Elsevier

Neuroscience & Biobehavioral Reviews

Volume 73, February 2017, Pages 182-190
Neuroscience & Biobehavioral Reviews

Review article
A comparative neurological approach to emotional expressions in primate vocalizations

https://doi.org/10.1016/j.neubiorev.2016.12.004Get rights and content

Highlights

  • Primate vocalizations carry emotional content but connection to humans is debated.

  • Neural circuitry for vocalization and emotion processing overlap in the IFG and STG.

  • We predict a STG-STS-IFG network of emotional vocalizations common to all hominids.

  • Degree of intentionality in production can sort out emotional vocalizations in primates.

Abstract

Different approaches from different research domains have crystallized debate over primate emotional processing and vocalizations in recent decades. On one side, researchers disagree about whether emotional states or processes in animals truly compare to those in humans. On the other, a long-held assumption is that primate vocalizations are innate communicative signals over which nonhuman primates have limited control and a mirror of the emotional state of the individuals producing them, despite growing evidence of intentional production for some vocalizations. Our goal is to connect both sides of the discussion in deciphering how the emotional content of primate calls compares with emotional vocal signals in humans. We focus particularly on neural bases of primate emotions and vocalizations to identify cerebral structures underlying emotion, vocal production, and comprehension in primates, and discuss whether particular structures or neuronal networks solely evolved for specific functions in the human brain. Finally, we propose a model to classify emotional vocalizations in primates according to four dimensions (learning, control, emotional, meaning) to allow comparing calls across species.

Introduction

Notwithstanding the potential differences in affect or the phenomenological aspect of feeling a particular emotion, that is, being consciously aware of it (Dawkins, 2000), which we do not address in this review, it is now well established that animals have an emotional life (Bekoff, 2007, Davila-Ross et al., 2011, de Waal, 2011, Panksepp, 2011a, Panksepp, 2011b, Parr et al., 2005). This understanding is particularly crucial for studies related to animal welfare and can be used to influence policies on the treatment of farm animals (Briefer, 2012). Additionally, it is also currently held that many, if not all, animal vocalizations convey emotional content, understood as both the fact that these vocalizations reflect the emotional state of the caller, and the fact that emotional information may be extracted by the listener (Briefer, 2012, Fichtel et al., 2001, Owren et al., 2011, Seyfarth and Cheney, 2003). The study of emotions has also been of much interest in the recent literature on nonhuman primates (henceforth, primates) at a more fundamental level, particularly because of their close proximity to humans. The possibility that primate vocalizations bear a strong emotional content has nevertheless mostly been considered in discussions related to the evolution of human language, usually as opposed to the presumed unique characteristics of human language. More precisely, nonhuman primate vocal communication systems have been considered similar to human emotional vocal production but different and potentially evolutionary unrelated to human speech, as opposed to their more controlled gestures (Tomasello, 2008). For instance, Tomasello (2008) states that primate vocalizations are “…tightly tied to specific emotions, and broadcast indiscriminately to everyone in the immediate vicinity” (p. 8). In this approach, the focus is put on the fact that primates may not be as capable as humans in controlling their calls or vocalizations, in stark contrast to the flexibility offered by human language and potentially available to other primates in gestural communication (Arbib et al., 2008).

Nevertheless, some studies also suggest that it may be incorrect to label all primate vocalizations as uncontrollable expressions of their emotions. Some of them undoubtedly are (Tomasello, 2008), but so are some equally uncontrollable human vocalizations such as screaming, groaning, crying, or laughing (Groswasser et al., 1988, Mariani et al., 1980). However, primates may also have more control over intentional calls (calls that are produced with the aim of fulfilling a goal) or referential calls (calls that indicate something to someone), which both fulfill a complementary communicative role to the conveying of emotions (Crockford et al., 2012, Liebal et al., 2014, Sievers and Gruber, 2016); finally some calls may have a learnt component (e.g. Watson et al., 2015). Call characteristics probably also depend on the intended audience. For instance, a call aimed at one’s own community has different acoustic characteristics than a call intended for intergroup communication (Liebal et al., 2014). Similarly, low- and high-frequency vocalizations are believed to serve different purposes during aggressive interactions (e.g. Ordóñez-Gómez et al., 2015). Interestingly, neurological research in primates has shown that directed and non-directed types of calls recruit different cerebral structures (Ghazanfar and Eliades, 2014, Ghazanfar and Logothetis, 2003).

