PROTOPOPOVA, HALL, & WYNNE 1 Association between increased behavioral persistence and stereotypy in the pet dog 2 Alexandra Protopopova, Nathaniel J. Hall, & Clive D. L. Wynne1 3 4 Department of Psychology, University of Florida, 945 Center Drive, Gainesville, FL 32611, 5 USA 6 7 Email addresses: aprotopo@ufl.edu, njhall1@ufl.edu, clive.wynne@asu.edu 8 9 Address correspondence to Alexandra Protopopova at 10 aprotopo@ufl.edu 11 1 (617) 838 4913 12 Department of Psychology 13 945 Center Drive 14 Gainesville, FL 32611 15 USA 16 17 1 18 Tempe, AZ 85287, USA 19 20 21 22 23 24 Present address: Department of Psychology, Arizona State University, 950 S. McAllister, PROTOPOPOVA, HALL, & WYNNE 25 Abstract 26 The aim of the present study was to evaluate whether dogs that exhibit stereotypy also show 27 higher behavioral persistence in an extinction-learning task. Thirteen pet dogs with stereotypy 28 and 13 breed-matched control dogs were assessed on a resistance to extinction test. Each dog 29 was trained for 40 trials using a food reinforcer to nose-touch the experimenter’s hand on a 30 continuous reinforcement schedule. After acquisition, the dogs entered an extinction phase, 31 during which food was no longer delivered. The numbers of nose-touches as well as inter- 32 response times during this phase were recorded. A linear regression found that stereotypy status 33 (t = -2.46, P = .027) and breed type (t = 2.44, P = .023) were significant predictors of the number 34 of responses in extinction. Dogs with stereotypy responded more in extinction than control dogs. 35 The mean number of responses was 13.4 (SD = 14.7) in the control group and 26.0 (SD = 15.3) 36 in the stereotypy group. These results suggest a link between previous laboratory and zoo animal 37 findings on the neurophysiology of stereotypy and the pet dog population. They also have 38 implications for the use of extinction procedures to reduce stereotypic behaviors in pet dogs, as 39 these dogs show enhanced resistance to extinction. 40 41 42 43 44 45 Key words: Dog; behavioral persistence; extinction learning; stereotypy. PROTOPOPOVA, HALL, & WYNNE 46 1. Introduction 47 Repetitive and unvarying behaviors without an apparent goal, hereafter “stereotypy,” occur 48 in both human and non-human animals. Stereotypy is common and widely studied in captive 49 animals housed in zoos and laboratories. Furthermore, stereotypy is widely considered an 50 indicator of poor welfare, deprived environments, and/or the result of CNS dysfunction (for a 51 review see Mason et al., 2007). 52 Pet dogs have also been reported to engage in stereotypy such as excessive circling, tail 53 chasing, flank-sucking, fly biting, self-mutilation, pacing, spinning, some repetitive 54 vocalizations, and fabric sucking (Moon-Fanelli & Dodman, 1998). About 3.4% of dogs 55 presenting at a Cornell University veterinary behavior clinic from 1991 to 2001 were diagnosed 56 with Canine Compulsive Disorder (CCD) (Bamberger et al., 2006), in which the above described 57 stereotypies represent the main clinical symptom. Furthermore, the American Kennel Club 58 (AKC) Canine Health Foundation listed CCD as a top health concern for some breeds of dogs, 59 such as Bull Terriers and Border Collies (AKC, 2012). In most cases, canine stereotypies 60 significantly decrease the welfare of both the affected dog and its owner. Owners report that such 61 repetitive behaviors interfere with the daily functioning of their dogs, preventing them from 62 being able to eat, play, and interact normally with people (Moon-Fanelli & Dodman, 1998; 63 Overall & Dunham, 2002). In addition, these dogs typically show some tendency to mutilate 64 themselves, for example by biting their tails, wearing out their paw pads, and circling until 65 complete exhaustion, leaving owners to explore undesirable treatments such as tail amputation 66 and even euthanasia of their pet (Moon-Fanelli & Dodman, 1998). 67 At this time, however, our understanding of the causes and factors related to canine 68 stereotypy is limited. The question remains whether dogs with stereotypy show systemic and PROTOPOPOVA, HALL, & WYNNE 69 fundamental behavioral differences from normal dogs. Alternatively, dogs with stereotypy and 70 normal dogs may not show any general behavioral differences, but instead may only differ in the 71 presence or absence of stereotypy. The fact that animals that exhibit one stereotypy are likely to 72 exhibit other seemingly unrelated problem behaviors and siblings often share a predisposition 73 toward stereotypic behaviors (Hewson et al., 1998), suggests that there may be more 74 fundamental behavioral differences between normal and affected dogs. These observations 75 support the assumption that there are some underlying predispositions among dogs with 76 stereotypy. 