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Motivation and emotion/Book/2022/Animal emotion

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Emotion in animals:
What is the emotional experience of animals?

Overview

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Emotion is an innate in humans across all cultures.[1][2][3] Naturally the question must be asked if emotions can be experienced and perceived by animals other than humans. Charles Darwin was thefirst reported scientist to investigate this question in 'The expression of the emotions of man'.[4] His research has laid the foundation from which this field has evolved. This area has now become more robust with more studies being performed. While studies examining the potential emotion of non-mammalian animals is still limited and relatively sparse, the examination of mammals however is far more extensive with some suggesting the reason mammals have more apparent emotions being the evolution of the visceral-limbic brain.[5] Evidence of this visceral-limbic brain and its role in emotion is displayed through what Panksepp calls emotional actions, consisting of: seeking, fear, rage, lust, care, panic, and play.[6] How animals perceive and display emotion is naturally most often explored through a human lens. As a result, animals commonly studied involve those most closely associated with ourselves, those being primates, to which we are related, and dogs, which we have evolved and changed through domestication. Unfortunately, emotional responses can only simply be interpreted with varying degrees of certainty as non-human animals are still unable to fully comprehend or vocalise concepts such as emotions. As emotion is something found in so many animals and seems so closely linked with ourselves as a species, there seems to be an evolutionary reason for which our emotions exist, at least that is what Darwin suggested all those years ago.

Focus Questions:

  • How do dogs display and perceive emotions?
  • How do primates display and perceive emotions?
  • What evolutionary purposes do emotions play?

Emotion in dogs

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Figure 1. Emotions of a dog - Konrad Lorenz

Domesticated dogs appear to have unusually complex emotions that are incredibly similar to those found in humans. A percentage of dogs also experience learned helplessness, which may not be entirely unique, however that percentage of dogs that develop this learned helplessness or long term depression is very close to the percentage of humans that develop these emotions in similar situations.[7] Similarly, dogs have been shown to act out in what seems to be jealousy when their owners interact with anything they perceive to be dog like.[8] When examining the brains of dogs through and fMRI it has been found that the caudate nucleus of a dog is capable of activation in response to certain stimuli, creating anticipation.[9][10] These appearances of seemingly complex emotions may be incorrectly attributed and simply perceived to be more complex than they may actually be, for instance, when a dog performs an action that is punishable they may display what can be perceived as guilt, however this may not be true guilt but rather anticipation for a punishment.[10]

How dogs display emotion

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As with most animals, dogs display emotion largely through their physicality. More so than other forms of animal such as fish, dogs have quite expressive and flexible faces, including their ears and tongues, as a result emotions experienced by dogs are most often expressed through facial features.[11][12][13] Additionally most dog breeds possess tails capable of dynamic movement which may also assist in acting as a marker for emotion.[14] In the case of dogs there does not seem to be a large difference between the face at rest and the face when happy or excited. The most common change when excited is the forward movement of the ears, other notable facial movements such as licking of the nose or blinking may occur more often in a perceived negative context rather than a positive one. The facial action most commonly associated with a dogs negative mood is the lowering of the ears.[11][12][13]

Figure 2. Hostile dog - Charles Darwin

The tail and it's movements are often noted as one of the more obvious forms of emotional display of a dog. Many people are familiar with the example of a dog frantically wagging its tail when happy however this is only one of many ways in which the tail can express its mood. Their are two major components upon which tail based emotional signals are based, these are movement and vertical positioning. The amount which a dog's tail is wagging side to side is usually an indicator of energy, the faster and more wildly a tail appears to be swinging, the more energy the dog is likely experiencing. While this can extend to negative energy such as anxiety, a wagging tail is often indication of play. However tail wagging does not necessarily indicate positive or negative affect, that instead is often discerned based on how high or low a tail is. A high tail often indicates confidence, arousal, or willingness to engage with others when wagging, a still, upright tail might indicate threat or willingness to challenge. A lower tail often indicates fear and anxiety or sometimes a show of subservience.[15][16][17]

Example When engaging with a dog, despite erratic movement the dog may be showing signs of play rather than aggression. If the dogs ears are forward and upright and it's tail is high and swinging quickly, the dog is likely in a good mood and can be safe to play with. Nonetheless, be cautious of any growling, this often indicates aggression, unless you are playing tug-of-war, the only time dogs seem to growl while playing.