In this review, our goal is to conciliate both views stemming from research on emotion and on the evolution of language, including the controversial topic of intentional vocal production in primates and other animals, to propose a unifying framework to analyze emotional vocalization in primates. We first give a comparative overview of the cerebral structures involved in the communicative and emotional processes before discussing the higher order cognitive bases of emotional communication across primates, particularly the processes of categorization (distinguishing A versus B) and discrimination (distinguishing A versus non-A). In this review, we will mainly focus on vocal expression and perception of emotions, but we will also connect our discussion to data from visual studies on facial expression or perception of emotions when points of convergence can be underlined. Additionally, we will address aspects about both production and perception of vocalizations and emotions to underline similarities and differences in the two systems across primates to converge towards a model of emotional vocalizations in primates.

Section snippets

Comparative methods in use to investigate the cerebral bases of behavior in primates

Historically, neuroscience owes much to primate research, particularly because such research has been conducted invasively on species including macaques (genus Macaca) and squirrel monkeys (genus Saimiri). As was the case for human affective neuroscience, studies of lesions were highly informative in the early days of neuropsychological research (Damasio, 1994). This technique consists of comparing the behavior of a test subject after a stroke or after removal of a brain area for clinical

Vocal communication: production

The structures responsible for vocal production can be investigated at three levels: respiratory, laryngeal, and supralaryngeal (Jürgens, 2002, Liebal et al., 2014). Whether the human larynx is truly different from that of other animals – particularly great apes – and whether this has any direct consequences for the uniqueness of human speech is under debate (Ankel-Simons, 2007, Fitch, 2012); thus, we assume here that the basic mechanisms of vocal production are similar in all primates,

Lateralization of the brain for vocal and emotional processing in primates

While lateralization has often been presented as a key specificity of the human brain, recent research has found similar effects in other primate brains in a broad array of studies ranging from gestural communication to listening to species-specific vocalizations (for a review, see Hopkins and Cantalupo, 2005). Nevertheless, many of the primate studies solely present behavioral evidence of lateralization and can therefore only be suggestive of the existence of such lateralization at the brain

Brain mechanisms involved in emotional processing in primates

In the visual domain, initial work done by Ekman in 1992 has suggested that positive and negative facial emotions are both expressed and understood in a universal manner in humans (Ekman, 1992). However, more recent work has revealed several limitations about the universality of emotion perception and the impact of human cultures on relevant visual information for emotional facial expression (Crivelli et al., 2016, Jack et al., 2012). Interestingly, a recent study compared the activation of the

Integrating brain mechanisms involved in vocal and emotional processing in primates

Our review has shown that much of the brain circuitry at work in the treatment of vocal signals, on the one hand, and emotional signals, on the other, appears to be highly conserved among primates and possibly with a gradient of similarity following the phylogenetic tree, with chimpanzees potentially closer to humans than monkeys to humans. The basic physical properties of the signal appear to be treated similarly across primates, as well as the subcortical structures responsible for their

Integrating intentional communication with emotional vocalizations in primates

Our review has also shown interesting convergences between the study of emotion and vocalizations in primates, suggesting that several aspects have to be taken into account when evaluating how primates process, evaluate, and categorize the emotional content of the calls they perceive. At the behavioral level, recent research has shown evidence that all primate calls should not be considered equally with respect to their emotional content. In particular, learned vocalizations (such as

Conclusion

To conclude, our review has shown that it is possible to combine the study of emotions and vocalizations in primates, without necessarily having to determine whether the emotional characteristic of primate vocalizations makes them innate by nature and impossible to control for the producer. We have shown that there are highly conserved cerebral structures and possibly patterns of connectivity involved in both the production and the perception of emotions and vocalizations in primates,

Acknowledgements

We thank the Swiss National Science Foundation (SNSF) for supporting the National Center of Competence in Affective Sciences (NCCR Grant 51NF40-104897 to DG) hosted by the Swiss Center for Affective Sciences. TG was supported by an SNSF Interdisciplinary Project (CR13I1_162720/1) grant by the SNSF during the writing of this article. TG thanks Christine Sievers for useful discussion about the content of this article. We thank three anonymous reviewers for their constructive comments on previous

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