77 Phenotypes, such as an individual’s general sensitivity to reinforcement, have previously 78 been associated with complex behavioral disorders such as Attention Deficit Hyperactivity 79 Disorder in people (Murray & Kollins, 2000). In addition, researchers have identified other 80 general phenotypes such as impulsivity (Neef et al., 2005) that differentiated their target 81 population from typically functioning individuals. Furthermore, Frith and Done (1983) found 82 that schizophrenic patients differed from others in their perseveration of responding. These 83 patients displayed a very low switch-over rate on a concurrent choice task (Frith & Done, 1983). 84 Such perseverative responding and problems with response inhibition largely characterize people 85 with autistic spectrum disorders (see review by Russo et al., 2005; but also see Geurt et al., 2009 86 and Van Eylen et al., 2011). Numerous animal studies, spanning a wide variety of species, have 87 investigated behavioral disinhibition as a behavioral process that may separate animals that show 88 stereotypic behaviors from those without behavioral stereotypies. Disinhibition of behavior may 89 result in elevated rates of switching behaviors, perseveration of behavior in tasks that require 90 inhibition, and shorter latencies to initiate behaviors (Garner et al., 2003). Whereas stereotypic 91 behavior, as we have described it above, refers to the behavior of the animal outside of an PROTOPOPOVA, HALL, & WYNNE 92 experimental procedure, repetitive responding within an experiment is termed perseveration 93 (Garner et al., 2003). Perseveration, as measured through resistance to extinction (a measure of 94 the continuation of responding after reinforcement is discontinued), was found to correlate with 95 presence or severity of stereotypic behavior in a study with bank voles (Garner & Mason, 2002), 96 two species of tits (Garner et al., 2003), Asiatic black bears (Vickery & Mason, 2003), Malayan 97 sun bears (Vickery & Mason, 2005), horses (Hemmings et al., 2007), and rhesus macaques (Lutz 98 et al., 2004; Pomerantz et al., 2012). Tanimura and colleagues (2008) found frequency of 99 stereotypy in mice was positively correlated with the number of errors in a reversal-learning task. 100 In other studies, perseveration was assessed through an analysis of change-over patterns in a 101 concurrent choice task with equal schedules of reinforcement on both choices (e.g. Campbell et 102 al., 2013; Dallaire et al., 2011; Gross et al., 2011; Garner et al., 2003); however, Gross and 103 colleagues (2011), unlike other studies reviewed here, did not find a correlation between 104 stereotypy and perseveration. Furthermore, a correlation between perseverative behavior and the 105 frequency of self-directed behavior or displacement activity (such as self-touching, scratching, 106 manipulating objects, etc.) was found in lion-tailed macaques, squirrel monkeys, and capuchin 107 monkeys (Judge et al., 2011). 108 The aim of this study was to extend the large literature on the association between 109 behavioral persistence and stereotypy to the pet dog population. We set out to examine whether 110 resistance to extinction is a fundamental behavioral phenotype that distinguishes pet dogs that 111 exhibit stereotypy from those that do not. We predicted that dogs with stereotypy would show 112 higher resistance to extinction on an arbitrary novel task than dogs from a normal population. As 113 previous research has differentiated between topographies of canine stereotypies and indicated PROTOPOPOVA, HALL, & WYNNE 114 that certain breeds have different topographies (Mills & Luescher, 2006), we also aimed to 115 explore these additional variables in our data set. 116 2. Materials and methods 117 Twenty-six dogs were recruited through advertisements online, social networking sites, local 118 veterinary clinics, and dog parks. All owners completed a questionnaire describing the dog’s 119 form, frequency, and intensity of the stereotypy. After completion of the questionnaire, a 120 consultation was conducted (by AP and NH) to verify that the dogs exhibited the reported 121 stereotypy. Dogs in the control group were matched to dogs with stereotypies by breed. If 122 possible, dogs were further matched by other criteria in the following order: dogs were siblings, 123 shared the same household, similar age, and same sex. Table 1 lists the subjects that participated 124 in the experiment. The different forms of stereotypy were classified into five categories: licking 125 (excessive licking and/ or sucking on part of the dog’s body or inanimate objects), circling 126 (repeatedly spinning in one direction), light chasing (excessively following shadows or 127 reflections), light fixating (starring at a light source for a prolonged time), and fly snapping 128 (snapping at the air as if catching invisible flies). 