Genes Brain and Behavior - 2018 - Ferretti - Understanding Others Emotion Recognition in Humans and Other Animals
Genes Brain and Behavior - 2018 - Ferretti - Understanding Others Emotion Recognition in Humans and Other Animals
Genes Brain and Behavior - 2018 - Ferretti - Understanding Others Emotion Recognition in Humans and Other Animals
DOI: 10.1111/gbb.12544
REVIEW
In this review, we will attempt to identify and understand com- achieved by the understanding of nonverbal facial expression of emo-
mon aspects of emotion expression and perception among animals. tions in others. This involves perceptual processing, which identifies
We provide a comparative perspective of the approaches used to geometric configurations of facial expressions, and the recognition of
study human and other animal emotion recognition ability, describing the emotional value of a stimulus.9
© 2018 John Wiley & Sons Ltd and International Behavioural and Neural Genetics Society
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2 of 12 FERRETTI AND PAPALEO
Relevantly, deficits in this cognitive domain are early and distinc- Nevertheless, the amygdala represents the main area on which
10–12
tive features of several psychiatric disorders. For example, abnor- most of emotional research converges.49,56–59 Contrary to the tradi-
malities in social cue identification are the defining characteristics of tional view, which identifies to this region a role in the processing of
autism spectrum disorder, are evident in schizophrenia, and can be threat and fear-specific stimuli,59–66 recent research also implicates
observed as a consequence of brain lesions and neurodegenerative the amygdala in the evaluation of positively valenced emotional stim-
diseases.13–18 Importantly, effective treatments for deficits in social uli, such as happy or surprised expressions36,67–75 with qualitatively
cognitive aspects are still missing. different responses. Through its broad pattern of connectivity with
Emotion recognition tasks are the most extensively used para- cortical and subcortical structures, the amygdala might play a broader
digms to assess human social cognition.14,15 These tests evaluate the role in the recognition of emotions, detecting and processing socially
ability of subjects to identify emotions depicted on static photographs salient cues.76 These findings have also been corroborated by neuro-
or dynamic reproductions of different facial expressions. One of the imaging studies associating dysfunctions in negative and positive
most validated set of expressions is the “Ekman's Faces,” which emotions processing in neuropsychiatric patients, with alterations in
depicts the faces of actors displaying the six basic emotions (disgust, amygdala responses.17,77–79
19–21
anger, fear, surprise, sadness and happiness ). To provide graded Additionally, a number of brain areas and connective pathways
levels of difficulty and address diverse severity levels of potential defi- implicated in emotion perception and processing require further
cits, emotions are presented in a range of intensity and in a combina- investigation. It is possible that within the same brain region there are
tion of different experimental designs.10,15,22–26 circuit- or cell-specific heterogeneities that control different aspects
Relevantly, most of our knowledge on the neural substrates of of emotion recognition and processing. This level of investigation is
emotion recognition derives from the use of similar tests in patients still unreachable in humans. Thus, the opportunity to investigate the
with brain lesions and from functional neuroimaging studies in healthy biological substrates of different social cognitive aspects in other
subjects and patients.9,17,27 Despite some level of heterogeneity, mammals (rodents in primis but also nonhuman primates) has the
mostly due to methodological factors, these studies indicate that the potential to improve our understanding of social dysfunctions, favor-
ability to recognize socially relevant information does not depend on
ing more focused and efficient therapeutic strategies.
restricted localized neuronal ensemble, but requires a network of neu-
ral systems which process the perception of social signals, and con-
nect this information with brain areas devoted to motivation, emotion 3 | EM O TI O N R E CO GN I T I ON I N
and adaptive behaviors.28–32 NONHUMAN ANIMALS
Functional models of facial expression processing propose that
the brain structures involved in face identification are anatomically The ability to express and perceive emotions is crucial not just for
separated from those involved in recognizing emotional humans. As a way to share experiences and communicate
expressions.33–35 Codifying identities involve the participation of intentions,8,80,81 it allows to better adapt to environmental challenges
areas implicated in the perception of static facial features, as the fusi- increasing survival chances.82 Emotion recognition ability is shared by
form face area in the ventral temporal lobes.32,36–40 Processing of a number of social species including nonhuman primates, horses, dogs
dynamic facial cues, as emotional expressions, requires regions as the and sheep.83–86 In rodents, despite the growing interest in emotional
9,34,41
inferior occipital gyrus and the superior temporal sulcus (STS ). research, this ability has not been directly assessed.
