Review
Measuring emotional processes in animals: the utility of a cognitive approach

https://doi.org/10.1016/j.neubiorev.2005.01.002Get rights and content

Abstract

Contemporary researchers regard emotional states as multifaceted, comprising physiological, behavioural, cognitive and subjective components. Subjective, conscious experience of emotion can be inferred from linguistic report in humans, but is inaccessible to direct measurement in non-human animals. However, measurement of other components of emotion is possible, and a variety of methods exist for monitoring emotional processes in animals by measuring behavioural and physiological changes. These are important tools, but they have limitations including difficulties of interpretation and the likelihood that many may be sensitive indicators of emotional arousal but not valence—pleasantness/unpleasantness. Cognitive components of emotion are a largely unexplored source of information about animal emotions, despite the fact that cognition–emotion links have been extensively researched in human cognitive science indicating that cognitive processes—appraisals of stimuli, events and situations—play an important role in the generation of emotional states, and that emotional states influence cognitive functioning by inducing attentional, memory and judgement biases. Building on this research, it is possible to design non-linguistic cognitive measures of animal emotion that may be especially informative in offering new methods for assessing emotional valence (positive as well as negative), discriminating same-valenced emotion of different types, identifying phenotypes with a cognitive predisposition to develop affective disorders, and perhaps shedding light on the issue of conscious emotional experiences in animals.

Introduction

When people experience a change in their emotional state or mood, there are concomitant changes in the way they think about the world (Bower, 1981, Mathews and MacLeod, 1985, Mellers et al., 1999). These cognitive changes occur in relation to emotions triggered briefly and discretely by known objects, and in relation to ongoing moods and longer-term emotional states associated with clinical affective disorders (Nygren et al., 1996, Mathews et al., 1996). They have been demonstrated in numerous tasks involving attention, perception, memory, expectations and risk assessment (Mathews and MacLeod, 1994, Mineka et al., 1998, Schwarz, 2000, Lerner and Keltner, 2000). Such tasks have been proposed as tools for assessing emotions and emotional reactions, particularly for people who might be unwilling or unable to give accurate self-report of the way they feel (Mayer and Bremer, 1985, Kuykendall et al., 1988, Parrott and Hertel, 1999). The purpose of this paper is to go one step further than this, and to review the potential value of using cognitive changes to assess emotion and mood states in non-human animals (hereafter, animals). We argue that theory and findings from this area of human psychology and cognitive science will help progress research on animal emotion, and that investigation of the role played by cognition in the generation and expression of emotional states in animals is critical to further development of our understanding of the processes and functions of affective systems in animals.

First, we consider definitions of the terms ‘emotion’ and ‘cognition’. We then briefly summarise methods by which animals' affective states are currently measured, and their limitations. We then present an overview of the cognition–emotion associations that occur in humans, and discuss theoretical accounts of these associations. Following this, we describe studies that have investigated cognition–emotion associations in animals, and show how theory and data from human research can provide a framework for generating novel non-linguistic techniques for measuring animal emotion. In concluding, we consider what cognitive methods for assessing animal affect might tell us about conscious emotion in animals.

In this paper, we use broad definitions of both emotion and cognition, while acknowledging that some of the researchers whose work we discuss may use these terms in more specific ways. We follow Shettleworth's (1998) comprehensive definition of cognition as referring to ‘the mechanisms by which animals acquire, process, store and act on information from the environment’. This definition can incorporate many different types of information processing, ranging from sensory perception and mechanisms of associative learning through to conscious, rational, linguistically based thought processes.

Emotions refer to processes which are likely to have evolved from basic mechanisms that gave animals the ability to avoid harm/punishment and seek valuable resources/reward (Panksepp, 1994, Rolls, 1999, Cardinal et al., 2002). For example, Rolls (1999) proposes that emotions are ‘states elicited by rewards and punishers, including changes in rewards and punishments’. Emotions include adaptive behavioural, physiological and neural processes and, in humans at least, they include a conscious subjective component—the feeling of the emotion (but see Zajonc, 1994, Winkielman and Berridge, 2004). Many scientists appear to be uncomfortable about using the term emotion when referring to animals, for fear that they automatically imply anthropomorphic assumptions of human-like subjective experience. Indeed, some psychologists maintain that the word emotion is best restricted to those states that clearly do include subjective feelings (Clore et al., 1994). To sidestep this issue, expressions like ‘emotional processes’ are used as code for the ‘not necessarily conscious emotion’ that occurs in animals (LeDoux, 1996). We too use this expression, but we also use the term emotion with the proviso that its use does not necessarily imply accompanying conscious, subjective states (Hinde, 1985, Berridge, 2003). Whenever we consider the conscious experience of emotion, we mention this explicitly.

‘Affect’ is another term commonly used by emotion researchers. Some (Clore et al., 1994, Berridge, 2003) regard affect as essentially involving the psychological qualities of pleasantness or unpleasantness (i.e. valence). However, we use the term here to refer to behavioural and physiological responses (and in conscious beings, feelings) that can vary both in terms of valence (pleasantness/unpleasantness) and also intensity (arousing or activating qualities). Indeed, valence and intensity/arousal can be considered to be the core features of affective and emotional processes.

