We are grateful to Canine Performance Sciences and Auburn University Departments of Psychology and Electrical &#38; Computer Engineering. This work was supported by the Association of Professional Dog Trainers.

Ethical approval for these methods was obtained from the Auburn University Institutional Animal Care and Use Committee and all methods were performed in accordance with their guidelines and regulations. For auditory exposure, progression through the sessions is based on week number. For stationing sessions, a specific session-specified performance criterion (e.g., at least eleven-second duration of chin targeting), must be met before the trainer may advance the dog to the next session in that training phase. Otherwise, t...

<ol>
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M., Deshpande, G., Waggoner, P., Katz, J. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Functional+Magnetic+Resonance+Imaging+of+the+Domestic+Dog:+Research,+Methodology,+and+Conceptual+Issues.">Functional Magnetic Resonance Imaging of the Domestic Dog: Research, Methodology, and Conceptual Issues.</a> Comparative Cognition &amp; Behavior Reviews. 11, 63-82 (2016).</li><li>Berns, G. S., Cook, P. 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S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=The+future+of+detector+dog+research.">The future of detector dog research.</a> Comparative Cognition &amp; Behavior Reviews. 14, 77-80 (2019).</li><li>Leidinger, C., Herrmann, F., Thone-Reineke, C., Baumgart, N., Baumgart, J. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Introducing+Clicker+Training+as+a+Cognitive+Enrichment+for+Laboratory+Mice.">Introducing Clicker Training as a Cognitive Enrichment for Laboratory Mice.</a> Journal of Visualized Experiments. (121), e55415 (2017).</li><li>Council, N. 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M., Spivak, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Scent+of+the+familiar:+An+fMRI+study+of+canine+brain+responses+to+familiar+and+unfamiliar+human+and+dog+odors.">Scent of the familiar: An fMRI study of canine brain responses to familiar and unfamiliar human and dog odors.</a> Behavioural Processes. 110, 37-46 (2015).</li><li>Berns, G. S., Brooks, A., Spivak, M. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Replicability+and+Heterogeneity+of+Awake+Unrestrained+Canine+fMRI+Responses.">Replicability and Heterogeneity of Awake Unrestrained Canine fMRI Responses.</a> PLoS One. 8 (12), e81698 (2013).</li><li>Cook, P., Prichard, A., Spivak, M., Berns, G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Jealousy+in+dogs?+Evidence+from+brain+imaging.">Jealousy in dogs? Evidence from brain imaging.</a> Animal Sentience. 117, 1-15 (2018).</li><li>Cook, P. F., Brooks, A., Spivak, M., Berns, G. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Regional+brain+activations+in+awake+unrestrained+dogs.">Regional brain activations in awake unrestrained dogs.</a> Journal of Veterinary Behavior-Clinical Applications and Research. 16, 104-112 (2016).</li><li>Cook, P. F., Prichard, A., Spivak, M., Berns, G. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Awake+canine+fMRI+predicts+dogs'+preference+for+praise+vs+food.">Awake canine fMRI predicts dogs' preference for praise vs food.</a> Social Cognitive and Affective Neuroscience. 11 (12), 1853-1862 (2016).</li><li>Cook, P. F., Spivak, M., Berns, G. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Neurobehavioral+evidence+for+individual+differences+in+canine+cognitive+control:+an+awake+fMRI+study.">Neurobehavioral evidence for individual differences in canine cognitive control: an awake fMRI study.</a> Animal Cognition. 19 (5), 867-878 (2016).</li><li>Cook, P. F., Spivak, M., Berns, G. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=One+pair+of+hands+is+not+like+another:+caudate+BOLD+response+in+dogs+depends+on+signal+source+and+canine+temperament.">One pair of hands is not like another: caudate BOLD response in dogs depends on signal source and canine temperament.</a> PeerJ. 2, e596 (2014).</li><li>Dilks, D. D., et al. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=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.</a> PeerJ. 3, e1115 (2015).</li><li>Prichard, A., Chhibber, R., Athanassiades, K., Spivak, M., Berns, G. S. <a target="_blank" href="http://www.ncbi.nlm.nih.gov/entrez/query.fcgi?db=PubMed&cmd=Search&doptcmdl=Citation&defaultField=Title+Word&term=Fast+neural+learning+in+dogs:+A+multimodal+sensory+fMRI+study.">Fast neural learning in dogs: A multimodal sensory fMRI study.</a> Scientific Reports. 8 (1), 14614 (2018).</li><li>Prichard, A., Cook, P. F., Spivak, M., Chhibber, R., Berns, G. 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The protocol described above separates the training of the stationing (chin rest) behavior from desensitization to the MRI environment. Further, it utilizes a generalization procedure of stationing in several dissimilar locations, to assist in the transfer of the stationing behavior to the real MRI scan environment; it does so without the need for extensive training time in the MRI scan environment, which can be expensive. Overall, the training and testing was completed in 14 hours and resulted in immediate transfer to n...

