Awake fMRI reveals a specialized region in dog temporal cortex for face processing

Awake fMRI reveals a specialized region in dog temporal cortex for face processing Daniel D. Dilks1 , Peter Cook1 , Samuel K. Weiller1 , Helen P. Berns1 , Mark Spivak2 and Gregory S. Berns1 1 Department of Psychology, Emory University, Atlanta, GA, USA 2 Comprehensive Pet Therapy, Atlanta, GA, USA ABSTRACT Recent behavioral evidence suggests that dogs, like humans and monkeys, are capable of visual face recognition. But do dogs also exhibit specialized cortical face regions similar to humans and monkeys? Using functional magnetic resonance imaging (fMRI) in six dogs trained to remain motionless during scanning without restraint or sedation, we found a region in the canine temporal lobe that responded significantly more to movies of human faces than to movies of everyday objects. Next, using a new stimulus set to investigate face selectivity in this predefined candidate dog face area, we found that this region responded similarly to images of human faces and dog faces, yet significantly more to both human and dog faces than to images of objects. Such face selectivity was not found in dog primary visual cortex. Taken together, these findings: (1) provide the first evidence for a face-selective region in the temporal cortex of dogs, which cannot be explained by simple low-level visual feature extraction; (2) reveal that neural machinery dedicated to face processing is not unique to primates; and (3) may help explain dogs’ exquisite sensitivity to human social cues. Submitted 13 May 2015 Accepted 30 June 2015 Published 4 August 2015 Corresponding author Gregory S. Berns, Academic editor Giorgio Vallortigara Additional Information and Declarations can be found on page 11 DOI 10.7717/peerj.1115 Copyright 2015 Dilks et al. Distributed under Creative Commons CC-BY 4.0 OPEN ACCESS Subjects Animal Behavior, Neuroscience Keywords fMRI, Dog, Face area INTRODUCTION For social animals, faces are immensely important stimuli, carrying a wealth of information, such as identity, sex, age, emotions, and communicative intentions of other individuals (Bruce & Young, 1998; Tate et al., 2006; Leopold & Rhodes, 2010). Given the importance of face recognition for social animals, it is perhaps not surprising that humans and monkeys have dedicated neural machinery for processing visual face information discrete from the neural machinery responsible for processing nonface visual information, such as for scenes, bodies, and objects (Gross, Rocha-Miranda & Bender, 1972; Desimone et al., 1984; Perrett et al., 1988; Tsao, Moeller & Freiwald, 2008; Kanwisher & Dilks, 2013). But what about other social animals, especially non-primates, like dogs? Dogs are a special case because they are both highly social with each other and have an additional evolutionary history with humans through domestication. As such, dogs may have evolved mechanisms especially tuned to social cues and therefore may have specialized How to cite this article Dilks et al. (2015), Awake fMRI reveals a specialized region in dog temporal cortex for face processing. PeerJ 3:e1115; DOI 10.7717/peerj.1115 neural machinery for face processing (Hare & Tomasello, 2005; Kaminski, Schulz & Tomasello, 2012; Miklosi & Topal, 2013). Behavioral evidence suggests that dogs may indeed process facial information (Racca et al., 2010; Somppi et al., 2014), but the neural mechanisms underlying the dogs’ behavior could be very different than humans or monkeys. For example, face recognition in dogs might rely on purely associative mechanisms, associating a face with a meaningful outcome (e.g., food). If so, then one would not expect face-specific processing in visual cortical areas, but rather activation in reward areas. Alternatively, dogs may have evolved specialized neural machinery for face recognition, and thus one would expect face-selective regions in visual cortex. To test these competing hypotheses about face-specific processing, using fMRI, we scanned six awake, unrestrained dogs (Berns, Brooks & Spivak, 2012). To obtain high-quality fMRI data, each dog (i) completed 2–4 months of behavioral training to teach them to hold still during scanning, and (ii) had a custom-made chinrest to help minimize head movement. During scanning, dogs were presented with movie clips of human faces, objects, scenes, and scrambled objects (dynamic stimuli) and static images of human faces, dog faces, objects, scenes, and scrambled faces (static stimuli) on a projection screen placed in the rear of the magnet (Fig. 1 and Video S1). MATERIALS AND METHODS Participants Participants were dogs (n = 8; 5 neutered males, 3 spayed females) from the Atlanta community. All were pets and/or released service dogs whose owners volunteer their time for fMRI training and experiments. For participation in previous experiments (Berns, Brooks & Spivak, 2012; Berns, Brooks & Spivak, 2013; Cook, Spivak & Berns, 2014), these dogs took part in a training program using behavior shaping, desensitization, habituation, and behavior chaining to prepare them to be comfortable with the physical confines of the MRI bore and the loud noise produced by scanning. Accordingly, all dogs had demonstrated an ability to remain still during training and scanning for periods of 60 s or greater. This study was performed in strict accordance with the recommendations in the Guide for the Care and Use of Laboratory Animals of the National Institutes of Health. The study was approved by the Emory University IACUC (Protocol #DAR-2001274-120814BA), and all dogs’ owners gave written consent for participation in the study. Training All dogs had previously undergone training which involved the presentation of images on a computer screen (Cook, Spivak & Berns, 2014). Thus, prior to participation in the current experiment, the dogs were accustomed to viewing images on a screen in the MRI. Prior to actual scanning, all dogs underwent practice sessions with a complete run through of all stimuli (described below), which were presented in a mock scanner on a computer screen. Dogs were approved for scanning by demonstrating that they could remain motionless for the duration of at least two, 20s-blocks of black and white images of human faces, dog faces, Dilks et al. (2015), PeerJ, DOI 10.7717/peerj.1115 2/13 Figure 1 Experimental setup in MRI. Dogs were trained to station within an individually customized chin rest placed inside a stock human neck coil. The upper surface coil was located just superior to the dog’s head. Images were rear projected onto a translucent screen placed at the end of the magnet bore. In the dynamic stimuli runs, color movie clips (3-s each) were shown in 21 s blocks of human faces, objects (toys), scenes, and scrambled objects. In the static stimuli runs, black and white images (600 ms on, 400 ms off) were shown in 20 s blocks of human faces, dog faces, everyday objects, scenes, and scrambled faces. The dynamic stimuli runs were used to localize a candidate face region in the tempo (...truncated)