Comprehensive Pet Therapy, Sandy Springs, GA, USA DOI Published 2014-09-30 Accepted 2014-09-04 Received 2014-07-03 Academic Editor Subject Areas,, Keywords fMRI, Canine cognition, Animal temperament, Caudate, Neuroimaging, Comparative neuroscience, Reward systems Copyright © 2014 Cook et al. Licence This is an open access article distributed under the terms of the, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed.

For attribution, the original author(s), title, publication source (PeerJ) and either DOI or URL of the article must be cited. Cite this article Cook PF, Spivak M, Berns GS. One pair of hands is not like another: caudate BOLD response in dogs depends on signal source and canine temperament. PeerJ 2: e596. Having previously used functional MRI to map the response to a reward signal in the ventral caudate in awake unrestrained dogs, here we examined the importance of signal source to canine caudate activation.

Hand signals representing either incipient reward or no reward were presented by a familiar human (each dog’s respective handler), an unfamiliar human, and via illustrated images of hands on a computer screen to 13 dogs undergoing voluntary fMRI. All dogs had received extensive training with the reward and no-reward signals from their handlers and with the computer images and had minimal exposure to the signals from strangers. All dogs showed differentially higher BOLD response in the ventral caudate to the reward versus no reward signals, and there was a robust effect at the group level.

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Further, differential response to the signal source had a highly significant interaction with a dog’s general aggressivity as measured by the C-BARQ canine personality assessment. Dogs with greater aggressivity showed a higher differential response to the reward signal versus no-reward signal presented by the unfamiliar human and computer, while dogs with lower aggressivity showed a higher differential response to the reward signal versus no-reward signal from their handler. This suggests that specific facets of canine temperament bear more strongly on the perceived reward value of relevant communication signals than does reinforcement history, as each of the dogs were reinforced similarly for each signal, regardless of the source (familiar human, unfamiliar human, or computer). A group-level psychophysiological interaction (PPI) connectivity analysis showed increased functional coupling between the caudate and a region of cortex associated with visual discrimination and learning on reward versus no-reward trials. Our findings emphasize the sensitivity of the domestic dog to human social interaction, and may have other implications and applications pertinent to the training and assessment of working and pet dogs.

Introduction The domestic dog is a rising star in behavioral neuroscience due both to his high trainability and likely co-evolution with humans over the last 10,000–30,000 years. Recently, dogs have even proved amenable to participation in awake, unrestrained neuroimaging, allowing researchers to further probe the workings of the canine mind in a non-invasive and ethical method (). The picture that is emerging suggests dogs are highly sensitive to social context and cues, both from other dogs and from humans. Unsurprisingly for a highly social species, dogs use an extensive and nuanced vocabulary of cues in both affiliative and antagonistic interactions with conspecifics (;;; ); they are perhaps more unique in their apparent interspecies sociality (), showing sensitivity to human cues as well. It has even been suggested that dogs might serve as better comparative models for human cognition than non-human apes (). They can perform fast mapping of novel words (), and appear to have brain regions specialized for processing the human voice (). Behavioral work shows that dogs can read naturalistic signals from humans that may be difficult for other species (;; ) (although see ).

Prior fMRI research in our lab has shown that the ventral caudate nucleus—a brain region known to be specialized for reward prediction and processing of positively valenced stimuli across species (;;; )—is differentially active in dogs in response to the scent of familiar humans versus familiar dogs and unfamiliar humans (). In line with behavioral evidence (), this suggests that, in a real sense, dogs may prefer the company of familiar humans over the company of either familiar or unfamiliar dogs.

While the amassing data are suggestive of specialized social sensitivity in the dog, the question remains to what extent simple conditioning and reinforcement history, as opposed to social specialization, can explain previous findings. To address one aspect of this question, we iterated on and expanded our earlier fMRI work with dogs. Having previously shown a replicable but heterogeneous ventral caudate response in dogs to signals from their handlers predicting either incipient food reward or no reward (; ), here we used fMRI to examine neural responses to these same signals presented by a familiar human and an unfamiliar human and to analogous but illustrated hand signals projected on a screen (referred to forthwith as “computer” signals). Although the subject dogs had an extensive reinforcement history with the human and computer signals, we hypothesized that differential caudate BOLD response in the reward versus no-reward condition—taken here to be indicative of strength of reward prediction—would be highest with the familiar human source, and lowest with the computer, in line with the possibility that social bond, and not just food-specific reinforcement history, affects the valence of familiar cues. There is growing evidence to suggest that human–dog social bonds are durable and complex, showing much of the same nuance as those of human–human social bonds (e.g.,; ).