative Brain Imaging Reveals Analogous and Divergent Patterns of Species and Face Sensitivity in Humans and Dogs.

Conspecific-preference in social perception is evident for multiple sensory modalities and in many species. There is also a dedicated neural network for face processing in primates. However, the evolutionary origin and the relative role of neural species sensitivity and face sensitivity in visuo-social processing are largely unknown. In this comparative study, species sensitivity and face sensitivity to identical visual stimuli (videos of human and dog faces and occiputs) were examined using functional magnetic resonance imaging in dogs (n = 20; 45% female) and humans (n = 30; 50% female). In dogs, the bilateral mid suprasylvian gyrus showed conspecific-preference, no regions exhibited face-preference, and the majority of the visually-responsive cortex showed greater conspecific-preference than face-preference. In humans, conspecific-preferring regions (the right amygdala/hippocampus and the posterior superior temporal sulcus) also showed face-preference, and much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Multivariate pattern analyses (MVPAs) identified species-sensitive regions in both species, but face-sensitive regions only in humans. Across-species representational similarity analyses (RSAs) revealed stronger correspondence between dog and human response patterns for distinguishing conspecific from heterospecific faces than other contrasts. Results unveil functional analogies in dog and human visuo-social processing of conspecificity but suggest that cortical specialization for face perception may not be ubiquitous across mammals.SIGNIFICANCE STATEMENT To explore the evolutionary origins of human face-preference and its relationship to conspecific-preference, we conducted the first comparative and noninvasive visual neuroimaging study of a non-primate and a primate species, dogs and humans. Conspecific-preferring brain regions were observed in both species, but face-preferring brain regions were observed only in humans. In dogs, an overwhelming majority of visually-responsive cortex exhibited greater conspecific-preference than face-preference, whereas in humans, much of the visually-responsive cortex showed greater face-preference than conspecific-preference. Together, these findings unveil functional analogies and differences in the organizing principles of visuo-social processing across two phylogenetically distant mammal species.

Social relationship-dependent neural response to speech in dogs.

In humans, social relationship with the speaker affects neural processing of speech, as exemplified by children's auditory and reward responses to their mother's utterances. Family dogs show human analogue attachment behavior towards the owner, and neuroimaging revealed auditory cortex and reward center sensitivity to verbal praises in dog brains. Combining behavioral and non-invasive fMRI data, we investigated the effect of dogs' social relationship with the speaker on speech processing. Dogs listened to praising and neutral speech from their owners and a control person. We found positive correlation between dogs' behaviorally measured attachment scores towards their owners and neural activity increase for the owner's voice in the caudate nucleus; and activity increase in the secondary auditory caudal ectosylvian gyrus and the caudate nucleus for the owner's praise. Through identifying social relationship-dependent neural reward responses, our study reveals similarities in neural mechanisms modulated by infant-mother and dog-owner attachment.

Who turns to the human? Companion pigs' and dogs' behaviour in the unsolvable task paradigm.

When facing an unsolvable problem, dogs exhibit spontaneous human-oriented behaviours (e.g. looking at the human partner, gaze alternations between the human and the target) sooner and for longer than domestic cats and hand-raised wolves. These behaviours have been interpreted as interspecific communicative acts aimed to initiate interaction. Here, we compare the emergence of human-oriented behaviours (e.g. orientation towards humans, orientation alternations, vocalizations) in similarly raised family dogs and miniature pigs utilising an unsolvable task paradigm which consists of Baseline (no task), Solvable and Unsolvable phases. Relative to the Baseline phase in which both species showed human-oriented behaviours to a similar extent, during the Unsolvable phase dogs showed more and pigs showed less such behaviours. Species-predispositions in communicative behaviour may explain why dogs have a higher inclination than pigs to initiate interspecific interactions with humans in problem-solving contexts.

Comparing interspecific socio-communicative skills of socialized juvenile dogs and miniature pigs.

