The neural basis of understanding the expression of the emotions in man and animals

Abstract

Humans cannot help but attribute human emotions to non-human animals. Although such attributions are often regarded as gratuitous anthropomorphisms and held apart from the attributions humans make about each other's internal states, they may be the product of a general mechanism for flexibly interpreting adaptive behavior. To examine this, we used functional magnetic resonance imaging (fMRI) in humans to compare the neural mechanisms associated with attributing emotions to humans and non-human animal behavior. Although undergoing fMRI, participants first passively observed the facial displays of human, non-human primate and domestic dogs, and subsequently judged the acceptability of emotional (e.g. 'annoyed') and facial descriptions (e.g. 'baring teeth') for the same images. For all targets, emotion attributions selectively activated regions in prefrontal and anterior temporal cortices associated with causal explanation in prior studies. These regions were similarly activated by both human and non-human targets even during the passive observation task; moreover, the degree of neural similarity was dependent on participants' self-reported beliefs in the mental capacities of non-human animals. These results encourage a non-anthropocentric view of emotion understanding, one that treats the idea that animals have emotions as no more gratuitous than the idea that humans other than ourselves do.

Keywords: anthropomorphism; emotion attribution; face perception; social cognition.

Fig. 1

Experimental design. (a) In the Implicit Task, participants perform a visual one-back on a series of naturalistic images showing human, non-human primate, and dog facial displays. Images appear in an event-related design intermixed with a phase-scrambled subset of the same images which provided a baseline for univariate contrasts. We refer to the task as ‘implicit’ only to designate that at the time of performing the task, participants were not explicitly directed to attend to or think about the images in a particular way, and were naïve to the fact that in a subsequent task they would be asked to consider the emotional states of each target. (b) The sequence of screens from an example trial in the Explicit Task, which participants learn about only after completing the Implicit Task. The task features the same images used in the Implicit Task (excluding scrambles). Each image is presented twice, once preceded by a verbal cue directing participants to accept or reject an emotion attribution about the target, and once by a verbal cue directing participants to accept or reject an expression attribution about the target (all verbal cues presented in Table 1). Once the image appears, participants have 1750 ms to commit a ‘Yes/No’ manual response. Every cue preceded an equal number of images from each target type and elicited a response of either ‘Yes’ (two-third of trials) or ‘No’ (one-third of trials) in the majority of respondents in an independent sample.

Fig. 2

Percent signal change in a priori ROIs. For each ROI, the leftmost set of bars represent the mean response across voxels (relative to fixation baseline) to the six conditions of the Explicit Task; the rightmost set of bars represent the mean response across voxels to each target in the Implicit Task (relative to the response to the scramble stimulus condition). For further details on the ROIs, see the main text and Supplementary Table S1. Statistical tests corresponding to the data plotted here are presented in Tables 3 and 4. OFC, orbitofrontal cortex; TPJ, temporoparietal junction; aSTS, anterior superior temporal sulcus; dmPFC, dorsomedial prefrontal cortex.

Fig. 3

Whole-brain analysis of target-independent effects. Statistical maps are cluster-level corrected at a FWE rate of 0.05. (a) ‘Explicit Task’. Regions showing significantly positive or negative responses in the ‘Emotion > Expression’ contrast for all targets. (b) ‘Implicit Task’. Regions showing a significantly positive response in the ‘Face  > Scramble’ contrast for all targets. (c) ‘Explicit/Implicit Task Conjunction’. The region of dorsomedial prefrontal cortex showing a target independent-effect in both tasks.

Fig. 4

Whole-brain analysis of target-dependent effects. Statistical maps are cluster-level corrected at a FWE rate of 0.05. (a) ‘Explicit Task’. Regions showing a differential response to Human targets relative to both Non-human targets (collapsing the ‘Emotion/Expression’ factor). (b) ‘Implicit Task’. Regions showing a differential response to Human targets relative to both Non-human targets.