Emotion recognition in nonhuman primates: How experimental research can contribute to a better understanding of underlying mechanisms

Nieuwburg, Elisabeth G.I.; Ploeger, Annemie; Kret, Mariska E.

doi:10.1016/j.neubiorev.2020.11.029

Cited by 32 publications

(26 citation statements)

References 103 publications

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“…Chimpanzees show jealous reactions when their own valuable social bonds are under threat (Webb et al, 2020); long-tailed macaques relax (i.e., show a decrease in circulating cortisol) while cooperating with a friend (Stocker et al, 2020), and several species consider "the glass half full rather than half empty" in judgement or cognitive bias tasks (Paul et al, 2020). In line with Panksepp's argument, recent research incorporating the behavioral, physiological, and cognitive components of emotions, is thus suggesting that not only do animals show emotional behavioral responses, they also seem to experience them as well as those of conspecifics (Kret et al, 2020;Nieuwburg et al, 2021).…”

Section: Our View On Measuring Emotions and Feelingsmentioning

confidence: 82%

“…For example, technological advances allow us to measure animals' emotional facial expressions (e.g., the chimpanzee's and other species' FACS of Waller et al, 2020). We can also noninvasively measure bodily expressions and physiological arousal by using thermography, pupillometry, heartrate measurements, hormone levels, and measurements of neural activation (reviewed by Nieuwburg et al, 2021). Similarly, we study emotionally biased decision-making and the perception of emotions in experimental paradigms with techniques such as touchscreens and eyetrackers (e.g., Parr & Heintz, 2009;Kret et al, 2016).…”

Section: Future Stepsmentioning

confidence: 99%

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My Fear Is Not, and Never Will Be, Your Fear: On Emotions and Feelings in Animals

2022

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Do nonhuman animals (henceforth, animals) have emotions, and if so, are these similar to ours? This opinion piece aims to add to the recent debate about this question and provides a critical re-evaluation of what can be concluded about animal and human emotions. Emotions, and their cognitive interpretation, i.e., feelings, serve important survival functions. Emotions, we believe, can exist without feelings and are unconsciously influencing our behavior more than we think, and possibly more so than feelings do. Given that emotions are expressed in body and brain, they can be inferred from these measures. We view feelings primarily as private states, which may be similar across closely related species but remain mostly inaccessible to science. Still, combining data acquired through behavioral observation with data obtained from noninvasive techniques (e.g., eyetracking, thermography, hormonal samples) and from cognitive tasks (e.g., decision-making paradigms, cognitive bias, attentional bias) provides new information about the inner states of animals, and possibly about their feelings as well. Given that many other species show behavioral, neurophysiological, hormonal, and cognitive responses to valenced stimuli equivalent to human responses, it seems logical to speak of animal emotions and sometimes even of animal feelings. At the very least, the contemporary multi-method approach allows us to get closer than ever before. We conclude with recommendations on how the field should move forward.

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Section: Our View On Measuring Emotions and Feelingsmentioning

confidence: 82%

Section: Future Stepsmentioning

confidence: 99%

My Fear Is Not, and Never Will Be, Your Fear: On Emotions and Feelings in Animals

2022

Self Cite

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“…3b) (prediction 2a not supported). There is evidence that RFM can help synchronise motor actions between players both in human and non-human animals (Palagi et al 2020;Nieuwburg et al 2021). The linkage between RFM and play equilibrium is particularly evident in tolerant (e.g.…”

Section: Discussionmentioning

confidence: 99%

“…The phenomenon of RFM has been demonstrated in several non-primate (Canis lupus familiaris, Palagi et al 2015;Suricata suricatta, Palagi et al 2019a;Helarctos malayanus, Taylor et al 2019) and primate species (Theropithecus gelada, Mancini et al 2013a;Pongo pygmaeus, Davila-Ross et al 2008; Pan troglodytes and Gorilla gorilla gorilla, Palagi et al 2019b). RFM can involve the perception-action mechanism and can have a role in emotion recognition (Palagi et al 2020;Nieuwburg et al 2021). By its potential role in favouring emotional sharing, RFM can have implications in determining the success of the play sessions.…”

Section: Introductionmentioning

confidence: 99%

The face never lies: facial expressions and mimicry modulate playful interactions in wild geladas