Unfortunately, as dogs have become domesticated and something sought out by people for various reasons breeding for selective traits are becoming more popular. Many of these selective traits can be entirely physiological such as longer legs for running or an overall smaller size for easier care, these modifications have resulted in some dogs having difficulty displaying emotion. In particular brachycephalic dogs have faces that are less flexible than they should be and may have find it hard to correctly emote, similarly some dog breeds are categorised by shorter tails which are far less expressive or perhaps larger heavier tails that are more difficult to lift higher and therefore show intention in physicality.[15][16][17] Be careful with dogs even with knowledge regarding emotional display, if something is growling at you that is seldom a good sign. Treat animals with care and make the choice to adopt a dog that needs a home rather than buying from a breeder.

How dogs perceive emotion

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Dogs have co-existed with humans for approximately 10,000 years,[18] as a result they seem to have become quite adept at reading our emotions as well as those of other dogs. Dog's perception of emotions and moods seem to come from both visual and auditory expression, and seem to be quite accurate as well being able to seemingly match vocal and facial emotion to each other in some way.[19] For facial perception no facial detail is preferred in dogs other than the cheeks, when examining a human face for emotion dogs seem to prefer the cheeks above any other landmarks.[20] Present in humans is the left gaze bias, the tendency to look toward the left visual hemisphere when facing someone and examining their face. This bias is not only present in humans but additionally other primates, suggesting that perhaps the right side of the face for primates contains more information regarding emotion than the left. Interestingly this does not seem to be innate in primates due to an awareness of ourselves engaging in this but rather through observation as now dogs seem to show this bias as well. This left gaze bias has been shown to appear in dogs when looking at the face of humans but not other dogs, suggesting this is a uniquely primate trait that dogs have picked up on upon spending centuries by our sides showing great emotional and cognitive intelligence.[21] Furthering this idea of emotional and cognitive intelligence, dogs additionally seem to be able to make decisions for themselves based upon the emotions displayed by humans, this suggests that dogs have a deep understanding of human emotion and adjust their action accordingly.[22] Despite how attenuated to our emotional displays dogs have become, they are still non-human animals and as a result have a tendency to favour information gathered from examining body language rather than faces which humans have put more emphasis on, potentially for the sake of being polite.[23] After so many generations with each other, it seems that dogs have started to know us just as well as we know ourselves, if not better.

Test your knowledge

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1 Dogs are capable of experiencing anticipation:

True
False

2 A straight still tail is sign of play:

True
False

3 The left gaze bias is exclusive to primates:

True
False


Emotion in primates

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Non-human primates are quite close comparatively to humans in many ways including that of the prehensile thumb and brain. As a result of these similarities, primates are considered to be the closest to humans in terms of emotional capacity and intelligence. Many primates have even shown empathy for each other as well as for humans, even experiencing the phenomenon by which seeing another primate yawn causes the other to yawn, more than that is the effect by which primates prefer the company of humans who display empathy to those that do not.[24] Naturally, with empathy comes the potential for caring for others in a great capacity. Rhesus monkeys are capable of acting in an extremely altruistic manner, sacrificing their own satiety and delicious food in order to save other rhesus monkeys from harm no matter how hungry they are.[25][26] This kindness can persist and influence a primates emotions even after conflict. Macaques have been shown to experience post-conflict anxiety, when the conflict occurs with one that they were close to this anxiety becomes even more intense suggesting macaques also experience the valuable relationship hypothesis.[27] Primates are not only similar to humans in what kind of emotions they perceive but also in how they perceive and display those emotions. When examining our emotional responses and theirs side by side it becomes clear to see how closely related we are. Even down to the brain structure responsible for emotion. It has been found that mechanisms involved in fear and anxiety in human brains is remarkably similar to those found in the brains of rhesus monkeys.[28][29]