Previous research proves dogs' outstanding success in socio-communicative interactions with humans; however, little is known about other domestic species' interspecific skills when kept as companion animals. Our aim was to assess highly socialized young miniature pigs' spontaneous reactions in interactions with humans in direct comparison with that of young family dogs. All subjects experienced similar amount of socialization in human families. In Study 1, we investigated the appearance of human-oriented behaviours without the presence of food (Control condition) when a previously provided food reward was withheld (Food condition). In Study 2, we measured responsiveness to two types of the distal pointing gesture (dynamic sustained and momentary) in a two-way object choice test. In the Control condition of Study 1, the duration of pigs' and dogs' orientation towards and their frequency of touching the human's body was similar. In the Food condition, these behaviours and orienting to the human's face were intensified in both species. However, pigs exhibited face-orientation to an overall lesser extent and almost exclusively in the Food condition. In Study 2, only dogs relied spontaneously on the distal dynamic-sustained pointing gesture, while all pigs developed side bias. The results suggest that individual familiarization to a human environment enables the spontaneous appearance of similar socio-communicative behaviours in dogs and pigs, however, species predispositions might cause differences in the display of specific signals as well as in the success of spontaneously responding to certain types of the human pointing gestures.

Humans rely on the same rules to assess emotional valence and intensity in conspecific and dog vocalizations.

Humans excel at assessing conspecific emotional valence and intensity, based solely on non-verbal vocal bursts that are also common in other mammals. It is not known, however, whether human listeners rely on similar acoustic cues to assess emotional content in conspecific and heterospecific vocalizations, and which acoustical parameters affect their performance. Here, for the first time, we directly compared the emotional valence and intensity perception of dog and human non-verbal vocalizations. We revealed similar relationships between acoustic features and emotional valence and intensity ratings of human and dog vocalizations: those with shorter call lengths were rated as more positive, whereas those with a higher pitch were rated as more intense. Our findings demonstrate that humans rate conspecific emotional vocalizations along basic acoustic rules, and that they apply similar rules when processing dog vocal expressions. This suggests that humans may utilize similar mental mechanisms for recognizing human and heterospecific vocal emotions.

Domestication and exposure to human social stimuli are not sufficient to trigger attachment to humans: a companion pig-dog comparative study.

Dogs exhibit human-analogue attachment to their owners, with similar function and mechanisms to that of infant-mother bond, but its origin is unclear. Comparative studies on socialised wolves and dogs emphasise genetic influence in dogs' preparedness for attachment to humans. We aimed to reveal if this genetic effect stems from general domestication or artificial selection that increased dogs' dependence on humans. We assessed and compared behavioural patterns of young companion pigs and dogs using a Strange Situation Test. Dogs but not pigs exhibited distinct behaviours towards their owner and a stranger along attachment-specific variables, so only dogs' relevant behaviours fulfilled attachment criteria. From the observed behaviours, three factors were formed: Attachment (to the owner), Anxiety (in a strange situation), and Acceptance (of a stranger). Results indicate (1) higher Attachment scores in dogs than pigs, (2) greater Acceptance scores in pigs, (3) positive correlation of Attachment and Anxiety in both, (4) similar time tendency of pigs' Attachment and Acceptance scores. These suggest that in pigs, domestication and early exposure to human social stimuli did not trigger attachment to humans. Thus, along with species predispositions, the unique dog-owner attachment can be facilitated by artificial selection that increased dogs' dependence on humans.

Neural evidence for referential understanding of object words in dogs.

Using words to refer to objects in the environment is a core feature of the human language faculty. Referential understanding assumes the formation of mental representations of these words.1,2 Such understanding of object words has not yet been demonstrated as a general capacity in any non-human species,3 despite multiple behavior-based case reports.4,5,6,7,8,9,10 In human event-related potential (ERP) studies, object word knowledge is typically tested using the semantic violation paradigm, where words are presented either with their referent (match) or another object (mismatch).11,12 Such mismatch elicits an N400 effect, a well-established neural correlate of semantic processing.12,13 Reports of preverbal infant N400 evoked by semantic violations14 assert the use of this paradigm to probe mental representations of object words in nonverbal populations. Here, measuring dogs' (Canis familiaris) ERPs to objects primed with matching or mismatching object words, we found a mismatch effect at a frontal electrode, with a latency (206-606 ms) comparable to the human N400. A greater difference for words that dogs knew better, according to owner reports, further supported a semantic interpretation of this effect. Semantic expectations emerged irrespective of vocabulary size, demonstrating the prevalence of referential understanding in dogs. These results provide the first neural evidence for object word knowledge in a non-human animal. VIDEO ABSTRACT.