Different lines of research support the idea that there might be some Communication of emotions strongly depends on the species.87
level of functional overlap and that these regions could cooperate in Accordingly, the ability to perceive emotions has been investigated
the representation of different facial aspects (for a review see42). with species-specific behavioral settings, which we describe in the fol-
The way salient visual cues, with affective and motivational signif- lowing sections.
icance, are integrated at the level of brain circuits has been matter of
investigation and debate in the last decades. One of the most estab-
3.1 | Nonhuman Primates
lished hypotheses implicates the amygdala as a rapid cortex-
independent system, not mediated by conscious awareness.43–47 Nonhuman primates live in societies of multiple individuals and are
Emotional stimuli, via the amygdala's influence on cortical sensory capable of complex social behaviors such as coalitions, postconflict
processing, would modulate attention and perception, particularly in affiliations and helping behaviors.88–91 One of the primary processes
dangerous situations.48–50 required for such complex social functions is the ability to recognize
Views challenging this hypothesis suggest that visual information emotions in others. There is large agreement that nonhuman primates,
might proceed by a similarly fast processing, simultaneously along par- such as humans, are able to use facial gestures5–7,84,92–98 to communi-
allel channels, which engage multiple brain sites, including the amyg- cate positive and negative emotions, with homologies to human
dala, orbital frontal cortices, anterior insula and anterior cingulate expressions. It is still not clear, however, how and to what extent pri-
51,52
cortex, among others. mates perceive others' expression of emotions. Study limitations
Discussing the contribution of these and other brain regions might arise from the diverse range of species used, varied protocols,
implicated in the diverse aspects of emotion recognition is complex small sample sizes, inconsistent age and sex among subjects and the
and beyond the scope of this review, but this topic has been the focus lack of a common metric for describing facial expressions across dif-
of previous outstanding reviews.9,15,30,31,42,53–55,258 ferent species. Emotion recognition has been studied exposing
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FERRETTI AND PAPALEO 3 of 12
subjects to drawings,92,99 static images, movies or real-life movement of the facial muscles surrounding the eye) to infer emo-
84,100
conspecifics, in association with eye-gaze scanning of the sub- tional states.85,86,127 Interestingly, both species showed adaptive
jects or match-to-sample protocols. 3D animation system modeled on behavioral responses, showing more avoidance for agonistic or
the human Facial Action Coding System (FACS)21,101 identified muscle stressed expressions compared to neutral ones.85,128
activity as a critical element in emotion discrimination.102 Together, Conspecific emotion recognition abilities have been identified
these studies highlighted that, like humans, nonhuman primates are also in domesticated dogs, whose facial displays involve various com-
able to recognize conspecific's emotions and to process facial expres- binations of movements of the ears, mouth, lips and eye-gaze
sions categorically, organizing information around discrete emotion shifts.129,130 In particular, combining the exposure to visual and audi-
categories.92 Similar to humans,103 information achieved by observing tory cue Albuquerque et al.83 showed that dogs are able to integrate
others' emotions has been shown to be used in an adaptive way, to information from different sensory signals, and to create an internal
predict future actions or scenarios, and to guide behavioral multimodal representation of categorized emotions, as previously
choices.104–106 shown in humans and monkeys.131,132
Electrophysiological studies on monkeys have provided functional Recent research, focused on the nature of the interaction with
information on emotion recognition neuronal substrates, and showed humans, showed that dogs are also able to discern information from a
some overlap in the brain regions human and nonhuman primates use variety of human signals.83,130,133–136 This evidence supports the idea
to processes facial expressions of emotions. Cells responding to facial that dogs, like horses, sheep,85,137 macaques and bonobos,104,138
expressions have been identified in different cortical regions. In partic- show heterospecific emotion recognition abilities. In particular, they
ular, the STS and the amygdala have been shown to respond to facial can all discriminate emotions in subjects of another species, suggest-
expressions1,41,107–109 with levels of specificity differing among differ- ing that this social cognitive ability evolved not just to directly guaran-
110–112 69,73
ent studies. Consistent with human evidence, the majority tee survival through intragroup interactions, but also to sustain proper
of neurophysiology studies indicate that cells in the amygdala evaluate evolutionary interspecies interactions.