How primates display emotion

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Like many animals, non-human primates primarily display emotion through their face. Most primates have very expressive faces, perhaps as a result of the need for easily readable emotions.[30] This can make understanding the emotions of primates far easier for a human than it would be for another animal as it is more natural to the current norm of interpreting emotion almost exclusively from other humans. Chimpanzees in particular have been shown to use multiple faces to show emotion. They have used smiles and teeth baring as a way to indicate their mood, not only toward real life stimulus but also toward recordings featuring objects intended to illicit a response in the chimpanzees such as needles or their favourite foods.[31] Primates and humans both have the left gaze bias. This is not a random quirk, it is because the right hemisphere of the brain is dominant in its role in emotional expression, as a result one side of our face is typically more expressive than others, hence the gaze bias when observing others. Naturally this effect occurs not only in humans but in other primates as well. Why this occurs is still yet unclear.[32][33] Many primates use more than simply their face for expression of emotion, vocalisation often plays a key role. Where in most animals vocalisation is often a tool to ward off predators or competition or is used to signal a readiness to mate, primates use vocalisation in order to convey emotions better, using tone and volume to often reflect whether they are in a positive mood or a negative mood or perhaps if they are ready to challenge an opponent.[32][34]

Example Koko was a gorilla who was quite adept at sign language. Through her understanding and skill at communication we have learnt much about gorillas like her. Koko had a pet cat which she named 'All Ball'. All Ball was later killed by a car. Upon discovering this Koko signed the word 'bad, sad, frown, cry, and trouble'. Reports say she could later be heard weeping.

Figure 3. Gorilla smiling

How primates perceive emotion

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Primates display emotions in an asymmetrical way and as a result also perceive emotions in this asymmetrical way among each other.[21] Overall primates perceive emotions in a very similar way to ourselves. Human understanding may be a tad more complex but the principles remain the same. Mirror neurons activate when we see another perform an action or display an emotion.[35] They still get scared and anxious when they perceive danger or a threat to their wellbeing.[28][29] They still recognise when they, or us, are feeling a particular emotion.[36] For all the differences in how we display ourselves, humans and primates are so much more similar in how we feel.

Test your knowledge

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1 Which primate has been known to show post-conflict anxiety

Macaque
Chimpanzee
Rhesus Monkey

2 The phenomenon exclusive to primate emotion is known as the...

Right gaze inclination
Left gaze bias
Left look inclination
Right look bias

3 What was the name of Koko's pet cat?

Ale Bale
Fall Ball
Arms Barns
All Ball


The evolution of emotion

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Given that many if not all animals experience emotions it may be true that they are vital to survival and as such have evolved early in multi-cell organisms. As humans now live in such a way that a great many survival skills are no longer necessary the use of emotions may be questioned by some, for instance Charles Darwin posited that emotions no longer serve a purpose among humans.[4] Despite one’s opinion on this matter it is an irrefutable fact that our emotions still greatly control our actions[37] though we are not alone in this, even other animals such as rats experience influence over their actions as a result of their emotions.[38] But why might our emotions have such a strong grip on our minds and lives? For what possible reason could we have evolved to be so easily influenced?

Emotion as a survival tool

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It is possible that emotion first evolved as a means to keep ourselves safe. When considering Ekman’s core emotions[39] some emotions and their role in keeping us safe seems obvious; fear enhances our abilities to survey or flee from threats and disgust acts as a guard against potentially hazardous substances we may ingest. This is most evident throughout two fear systems, one fast and one slow. Where one fear system immediately detects something that could be dangerous, our slow fear system works at classifying the potential threat in greater detail, to decide if it is worth spending extra energy to get further away or to fight rather than to simply jump and continue walking.[40] Though some seem more difficult to find what their purpose may have been. Some have suggested that happiness exists to suggest to us that there is no present threat, or that sadness is designed to garner sympathy.[41] These explanations are certainly plausible, however they are not currently robust enough to be fully accepted. Instead some believe that the evolution of emotion is not to directly assist in survival but rather to indirectly assist by helping us connect with those of our own species[factual?].

