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.

From automata to animate beings: the scope and limits of attributing socialness to artificial agents

“…Integrating findings and approaches from additional related fields stands to advance understanding of not only the factors that drive the attribution of socialness to artificial agents, but also the temporal dynamics. To this end, future work could benefit from considering work on human attachment and relationship formation, as well as the emerging field of human–animal interactions . Studies on these latter interactions not only provide converging evidence on behavioral and brain mechanisms of socialness attribution, but also can help us to understand how long‐term interaction with nonhuman agents shapes these attributions over time by studying pet owners versus nonpet owners .…”

“…To this end, future work could benefit from considering work on human attachment and relationship formation, as well as the emerging field of human–animal interactions . Studies on these latter interactions not only provide converging evidence on behavioral and brain mechanisms of socialness attribution, but also can help us to understand how long‐term interaction with nonhuman agents shapes these attributions over time by studying pet owners versus nonpet owners . Thus, thinking openly and creatively about how work from distinct but complementary disciplines might inform our understanding about humans’ evolving relationship with socially savvy technology.…”

From automata to animate beings: The scope and limits of attributing socialness to artificial agents

“…Integrating findings and approaches from additional related fields stands to advance understanding of not only the factors that drive the attribution of socialness to artificial agents, but also the temporal dynamics. To this end, future work could benefit from considering work on human attachment and relationship formation 171 , as well as the emerging field of human-animal interactions [172][173][174] . Studies on these latter interactions not only provide converging evidence on behavioural and brain mechanisms of socialness attribution 173 , but also can help us to understand how long-term interaction with non-human agents shapes these attributions over time by studying pet owners versus non-pet owners 172,174 .…”

The neuroscience of understanding the emotions of others

“…These regions are thought to implement executive functions for retrieving relevant abstract knowledge and selecting among competing interpretations of complex stimuli (Satpute, Badre, & Ochsner, 2013; Fairhall & Caramazza, 2013; Goldberg, Perfetti, Fiez, & Schneider, 2007; Green, Fugelsang, Kraemer, Shamosh, & Dunbar, 2006), functions that, in the domain of emotional and social inference, typically take the form of mental-state inferences (Spunt, Ellsworth, & Adolphs, 2016; Spunt, Kemmerer, & Adolphs, 2016; Skerry & Saxe, 2015; Kim et al, 2015; Skerry & Saxe, 2014). Indeed, meta-analyses of neuroimaging studies of theory-of-mind reasoning in its various forms reliably implicate these same regions (Van Overwalle & Baetens, 2009; Amodio & Frith, 2006; Gallagher & Frith, 2003), and the specific association with tasks used to assess theory-of-mind is particularly reliable for the dmPFC (Schurz, Radua, Aichhorn, Richlan, & Perner, 2014).…”

“…Addressing both of these issues will require careful attention to task design, and will likely require obtaining behavioral performance measures as well as experimental designs informed by computational models. It will also require a close consideration of individual differences (e.g., goals, beliefs, prior experience) that might lead different observers to different interpretations of an emotional stimulus (e.g., Spunt & Adolphs, 2015; Spunt, Ellsworth, & Adolphs, 2016). …”