Success in the Natural Detection Task is influenced by only a few factors generally believed to affect dogs' olfactory performance.

Research into dogs' olfactory ability is growing rapidly. However, generalising based on scientific results is challenging, because research has been typically conducted on a few specially trained subjects of a few breeds tested in different environmental conditions. We investigated the effects of temperature and humidity (outdoors), age, test location, sex, neutering status, and repeated testing (outdoors and indoors) on the olfactory performance of untrained family dogs (N = 411) of various breeds. We employed the Natural Detection Task with three difficulty levels, from which we derived two performance metrics: Top Level and Success Score. Temperature (0-25 °C) and humidity (18-90%) did not affect olfactory performance. Young adult dogs surpassed other age groups in reaching the Top Level. Sex and neutering status showed no discernible influence on Top Level and Success Score. Dogs performed better in both metrics when tested indoors compared to outdoors. In the test-retest procedure no significant learning effect was observed. We confirmed on untrained companion dogs that olfactory performance declines with age and rejected some factors that have been previously hypothesised to significantly affect dogs' olfactory success. The influence of the testing environment was notable, emphasising the need to consider various factors in understanding dogs' olfactory capabilities.

Mean-based neural coding of voices.

The social significance of recognizing the person who talks to us is obvious, but the neural mechanisms that mediate talker identification are unclear. Regions along the bilateral superior temporal sulcus (STS) and the inferior frontal cortex (IFC) of the human brain are selective for voices, and they are sensitive to rapid voice changes. Although it has been proposed that voice recognition is supported by prototype-centered voice representations, the involvement of these category-selective cortical regions in the neural coding of such "mean voices" has not previously been demonstrated. Using fMRI in combination with a voice identity learning paradigm, we show that voice-selective regions are involved in the mean-based coding of voice identities. Voice typicality is encoded on a supra-individual level in the right STS along a stimulus-dependent, identity-independent (i.e., voice-acoustic) dimension, and on an intra-individual level in the right IFC along a stimulus-independent, identity-dependent (i.e., voice identity) dimension. Voice recognition therefore entails at least two anatomically separable stages, each characterized by neural mechanisms that reference the central tendencies of voice categories.

FMRI repetition suppression for voices is modulated by stimulus expectations.

According to predictive coding models of sensory processing, stimulus expectations have a profound effect on sensory cortical responses. This was supported by experimental results, showing that fMRI repetition suppression (fMRI RS) for face stimuli is strongly modulated by the probability of stimulus repetitions throughout the visual cortical processing hierarchy. To test whether processing of voices is also affected by stimulus expectations, here we investigated the effect of repetition probability on fMRI RS in voice-selective cortical areas. Changing ('alt') and identical ('rep') voice stimulus pairs were presented to the listeners in blocks, with a varying probability of alt and rep trials across blocks. We found auditory fMRI RS in the nonprimary voice-selective cortical regions, including the bilateral posterior STS, the right anterior STG and the right IFC, as well as in the IPL. Importantly, fMRI RS effects in all of these areas were strongly modulated by the probability of stimulus repetition: auditory fMRI RS was reduced or not present in blocks with low repetition probability. Our results revealed that auditory fMRI RS in higher-level voice-selective cortical regions is modulated by repetition probabilities and thus suggest that in audition, similarly to the visual modality, processing of sensory information is shaped by stimulus expectation processes.

Out-of-reach rewards elicit human-oriented referential communicative behaviours in family dogs but not in family pigs.