Emotion as a social tool

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Some suggest that emotion exists not as a tool for the individual but rather as a tool for the collective. Given that for the most part basic emotions seem to be intrinsic to people regardless of culture,[2] through facial expressions it stands to reason that emotions are a social tool. Why else would we outwardly display our emotions if not to quickly and concisely express them to each other when it is a matter of life or death? Why would we have mirror neurons that activate in response to viewing emotions?[35] Why would we experience empathy and emotion contagion if not for the sake of being better in sync with our group so we may better survive together?[42] This use of emotion to further our species also explains why we feel sympathy or empathy, when we see one of our own suffer and move to help[25][26] it is so we can continue to breed and let our species continue to grow and flourish. Emotion may not be the thing that sets us apart like higher brain function or opposable thumbs but it may nonetheless be what keeps us from extinction.

Conclusion

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Emotion is innate, not only in humans, but in so many animals around us. We can see that with and without our intervention animals like dogs and primates can learn better understanding of each other. Through our interference, the understanding a dog can have may be increased further than it ever could have, though we still take away their ability to express for our own personal gain[improve clarity]. Through our studies of primates we find that we are the same, that we have such a great capacity for not only expressing ourselves loudly but also in compassion, in love and grief. We may have initially developed emotion to survive, and for a time we may have thought it was what separated us from animals, but now we can see that it is truly what brings us together with the animals, what enables us to treat them when they’re injured or adopt them when they need shelter. Emotion is what keeps us animal.