stimuli with both negative and positive valence, but draw a sharp dif-
ference between them, showing different activation patterns.112–115 3.3 | Rodents
Recognition of emotional facial expressions can be considered an
Understanding how rodents interact, and which are the key compo-
initial step, in some case predictive, of empathic responses.116,117 Rel-
nents that regulate their sociability is a central question in neurosci-
evantly, in monkeys, neurons responding to facial expressions with
ence. Indeed, rodents are currently the most widely used laboratory
affiliative value (lip smacking) have been documented among mirror
animal species with preferential access to numerous advanced tech-
neurons of the F5 in the ventral premotor cortex.118 This finding,
nologies (e.g. clustered regularly interspaced short palindromic repeats
together with other evidence of premotor cortex involvement in facial
119 (CRISPR), flox- and cre-lines, opto- and chemo-genetics) to investigate
emotion perception, supports the hypothesis that the activation of
with genetic-, cell- and circuit-level specificity the mechanisms under-
the brain areas involved in the perception of other's expressions might
lying complex behaviors.
be involved in matching other's affective states.120
Most rodents are social animals, living substantial parts of their
Findings at the single-unit level, together with functional imaging
lives in groups of variable size and displaying a rich repertoire of social
evidence in humans, are clarifying the contribution and specificity of
behaviors. Similar to humans and to the other animal species
selective neurons in emotion processing leading to new interpreta-
described above, rodents have been recently shown to be able to per-
tions about the roots of complex cognitive functions. More functional
ceive and react to the emotional state of conspecifics,123,139–147 and
knowledge on the role of brain circuits could be achieved by the use
in some cases, to produce complex pro-social behaviors possibly
of appropriate emotion-based paradigms in rodents, as indicated by
related to empathy.122,148,149 However, research on rodent emotion
recent findings, which support the existence of conserved brain sub-
recognition in settings similar to the ones described above is still
strate among species.121–126
underdeveloped. In the next sections, we will discuss a number of dif-
ferent behavioral paradigms that, in different ways, imply recognition
3.2 | Horses, sheep and dogs of expression of emotions in rodents.
The ability to perceive emotional information from facial expressions
was initially attributed exclusively to species with sophisticated orofa- 3.3.1 | Rats
5,6
cial motor systems such as humans and nonhumans primates. How- One of the first evidence that rodents could recognize and react to
ever, different studies indicate that other species, characterized by the emotional state of a conspecific comes from an experiment show-
living in stable social groups, and presenting highly developed visual ing that rats, trained in a lever-press task to receive food, suspended
systems, such as horses, sheep and dogs, are able to understand and this reward-motivated behavior when the lever-press action was asso-
react to expressions of emotions in conspecifics' faces. Relevantly, ciated with an electric shock delivered to a conspecific, visible from
these species use facial features (in particular eyes and ears) to display across a barrier.142 The psychological process at the base of this
emotional information. By using an adapted version of the human behavior was later defined as emotional contagion and refers to the
FACS21,85,127 and life-size photographs, it was found that, similar to ability of a subject to match its emotional state to the one of a con-
humans, both horses and sheep are able to perceive informative sig- specific in pain or distress.139,140,150,151 The most studied type of
nals (in particular the amount of sclera visible, pupil dilation and the emotional contagion, called “vicarious freezing,” is represented by a
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4 of 12 FERRETTI AND PAPALEO
freezing response observed in a rat witnessing a conspecific being In particular, prairie voles exhibited increased allogrooming (lick-
139,151
shocked and displaying fear responses. Relevantly, this form of ing and grooming behavior) toward a cage-mate, which was separately
social communication mostly highlighted between cage-mate conspe- exposed to a fear-conditioning protocol. Consolation behavior did not
cifics has been shown to depend on a variety of social and nonsocial require the pre-exposure of the observer to the shock experience, but
151
factors, such as housing conditions (isolated vs group ) and to a pre- was shown to strongly depend on familiarity between individuals. This