129 Each dog was tested in its home by one experimenter, either the first author (AP), who was 130 not bind to the hypothesis of the study (n = 22) or the dog’s owner, who was blind to the 131 hypothesis, if the dog was fearful towards AP (n = 4). All sessions were videotaped. Each dog 132 received one continuous session, which was divided into two phases: acquisition and extinction. 133 During the whole session, the experimenter stood still with her left hand down by her side with 134 the palm facing the dog, and her right hand behind her back. During the initial learning phase, 135 the dog was given a small piece of hot dog (~ 0.5 cm3) every time it touched the experimenter’s 136 palm with its nose. Upon a nose-touch, the experimenter withdrew the left hand and placed it PROTOPOPOVA, HALL, & WYNNE 137 behind her back and, with her right hand, reached into a container with food and delivered one 138 food item. If 1 min passed with no response during this phase, the experimenter re-presented the 139 left hand while calling the dog by name once. If three presentations of the hand with no response 140 passed, the experiment was concluded and the dog’s data not included in the analysis (three dogs 141 were excluded this way: two dogs in the stereotypy and one in the control group). The initial 142 learning phase lasted until the dog received 40 treats. After the 40th treat, the extinction phase 143 began. During this phase, no more treats were given to the dog for touching the hand. Upon a 144 nose-touch, the experimenter withdrew her left hand, placed it briefly behind her back, reached 145 into the container with her right hand, placed her right hand behind her back, and then re- 146 presented her left hand. The extinction phase ended when 1 min passed without a response from 147 the dog. Behavioral persistence was quantified as the number of responses in the extinction 148 phase of the session. In order to investigate differences in time to learn the task or any 149 motivational differences between dogs, inter-response times in both the learning and extinction 150 phases were also calculated. Data was collected through an analysis of video recordings by a 151 coder blind to the hypothesis of the study. In order to assess inter-observer reliability, 9 out of 26 152 (35%) videos were coded by two independent observers. Agreement was scored when two 153 observers concurred on the occurrence of a nose-touch within 1 s of each other. The median 154 interobserver agreement was 98.5%, ranging from 74.4 to 100%. 155 156 The study was conducted with the approval of the University of Florida Institutional Animal Care and Use Committee. 157 2.1. Statistical analysis 158 The 10 different breeds of the subjects were combined into four breed types. Breed Type 1 159 consisted of terrier breeds (Bull Terriers, American Pit Bull Terriers, and Terrier mixes). Breed PROTOPOPOVA, HALL, & WYNNE 160 Type 2 consisted of herding breeds (Australian Shepherds, Shetland Sheepdogs, Australian 161 Cattle Dogs, and Border Collies). Breed Type 3 consisted of hounds (Miniature Dachshunds). 162 Breed Type 4 consisted of working and guarding breeds (Blackmouth Curs and Dobermans). A 163 linear regression model through Wald backward elimination with criteria for inclusion set at P < 164 0.25 and for removal at P > 0.05 (Mickey and Greenland, 1989) was used to investigate the 165 effect of stereotypy status, breed type, age, sex, and experimenter type (AP or owner) on the 166 number of responses in extinction. To further explore breed differences, two contrasts were 167 conducted: (1) to evaluate the differences between breeds typically implicated in exhibiting 168 stereotypy (herders and terriers compared to hounds and working dogs) and (2) to compare 169 terriers to herders. Topography of the stereotypy was not included in the model as only half of 170 the dogs exhibited stereotypy; therefore, differences in the number of responses in extinction by 171 the topography of the stereotypy were assessed using a one-way analysis of variance. To assess 172 time to acquisition, speed of responding and motivation to respond in extinction, the differences 173 in inter-response times were evaluated with separate paired-sample t-tests. All statistical 174 calculations were conducted with the statistical package SPSS® (International Business Machines 175 Corp., Armonk, NY, USA). 