See also

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References

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  1. ↑ Goldie, Peter (2007-11). "Emotion". Philosophy Compass 2 (6): 928–938. doi:10.1111/j.1747-9991.2007.00105.x. ISSN 1747-9991. https://onlinelibrary.wiley.com/doi/10.1111/j.1747-9991.2007.00105.x. 
  2. ↑ 2.0 2.1 Ekman, Paul; Friesen, Wallace V. (1971). "Constants across cultures in the face and emotion.". Journal of Personality and Social Psychology 17 (2): 124–129. doi:10.1037/h0030377. ISSN 1939-1315. http://doi.apa.org/getdoi.cfm?doi=10.1037/h0030377. 
  3. ↑ Handbook of emotions. Michael, January 10- Lewis, Jeannette M. Haviland-Jones. New York: Guilford Press. 1993. ISBN 0-89862-988-8. OCLC 26934682. https://www.worldcat.org/oclc/26934682. 
  4. ↑ 4.0 4.1 Darwin, Charles ([©1955]). The expression of the emotions in man and animals.. New York,: Philosophical Library. ISBN 0-8371-2291-0. OCLC 250684. https://www.worldcat.org/oclc/250684. 
  5. ↑ Panksepp, Jaak (1982-09). "Toward a general psychobiological theory of emotions". Behavioral and Brain Sciences 5 (3): 407–422. doi:10.1017/S0140525X00012759. ISSN 1469-1825. https://www.cambridge.org/core/journals/behavioral-and-brain-sciences/article/abs/toward-a-general-psychobiological-theory-of-emotions/B09ABA6E2B1333EFFBD687253617E698. 
  6. ↑ Panksepp, Jaak (2005-03-01). "Affective consciousness: Core emotional feelings in animals and humans". Consciousness and Cognition. Neurobiology of Animal Consciousness 14 (1): 30–80. doi:10.1016/j.concog.2004.10.004. ISSN 1053-8100. https://www.sciencedirect.com/science/article/pii/S1053810004001187. 
  7. ↑ Seugman, Martin E. P.; Groves, Dennis P. (1970-09-01). "Nontransient learned helplessness". Psychonomic Science 19 (3): 191–192. doi:10.3758/BF03335546. ISSN 0033-3131. https://doi.org/10.3758/BF03335546. 
  8. ↑ Harris, Christine R.; Prouvost, Caroline (2014-07-23). "Jealousy in Dogs". PLOS ONE 9 (7): e94597. doi:10.1371/journal.pone.0094597. ISSN 1932-6203. PMID 25054800. PMC PMC4108309. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0094597. 
  9. ↑ Berns, Gregory S.; Brooks, Andrew M.; Spivak, Mark (2012-05-11). "Functional MRI in Awake Unrestrained Dogs". PLOS ONE 7 (5): e38027. doi:10.1371/journal.pone.0038027. ISSN 1932-6203. PMID 22606363. PMC PMC3350478. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0038027. 
  10. ↑ 10.0 10.1 Waal, F. B. M. de (1996). Good natured : the origins of right and wrong in humans and other animals. Cambridge, Mass.: Harvard University Press. ISBN 978-0-674-03317-7. OCLC 607847395. https://www.worldcat.org/oclc/607847395. 
  11. ↑ 11.0 11.1 Bremhorst, A.; Mills, D. S.; Würbel, H.; Riemer, S. (2022-02-01). "Evaluating the accuracy of facial expressions as emotion indicators across contexts in dogs". Animal Cognition 25 (1): 121–136. doi:10.1007/s10071-021-01532-1. ISSN 1435-9456. PMID 34338869. PMC PMC8904359. https://doi.org/10.1007/s10071-021-01532-1. 
  12. ↑ 12.0 12.1 Bremhorst, Annika; Sutter, Nicole A.; Würbel, Hanno; Mills, Daniel S.; Riemer, Stefanie (2019-12-17). "Differences in facial expressions during positive anticipation and frustration in dogs awaiting a reward". Scientific Reports 9 (1): 19312. doi:10.1038/s41598-019-55714-6. ISSN 2045-2322. PMID 31848389. PMC PMC6917793. https://www.nature.com/articles/s41598-019-55714-6. 
  13. ↑ 13.0 13.1 Caeiro, Cátia; Guo, Kun; Mills, Daniel (2017-11-14). "Dogs and humans respond to emotionally competent stimuli by producing different facial actions". Scientific Reports 7 (1): 15525. doi:10.1038/s41598-017-15091-4. ISSN 2045-2322. PMID 29138393. PMC PMC5686192. https://www.nature.com/articles/s41598-017-15091-4. 
  14. ↑ Siniscalchi, Marcello; D’Ingeo, Serenella; Minunno, Michele; Quaranta, Angelo (2018-08). "Communication in Dogs". Animals 8 (8): 131. doi:10.3390/ani8080131. ISSN 2076-2615. PMID 30065156. PMC PMC6116041. https://www.mdpi.com/2076-2615/8/8/131. 