The terms affect and emotion are often used interchangeably, and we will use them in this way. However, they are sometimes given specific and distinct meanings. In human research, affective states in their pure form can be viewed as largely equivalent to ‘free-floating’ mood states (Watson et al., 1988, Russell, 2003). On the other hand, emotion in its strictest sense refers to affective states that are attached in some way to an object. Thus, emotions are likely to involve a greater degree of information processing (e.g. appraisal of the object) than pure affective or mood states, and may also incorporate actions or ‘action tendencies’ (Frijda, 1986, Öhman et al., 2000) towards the object concerned (e.g. in anger, the tendency to hit). When we want to make a distinction between free-floating affect or mood, and object-focused emotions, we will make this clear in the text.

As should be clear from the above, human emotional processes and their outcomes are now generally regarded as multifaceted, comprising physiological, behavioural and subjective components (Lerner and Keltner, 2000, Frijda, 1986, Izard, 1977, Plutchik, 1980, Tomkins, 1980, Ekman, 1984, Scherer, 1984, Frijda, 1988, McNaughton, 1989, Smith and Lazarus, 1993, Lang, 1993, Bradley and Lang, 2000, Clore and Ortony, 2000). For example, fear may involve not only a subjective feeling of dread or terror, but also increased heart rate, sweaty palms, a facial grimace and an increased tendency to run away. Although these different components usually act in concert, they are potentially dissociable, not always operating as a functional whole (Meadows and Kaplan, 1994, Reisenzein, 2000). Emotional processes can thus be viewed as adaptive events or states that are likely to occur across the animal kingdom, but that may or may not have subjective components, depending on the species and circumstances involved (LeDoux, 1996, LeDoux, 1994). Such an outlook renders the non-conscious processes involved in emotional functioning open to empirical investigation, even in animals for whom conscious emotional experiences cannot be proven to occur (LeDoux, 1996), and allows independent investigation of the different facets of an emotional event (LeDoux, 1996, Tooby and Cosmoides, 1990, Levenson, 1994, Öhman, 1999).

This componential view of emotion also identifies a cognitive component—changes in information processing that occur in conjunction with changes in affect—to be an integral part of the emotional process (Clore and Ortony, 2000). This is in line with predominantly human-based cognitive theories of emotion, and with the ever increasing body of evidence linking biases in cognitive processing with affective state (Mathews and MacLeod, 1994, Mineka et al., 1998, Schwarz, 2000). But the blurring of boundaries between cognitive and affective processes remains controversial. Some take the view that emotional processes cannot occur independently of cognitive processes arguing that, for example, the mere act of identifying a stimulus is a cognitive process which must occur before an emotional response can be made (Forgas, 2000), or that cognitive evaluations of stimuli are always involved in emotions (Lazarus, 1999). Others argue that cognitive and emotional processes are essentially distinct, both conceptually and neurobiologically. Panksepp (2003), for example, strongly supports the traditional delineation of cognitive and affective processes in humans and animals alike. Although conceding that cognition and affect are often inextricably linked in normal humans, he regards the two systems as ultimately independent: functionally, anatomically, pharmacologically and phylogenetically. In particular, he regards the affect system as essentially subcortical, visceral and embodied. The cognitive system, although often working in concert with affect, he views as essentially cortical, evolutionarily more recent, and likely to show more variation across (e.g. mammalian) species. Zajonc, 1980, Zajonc, 2000 asserts a similar position with respect to humans, arguing that affective states can be induced with no cognitive involvement whatsoever (‘preferences without inferences’; see also Russell (2003)).

We agree that subcortical systems are central to the generation and expression of emotion and affect, but we also agree that in humans at least, cortical, cognitive processes are often intimately involved in the production and output of affective and emotional states. It is therefore of interest and importance to investigate whether and to what degree such processes are also involved in the affective states of animals. The extent to which our advocacy of research into cognition–emotion links in animals may be taken to support one or other position is unintentional. We merely propose that such links are of both practical and theoretical interest, and may in due course offer emotion researchers an extra dimension to the cognition–affect debate.

Section snippets

The measurement of emotional processes in animals

Measurement of the emotional or affective state of an animal is of interest to researchers in a number of fields, including affective neuroscience, psychopharmacology, evolutionary zoology, comparative psychology and animal welfare science. Although the ultimate goals of these disciplines are different, the challenge of reliably establishing the on-going affective state or emotional reaction of an animal to a stimulus or situation, is essentially the same. The problem is simple. Humans, on the

Cognitive components of emotional processing in humans

Cognitive processes can be regarded as ‘components’ of human emotion states or events, both in the form of appraisals which can trigger the occurrence of particular emotions, and cognitive outputs which can result from emotional states. To effectively interpret findings regarding emotion–cognition links in animals, and to drive further research in this area, attention must be paid to the processes by which affective states and cognitive processes interact. Human-based research in this area

Measuring the cognitive component of emotion in animals

As we outlined earlier, a wide variety of physiological and behavioural measures are currently used to indicate the emotional or affective states experienced by animals, though all have their limitations. Cognitive components of emotion are a relatively unexplored potential additional source of information about animal emotions (Toates, 1995, Mendl and Paul, 2004). Most of the cognitive outputs of emotion that have been studied experimentally in humans involve language-based tasks. However,

Conclusions

In humans, appraisals or cognitive processing of some kind appear to be involved in determining the occurrence of emotional events. Cognition is also a critical part of the expression or output of emotional processing. Biases in judgement, memory and attention have been repeatedly shown to vary according to emotional state. Indeed, even basic sensations such as pain appear to include cognitive components or correlates (Rainville, 2002).

Within clinical psychology, considerable interest has been

Acknowledgements

We thank BBSRC and UFAW for supporting our research in this area.

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