vious experience of the observer with the pain.139 work has also highlighted oxytocin signaling pathways as common
Emotion contagion, described also in humans82,152 and nonhuman neuronal substrates of consolation in prairie voles,122 consistent with
primates,153,154 is considered an automatic response. Promoting the human findings.171–174 Thus, among rodents, the development of new
mimicking of facial or body expressions in response to a relevant genetic technologies specifically for prairie voles might open the way
experience, it facilitates the transfer of information among individuals for more mechanistic insights related to pair bond.175
and consequently leads to adaptation.82
Rats have been shown to perceive and react to changes in the 3.3.3 | Mice
emotional state of conspecifics even when freezing responses induced Like other mammals, mice show complex social behaviors as well as a
by emotion contagion were not directly implicated.124,144,155,156 In high level of reciprocal social interaction. The numerous social tasks
particular, the exposure of an observer rat to a cage-mate demonstra- that have been developed and that are currently available for mice
tor, which experienced a fear-conditioning protocol immediately allow efficient assessment of reciprocal social exploration, communal
before, induced increased social approach and allogroming toward the nesting, sexual and parenting behaviors, territorial scent marking,
144
stressed rats, indicative of affective response. Using a similar aggressiveness, social memory for familiar/unfamiliar conspecifics,
approach in unfamiliar conspecific, Rogers-Carter et al.124 reported social hierarchies and motivation toward social stimuli.176–182 How-
that the choice to approach or avoid a recently shocked demonstrator ever, studies confirming emotion recognition abilities in mice are rela-
was dependent on its age, as stressed juvenile rats induced increased tively scarce compared to rats and prairie voles. In particular, there is
social exploration, while adults induced the opposite effect. not yet evidence that mice can show similar pro-social, pair bond or
In recent years, a number of paradigms have been developed consolatory behaviors as reported above. In the seminal work of Lang-
based on the evidence that emotions, fear in particular, can be used ford et al.,183 an observer mouse was exposed to a conspecific in pain,
by rodents as a way to transmit information with an adaptive after the injection of abdominal acetic acid. Witnessing the pain of
value.103,123,144,157–160 In rats, social interaction and information another was sufficient to increase the individual response to the same
exchange with a previously conditioned cage-mate, was shown to experience. Relevantly, modulation of pain sensitivity, later confirmed
increase fear responses of the observer in a subsequent-conditioning by other studies,184–186 was found to be regulated by the degree of
144
paradigm and to induce fear in relation to a tone cue predictive of relatedness between the interacting individuals.183,186
distress in others but otherwise benign.157 Relevantly, the ‘fear condi- Emotional contagion of fear has also been shown to occur in
tioning by-proxy’ protocol, 157,161
described in more detail in this same mice,123,143,187,188 and to be dependent on several aspects such as
issue by Monfils and Agee 162
has been found to be modulated by genetic background,141 familiarity,123,143 social context and sta-
social factors, such as familiarity161 and dominance status: subordi- tus159,189 and on previous experience of the shock by the observer.188
nate subjects show increased responses when fear-associations are Mice are able to learn by observing others' emotions (fear) in a variety
transmitted by a dominant conspecific.163 of conditions: fear association to a cue can be learned by observing a
Together, these findings clearly indicate that rats are able not just conspecific experiencing classical fear conditioning.123,141,190 Simi-
to perceive and automatically react to other's emotions, but also to larly, in socially learned predator recognition, previously described in
show affective responses, and learn new associations by socially inter- primates,153,191 birds and fishes,192,193 Kavaliers et al.194,195 found
acting with conspecific emotional responses. The importance of rec- that observer mice, exposed to a demonstrator attacked by biting flies,
ognizing emotional states in rats is supported and extended by a are able to learn self-burying avoidance responses by simple observa-
number of studies in which the detection of distress in a conspecific tion. Thus, similar to other animals, mice seem to be able to recognize
was followed by spontaneous pro-social responses, such as helping in altered emotional states in conspecifics and to use socially transmitted
148,149,164–167
freeing from a restraint or delivering food. A review of information in an adaptive way.