  15. ↑ 15.0 15.1 Hecht, Julie; Horowitz, Alexandra (2017-05-06). Weiss, Emily. ed. Introduction to dog behavior (in en). Chichester, UK: John Wiley & Sons, Ltd. pp. 3–30. doi:10.1002/9781119421313.ch1. ISBN 978-1-119-42131-3. https://onlinelibrary.wiley.com/doi/10.1002/9781119421313.ch1. 
  16. ↑ 16.0 16.1 The domestic dog : its evolution, behavior and interactions with people. James Serpell, Priscilla Barrett (Second edition ed.). Cambridge, United Kingdom. 2017. ISBN 978-1-107-02414-4. OCLC 957339355. https://www.worldcat.org/oclc/957339355. 
  17. ↑ 17.0 17.1 Handelman, Barbara (2008). Canine behavior : a photo illustrated handbook (First edition ed.). Wenatchee, WA. ISBN 978-0-9765118-9-2. OCLC 1057341362. https://www.worldcat.org/oclc/1057341362. 
  18. ↑ Bergström, Anders; Frantz, Laurent; Schmidt, Ryan; Ersmark, Erik; Lebrasseur, Ophelie; Girdland-Flink, Linus; Lin, Audrey T.; Storå, Jan et al. (2020-10-30). "Origins and genetic legacy of prehistoric dogs". Science 370 (6516): 557–564. doi:10.1126/science.aba9572. ISSN 0036-8075. PMID 33122379. PMC PMC7116352. https://www.science.org/doi/10.1126/science.aba9572. 
  19. ↑ Albuquerque, Natalia; Guo, Kun; Wilkinson, Anna; Savalli, Carine; Otta, Emma; Mills, Daniel (2016-01-31). "Dogs recognize dog and human emotions". Biology Letters 12 (1): 20150883. doi:10.1098/rsbl.2015.0883. PMID 26763220. PMC PMC4785927. https://royalsocietypublishing.org/doi/10.1098/rsbl.2015.0883. 
  20. ↑ Correia-Caeiro, Catia; Guo, Kun; Mills, Daniel S. (2020-05-01). "Perception of dynamic facial expressions of emotion between dogs and humans". Animal Cognition 23 (3): 465–476. doi:10.1007/s10071-020-01348-5. ISSN 1435-9456. PMID 32052285. PMC PMC7181561. https://doi.org/10.1007/s10071-020-01348-5. 
  21. ↑ 21.0 21.1 Guo, Kun; Meints, Kerstin; Hall, Charlotte; Hall, Sophie; Mills, Daniel (2009-05-01). "Left gaze bias in humans, rhesus monkeys and domestic dogs". Animal Cognition 12 (3): 409–418. doi:10.1007/s10071-008-0199-3. ISSN 1435-9456. https://doi.org/10.1007/s10071-008-0199-3. 
  22. ↑ Albuquerque, Natalia; Mills, Daniel S.; Guo, Kun; Wilkinson, Anna; Resende, Briseida (2022-04-01). "Dogs can infer implicit information from human emotional expressions". Animal Cognition 25 (2): 231–240. doi:10.1007/s10071-021-01544-x. ISSN 1435-9456. PMID 34390430. PMC PMC8940826. https://doi.org/10.1007/s10071-021-01544-x. 
  23. ↑ Correia-Caeiro, Catia; Guo, Kun; Mills, Daniel (2021-03-01). "Bodily emotional expressions are a primary source of information for dogs, but not for humans". Animal Cognition 24 (2): 267–279. doi:10.1007/s10071-021-01471-x. ISSN 1435-9456. PMID 33507407. PMC PMC8035094. https://doi.org/10.1007/s10071-021-01471-x. 
  24. ↑ Empathy : from bench to bedside. Jean Decety. Cambridge, Mass.: MIT Press. 2012. ISBN 978-0-262-29861-2. OCLC 774392935. https://www.worldcat.org/oclc/774392935. 
  25. ↑ 25.0 25.1 Wechkin, Stanley; Masserman, Jules H.; Terris, William (1964-01-01). "Shock to a conspecific as an aversive stimulus". Psychonomic Science 1 (1): 47–48. doi:10.3758/BF03342783. ISSN 2197-9952. https://doi.org/10.3758/BF03342783. 
  26. ↑ 26.0 26.1 Masserman, Jules H.; Wechkin, Stanley; Terris, William (1964-12-01). ""altruistic" behavior in rhesus monkeys". American Journal of Psychiatry 121 (6): 584–585. doi:10.1176/ajp.121.6.584. ISSN 0002-953X. https://ajp.psychiatryonline.org/doi/abs/10.1176/ajp.121.6.584. 
  27. ↑ Aureli, F. (1997). Post-conflict anxiety in nonhuman primates: The mediating role of emotion in conflict resolution. Aggressive Behavior, 23(5), 315–328. doi:10.1002/(sici)1098-2337(1997)23:5<315::aid-ab2>3.0.co;2-h
  28. ↑ 28.0 28.1 Kalin, Ned H.; Sheltona, Steven E. (2003-12). "Nonhuman Primate Models to Study Anxiety, Emotion Regulation, and Psychopathology". Annals of the New York Academy of Sciences 1008 (1): 189–200. doi:10.1196/annals.1301.021. http://doi.wiley.com/10.1196/annals.1301.021. 
  29. ↑ 29.0 29.1 Rolls, EDMUND T. (1986-01-01). Plutchik, Robert. ed. Chapter 5 - NEURAL SYSTEMS INVOLVED IN EMOTION IN PRIMATES (in en). Academic Press. pp. 125–143. doi:10.1016/b978-0-12-558703-7.50011-5. ISBN 978-0-12-558703-7. https://www.sciencedirect.com/science/article/pii/B9780125587037500115. 
