A framework for studying emotions across species

Abstract

Since the 19th century, there has been disagreement over the fundamental question of whether "emotions" are cause or consequence of their associated behaviors. This question of causation is most directly addressable in genetically tractable model organisms, including invertebrates such as Drosophila. Yet there is ongoing debate about whether such species even have "emotions," as emotions are typically defined with reference to human behavior and neuroanatomy. Here, we argue that emotional behaviors are a class of behaviors that express internal emotion states. These emotion states exhibit certain general functional and adaptive properties that apply across any specific human emotions like fear or anger, as well as across phylogeny. These general properties, which can be thought of as "emotion primitives," can be modeled and studied in evolutionarily distant model organisms, allowing functional dissection of their mechanistic bases and tests of their causal relationships to behavior. More generally, our approach not only aims at better integration of such studies in model organisms with studies of emotion in humans, but also suggests a revision of how emotion should be operationalized within psychology and psychiatry.

Figure 1

Charles Darwin's examples of emotional expressions. (a) Expression of terror in a human; (b) chimpanzee “disappointed and sulky;” (c, d) hostility in a cat (c) and a dog (d). From Darwin (1872).

Figure 2

Emotions as central, causative states. Proposed (a) and alternative (b) views of the causal relationship between emotions and behavior. (a) In our model, a central emotion state causes multiple parallel responses. “Stimuli” include both exteroceptive and interoceptive (feedback) components. (b) In more conventional views emotions are distinguished by multiple components that need to be coordinated and often synchronized (Barrett et al, 2007; Russell, 2003; Scherer, 2009; Salzman and Fusi, 2010). While we agree that emotions involve all these components, our view differs in not including these components as part of the emotion state itself, but rather as consequences of it. Reproduced with modification from (Moors, 2009).

Figure 3

The relationship between central emotion states and subjective feelings. (a, b) Behaviorist version of view in which emotional stimuli evoke behavior and other responses in animals (a) without the involvement of any causative central state. In humans (b) the subjective feeling of emotion is assumed to arise from our conscious awareness of the behavioral and somatic responses to the stimuli (James, 1884). (c, d) In our view, responses to emotional stimuli are mediated by central emotion states, which are evoked by those stimuli in both animals (c) and humans (d). Those central states produce subjective feelings in parallel with behavioral and somatic responses in humans (d). We argue that central states also play an important role in emotional expression in animals (c), irrespective of whether they have a subjective perception of those states or not.

Figure 4

Dimensional Models of Emotion. (a) A 2-D space representing what is often called “core affect”, the most popular construct in psychological theories of emotional experience (Barrett and Russell, 1999; Russell, 2003), but also applied more broadly to other animals (Mendl et al, 2010; Rolls, 1999). (b) Example of a multi-dimensional model for separating different emotions into different domains of a state-space. According to some views, the space in which emotion states can be located is extremely high-dimensional, consisting of all the different parameters one can measure (e.g., Salzman and Fusi, 2010) and essentially formalizing a multivariate version of emotion as depicted in Figure 2b. Fig. 2a reproduced with permission from Calder et al. (2001).

Figure 5

Examples of Darwin's Second Principle of Antithesis. According to this principle, opposite emotions produce behaviorally opposite expressions. (a) In humans, sadness (a1) and happiness (a2) are expressed by opposite configurations of the mouth. (b) Antithetical postures in dogs, from Darwin (1872). (c) A potential example of antithesis in Drosophila. Male flies elevate both wings close to the vertical in a “threat display” during agonistic interactions with conspecific males (c1), while they extend one wing horizontally to vibrate it in order to produce a courtship “song” during mating (c2). Axes indicate the different angles of view (c1, frontal; c2, overhead). This example also illustrates the social communication function of some types of emotional expression.

Figure 6

Experimental examples of persistent activity in flies and worms. (a) Persistent elevation of locomotor activity evoked by repeated mechanical startle (using brief air puffs) in Drosophila. From Lebestky et al. (2009). (b) Persistent roaming behavior in C. elegans evoked by optogenetic stimulation of a specific subset of interneurons under the control of the mod-1 promoter. (c) Circuit model summarizing control of persistent and opponent dwelling and roaming states (b, c, after Flavell et al. (2013)). (d) Transient optogenetic activation of P1 neurons in Drosophila using a red-shifted version of channelrhodopsin-2 (green bars) evokes persistent wing extension behavior (black rasters). (d after Inagaki et al., (2013).

Figure 7

Schematic illustrating components of the central circadian oscillator in Drosophila. PER, TIM, CYC and CLK are transcription factors that participate in a negative feedback autoregulatory loop. The output of this oscillator coordinates multiple organismal processes that display circadian periodicity. After Nitabach and Taghert (2008).