Magnetic resonance imaging (MRI) conducted on unrestrained awake dogs is a new method, creating a fresh way to examine function and structure in the dog brain. The first published accounts of MR image acquisition from unrestrained awake dogs were published in 2009 (structural) and 2012 (functional)1,2. There are several advantages of functional magnetic resonance imaging (fMRI) for studying brain function in unrestrained awake dogs. First, the data collection is similar to that of humans, and therefore more readily generalizable across species3. Second, there is no need for anesthesia, eliminating any undesirable aftereffects. Third, brain activity is altered by anesthesia and hence cognitive function can be better assessed without anesthesia4. Fourth, while fluid/food deprivation and physical restraint allow researchers to probe nonsedated animals (e.g., rodent, avian, and primate models), those animals can be in very different cognitive states from their non-deprived and unrestrained counterparts3.
At the moment, there are five laboratories around the world that are scanning awake dogs (Atlanta, USA; Auburn, USA; Budapest, Hungary; Quer&#233;taro, Mexico; Vienna, Austria), and there is no standardized method for training dogs to willfully undergo an MRI scan5,6,7. All the training methods share the common goal of training dogs to remain still for extended periods of time, which is necessary for quality brain scans. While all methods work via the principles of reinforcement learning, how exactly it is implemented varies, and we do not yet know the impact of this variance on the results. Therefore, if a proposed training method is accepted and comes to be widely used, it may reduce some amount of undesirable variance in the data. In this article, we focus on the training method for stationing in the MRI scanner. MRI scanning is expensive, and the proposed method we developed has the purpose of being cost-effective and thus generalizable to trainers around the world without regular access to an MRI scanner for training.
The method consists of two major components: training and testing. Training consists of two phases. Phase one is training the dog to chin target (i.e., station) in an open environment and phase two is training the dog to station in a mock MRI. Desensitization to the MRI occurs throughout the training phases, during separate, dedicated Auditory Exposure sessions. Testing consists of stationing in a portable mock MRI, in five different testing locations. The utility of this testing phase is to generalize the stationing behavior, facilitating transfer to the real MRI environment. The overall protocol is summarized in Figure 1.
<img alt="Figure 1" class="xfigimg" src="/files/ftp_upload/60192/60192fig1a.jpg" /> 
Figure 1: Protocol timeline. The protocol timeline is divided into two components, Training and Testing. Training is further divided into two phases, Open Environment and Mock MRI. Separate Auditory Exposure sessions occur during training as well. Testing consists of stationing in a portable mock MRI, in five different transfer locations (T1-T5). Once the dog has generalized the stationing behavior to criterion in five distinct transfer locations, the dog is ready for data collection in the real MRI environment. <a href="https://www.jove.com/files/ftp_upload/60192/60192fig1large.jpg" target="_blank">Please click here to view a larger version of this figure.</a>
Depending on the phase, training and testing takes 25 to 75 minutes per week, per dog: one 10-minute Auditory Exposure session and two or more 5 to 30-minute Stationing sessions. This protocol can be completed in 25 weeks. During transfer testing, dogs execute several bouts of a 5-minute motionless down/stay and chin rest in a portable mock MRI (bore, radiofrequency coil, 90+ dB audio, ear padding) in five dissimilar locations. Transfer sessions occur once per week for 30-60 minutes, over five consecutive weeks. During MRI testing, dogs execute several bouts of the final stationing behavior during a 60-minute session of structural and functional data acquisition in a real MRI scanner.
Throughout training and testing, a chin rest is the behavior of focus. A chin rest is the dog touching his chin to an object&#39;s surface following some cue to target (i.e., rest his chin) to that surface. That cue to target can be physical (e.g., gesture, lure), verbal (e.g., spoken word &#34;rest&#34;), or an object (e.g., access to the chin rest itself). Fluent performance of the chin targeting behavior is critical to limiting head motion. In this protocol, the chin rest behavior is conditioned, maintained, and generalized to occur in multiple contexts (different rest apparatuses, in multiple locations) with increasing target duration (up to five minutes). Additionally, the trainer conditions and maintains strong performance of behaviors down and stay, as well as good stimulus control over the release cue &#34;Okay,&#34; the conditioned reinforcer and behavioral event marker &#34;click,&#34; and the Keep Going Signal (KGS) &#34;good&#34;8. Over the course of the protocol, multiple stimuli and apparatuses are introduced at specific stages and for specific intervals. These materials are easily and inexpensively procured. For full details, see the Table of Materials.