  30. ↑ Andrew, R. J. (1963-11-22). "Evolution of Facial Expression: Many human expressions can be traced back to reflex responses of primitive primates and insectivores.". Science 142 (3595): 1034–1041. doi:10.1126/science.142.3595.1034. ISSN 0036-8075. https://www.science.org/doi/10.1126/science.142.3595.1034. 
  31. ↑ Parr, Lisa A. (2001-11-01). "Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes)". Animal Cognition 4 (3): 223–229. doi:10.1007/s100710100085. ISSN 1435-9448. https://doi.org/10.1007/s100710100085. 
  32. ↑ 32.0 32.1 Gruber, Thibaud; Grandjean, Didier (2017-02). "A comparative neurological approach to emotional expressions in primate vocalizations". Neuroscience & Biobehavioral Reviews 73: 182–190. doi:10.1016/j.neubiorev.2016.12.004. https://linkinghub.elsevier.com/retrieve/pii/S0149763416305693. 
  33. ↑ Hauser, Marc D. (1993-07-23). "Right Hemisphere Dominance for the Production of Facial Expression in Monkeys". Science 261 (5120): 475–477. doi:10.1126/science.8332914. ISSN 0036-8075. https://www.science.org/doi/10.1126/science.8332914. 
  34. ↑ Parr, Lisa A; Waller, Bridget M; Fugate, Jennifer (2005-12-01). "Emotional communication in primates: implications for neurobiology". Current Opinion in Neurobiology. Motor sytems / Neurobiology of behaviour 15 (6): 716–720. doi:10.1016/j.conb.2005.10.017. ISSN 0959-4388. PMID 16274983. PMC PMC2826104. https://www.sciencedirect.com/science/article/pii/S0959438805001662. 
  35. ↑ 35.0 35.1 Parr, Lisa A; Waller, Bridget M; Fugate, Jennifer (2005-12-01). "Emotional communication in primates: implications for neurobiology". Current Opinion in Neurobiology. Motor sytems / Neurobiology of behaviour 15 (6): 716–720. doi:10.1016/j.conb.2005.10.017. ISSN 0959-4388. PMID 16274983. PMC PMC2826104. https://www.sciencedirect.com/science/article/pii/S0959438805001662. 
  36. ↑ Parr, Lisa A. (2001-11-01). "Cognitive and physiological markers of emotional awareness in chimpanzees (Pan troglodytes)". Animal Cognition 4 (3): 223–229. doi:10.1007/s100710100085. ISSN 1435-9448. https://doi.org/10.1007/s100710100085. 
  37. ↑ Barrett, Lisa Feldman; Adolphs, Ralph; Marsella, Stacy; Martinez, Aleix M.; Pollak, Seth D. (2019-07). "Emotional Expressions Reconsidered: Challenges to Inferring Emotion From Human Facial Movements". Psychological Science in the Public Interest 20 (1): 1–68. doi:10.1177/1529100619832930. ISSN 1529-1006. PMID 31313636. PMC PMC6640856. http://journals.sagepub.com/doi/10.1177/1529100619832930. 
  38. ↑ Rygula, Rafal; Pluta, Helena; Popik, Piotr (2012-12-26). "Laughing Rats Are Optimistic". PLOS ONE 7 (12): e51959. doi:10.1371/journal.pone.0051959. ISSN 1932-6203. PMID 23300582. PMC PMC3530570. https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0051959. 
  39. ↑ Ekman, Paul (1992). "Are there basic emotions?". Psychological Review 99 (3): 550–553. doi:10.1037/0033-295X.99.3.550. ISSN 1939-1471. http://doi.apa.org/getdoi.cfm?doi=10.1037/0033-295X.99.3.550. 
  40. ↑ Human emotions : a reader. Jennifer M. Jenkins, Keith Oatley, Nancy L. Stein. Malden, Mass.: Blackwell. 1998. ISBN 0-631-20747-3. OCLC 37854231. https://www.worldcat.org/oclc/37854231. 
  41. ↑ Shariff, Azim F.; Tracy, Jessica L. (2011-12). "What Are Emotion Expressions For?". Current Directions in Psychological Science 20 (6): 395–399. doi:10.1177/0963721411424739. ISSN 0963-7214. http://journals.sagepub.com/doi/10.1177/0963721411424739. 
  42. ↑ Nieuwburg, Elisabeth G. I.; Ploeger, Annemie; Kret, Mariska E. (2021-04-01). "Emotion recognition in nonhuman primates: How experimental research can contribute to a better understanding of underlying mechanisms". Neuroscience & Biobehavioral Reviews 123: 24–47. doi:10.1016/j.neubiorev.2020.11.029. ISSN 0149-7634. https://www.sciencedirect.com/science/article/pii/S0149763420306692. 
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