Functional mapping of the somatosensory cortex using noninvasive fMRI and touch in awake dogs.

Dogs are increasingly used as a model for neuroscience due to their ability to undergo functional MRI fully awake and unrestrained, after extensive behavioral training. Still, we know rather little about dogs' basic functional neuroanatomy, including how basic perceptual and motor functions are localized in their brains. This is a major shortcoming in interpreting activations obtained in dog fMRI. The aim of this preregistered study was to localize areas associated with somatosensory processing. To this end, we touched N = 22 dogs undergoing fMRI scanning on their left and right flanks using a wooden rod. We identified activation in anatomically defined primary and secondary somatosensory areas (SI and SII), lateralized to the contralateral hemisphere depending on the side of touch, and importantly also activation beyond SI and SII, in the cingulate cortex, right cerebellum and vermis, and the sylvian gyri. These activations may partly relate to motor control (cerebellum, cingulate), but also potentially to higher-order cognitive processing of somatosensory stimuli (rostral sylvian gyri), and the affective aspects of the stimulation (cingulate). We also found evidence for individual side biases in a vast majority of dogs in our sample, pointing at functional lateralization of somatosensory processing. These findings not only provide further evidence that fMRI is suited to localize neuro-cognitive processing in dogs, but also expand our understanding of in vivo touch processing in mammals, beyond classically defined primary and secondary somatosensory cortices.

Functionally analogous body- and animacy-responsive areas are present in the dog (Canis familiaris) and human occipito-temporal lobe.

Comparing the neural correlates of socio-cognitive skills across species provides insights into the evolution of the social brain and has revealed face- and body-sensitive regions in the primate temporal lobe. Although from a different lineage, dogs share convergent visuo-cognitive skills with humans and a temporal lobe which evolved independently in carnivorans. We investigated the neural correlates of face and body perception in dogs (N = 15) and humans (N = 40) using functional MRI. Combining univariate and multivariate analysis approaches, we found functionally analogous occipito-temporal regions involved in the perception of animate entities and bodies in both species and face-sensitive regions in humans. Though unpredicted, we also observed neural representations of faces compared to inanimate objects, and dog compared to human bodies in dog olfactory regions. These findings shed light on the evolutionary foundations of human and dog social cognition and the predominant role of the temporal lobe.

Validation of a New Coil Array Tailored for Dog Functional Magnetic Resonance Imaging Studies.

Comparative neuroimaging allows for the identification of similarities and differences between species. It provides an important and promising avenue, to answer questions about the evolutionary origins of the brain´s organization, in terms of both structure and function. Dog functional magnetic resonance imaging (fMRI) has recently become one particularly promising and increasingly used approach to study brain function and coevolution. In dog neuroimaging, image acquisition has so far been mostly performed with coils originally developed for use in human MRI. Since such coils have been tailored to human anatomy, their sensitivity and data quality is likely not optimal for dog MRI. Therefore, we developed a multichannel receive coil (K9 coil, read "canine") tailored for high-resolution functional imaging in canines, optimized for dog cranial anatomy. In this paper we report structural (n = 9) as well as functional imaging data (resting-state, n = 6; simple visual paradigm, n = 9) collected with the K9 coil in comparison to reference data collected with a human knee coil. Our results show that the K9 coil significantly outperforms the human knee coil, improving the signal-to-noise ratio (SNR) across the imaging modalities. We noted increases of roughly 45% signal-to-noise in the structural and functional domain. In terms of translation to fMRI data collected in a visual flickering checkerboard paradigm, group-level analyses show that the K9 coil performs better than the knee coil as well. These findings demonstrate how hardware improvements may be instrumental in driving data quality, and thus, quality of imaging results, for dog-human comparative neuroimaging.

Pet dogs' Behavioural Reaction to Their Caregiver's Interactions with a Third Party: Join in or Interrupt?

Pet dogs are promising candidates to study attachment-related and potentially jealousy-like behaviours in non-human animals, as they form a strong and stable bond with their human caregivers who often engage in affiliative interactions with diverse social partners. Nevertheless, it is still debated whether non-human animals are capable of experiencing such complex emotions. Even though caregivers frequently report observations of jealousy-like behaviours in dogs, behavioural studies in dogs have thus far led to contradictory results. Adding to this complexity, dogs appear extraordinarily skilled in understanding humans' communicative behaviour and can flexibly and diversely interact with them in social contexts. Here, we aimed at investigating (1) whether dogs indeed respond in a jealousy-consistent manner when seeing their caregiver interact in an affiliative way with a remotely controlled, realistic-looking fake dog, or (2) whether they would rather synchronize their reaction to the fake dog with the caregiver's behaviour, or (3) whether they respond directly to the caregiver without paying much attention to the third party. To address what drives the dogs' behaviours in this triadic situation, we compared four groups of dogs who first observed and then joined the interaction of either the caregiver or a stranger greeting or medically examining the fake dog. We found that the dogs initially responded negatively or neutrally when the fake dog entered the room but changed to more positive reactions when the caregiver approached the fake dog, especially if initiating a positive interaction. When being released, more dogs showed friendly behaviours towards the fake dog when the caregiver-rather than the stranger-was interacting with it. At the same time, however, the dogs tried to block the interaction of the caregiver with the fake dog more often than the one of the stranger. In conclusion, we did not find clear evidence for jealousy-like behaviours in dogs during the human-fake dog interactions, but we observed indicators of behavioural synchronization with the caregivers, suggesting that the caregivers' affiliative behaviours directed at a third party may more often facilitate positive than negative interactions in dogs.