<table border="1" fo:keep-together.within-page="1" fo:keep-with-next.within-page="always">
	<tbody>
		<tr>
			<td>Acrylic Mock Radiofrequency Coil</td>
			<td>Menards</td>
			<td>TU59018594</td>
			<td>Mock Radiofrequency (RF) Coil: 8&#34; diameter x 4&#39; Concrete Form Tube. Makes four mock RF coils; cut form tube in four even lengths for four 8&#34; diameter x 1&#39; mock RF coils.</td>
		</tr>
		<tr>
			<td>Agility Tunnel</td>
			<td>J&#38;J Dog Supplies</td>
			<td>TT053</td>
			<td>Open Agility Training Tunnel</td>
		</tr>
		<tr>
			<td>Bluetooth Speaker</td>
			<td>Sharkk</td>
			<td>SP-SK896WTR-GRY</td>
			<td>Portable Scan Audio Playback: Waterproof Bluetooth Speaker Sharkk 2O IP67 Bluetooth Speaker Outdoor Pool Beach and Shower Portable Wireless Speaker</td>
		</tr>
		<tr>
			<td>Cardboard Concrete Form Tube</td>
			<td>Menards</td>
			<td>TU10120014</td>
			<td>Stationary Mock MRI Bore: Sonotube 24&#34; diameter x 12&#39; Standard Wall Water-Resistant Concrete Form. Makes two mock bores; cut form tube in half for two 24&#34; diameter x 6&#39; bores.</td>
		</tr>
		<tr>
			<td>Chuckit Ball</td>
			<td>Chuckit!</td>
			<td>17030</td>
			<td>Toy Reward: Chuckit! Ultra Ball</td>
		</tr>
		<tr>
			<td>Decibel X</td>
			<td>Skypaw</td>
			<td></td>
			<td>Decibel meter phone app</td>
		</tr>
		<tr>
			<td>Exercise Mat</td>
			<td></td>
			<td></td>
			<td>Foam chin rest: cut mat in half lengthwise. Roll up, and secure roll with hot glue. Cut chin-size notch in center with X-ACTO knife. Hot-glue velcro to bottom surface.</td>
		</tr>
		<tr>
			<td>Folding Table</td>
			<td></td>
			<td></td>
			<td>3&#39; x 6&#39; folding table</td>
		</tr>
		<tr>
			<td>Microfiber Car Wax Applicator Pad</td>
			<td>Viking Car Care</td>
			<td>862400</td>
			<td>Viking Car Care Microfiber Applicator Pads</td>
		</tr>
		<tr>
			<td>Natural Balance Treat Log</td>
			<td>Natual Balance</td>
			<td>236020</td>
			<td>Food Reward: E.g., Chicken Formula Dog Food Roll, 3.5-lb roll</td>
		</tr>
		<tr>
			<td>Plywood</td>
			<td></td>
			<td></td>
			<td>Platform: 2&#34;x4&#34;x6&#39; length of wood affixed to 3&#39;x6&#39; plywood board. Hot glue exercise mat on plywood board for traction. Braces: 3 4x4x4&#34; cubes cut at 45-degree angle affixed to ends of 1&#34;x4&#34;x3&#39; lengths of wood. Makes 3 braces.</td>
		</tr>
		<tr>
			<td>Sand Bags</td>
			<td>J&#38;J Dog Supplies</td>
			<td>AG155</td>
			<td>J&#38;J Professional Quality Sandbags x 2</td>
		</tr>
		<tr>
			<td>Speaker System</td>
			<td>Pioneer Electrics</td>
			<td>HTD645DV</td>
			<td><a href="https://www.pioneerelectronics.com/pio/pe/images/portal/cit_11221/93327312Operating%20Instructions%20S-HTD630.pdf" target="_blank">Stationary Scan Audio Playback: Pioneer HTD645DV 5 Disk DVD Home Theater System with Wireless Surround Speakers. Operating Instructions.</a></td>
		</tr>
		<tr>
			<td>Towel</td>
			<td></td>
			<td></td>
			<td>standard towel</td>
		</tr>
	</tbody>
</table>