Human-oriented referential communication has been evidenced not only in domestic but also in some wild species, however, the importance of domestication-unrelated species' characteristics in the emergence of this capacity remains largely unexplored. One shared property of all species reported to exhibit referential communication is the efficient use of visual social signals. To assess the potential role of species-specific characteristics in the emergence of human-oriented referential communication, we compared similarly socialised companion animals from two domestic species: dogs, which rely heavily on conspecific visual social signals; and pigs, which do not. We used an out-of-reach reward paradigm with three conditions: both human and reward present, only human present, only reward present. Both species exhibited certain behaviours (e.g. orientation towards the human, orientation alternation between the human and the reward) more often in the human's presence. However, only dogs exhibited those behaviours more often in the simultaneous presence of the human and the reward. These results suggest similar readiness in dogs and pigs to attend to humans but also that pigs, unlike dogs, do not initiate referential communication with humans. The ability to referentially communicate with humans may not emerge in mammals, even if domesticated companion animals, that lack certain species characteristics, such as efficient intraspecific visual communication.

Investigating responses to object-labels in the domestic dog (Canis familiaris).

Since the dawn of comparative cognitive research, dogs were suspected to possess some capacity for responding to human spoken language. Neuroimaging studies have supported the existence of relevant mechanisms, but convincing behavioral performance is rare, with only few exceptional dogs worldwide demonstrating a lexicon of object-labels they respond to. In the present study we aimed to investigate if and how a capacity for processing verbal stimuli is expressed in dogs (N = 20), whose alleged knowledge of verbal labels is only backed-up by owner reports taken at face value, and concerning only a few words (on average 5). Dogs were tested in a two-choice paradigm with familiar objects. The experiment was divided into a cue-control condition (objects visible to the owner vs. shielded by a panel, thereby controlling the owner's ability to emit cues to the dog) and a response type condition (fetching vs. looking). Above chance performance in fetching and looking at the named object emerged on the level of the sample as a whole. Only one individual performed reliably above chance, but the group-level effect did not depend on this data point. The presence of the panel also had no influence, which supports that performance was not driven by non-verbal cues from the owners. The group-level effect suggests that in typical dogs object-label learning is an instable process, either due to the animals primarily engaging in contextual learning or possibly analogous to the early stages of implicit, statistical learning of words in humans and opposed to the rapid mapping reported in exceptional dogs with larger passive vocabulary.

Dog brains are sensitive to infant- and dog-directed prosody.

When addressing preverbal infants and family dogs, people tend to use specific speech styles. While recent studies suggest acoustic parallels between infant- and dog-directed speech, it is unclear whether dogs, like infants, show enhanced neural sensitivity to prosodic aspects of speech directed to them. Using functional magnetic resonance imaging on awake unrestrained dogs we identify two non-primary auditory regions, one that involve the ventralmost part of the left caudal Sylvian gyrus and the temporal pole and the other at the transition of the left caudal and rostral Sylvian gyrus, which respond more to naturalistic dog- and/or infant-directed speech than to adult-directed speech, especially when speak by female speakers. This activity increase is driven by sensitivity to fundamental frequency mean and variance resulting in positive modulatory effects of these acoustic parameters in both aforementioned non-primary auditory regions. These findings show that the dog auditory cortex, similarly to that of human infants, is sensitive to the acoustic properties of speech directed to non-speaking partners. This increased neuronal responsiveness to exaggerated prosody may be one reason why dogs outperform other animals when processing speech.

Representation of rewards differing in their hedonic valence in the caudate nucleus correlates with the performance in a problem-solving task in dogs (Canis familiaris).

