Exploring the dog–human relationship by combining fMRI, eye-tracking and behavioural measures

www.nature.com/scientificreports OPEN Exploring the dog–human relationship by combining fMRI, eye‑tracking and behavioural measures Sabrina Karl1*, Magdalena Boch2,3, Anna Zamansky4, Dirk van der Linden5, Isabella C. Wagner2, Christoph J. Völter1, Claus Lamm2,6 & Ludwig Huber1,6 Behavioural studies revealed that the dog–human relationship resembles the human mother–child bond, but the underlying mechanisms remain unclear. Here, we report the results of a multi-method approach combining fMRI (N = 17), eye-tracking (N = 15), and behavioural preference tests (N = 24) to explore the engagement of an attachment-like system in dogs seeing human faces. We presented morph videos of the caregiver, a familiar person, and a stranger showing either happy or angry facial expressions. Regardless of emotion, viewing the caregiver activated brain regions associated with emotion and attachment processing in humans. In contrast, the stranger elicited activation mainly in brain regions related to visual and motor processing, and the familiar person relatively weak activations overall. While the majority of happy stimuli led to increased activation of the caudate nucleus associated with reward processing, angry stimuli led to activations in limbic regions. Both the eye-tracking and preference test data supported the superior role of the caregiver’s face and were in line with the findings from the fMRI experiment. While preliminary, these findings indicate that cutting across different levels, from brain to behaviour, can provide novel and converging insights into the engagement of the putative attachment system when dogs interact with humans. The unique relationship between (pet) dogs and their human caregivers bears a remarkable resemblance to the attachment bond of human infants with their mothers: dogs are dependent on human care and their behaviour seems specifically geared to engage their human partner’s caregiving system1. Some researchers (e.g.2–4) have used concepts and methodologies of the human attachment t heory5,6 to investigate whether the dog–human relationship conforms to the characteristics of the human attachment bond (reviewed i n7). In humans, the original theory of attachment has focused on parental attachment, the strong and persistent emotional tie between the child and the caregiver that develops very early in life and serves to protect the child5,6. The proximate function is to maintain the proximity between the mother and the child, especially in stressful or dangerous situations8. To distinguish true attachment from other affectional bonds, four behavioural criteria were proposed: (a) staying near to and resisting separation from the attachment figure (proximity maintenance), (b) feeling distress upon involuntary separation from the attachment figure (separation distress), (c) using the attachment figure as a base for exploring the environment free of anxiety (secure base), (d) seeking out the attachment figure for contact and assurance in times of emotional distress (safe haven)9. A classic test paradigm to characterize attachment relationships is the Strange Situation Procedure (SSP), a set of short episodes of mildly stressful situations of separation and reunion in an unfamiliar e nvironment10–12. Comparative psychologists not only have described the similarities of the human mother–child bond and the human–dog r elationship13–15, but also sought empirical evidence by applying modified versions of the Strange Situation Procedure. Indeed, 1 Clever Dog Lab, Comparative Cognition, Messerli Research Institute, University of Veterinary Medicine Vienna, Medical University of Vienna, University of Vienna, 1210 Vienna, Austria. 2Social, Cognitive and Affective Neuroscience Unit, Department of Cognition, Emotion, and Methods in Psychology, Faculty of Psychology, University of Vienna, 1010 Vienna, Austria. 3Department of Cognitive Biology, Faculty of Life Sciences, University of Vienna, 1090 Vienna, Austria. 4Information Systems Department, University of Haifa, 3498838 Haifa, Israel. 5Department of Computer and Information Sciences, Northumbria University, Newcastle‑upon‑Tyne NE1 8ST, UK. 6These authors contributed equally: Claus Lamm and Ludwig Huber. *email: Sabrina.Karl@ vetmeduni.ac.at Scientific Reports | (2020) 10:22273 | https://doi.org/10.1038/s41598-020-79247-5 1 Vol.:(0123456789) www.nature.com/scientificreports/ researchers found clear evidence of all four attachment criteria in dogs2,3,16–24. Even more striking, the secure base effect in dogs is specific and tuned to the bond with the caregiver25,26. That the bond between (adult) dogs and the human caregiver is similar to the one between human infants and their mother is an exciting hypothesis, but so far it relies mainly on behavioural and endocrinal evidence. A rigorous test of this hypothesis requires knowledge of the neural networks associated with attachment-related processes. So far, we know that humans share with almost all vertebrates a basic diencephalic and tegmental “social behaviour network”27. Neuroimaging studies of human mothers viewing their children showed that intimate parent–child emotional states are connected to functionally specialized brain areas28. This includes, foremost, areas of the so-called limbic system, including the amygdala, the ventral striatum, the ventral tegmental area (VTA), the globus pallidus (GP29) and the substantia nigra, as well as the h ippocampus30. These areas, in humans but also more generally in mammals, are usually associated with affective processes, and may thus support the activation of human attachment-related functions in parenting. In addition, the orbitofrontal cortex (OFC) and the periaqueductal grey (PAG31), the dorsal anterior cingulate cortex (dACC), the anterior insula (AI) and the ventrolateral prefrontal cortex (VLPFC32,33) show increased activation in mothers upon seeing their own child. Especially seeing their own child’s smiling face caused increased activation of these mesocorticolimbic reward brain regions in their mothers34. Unfortunately, it is not clear if the same brain regions are activated when the child faces its mother. Several recent studies have investigated how dogs perceive humans, and in particular our faces. These revealed that dogs can assess humans’ attentional s tates35,36, and discriminate their caregiver from another familiar person37, or from a s tranger38; the latter was confirmed by converging evidence from two studies using different methods, combining active choice on a touchscreen d evice39 and passive looking preference using an eye-tracking device40. Especially interesting is the dog’s ability to discriminate between positive and negative facial expressions of humans and to react appropriately conferring to the valence of the faces41–46 (for review see47). Neuroimaging provides an excellent window into the working brain of humans during perception and the associated mental processes, and this non-inva (...truncated)