training dogs for awake, unrestrained functional magnetic resonance imaging

We present a canine functional Magnetic Resonance Imaging (fMRI) training protocol that can be done in a cost-effective manner, with high-energy dogs, for acquisition of functional and structural data. This method of training dogs for awake, unrestrained fMRI employs a generalization procedure of stationing in several dissimilar locations to facilitate transfer of the stationing behavior to the real MRI scan environment; it does so without the need for extensive training time in the MRI scan environment, which can be expensive. Further, this method splits the training of a stationing (i.e., chin rest) behavior from desensitization to the MRI environment (i.e., 100+ decibel scan audio), the latter accomplished during dedicated Auditory Exposure conditioning sessions. The complete training and testing protocol required 14 hours and resulted in immediate transfer to novel locations. We also present examples of canine fMRI data that have been acquired from visual face processing and olfactory discrimination paradigms.

The mean number of repetitions of each session level is listed in Table 1. The complete training and testing protocol required 14 h (M = 13.55 h, range 12-16 h) and consisted of 90 sessions (range 87-93 sessions). Open environment training lasted 4.38 h (range 3-5 h), mock MRI training lasted 5.4 h (range 4.2-6.5 h), and transfer was 2.5 h divided into five 30 min sessions. Maintenance sessions at level 19 were conducted during transfer and are reflected in the complete t...

Watch this Scientific Journal Video about Training Dogs for Awake, Unrestrained Functional Magnetic Resonance Imaging at JoVE.com

Training Dogs for Awake, Unrestrained Functional Magnetic Resonance Imaging

Magnetic resonance imaging (MRI) on unrestrained awake dogs is a new method with several advantages over imaging with physical or chemical restraint. This protocol introduces a cost-effective training method that minimizes training in the MRI environment, which can be expensive, and maximizes the subject pool available for canine functional MRI.

We present a canine functional Magnetic Resonance Imaging (fMRI) training protocol that can be done in a cost-effective manner, with high-energy dogs, for ...