pro-social evidence in rodents in relation to empathy-related behav- Emotional contagion of pain and fear has been associated with
iors has been recently discussed in References.145,147,148 automatic adaptive responses that do not require self-other
differentiation,196,197 and do not imply affective behavior. Relevantly,
3.3.2 | Prairie voles behavioral tests designed to assess this function in rodents produced
The prairie vole (Microtus ochrogaster) is a rodent species character- similar responses in rats, prairie voles and mice. Differently, the ability
ized by high sociability and monogamous behavior.168,169 Prairie vole to distinguish self from other is a key feature of what has been called
ability to perceive the emotional state of conspecifics was recently “emotional empathy”,147 in which state matching between subjects
highlighted in a study, which, for the first time, described consolation can occur, but more relevantly, modulation by cognitive processes is
behavior in rodents.122 Consolation, previously studied in humans, involved. This modulation can lead to affective/pro-social behaviors
88,170
nonhuman primates, elephants and canines, is defined as an such as helping behaviors and consolation. Similar behaviors have
increase in affiliative behavior directed toward a distressed individual. been so far described in rats and prairie voles,122,148,149,164–167 but
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FERRETTI AND PAPALEO 5 of 12
not in mice. Whether mice are capable of processes implying self- rodents might express emotions, and whether these signals are per-
other differentiation leading to complex social responses induced by ceived and used by conspecifics.
emotional states of conspecifics is still an open question.
It is possible that different protocols might be required to high- 4.2 | Olfaction
light the boundaries of social cognition in mice. The use of detailed
As one of the oldest sensory modalities, olfaction occupies a unique
description and quantification of the diverse subpopulations of sub-
position in emotion communication. In neuroanatomical terms, odor
jects which show determined social features (as done for example in
information has a direct connection to brain areas (such as the amyg-
rats studies124,157), has the potential to add depth to mouse social
dala, the hippocampus and orbitofrontal cortex among others)
cognition studies, highlighting possible underestimated social behav-
strongly associated with emotion processing and survival responses,
iors, and favoring personality/genetic traits. An important lesson to be
both in humans and other animals.209–213 In human emotion recogni-
considered from previous studies on nonsocial cognitive functions is
tion tasks, odors have been identified as critical factors modulating
that behavioral paradigms in rats cannot be always equivalently trans-
the perception and coding of facial expressions. Anxiety- or fear-
lated to mice. Thus, behavioral tests should be developed considering
related chemosignals have been shown to improve the perception of
the different ethological characteristics of these two rodent species.
related expressions and interfere with the perception of opposite
expressions.214–216
4 | E M O T I ON RE C O G N I T I O N S E N S O RY In rodents, investigating the causal contribution of olfactory cues
C HA N N E L S in emotion communication presents some technical challenges. Para-
digms using invasive approaches, such as lesions or chemical nasal
Based on human characteristics, research on emotion recognition has administration (such as zinc sulfate,217), might not be appropriate for
primarily focused on visual parameters. Using similar tests across sophisticated behavioral analysis as they have profound physical side
social species allows the investigation of the evolutionary roots of a effects.