176 3. Results 177 A linear regression analysis was conducted to predict the number of responses in extinction 178 using sex, age, breed type, experimenter used, and stereotypy status as predictors. The final 179 model consisted of breed type and stereotypy status as statistically significant predictors of the 180 number of responses in extinction (F(2) = 5.76, P = .009) (Table 2). The adjusted R2 value was 181 0.276. The mean number of responses was 13.4 (SD = 14.7) in the control group and 26.0 (SD = 182 15.3) in the stereotypy group (Fig. 1). Breed Type 1 (terriers) had a mean number of responses PROTOPOPOVA, HALL, & WYNNE 183 of 14.2 (SD = 14.8), Breed Type 2 (herders) had a mean number of responses of 17.3 (SD = 184 14.9), Breed Type 3 (hounds) had a mean number of responses 30.5 (SD = 6.4), and Breed Type 185 4 (working dogs) had a mean number of responses of 34.0 (SD = 18.4). Herders and terriers 186 responded significantly less in extinction than hounds and working dogs (t = 2.19, df = 20, P = 187 .0.041), whereas no differences were found between terriers and herders (t = 0.36, df = 20, P > 188 .05), 189 There were no differences between the dogs with stereotypy and the control dogs in inter- 190 response times in either acquisition (mean was 15.9 in the stereotypy group and 11.3 in the 191 control group; t = 1.45, df = 12, P > .05) or extinction (mean was 7.8 in the stereotypy group and 192 8.8 in the control group; t = -0.49, df = 12, P > .05). 193 The number of responses in extinction did not differ by the form of the stereotypy (F(3) = 194 3.03, P > .05). Dogs that engaged in excessive licking responded on average 28.0 times, dogs 195 that engaged in chasing lights responded on average 23.3 times, and dogs that engaged in 196 circling or spinning responded on average 26.8 times. 197 Discussion 198 As predicted, pet dogs that engaged in stereotypic behaviors responded more in extinction 199 indicating higher behavioral persistence than normal dogs. The results suggest that dogs with 200 stereotypy differ from the normal population in their resistance to extinction or perseverance. 201 The finding that dogs with stereotypy differ on a more general behavioral phenotype independent 202 of stereotypic behavior might explain why Overall and Dunham found that 75% of dogs with 203 CCD also suffered from other, seemingly unrelated behavioral problems, such as aggression and 204 separation anxiety (Overall & Dunham., 2002). Dogs that emit stereotypy in the home continue PROTOPOPOVA, HALL, & WYNNE 205 to emit behaviors after the reinforcer has been removed longer than other dogs. This insensitivity 206 to changes in reinforcement likely has broad behavioral impacts on these dogs. 207 Interestingly, greater resistance to extinction was a general finding across our entire sample 208 of stereotypic dogs. We found that breed type, along with the presence of stereotypy, had an 209 effect on resistance to extinction. Hounds and working breeds responded more in extinction than 210 did terriers or herders. Although some breeds are thought to be prone to stereotypy and even 211 specific topographies of stereotypy, resistance to extinction appeared to uniformly distinguish 212 between presence and absence of stereotypy across both breeds and type of stereotypy. 213 These results suggest that dogs with stereotypy behave similarly to other animals with 214 stereotypy. Dogs, just like bank voles, tits, Asiatic black bears, Malayan sun bears, horses, and 215 old world monkeys showed a correlation between higher behavioral persistence on an extinction 216 learning task and stereotypy (Garner et al., 2003; Garner & Mason, 2002; Vickery & Mason, 217 2003; Vickery & Mason, 2005; Hemmings et al., 2007; Lutz et al., 2004; Pomerantz et al., 2012). 218 Behavioral persistence, or recurrent perseveration, has been linked to basal ganglia disruption in 219 people, rodents, and monkeys (Garner, 2006) and may thus suggest treatment with dopaminergic 220 agents (Rapoport et al., 1992). 221 There were no differences between the dogs with stereotypy and the control dogs in inter- 222 response times in either acquisition or extinction. Dogs with stereotypy took just as long to learn 223 the task. Furthermore, the speed of responding in extinction did not differ between the two 224 groups. This suggests that both groups of dogs were equally motivated to learn the task and that 225 time during learning could not have been responsible to the differences in resistance to 226 extinction. PROTOPOPOVA, HALL, & WYNNE 227 One limitation of this study was that the presence or absence of stereotypy was determined 228 from owner-reports and a brief visit to the dog’s home by the experimenters. No quantification of 229 the severity or specific topography