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

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.

Tailored haemodynamic response function increases detection power of fMRI in awake dogs (Canis familiaris).

Functional magnetic resonance imaging (fMRI) of awake and unrestrained dogs (Canis familiaris) has been established as a novel opportunity for comparative neuroimaging, promising important insights into the evolutionary roots of human brain function and cognition. However, data processing and analysis pipelines are often derivatives of methodological standards developed for human neuroimaging, which may be problematic due to profound neurophysiological and anatomical differences between humans and dogs. Here, we explore whether dog fMRI studies would benefit from a tailored dog haemodynamic response function (HRF). In two independent experiments, dogs were presented with different visual stimuli. BOLD signal changes in the visual cortex during these experiments were used for (a) the identification and estimation of a tailored dog HRF, and (b) the independent validation of the resulting dog HRF estimate. Time course analyses revealed that the BOLD signal in the primary visual cortex peaked significantly earlier in dogs compared to humans, while being comparable in shape. Deriving a tailored dog HRF significantly improved the model fit in both experiments, compared to the canonical HRF used in human fMRI. Using the dog HRF yielded significantly increased activation during visual stimulation, extending from the occipital lobe to the caudal parietal cortex, the bilateral temporal cortex, into bilateral hippocampal and thalamic regions. In sum, our findings provide robust evidence for an earlier onset of the dog HRF in two visual stimulation paradigms, and suggest that using such an HRF will be important to increase fMRI detection power in canine neuroimaging. By providing the parameters of the tailored dog HRF and related code, we encourage and enable other researchers to validate whether our findings generalize to other sensory modalities and experimental paradigms.

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

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.

Dogs accurately track a moving object on a screen and anticipate its destination.

The prediction of upcoming events is of importance not only to humans and non-human primates but also to other animals that live in complex environments with lurking threats or moving prey. In this study, we examined motion tracking and anticipatory looking in dogs in two eye-tracking experiments. In Experiment 1, we presented pet dogs (N = 14) with a video depicting how two players threw a Frisbee back and forth multiple times. The horizontal movement of the Frisbee explained a substantial amount of variance of the dogs' horizontal eye movements. With increasing duration of the video, the dogs looked at the catcher before the Frisbee arrived. In Experiment 2, we showed the dogs (N = 12) the same video recording. This time, however, we froze and rewound parts of the video to examine how the dogs would react to surprising events (i.e., the Frisbee hovering in midair and reversing its direction). The Frisbee again captured the dogs' attention, particularly when the video was frozen and rewound for the first time. Additionally, the dogs looked faster at the catcher when the video moved forward compared to when it was rewound. We conclude that motion tracking and anticipatory looking paradigms provide promising tools for future cognitive research with canids.

Training pet dogs for eye-tracking and awake fMRI.

In recent years, two well-developed methods of studying mental processes in humans have been successively applied to dogs. First, eye-tracking has been used to study visual cognition without distraction in unrestrained dogs. Second, noninvasive functional magnetic resonance imaging (fMRI) has been used for assessing the brain functions of dogs in vivo. Both methods, however, require dogs to sit, stand, or lie motionless while yet remaining attentive for several minutes, during which time their brain activity and eye movements are measured. Whereas eye-tracking in dogs is performed in a quiet and, apart from the experimental stimuli, nonstimulating and highly controlled environment, MRI scanning can only be performed in a very noisy and spatially restraining MRI scanner, in which dogs need to feel relaxed and stay motionless in order to study their brain and cognition with high precision. Here we describe in detail a training regime that is perfectly suited to train dogs in the required skills, with a high success probability and while keeping to the highest ethical standards of animal welfare-that is, without using aversive training methods or any other compromises to the dog's well-being for both methods. By reporting data from 41 dogs that successfully participated in eye-tracking training and 24 dogs IN fMRI training, we provide robust qualitative and quantitative evidence for the quality and efficiency of our training methods. By documenting and validating our training approach here, we aim to inspire others to use our methods to apply eye-tracking or fMRI for their investigations of canine behavior and cognition.