 by: Robin Foster, PhD, CAAB
It's hard to come to terms with the realities of owning an old dog. My lovely English Setter turned 12 years old in March. For 11 of these 12 years, we started nearly every morning with a jog through the wooded trails near my home. Each week I ran 15 to 20 miles, and my dog probably ran twice that distance racing ahead and then behind me, chasing squirrels and interesting smells. All his life the one thing my dog has really loved to do is to go for walks. He's never been interested in chasing balls or playing with toys—but about a year ago our daily walks had quite suddenly become meandering and ambling saunters. When I first noticed that he had slowed down and lost muscle tone, I thought maybe he was just out of shape so I pushed him a little bit harder. But it became clear that his stamina wasn't what it used to be and he was losing coordination in his hindquarters, as some large dogs do. That's when I decided that we would just have pleasant leisurely long walks exploring the scenic parks of the Northwest coastal areas. Our walks Included a lot of sniffing and rest breaks, and I had to make sure they were shorter than 3 miles and didn't have steep uphill climbs, which he struggled with. The slower pace of our walks was very pleasant. It gave me an opportunity to enjoy the scenery and really see the beautiful plants and wildlife of the region, including bald eagles, hawks, spring peepers, coyotes, rabbits, bumble bees, and hummingbirds. I took time to study the mountain profiles and watch the clouds move lazily across the sky. As the months went by I began to notice that my clothes were feeling a bit snug. There are a number of reasons I gained 20 pounds last year, but the change in exercise routine with my aging dog was definitely one of them. At some critical point I began asking for advice. My friends had so many great ideas that would surely work. I should join the local rowing club. I should lift weights at the gym. I should take up biking. The problem with all these wonderful ideas is that they would mean spending time exercising that I would normally spend with my dog. And honestly, I would rather be overweight than miss out on any time with him. I consider myself a reasonably intelligent person with common sense, but I was stumped. After months of increasing distress and a growing waistline, a few weeks ago I came up with what I believe is a satisfactory solution, and I wanted to share it with a community of dog owners who might at some point find themselves in a similar situation. Each morning for the past two weeks my dog and I have set out on our 90-minute walk. He ambles along casually, stops to sniff or pee on every bush, and sometimes he just lays down in the shade to cool off and rest. At the same time, with leash in hand, I have done a challenging cardio workout by running in place for about 30 minutes, moving forward just enough to keep up with my dog. Sometimes I run in place backwards, do jumping jacks, or alternating knee lifts. If the park has a set of stairs, I tie my dog at the bottom where he lays down comfortably and watches while I run up and down the stairs, sometimes two at a time. If our walk takes us along a street, I step up and down on the curb in sets of 50. The Northwest is known for its very large cedars, so when I pass a tree that's at least 18 inches in diameter, I pause to do wall push ups against the trunk. Yoga is another activity that I really enjoy, so about halfway through our dog walk, I stop at a park bench or picnic table for about 20 minutes to do some standing yoga—the warrior pose, extended triangle, upward salute, and forward bend being some of my favorites. My dog lays under the table either watching me or other dogs who pass by. I've only recently started to put the ‘old dog walk exercise routine’ into place, so I don't yet have any evidence that it will improve my fitness or melt off the pounds, but I'm feeling optimistic (and I’ll give some credit for my positive attitude to the increase in my daily exercise.) The most rewarding part of the new routine is that my dog gets to spend quality outdoor time in the park, is comfortable with the pace, and seems to simply enjoy spending time with me. by Robin Foster, PhD, CAAB, CHBC A clicker-trained OTTB is torn between approaching and running away when he sees his owner walking into the pasture, but, as soon as he hears the sound of the clicker, he trots toward her for a treat. A Grand-Prix warmblood hears the barn door open in the morning and starts to pace, call, and paw at the ground until her grain is delivered. A two-year old wild mustang was fearful of most humans at first, but after he learned to target people with his muzzle for a hand-fed treat, the young horse now boldly walks up to every stranger and bumps the person with his nose. These examples are familiar to horse owners. They confirm that food is a powerful motivator of both desirable and unwanted behavior, and more importantly, they also illustrate that cues associated with food are quickly learned and also have the power to influence behavior. In each example, the horses responded to a cue that predicted food. When food is used as a reward in training, contrived cues—such as a clicker, special word, or gesture—may be specifically introduced to signal that food is forthcoming. A number of accidental cues also predict food that may not be part of the training plan, but are meaningful to the animal. Examples of accidental cues include: objects always present during training (a particular person, a target, a treat bag, a special halter); the location where food is delivered (from the hand, a dish, or a hay net); and the training context (facility, arena, paddock, or stall). An abundance of research confirms that cues associated with rewards have a powerful influence on motivation and behavior. Most research on reward learning has involved rodents in controlled laboratory studies, but the reward centers and neural pathways in the brains of all vertebrates are remarkably similar, and many of the findings in rodents apply to humans, horses, and other mammals, as well. What are Sign Tracking and Goal Tracking? "Sign-tracking” [1] (ST) refers to the finding that, for some animals, the cues associated with food and other rewards become powerful “motivational magnets”, charged with value (referred to in the scientific literature as incentive salience.) Sign-trackers approach and manipulate the cue first, before approaching the food. In animals that develop ST responses, simply being in contact with the cue is rewarding, and the cue functions as an effective conditioned reinforcer.