Neural Responses of Pet Dogs Witnessing Their Caregiver's Positive Interactions with a Conspecific: An fMRI Study

Abstract

We have limited knowledge on how dogs perceive humans and their actions. Various researchers investigated how they process human facial expressions, but their brain responses to complex social scenarios remain unclear. While undergoing fMRI, we exposed pet dogs to videos showing positive social and neutral nonsocial interactions between their caregivers and another conspecific. Our main interest was how the dogs responded to their caregivers (compared to a stranger) engaging in a pleasant interaction with another dog that could be seen as social rival. We hypothesized that the dogs would show activation increases in limbic areas such as the amygdala, hypothalamus, and insula and likely show higher attention and arousal during the positive caregiver-dog interaction. When contrasting the social with the nonsocial interaction, we found increased activations in the left amygdala and the insular cortex. Crucially, the dogs' hypothalamus showed strongest activation when the caregiver engaged in a positive social interaction. These findings indicate that dogs are sensitive to social affective human-dog interactions and likely show higher valence attribution and arousal in a situation possibly perceived as a potential threat to their caregiver bonds. Our study provides a first window into the neural correlates of social and emotional processing in dogs.

Keywords: attachment; canine neuroimaging; human–animal interaction.

Figure 1

Human–dog interaction video scenes. Caregiver (A and B) and stranger (C and D) in the either social interaction (A and C) or nonsocial interaction (B and D); experimental design and time course of fMRI task (E).

Figure 2

Viewing of human–dog interaction. Compared to baseline, activation was observed in the ectomarginalis, splenialis, sylvius, ectosylvius, and suprasylvius gyri (see Table 1). Statistical parametric maps were thresholded on voxel-level at P < 0.005 uncorrected and on cluster-level at P < 0.05 FWE-corrected for multiple comparisons.

Figure 3

Social versus Nonsocial Interactions. Activation was observed in four bilateral clusters comprising the gyrus suprasylvius, gyrus sylvius rostralis, and gyrus ectosylvius rostralis (see Table 2). Statistical parametric map was thresholded on voxel-level at P < 0.005 uncorrected and on cluster-level at P < 0.05 FWE-corrected for multiple comparisons.

Figure 4

Interaction of (Caregiver vs. Stranger) versus (Social vs. Nonsocial). Contrast was defined as (Caregiver Social—Caregiver Nonsocial)—(Stranger Social—Stranger Nonsocial). Hypothalamus activation was found for the target contrast, t = 5.68, P = 0.00007, cluster size = 27 mm³ or 8 voxels, surviving P < 0.05 FWE small volume correction using the hypothalamus anatomical mask. Additionally, a VOI analysis for the hypothalamus revealed a significant effect for the target contrast t = 1.83, P < 0.0473.

Figure 5

Volume of interest analysis. Activation for the social versus nonsocial conditions was increased in the left amygdala, bilateral insular cortex, bilateral ectosylvian gyrus and bilateral gyrus suprasylvian medius. Y-axes depict parameter estimates [a.u.] and error bars indicate the standard error of the mean.