Functional MRI in Awake Dogs Predicts Suitability for Assistance Work

www.nature.com/scientificreports OPEN received: 12 October 2016 accepted: 26 January 2017 Published: 07 March 2017 Functional MRI in Awake Dogs Predicts Suitability for Assistance Work Gregory S. Berns1, Andrew M. Brooks2, Mark Spivak2 & Kerinne Levy3 The overall goal of this work was to measure the efficacy of fMRI for predicting whether a dog would be a successful service dog. The training and imaging were performed in 49 dogs entering service training at 17–21 months of age. 33 dogs completed service training and were matched with a person, while 10 were released for behavioral reasons (4 were selected as breeders and 2 were released for medical reasons.) After 2 months of training, fMRI responses were measured while each dog observed hand signals indicating either reward or no reward and given by both a familiar handler and a stranger. Using anatomically defined ROIs in the caudate, amygdala, and visual cortex, we developed a classifier based on the dogs’ subsequent training outcomes. The classifier had a positive predictive value of 94% and a negative predictive value of 67%. The area under the ROC curve was 0.91 (0.80 with 4-fold cross-validation, P = 0.01), indicating a significant predictive capability. The magnitude of response in the caudate was positively correlated with a successful outcome, while the response in the amygdala depended on the interaction with the visual cortex during the stranger condition and was negatively correlated with outcome (higher being associated with failure). These results suggest that, as indexed by caudate activity, successful service dogs generalize associations to hand signals regardless who gives them but without excessive arousal as measured in the amygdala. The advent of awake fMRI in dogs has opened up numerous possibilities for decoding how the dog’s brain is organized1–3. But like many of the early human fMRI studies, these nascent efforts have been plagued by small sample sizes. Some results have been replicated, increasing confidence in the technique4–6. At the same time, there have also been hints of substantial individual differences between dogs’ brain responses that, like humans, relate to important aspects of behavior, temperament, and personality7,8. We have previously observed a temperament-dependent increase in neural activity in the caudate when dogs are presented with a hand-signal associated with incipient receipt of food reward8. Dogs who came from a service-dog training program were more likely to show a caudate response to a hand signal when interacting with their owner/handler, while other dogs (e.g. from shelters and pets with no service-training) were more likely to show a caudate response to the signal when interacting with an unfamiliar person. Are these differences a result of service-training, or might there be a neurobiological phenotype that contributes to a dog’s ability to perform tasks required of service dogs? If the latter, then it should be possible to identify attributes and neurobiological correlates that predict successful completion of service-training. Most dogs are not suited to be service dogs. Although there is no industry standard, a well-managed service-dog program considers heredity in breeding, optimal nutrition during gestation and nursing, neonatal care of pups and nutrition after weaning, maintenance of hygienic environments, and provision of socialization opportunities with other dogs, animals, and people. Even so, up to 70% of dogs from such programs are deemed unsuitable for service work. By many estimates, the cost of training a service dog is $20,000 to $50,000. If dogs that are predisposed to fail training could be identified earlier, the average cost would decline. There have been several studies of juvenile dogs, using behavioral tests and questionnaire ratings, that have examined the possibility of identifying high-potential working dogs. The earliest studies of puppy temperament indicated some trait consistency, but not to the extent of a predictive test9. Later studies showed that working dogs, on average, had different behavioral traits but these were not consistent enough to predict individual performance as adults10–12. As dogs get older, their behavior becomes more consistent, achieving some level of stability between 1 Psychology Department, Emory University, Atlanta, GA, USA. 2Dog Star Technologies, Sandy Springs, GA, USA. Canine Companions for Independence, Santa Rosa, CA, USA. Correspondence and requests for materials should be addressed to G.S.B. (email: ) 3 Scientific Reports | 7:43704 | DOI: 10.1038/srep43704 1 www.nature.com/scientificreports/ Breed GLD LAB LGX Total Female 0 6 13 19 Male 1 2 21 24 Total 1 8 34 43 Table 1. Demographics of dogs with both MRI data and outcomes. GLD =golden retriever; LAB = Labrador retriever; LGX =  lab/golden cross. 12 and 24 months of age, to the point where temperament questions and behavioral tests become modestly predictive of suitability for service work13,14. However, the variability of inter-rater agreement and test-retest reliability has raised questions about the utility of these approaches15,16. To determine if a pattern of brain responses can predict completion of training and placement in a service job, we performed a prospective fMRI study of 49 dogs at the beginning of their service-training. We focused on three brain regions as potential biomarkers of success or failure: 1) caudate for reward sensitivity4,17; 2) amygdala for arousal18; and 3) a region of temporal cortex previously shown to be responsive to faces5. Methods Participants. All dogs participating in the study came from Canine Companions for Independence (CCI, Santa Rosa, CA). CCI’s dogs undergo a controlled socialization process. After they are weaned, puppies are raised by a volunteer puppy-raiser until 17–21 months of age. Then, the dogs are returned to one of CCI’s training facilities for service training, which can take 6–9 months. Dogs that complete the training “graduate” into one of several roles: 1) service dog (assists adults with physical disabilities with daily activities); 2) skilled companion (assists adults and children under the guidance of a facilitator, e.g. parent or spouse); 3) facility dog (works with a facilitator in an institutional setting, e.g. hospital); 4) hearing dog (trained to recognize specific sounds and alert the person); and more recently, 5) PTSD dog (provides social buffer, conducts room searches and provides “allclear” signal). Those who are unable to complete training, for either medical or behavioral reasons, are “released” and adopted, often by the puppy-raiser. The study was approved by both the Emory Institutional Animal Care and Use Committee and the UC Berkeley Animal Care and Use Committee. All methods and protocols were carried out in accordance with federal regulations under the Animal Welfare Act. Between 11/2014 and 11/2015, 54 dogs were selected for participation (...truncated)