specific function and its neuronal substrates. In highly social species Studies on olfactory cues mainly focused on the observation of the
strongly relying on visual cues, such as primates, horses, sheep and autonomic or behavioral responses induced by the exposure to the odor
dogs, emotion recognition ability involves the integration of multi- of conspecifics in a negative emotional state.218,219 For example, rats
modal signals,83,198,199 with vision playing the primary role. More chal- trained in a lever-press paradigm have been shown to suspend an ongo-
lenging is to understand how emotional states are communicated and ing response when air from the cage of stressed conspecifics was intro-
perceived in rodents, which are nocturnal animals and evolutionarily duced into the test chamber. The odor of unstressed rats, instead,
might rely less on visual cues and more on other sensory systems. In produced no behavioral change, indicating that rats can distinguish con-
the next sections, we discuss the relevance of different sensory specific odors on the base of their emotional valence.220 Similarly, a
modalities in emotion processing. number of evidence suggests that mice react to the odors of conspe-
cifics in altered emotional states: mice avoid an alley filled with the odor
4.1 | Vision of a stressed mouse,221 while showing interest for a new neutral
odor.222 Notably, behavioral responses toward odors of stressed con-
Detection of visual cues can drive very fast adaptive behavioral
specifics appear to be influenced by social and environmental factors:
responses. In humans and primates, visual cues represent the primary
mice individually exposed to the odor of a stressed mouse, in a tube,
modality to recognize others' emotions, which has fostered the devel-
show avoidance, but, conversely, show complex responses (such as
opment of the great variety of facial expressions.84,200
increased arousal, sampling of the surrounding air and rearing) when
In rodents, vision mediates a number of behavioral responses
housed with peers in their home cage.223
linked to emotion perception, such as defense behavior201 and threat
avoidance.194,202 Similarly, emotion contagion has been show to
depend on visual cues.183 However, the visual signals conveying emo-
4.3 | Hearing
tional information are scarcely explored. A small number of studies Modulation of facial expressions perception by auditory cues has been
have described facial expression in mice and rats, mostly as indicators observed both at behavioral and cerebral level in human and nonhu-
of animal welfare or reward processing.203–207 Whether these expres- man primates.198,224 In particular, neuronal responses in the amygdala
sions are perceived as relevant cues by conspecifics has not been have been shown to integrate crossmodal sensory cues during emo-
determined yet. Similarly, information is poor about the perception of tion perception.224
conspecific body postures, which in rodents are largely used to com- Rodents are able to communicate using distinct types of sound
municate states or intention during a social encounter (such as pain, signals, the majority of which are not audible to humans as they are
pleasure, playful attitudes or dominant/submissive intentions). emitted in the ultrasonic range (USVs). While in both rat and mice
A recent study employed machine-learning software to capture USVs happen particularly in the presence of conspecifics,225–229 evi-
and categorize mouse posture modules in 3D imaging of mice behav- dence in the literature suggests that this mode of communication
ing in a variety of experimental contexts. The work showed body lan- could be more relevant for signaling emotional changes for rats than
208
guage modules that are not detectable by human eye. The use of for mice. The study of the behavioral responses of receiver conspe-
similar systematic approaches will be highly relevant to describe how cifics to specific USV frequencies is important to understand how
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6 of 12 FERRETTI AND PAPALEO
emotional information is conveyed by these signals. The emission of described, from humans to mice.122,123,139,154,184,191,248,249 Similarly,
22-kHz frequencies, associated with negative states and various aver- the ability to perceive and use salient information from conspecifics
sive situations230–232 has been shown to produce reduced locomotion emotional states is shared from primates to rodents.249 In particular,
and cessation of social activities in receiver rats even if the receiver the strength of both emotion contagion and observational learning is
was separate from the sender and the signal was played back.233,234 enhanced by social factors such as familiarity and related-
22-kHz USVs have been recently implicated in the transmission ness123,159,161,183 indicating that information communicated by famil-
of fear, conveying fear-eliciting information when directed at a cage- iar individuals might be evaluated more efficiently.
mate who previously experienced fear.150 However, playbacks of this Studies of emotion contagion in rodents imply the perception
USV frequency emitted during shock are not consistently associated of other's emotional states. However, these processes appear to
with vicarious freezing in observer rats, suggesting other sensory sig- be mediated by rapid automatic responses, so their study might
nals might be crucial in determining the fear response.139 not be that informative in understanding social cognitive compo-
USVs in rats are not just a means to delivering negative signals.