We have investigated dogs' (Canis familiaris) abilities in associating different sounds with appetitive stimuli of different incentive values. The association's establishment was first tested on family dogs (n = 20) in a problem-solving behavioural paradigm (experiment 1), then in a problem-solving behavioural paradigm as well as an fMRI study on specially trained family dogs (n = 20) (experiment 2). The aim was to show behavioural and parallel neural effects of the association formed between the two sounds and two different associated appetitive stimuli. The latency of solving the problem was considered an indicator of the motivational state. In our first experiment, where only behaviour was studied, we found that dogs were quicker in solving a problem upon hearing the sound associated with food higher in reward value, suggesting that they have successfully associated the sounds with the corresponding food value. In our second experiment, this behaviour difference was not significant. In the fMRI study, the cerebral response to the two sounds was compared both before and after the associative training. Two bilateral regions of interest were explored: the caudate nucleus and the amygdala. After the associative training, the response in the caudate nucleus was higher to the sound related to a higher reward value food than to the sound related to a lower reward value food, which difference was not present before the associative training. We found an increase in the amygdala response to both sounds after the training. In a whole-brain representational similarity analysis, we found that cerebral patterns in the caudate nucleus to the two sounds were different only after the training. Moreover, we found a positive correlation between the dissimilarity index in the caudate nucleus for activation responses to the two sounds and the difference in latencies (i.e. high reward value associated sound condition latency-low reward value associated sound condition latency) to solve the behavioural task: the bigger the difference between the conditions in latency to solve the task, the greater the difference in the neural representation of the two sounds was. In summary, family dogs' brain activation patterns reflected their expectations based on what they learned about the relationship between two sounds and their associated appetitive stimuli.

Genetic distance from wolves affects family dogs' reactions towards howls.

Domestication dramatically changes behaviour, including communication, as seen in the case of dogs (Canis familiaris) and wolves (Canis lupus). We tested the hypothesis that domestication may affect an ancient, shared communication form of canids, the howling which seems to have higher individual variation in dogs: the perception and usage of howls may be affected by the genetic relatedness of the breeds to their last common ancestor with wolves ('root distance') and by other individual features like age, sex, and reproductive status. We exposed 68 purebred dogs to wolf howl playbacks and recorded their responses. We identified an interaction between root distance and age on the dogs' vocal and behavioural responses: older dogs from more ancient breeds responded longer with howls and showed more stress behaviours. Our results suggest that domestication impacts vocal behaviour significantly: disintegrating howling, a central, species-specific communication form of canids and gradually eradicating it from dogs' repertoire.

Neural processes underlying statistical learning for speech segmentation in dogs.

To learn words, humans extract statistical regularities from speech. Multiple species use statistical learning also to process speech, but the neural underpinnings of speech segmentation in non-humans remain largely unknown. Here, we investigated computational and neural markers of speech segmentation in dogs, a phylogenetically distant mammal that efficiently navigates humans' social and linguistic environment. Using electroencephalography (EEG), we compared event-related responses (ERPs) for artificial words previously presented in a continuous speech stream with different distributional statistics. Results revealed an early effect (220-470 ms) of transitional probability and a late component (590-790 ms) modulated by both word frequency and transitional probability. Using fMRI, we searched for brain regions sensitive to statistical regularities in speech. Structured speech elicited lower activity in the basal ganglia, a region involved in sequence learning, and repetition enhancement in the auditory cortex. Speech segmentation in dogs, similar to that of humans, involves complex computations, engaging both domain-general and modality-specific brain areas. VIDEO ABSTRACT.

Rapid learning of object names in dogs.

Learning object names after few exposures, is thought to be a typically human capacity. Previous accounts of similar skills in dogs did not include control testing procedures, leaving unanswered the question whether this ability is uniquely human. To investigate the presence of the capacity to rapidly learn words in dogs, we tested object-name learning after four exposures in two dogs with knowledge of multiple toy-names. The dogs were exposed to new object-names either while playing with the objects with the owner who named those in a social context or during an exclusion-based task similar to those used in previous studies. The dogs were then tested on the learning outcome of the new object-names. Both dogs succeeded after exposure in the social context but not after exposure to the exclusion-based task. Their memory of the object-names lasted for at least two minutes and tended to decay after retention intervals of 10 min and 1 h. This reveals that rapid object-name learning is possible for a non-human species (dogs), although memory consolidation may require more exposures. We suggest that rapid learning presupposes learning in a social context. To investigate whether rapid learning of object names in a social context is restricted to dogs that have already shown the ability to learn multiple object-names, we used the same procedure with 20 typical family dogs. These dogs did not demonstrate any evidence of learning the object names. This suggests that only a few subjects show this ability. Future studies should investigate whether this outstanding capacity stems from the exceptional talent of some individuals or whether it emerges from previous experience with object name learning.