Awake canine fMRI predicts dogs’ preference for praise vs food
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Awake canine fMRI predicts dogs' preference for praise vs food
Peter F. Cook 1
Ashley Prichard 1
Mark Spivak 0
Gregory S. Berns 1
0 Comprehensive Pet Therapy , Atlanta, GA 30328 , USA
1 Department of Psychology, Emory University , Atlanta, GA 30322 , USA
Dogs are hypersocial with humans, and their integration into human social ecology makes dogs a unique model for studying cross-species social bonding. However, the proximal neural mechanisms driving dog-human social interaction are unknown. We used functional magnetic resonance imaging in 15 awake dogs to probe the neural basis for their preferences for social interaction and food reward. In a first experiment, we used the ventral caudate as a measure of intrinsic reward value and compared activation to conditioned stimuli that predicted food, praise or nothing. Relative to the control stimulus, the caudate was significantly more active to the reward-predicting stimuli and showed roughly equal or greater activation to praise vs food in 13 of 15 dogs. To confirm that these differences were driven by the intrinsic value of social praise, we performed a second imaging experiment in which the praise was withheld on a subset of trials. The difference in caudate activation to the receipt of praise, relative to its withholding, was strongly correlated with the differential activation to the conditioned stimuli in the first experiment. In a third experiment, we performed an out-of-scanner choice task in which the dog repeatedly selected food or owner in a Y-maze. The relative caudate activation to food- and praise-predicting stimuli in Experiment 1 was a strong predictor of each dog's sequence of choices in the Y-maze. Analogous to similar neuroimaging studies of individual differences in human social reward, our findings demonstrate a neural mechanism for preference in domestic dogs that is stable within, but variable between, individuals. Moreover, the individual differences in the caudate responses indicate the potentially higher value of social than food reward for some dogs and may help to explain the apparent efficacy of social interaction in dog training.
fMRI; dogs; social; reward
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As the first domesticated species, dogs have a unique
relationship with humans. Dogs have been integrated into modern
social life in many cultures, with millions serving as companion
animals. As such, dogs benefit from a clear tendency of humans
to bond socially with dogs (Odendaal and Meintjes, 2003; Beck
and Madresh, 2008; Nagasawa et al., 2009; Stoeckel et al., 2014).
But what is the nature of the relationship from the dog’s
perspective? And, given the high degree of individual variability in
dogs (see Scott and Fuller, 2012), how consistent across
individuals are the biological underpinnings of this
relationship? A better understanding of the proximal mechanisms
driving dog–human interaction and the extent to which these vary
across individuals will illuminate the dog–human social
relationship. It is worth highlighting just how unique this
crossspecies relationship is. Although commensalism and symbiosis
are not uncommon in the animal kingdom, a species-wide
extension of social bonding mechanisms to include a wholly
unrelated species is apparently very rare, and raises the intriguing
possibility that human social behavior has served as a strong
adaptive pressure in the evolution of domestic dog sociobiology
(Reid, 2009). Quantifying the relative value of food vs praise
would also help inform ongoing and contentious debates
regarding the most effective methods in dog training (e.g.
McKinley and Young, 2003; Hiby et al., 2004; Blackwell et al.,
2008).
Dogs are gifted at attending to, and interpreting, subtle
human social cues (Lakatos et al., 2012; Merola et al., 2012;
M u¨ller et al., 2015), and a behavioral literature suggests that
dogs act as if socially attached to humans (Topal et al., 1998;
Palmer and Custance, 2008; although see: Prato-Previde et al.,
2003; Rehn et al., 2013). Despite this, the motivations behind dog
behavior toward humans can be difficult to disentangle from
behavior alone. In terms of measuring preference, dog social
behaviors are highly susceptible to prior patterns of food
reinforcement (Bentosela et al., 2008; Elgier et al. 2009), and dogs
frequently treat interaction with their owner as an avenue to
acquire food (Cook et al., 2014a), even suppressing interest in
food under communicative situations (Pongracz et al., 2013). In
direct tests of behavioral preference, some dogs select their
owners and others food (Gacsi et al., 2005; Topal et al., 2005;
Feuerbacher and Wynne, 2014, 2015)—but the behavior appears
to be contingent on testing method, socialization history,
reinforcement history and potentially many other factors
including attention, stimulus salience and satiety. Further, although
social reinforcement is a commonly used tool in dog training
(Hiby et al., 2004), and many trainers believe it to be effective, it
is qui (...truncated)