One pair of hands is not like another: caudate BOLD response in dogs depends on signal source and canine temperament

Abstract

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. 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.

Special issue: The “dominance” debate and improved behavioral measures—Articles from the 2014 CSF/FSF

“…I think it is far more plausible and logical that species that have and use identifiable patterns in signaling in a non-random manner to reflect and manage asymmetries in knowledge and relationships, have the capacity, given the evolution of the mammalian brain, to understand social organization and what risks shifts in it pose to them. These conclusions are supported by elegant, emergent imaging work (Berns et al, 2013(Berns et al, , 2015Cook et al, 2014). The unit of evolution is the individual so one should have the expectation that recognizing, understanding and participating in management of behavioral asymmetries in a labile environment would be a skill upon which selection would work in social animals.…”

Functional Magnetic Resonance Imaging of the Domestic Dog: Research, Methodology, and Conceptual Issues

“…Alternatively, dogs with higher aggressivity levels showed greater activation for reward signals given by an unfamiliar person or computer. Cook et al (2014) note that, because the striatal response is dependent upon arousal and stimulus salience, higher aggressiveness correlates to higher salience for the novel situations of unfamiliar person and computer, and that lower aggressiveness correlates to lower anxiety and higher salience with a familiar person. In their conclusion, the authors stress the possibility of differences across dogs in their reactions to various contexts, and emphasize the need for consideration of this possibility when making claims from dog studies without temperament testing.…”

“…To further expand on their developments in dog fMRI, Cook, Spivak, and Berns (2014) modified their reward/no-reward task to assess activation differences driven both by subject temperament and stimulus source. The same dogs as used in Berns et al (2013) were employed in this study, and all were evaluated for 14 factors of temperament (e.g., attachment, trainability, Hsu & Serpell, 2003) using the owner self-report Canine Behavioral Assessment and Research Questionnaire (C-BARQ).…”

“…In order to investigate the driving social relationship between a human and dog, the authors again utilized the dopamine theory of reward-error prediction, hypothesizing that if the relationship between a dog and its most familiar person includes reward expectancy, then caudate activation will be greater when the scent of that person is being processed, as opposed to another person or a dog. The same dogs that were used in their prior research (Berns et al, 2012; Berns et al, 2013; Cook et al, 2014) were enlisted for this study. Additional training was needed to acclimatize the dogs to smelling odors on a cotton swab while withholding approach.…”

“…In the first published fMRI investigation of face processing in awake dogs, Dilks et al (2015) presented eight fMRI-experienced canine subjects (Cook et al, 2014) with movie clips and static images. The dogs viewed movie clips of human faces, scenes, objects, and scrambled objects, each for three seconds.…”