nents controlled by conscious processing. Meanwhile, more com-
50-kHz vocalizations have been associated with positive states and
plex social cognitive functions, such as social transmission of
affiliative behaviors, such as mating, play, proximity and also social
information, consolation and helping behavior, recently
contact with a human.235,236 This frequency might convey information
highlighted in rodents, indicate the existence of emotion recogni-
reinforcing social connection237,238 and stimulating approach behav-
tion abilities, but are focused on the adaptive use of such informa-
ior, as observed in radial arm maze USV playback paradigms.238,239
tion, and are fundamentally based on negative-valenced emotional
In mice, USV emission has been primarily reported in reproductive
states (fear or stress).
contexts, such as the exposure of a male to a female in estrus, or to
We believe that a converging approach, which takes into account
female urine227,240,241 and to solicit maternal care.242,243 USVs emit-
the knowledge acquired by different ethological and biological fields
ted during female-female244 or juvenile social encounters228 are less
in different animals, as well as a combined and parallel effort from
evident, but have been reported to positively correlate with social
clinical studies and preclinical research in rodents will be successful.
exploration, suggesting a role in promoting sociability.
Moreover, a categorical approach to study the sensory modalities
Evidence that implicates mouse USVs in the communication of
used by rodents to communicate emotions might offer a broader
negative emotions is similarly scarce. Only one study141 reported that
vocalizations emitted by mice exposed to a shock, or their playback spectrum of action in the description of the emotion-processing dys-
might be sufficient to induce fear responses in observer mice. How- functions possibly associated with neuropsychiatric disorders.
ever, more evidence is needed to better understand the role of mice Recent studies, mostly in rats, started to elucidate brain structures and
USVs do not represent the only auditory signal with an emotional confirming some overlapping substrate across species, particularly the
valence that rodents can detect. Recent evidence indicates we might amygdala, insula and anterior cingulate cortex. However, the brain circuits
have underestimated rodent ability to process a range of nonspecies- involved in emotion recognition are still unexplored.
specific auditory cues. The work of Pereira et al. 245
showed that a Finally, genetic factors have been strongly implicated in social cog-
sudden change in the auditory environment, such as the lack of sound nition deficits associated with several psychiatric conditions.250–254
associated with freezing, is sufficient to trigger freezing in an observer Similarly, recent evidence indicates that genetic factors might modulate
rat previously exposed to the same fear experience. On a similar note, emotion-processing behaviors in mice as well (eg, see184,190,255–257).
possibly related to both acoustic and tactile sensory channels, another Thus, a better understanding of the contribution of genetic factors
study in rats247 found that the sniffing rate during a social encounter to emotion recognition abilities could also facilitate the identifica-
correlates with dominance status: in particular, a decrease in respira- tion of at-risk subpopulations and the development of targeted
tory frequency, separated by olfaction, is one of the signals subordi- medical approaches based on the genetic background of each
nate rats use to reduce chances of aggression from dominant rats. individual.
Sniffing could then be used as a signal to communicate states or
intentions,246,247 and be part, together with whisking, head move-
ments and USV emission, of a facial system used to express emotions. ACKNOWLEDGMENTS
This work was supported by funding from the Istituto Italiano di Tec-
nologia, the Brain and Behavior Research Foundation (2015 NARSAD
5 | CO NC L USIO NS A ND PE R SPE C TIVE S
n. 23234) and the Compagnia di San Paolo (n. 2015-0321).
The evidence reported in this review supports the notion that emo-
tion recognition abilities are largely conserved among different mam-
CON F L I C T S OF IN TE RE S T
mals and represents a critical aspect of social cognition.
The authors declare that they have no competing interests.
Despite the diversity in the modalities to express and/or perceive
emotions, humans and other animals seem to share many homologies
in their responses to other's emotions. Some of these responses, such ORCID
as emotion contagion, can be similarly observed in all the species we Francesco Papaleo https://orcid.org/0000-0002-6326-0657
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