Gallo

Zanoli

Caselli

et al. 2022

Behav Ecol Sociobiol

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Play fighting, the most common form of social play in mammals, is a fertile field to investigate the use of visual signals in animals’ communication systems. Visual signals can be exclusively emitted during play (e.g. play faces, PF, context-dependent signals), or they can be released under several behavioural domains (e.g. lip-smacking, LS, context-independent signals). Rapid facial mimicry (RFM) is the involuntary rapid facial congruent response produced after perceiving others’ facial expressions. RFM leads to behavioural and emotional synchronisation that often translates into the most balanced and longest playful interactions. Here, we investigate the role of playful communicative signals in geladas (Theropithecus gelada). We analysed the role of PF and LS produced by wild immature geladas during play fighting. We found that PFs, but not LS, were particularly frequent during the riskiest interactions such as those including individuals from different groups. Furthermore, we found that RFM (PF→PF) was highest when playful offensive patterns were not biased towards one of the players and when the session was punctuated by LS. Under this perspective, the presence of context-independent signals such as LS may be useful in creating an affiliative mood that enhances communication and facilitates most cooperative interactions. Indeed, we found that sessions punctuated by the highest frequency of RFM and LS were also the longest ones. Whether the complementary use of PF and LS is strategically guided by the audience or is the result of the emotional arousal experienced by players remains to be investigated. Significance Statement Facial expressions and their rapid replication by an observer are fundamental communicative tools during social contacts in human and non-human animals. Play fighting is one of the most complex forms of social interactions that can easily lead to misunderstanding if not modulated through an accurate use of social signals. Wild immature geladas are able to manage their play sessions thus limiting the risk of aggressive escalation. While playing with unfamiliar subjects belonging to other groups, they make use of a high number of play faces. Moreover, geladas frequently replicate others’ play faces and emit facial expressions of positive intent (i.e. lip-smacking) when engaging in well-balanced long play sessions. In this perspective, this “playful facial chattering” creates an affiliative mood that enhances communication and facilitates most cooperative interactions.

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“…4 N-Q). Taken together, the results of the video-playback experiment indicate that oxytocin is necessary and sufficient for zebrafish to discriminate between conspecifics only based on their altered states, suggesting the occurrence of the oxytocin-dependent ability to discriminate distressed from neutral behavior in conspecifics (aka emotion recognition [21,22]) in zebrafish. This is in line with responses in humans and mammals that implicate the recognition of a fearful state in others and not simply their behavior [23,24].…”

Section: Main Textmentioning

confidence: 74%

Oxytocin regulation of social transmission of fear in zebrafish reveals its evolutionary conserved role in emotional contagion

Akinrinade

Kareklas

Gliksberg

et al. 2021

Preprint

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Emotional contagion is the most ancestral form of empathy that relies on simple perception-action mechanisms, on top of which more complex forms of empathic behaviors, such as consolation and helping, have evolved. Here we tested to what extent the proximate mechanisms of emotional contagion are evolutionary conserved by assessing the role of oxytocin, known to regulate empathic behaviors in mammals, in social fear contagion in zebrafish, which represents an evolutionary divergent line to that of tetrapods, within vertebrates. Using mutants for the ligand of the fish oxytocin nonapeptide and both of its receptors in zebrafish we showed that oxytocin is necessary for observer zebrafish to copy the distressed behavior of conspecific demonstrators. Exogeneous administration of oxytocin to the ligand mutant rescued the ability of observers to express social fear transmission, indicating that oxytocin is not only necessary but also sufficient for emotional contagion. The brain regions in the ventral telencephalon that are associated with emotional contagion in zebrafish are homologous to those known to be involved in the same process in rodents (e.g. striatum, lateral septum), and receive direct projections from oxytocinergic neurons located in the preoptic area. Finally, we ruled out the hypothesis that social transmission of fear in zebrafish merely relies on behavior contagion by motor imitation, and we showed that it rather relies on emotion discrimination. Together our results support an evolutionary conserved role for oxytocin as a key regulator of basic empathic behaviors across vertebrates.

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Emotion recognition in nonhuman primates: How experimental research can contribute to a better understanding of underlying mechanisms

Cited by 32 publications

References 103 publications

My Fear Is Not, and Never Will Be, Your Fear: On Emotions and Feelings in Animals

My Fear Is Not, and Never Will Be, Your Fear: On Emotions and Feelings in Animals

The face never lies: facial expressions and mimicry modulate playful interactions in wild geladas

Oxytocin regulation of social transmission of fear in zebrafish reveals its evolutionary conserved role in emotional contagion

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