Magnetic Resonance Imaging conducted in unrestrained dogs is a new method that creates a fresh way of examining function and structure in the dog brain. The method is humane, cost effective, and it works, not only for dogs in this research context, but as a scaffold for other husbandry behavior training programs. The transferring classical counter-conditioning strategies help the dogs to rapidly acclimate a robust stationing behavior to the scanner environment.Because the protocol is cost effective, it is generalizable to trainers around the world without regular access to an MRI scanner. For active, auditory exposure sessions, transport the dog to a familiar indoor training room. And play scan audio at the session's specified volume.After ten seconds, engage in 20 seconds of toy play with the dog while the scanner noise is still audible. After 20 seconds of play, retrieve the toy from the dog and pause the noise. Then wait with the dog in silence without the reward for 10 seconds before starting the next trial.Conduct one session of 10 trials per week for 12 weeks increasing the decibel volume over the sessions throughout the duration of the training period. To capture the chin target to towel with the dog standing, sitting, or in the down position, click, then treat to allow the dog to investigate the towel. Once the dog will investigate the towel reliably, click then treat for any nose to towel and subsequent chin to towel contact until the towel contact duration reaches at least two seconds for up to five minutes per session.When the dog will chin target for at least 26 seconds, click then treat for any investigation of the foam chin rest apparatus. After several reinforced investigations of the apparatus, cue rest and click then treat for one to two seconds of chin contact for five to 15 minutes of training until 40 seconds of contact is achieved. For mock MRI stationing sessions, invite the dog to jump or lift the dog into the mock bore and cue the dog to lie down, clicking then treating.Cue the dog to rest. And click then treat for one to 12 seconds of chin targeting to the foam chin rest in the elevated bore in 5 to 15 minute sessions until the duration increases to 60 seconds. Reinforce less precise approximations of the behavior initially, as the trainer will have the opportunity to selectively reinforce for better alignment precision in later reps.When the dog can chin target in the mock bore for at least 60 seconds, cue down and rest, and outfit the dog with ear padding. Place scan audio at a barely audible volume between zero and 40 decibels. And click then treat for one to 12 seconds of chin contact in 15 to 30 minute training sessions until the duration lasts at least 107 seconds.When the dog can sustain five minutes in down stay in the chin rest in the mock bore and mock RF coil, while wearing ear padding with the scanner noise playing at 80 to 110 decibels, stand or sit beside portable mock bore with the mock RF coil, and gesture to the dog to enter the new bore. Cue down and rest, and outfit the animal with ear padding. Place scan audio at 80 to 110 decibels.And click then treat for 1 to 30 seconds of stationing in the new location. Next probe for the criterion duration, reinforcing at 5 minutes or when the dog breaks. Once the dog has generalized the stationing behavior to criterion in five distinct transfer locations, the dog is ready for data collection in the real MRI environment.Here, the maximum duration of four dogs trained in this protocol, as demonstrated for the last three sessions at the end of training and the different training locations is shown. The performance was stable at the end of stationing training and all of the dogs transferred to the mock training locations with a max duration equivalent to training. Three of the dogs transferred to the MRI scanner and demonstrated repeated bouts of the max possible duration of 206 seconds.The one dog that did not transfer to the MRI scanner had a larger head than the other dogs and could not comfortably fit within the coil, likely contributing to its unwillingness to participate in the scans. Once trained to participate in functional MRI scans, we can glean sensory processing information within several modalities. For example, adjacent but different brain areas at the temporal cortex in the dog brain are active for processing dog and human faces.Green regions represent areas of the brain more active for human faces contrasted with dog faces. While red regions represent areas of the brain more active for dog faces, contrasted with human faces. While the olfactory bulb, periamygdala, anterior olfactory cortex, entorhinal cortex, and piriform lobes are active in both awake and anesthetized dogs, the regions implicating higher order cognitive processing are activated mainly in awake dogs.The protocol is designed around the idea that head motion is incompatible with a robust chin rest behavior, which is generalized to occur in multiple settings. While canine functional MRI is in its naissance stages, the future is promising for the continued use of humanity's best friend in understanding brain behavior relationships. For example, our findings can advance the understanding of how to better select, train, and employ dogs for tasks that benefit society such as detecting hazardous threats like explosives.With the robust method of scanner acclimation, the limitations of the utility of the scanner are bound only by the creativity of the researcher's questions and experimental designs.

training-dogs-for-awake-unrestrained-functional-magnetic-resonance

Research

JoVE Journal

Behavior

7.3K Views.  Auburn University. Magnetic Resonance Imaging conducted in unrestrained dogs is a new method that creates a fresh way of examining function and structure in the dog brain. The method is humane, cost effective, and it works, not only for dogs in this research context, but as a scaffold for other husbandry behavior training programs. The transferring classical counter-conditioning strategies help the dogs to rapidly acclimate a robust stationing behavior to the scanner environment.Because the protocol is c...