of the stereotypy was attempted. Future research can evaluate 230 whether correlations exist in the frequency, intensity, or duration of stereotypy and behavioral 231 persistence. Such an analysis would be possible in laboratory or shelter-housed animals. A 232 second limitation was that the majority of the subjects were assessed by an experimenter not 233 blind to the hypothesis of the study. The video coders were blind to the hypothesis, however, a 234 possibility remains that the experimenter may have unconsciously cued the dogs to either 235 respond or stop responding. However, the type of experimenter (AP or owner) did not predict 236 differences in the number of responses in extinction. Future experiments should verify the results 237 of this study by using an experimenter, blind to both the hypothesis and the stereotypy status of 238 the dogs. 239 The specific form of the stereotypy in animals might arise as a normal behavior that has 240 been reinforced at some point either through natural environmental consequences, such as 241 itching the tail in the case of tail chasing, but has persevered even in the current absence of 242 reinforcement. Our results provide support for this hypothesis by showing that extinction 243 learning is impaired in this population. An interesting future study may be to examine the ability 244 to experimentally create specific forms of artificial behavior analogous to stereotypy using such 245 reinforcement methods. In humans, perseverative responding (repetitive sequences of button 246 presses) was induced through reinforcement procedures (Schwartz, 1982). 247 These findings have implications for the management and behavioral treatment of 248 stereotypy; extinction procedures that withhold reinforcement might not be as effective in this 249 population as in others not showing stereotypy. However, it remains to be seen whether these PROTOPOPOVA, HALL, & WYNNE 250 animals are insensitive to procedures that include reinforcement for alternative behaviors or 251 punishment for the stereotypic behavior. 252 Future research should continue to investigate other behavioral correlates with stereotypy, 253 aside from resistance to extinction. For example, Parker and colleagues (2008) showed that 254 stereotypy in horses correlates with impairment in learning to choose a more immediate 255 reinforcer in a choice task. Future research may evaluate whether similar behavioral phenomena 256 exist in pet dogs. 257 4. Conclusions 258 Dogs that exhibit stereotypy in the home also show higher resistance to extinction in a 259 reversal learning task. Dogs with stereotypy took longer to extinguish responding than the breed- 260 matched control dogs. No differences were seen in inter-response times in either acquisition or 261 extinction, suggesting that motivation or impaired learning ability cannot explain these results. 262 No systematic differences were seen between the topographies of stereotypy. 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Research in 350 Autism Spectrum Disorders, 5(4), 1390-1401. 351 352 353 354 355 Vickery, S. S., & Mason, G. J. (2003). Behavioral persistence in captive bears: implications for reintroduction. Ursus, 35-43. Vickery, S. S., & Mason, G. J. (2005). Stereotypy and perseverative responding in caged bears: further data and analyses. Applied Animal Behaviour Science, 91(3), 247-260. PROTOPOPOVA, HALL, & WYNNE 356 Figure 1. The average number of responses in extinction and the standard error in the stereotypy 357 and the control are presented. Dots represent individual data. PROTOPOPOVA, HALL, & WYNNE 1 Table 1. The form and frequency of stereotypy (for experimental dogs, as reported by the 2 owner), age and sex of each dog. Control dogs that lived in the same household as their 3 counterparts are represented with an asterisk. Control dogs that were siblings of their 4 counterparts are represented with a dagger sign. Dogs shaded in gray were tested by the owner. STEREOTYPY CONTROL GROUP GROUP Frequency of Breed Bull Terrier Age Sex Stereotypy Stereotypy Age Sex 9 M Licking 1/ day 9 M 1 M Circling 10/ day 2 F 1 M Circling 1/day 4 M Light chasing, light Border Collie 4 F fixating 1/day 4 M Shetland Sheepdog 7 M Circling 3/ day 8 M 8 F Circling 1/day 8 F* † Circling, light fixating, Australian Shepherd 2 F fly snapping 3/day 6 F* Cattle Dog mix 5 F Circling 5/day 5 F American Pit Bull 5 M Light chasing 1/ day 2 M Blackmouth Cur 3 F Light chasing 1/day 3 M*† Miniature 3 F Licking, circling 5/day 9 M* Terrier PROTOPOPOVA, HALL, & WYNNE Dachshund 5 6 Doberman 2 M Licking 1/day 5 M Terrier mix 3 F Light chasing 1/day 3 F Number'of'responses'in'ex/nc/on' 60! 50! 40! 30! 20! 10! 0! Stereotypy! Control! !