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Full-Text PDF (Final Published Version) Paul, E. S. , Sher, S., Tamietto, M., Winkielman, P., & Mendl, M. T. (2020). Towards a comparative science of emotion: Affect and Consciousness in humans and animals. Neuroscience and Biobehavioral Reviews, 108, 749-770. https://doi.org/10.1016/j.neubiorev.2019.11.014 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.1016/j.neubiorev.2019.11.014 Link to publication record in Explore Bristol Research PDF-document This is the final published version of the article (version of record). It first appeared online via Elsevier at https://www.sciencedirect.com/science/article/pii/S0149763419303677. Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/red/research-policy/pure/user-guides/ebr-terms/ Neuroscience and Biobehavioral Reviews 108 (2020) 749–770 Contents lists available at ScienceDirect Neuroscience and Biobehavioral Reviews journal homepage: www.elsevier.com/locate/neubiorev Review article Towards a comparative science of emotion: Affect and consciousness in humans and animals T Elizabeth S. Paula,*, Shlomi Sherb, Marco Tamiettoc,d, Piotr Winkielmane,f, Michael T. Mendla a Bristol Veterinary School, University of Bristol, Langford House, Langford, Bristol, BS40 5DU, UK b Department of Psychology, Pomona College, Claremont, CA, USA c Department of Medical and Clinical Psychology, Tilburg University, Tilburg, the Netherlands d Department of Psychology, University of Torino, Torino, Italy e Department of Psychology, University of California, San Diego, La Jolla, CA, 92093, USA f Faculty of Psychology, SWPS University of Social Sciences and Humanities, 03-815, Warsaw, Poland ARTICLE INFO ABSTRACT Keywords: The componential view of human emotion recognises that affective states comprise conscious, behavioural, Affect physiological, neural and cognitive elements. Although many animals display bodily and behavioural changes Animals consistent with the occurrence of affective states similar to those seen in humans, the question of whether and in Componential which species these are accompanied by conscious experiences remains controversial. Finding scientifically valid Consciousness methods for investigating markers for the subjective component of affect in both humans and animals is central Interoception to developing a comparative understanding of the processes and mechanisms of affect and its evolution and Neural correlates Subjective emotion distribution across taxonomic groups, to our understanding of animal welfare, and to the development of animal Unconscious emotion models of affective disorders. Here, contemporary evidence indicating potential markers of conscious processing in animals is reviewed, with a view to extending this search to include markers of conscious affective processing. We do this by combining animal-focused approaches with investigations of the components of conscious and non-conscious emotional processing in humans, and neuropsychological research into the structure and func- tions of conscious emotions. 1. Introduction species have the capacity for consciousness of any kind, emotional or other (e.g. Dawkins, 2000, 2001, 2017; LeDoux, 1996; Macphail, 1998; For humans, emotions are quintessentially about feelings: con- Rolls, 1999, 2005, 2007; although see Panksepp, 1994, 2005; and sciously experienced, subjectively focused, reportable, affective states. Wemelsfelder, 2001, for alternative views). And second, for those spe- Measuring these states seems easy enough; all we need to do is ask. On cies with a capacity for consciousness, we do not have methods for closer inspection, complications arise: Different methodologies and establishing whether and what sorts of conscious emotions they ex- questionnaires may tap different facets of felt emotion or affect, and perience. there may not always be perfect correspondence between their findings. These problems are relevant to almost all scientists studying non- Some people will be poor at recognising or articulating their emotions, human affect. The expanding field of affective neuroscience relies while others will lie about how they actually feel. And when emotion heavily on comparative studies of emotion or emotion-like states in reports have a retrospective component, they can be subject to con- both humans and animals (e.g. Alcaro et al., 2007; Berridge, 2000; structive biases of memory (Redelmeier and Kahneman, 1996). But, Buchel and Dolan, 2000; Lang et al., 2000; LeDoux, 2000; Phelps and ultimately, the gold standard of subjective emotion measurement in LeDoux, 2005). Much animal-based research in psychopharmacology healthy adult humans remains linguistic report (Barrett, 2006a; Bradley makes use of parallels between the emotional systems of humans and and Lang, 2000; LeDoux, 2014a, LeDoux and Hoffmann, 2018; Oatley other species (e.g. Frazer and Morilak, 2005; Haug and Whalen, 1999; and Jenkins, 1996). Unfortunately, this state of affairs leaves a major Pawlak et al., 2008). But we cannot make confident comparisons be- problem for anyone interested in conscious emotional or affective states tween humans and animals in the critical domain of conscious affect. in non-human animals, because animals cannot tell us how they feel. In For example, when pharmacological interventions have parallel effects fact, the problem is twofold. First, we do not know for sure which on aspects of human and animal behaviour, it is reasonable to suppose, ⁎ Corresponding author. E-mail address: [email protected] (E.S. Paul). https://doi.org/10.1016/j.neubiorev.2019.11.014 Received 1 May 2019; Received in revised form 8 October 2019; Accepted 18 November 2019 Available online 26 November 2019 0149-7634/ © 2019 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/BY/4.0/). E.S. Paul, et al. Neuroscience and Biobehavioral Reviews 108 (2020) 749–770 but difficult to decisively demonstrate, that they have similar effects on attentional, perceptual, and inferential processes (appraisals), (iii) ac- feelings or conscious experiences (e.g. Kregiel et al., 2016; Vera-Chang tion—–changes in the predisposition for or execution of specific re- et al., 2018). Animal welfare researchers face a similar problem. The sponses, (iv) expression—–changes in facial, vocal, postural appear- evaluation of interventions to improve the well-being of animals is ance, and (v) physiology—–changes in physiological and neural limited by our capacity to identify the character, or even the existence, activity. of their conscious affective states (Dawkins, 2017; Mendl and Paul, The use of terms and definitions in the context of animal emotions 2004). has long been a matter of confusion and controversy (e.g. see Duffy, Traditionally, the topic of conscious affect in animals has been re- 1934; Mandler, 1975). Whether words such as “emotion”, “fear”, garded as all but taboo, with the possibility of conscious processes in “sadness” or “joy” should ever be used when talking about animals has animals having long been seen as fundamentally inaccessible to em- been extensively debated (e.g. see Berridge, 2018; Damasio, 1999; pirical investigation (e.g. LeDoux, 1996; Skinner, 1953). But in recent Davidson, 2003; LeDoux, 1996, 2014a; LeDoux and Hofmann, 2018; years there has been a rapid expansion of the fields of comparative Winkielman and Berridge, 2004). LeDoux (1996, 2012, 2014a, LeDoux emotion and affective neuroscience (e.g. see Anderson and Adolphs, and Brown, 2017; LeDoux and Hofmann, 2018) has suggested that the 2014; de Waal, 2011; Mendl et al., 2010; Paul et al., 2005), and over a words “emotion” and “fear” by themselves imply human-like conscious similar period, there has been an equally dramatic rise in research into or phenomenal states and inner experiences, and proposes instead that the neuroscience of consciousness (e.g., Dehaene, 2014; Koch et al., terms such as “emotional processing” and “survival circuits” should be 2016). Together and in turn, these developments have prompted some used with regard to animals. Damasio (1994) used the phrase “primary early signs of serious academic interest in the study of conscious affect emotions” to refer to the automatic emotional processes in animals and and its evolutionary antecedents, with a number of recently published humans that are not necessarily conscious, and “feelings” to refer to papers considering this difficult issue directly (Berridge, 2018; LeDoux those that are. Berridge and colleagues (Berridge, 2000; Berridge et al., and Hofmann, 2018Paul and Mendl, 2018; Smith and Lane, 2015, 2009; Winkielman and Berridge, 2004) have used quotation marks 2016). In the present review, we focus on the methodological and around the terms “liking” and “wanting” to highlight agnosticism re- theoretical issues emerging from studies of human consciousness and garding the presence or absence of conscious experience of these states human emotion which are directly pertinent to investigations of con- in experimental animals. scious affective processes in animals. We take the view that, in the absence of an entirely new nomen- In Section 2, we start with a brief discussion of emotion terminol- clature, “emotion” in its broadest sense, remains convenient to use as an ogies in the context
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