[2] [3] Not all animals develop ST behavior. Certain individuals are predisposed to develop ST, but for others the cue does not become charged with value. These animals respond by “goal-tracking” (GT) and move directly to the location where the food will be delivered.[4] The cue predicts reward for both sign-trackers and goal-trackers the cue predicts reward, but the animals’ responses are markedly different. ST has been extensively studied in laboratory animals. It is essentially unknown in applied animal behavior, but almost certainly occurs. Using clicker training as an illustrative example, a horse predisposed to ST may persistently watch, approach, touch, and even mouth the clicker, before shifting its attention and moving to the location where the food will be delivered, such as an outstretched hand or food dish. In some cases the ST animal may even become unusually fixated on the clicker. In contrast, a GT horse will move immediately to the location of food delivery when it hears the clicker sound. Some individuals are more likely to engage in ST and others in GT. These distinct responses to cues are stable and may be governed by distinct learning systems.[5] Researchers studying individual differences are interested in how environment, neurobiology and genetic make-up interact to influence the incentive value of cues associated with rewards, including food, drugs, and sex. Why is Sign Tracking a Concern in Training? ST is an expected and common response to cues that are associated with rewards. Even though it is “normal”, ST has been linked to other behavior and learning patterns that can interfere with training and raise welfare concerns, and a goal in training should be to minimize the incidence of ST behavior. A few of these issues are described in the following sections. Sign-tracking has been linked to an increased risk for compulsive behavior and addiction[6] Sign-trackers may be especially prone to compulsive behaviors and addiction, because they place excessive incentive value on reward cues. In contrast, GT individuals are resistant to compulsive behavior and addiction.[7] [8] ST has been used as model of eating disorders and drug addiction, and is believed to reflect an “addiction-prone phenotype”.[9] It is widely recognized that food and drugs can take control over an individual’s thoughts and actions, depending on individual’s vulnerability to addiction as well as the qualities of the food or drug. Animals prone to ST are unable to shift their thoughts and actions away from both the food and cues associated with food (or cues associated with drugs.) Similarly, in humans, binge eaters are attracted by food-cues (e.g., food smells), and drug addicts are strongly attracted to drug-cues (e.g., syringes). Unusually strong attraction to the cue seen in sign-trackers can lead to excessive indulgence in the food or drug. The value of the cue can be enhanced in sign-trackers—but not in goal-trackers—by exposing the animal to drugs like cocaine and amphetamines that sensitize the reward-learning neural pathways.[10] Whether certain foods can similarly sensitize the reward-learning neural pathways isn’t known, but is possible. Behavior change protocols often recommend using high quality treats, and trainers often complain that high value treats seem to take control over a horse’s thoughts and actions, and can even interfere with training. “Lusting while loathing”[11] can be triggered by cues associated with rewards Desire and pleasure areas of the brain are activated by food, drugs, sex, and other pleasurable stimuli, as well as by cues linked to these stimuli. An important scientific discovery is that wanting (desire) and liking (pleasure) appear to be distinct experiences with different neural pathways. Wanting is the motivation to seek out and consume, and liking is the warm and fuzzy feeling of satisfaction. The urgent, intense, cravings of extreme wanting characteristic of addictive and compulsive behaviors may hold no pleasure whatsoever, and may even be distressing. Desire is easy to recognize through behaviors such as approach and consumption; pleasure is much more challenging to directly observe and objectively measure in animals, but even in rats the body language associated with liking and wanting are distinct if one observes closely enough.[12] “When rats taste something sweet, they do what human babies do – poke their tongues out and lick their lips. The more they enjoy a taste, the more their tiny tongues waggle with delight…. Tongue-waggling and lip-licking, believe it or not, are Berridge’s pleasure barometers.”[13] Learning to recognize the body language of liking, and to distinguish it from wanting, has welfare implications when using food-reward training. Wanting may motivate behavior, but it doesn’t follow that the experience is pleasurable. Sign-trackers are susceptible to and unable to inhibit desire, even when the pleasure of consuming the food or drug diminishes. For sign-trackers both desire and pleasure will be high at first, but the wanting will persist—triggered by the sight, smell, and proximity of the reward—even when the pleasure is gone. For goal-trackers, desire and pleasure are more closely linked and the animal will lose interest as it becomes satiated; desire will decrease as pleasure diminishes because the cues that predict treats hold no incentive value. Sign-trackers may be vulnerable to fear conditioning Sign-trackers attribute excessive value to a learned cue, regardless of its emotional valence. Most studies on ST and GT have focused on cues that predict food and drugs, but sign-trackers also appear to be vulnerable to PTSD[14] and may have more severe responses to fear-conditioned cues. PTSD and addiction are very different, but there is a strong link between PTSD and substance abuse. Both share an increased “hyperreactivity to trauma- or drug-related cues.” [15] A recent study in rats found that sign-trackers were vulnerable to fear incubation (i.e., the animal’s fear worsened in the absence of conditioning experiences), whereas goal-trackers had normal fear responses that decreased over time. In addition, ST mice have higher corticosterone levels, which is a marker of vulnerability to drug abuse and is associated with stress and fear.[16] Fear and avoidance contribute to many behavior problems in horses, and an animal’s vulnerability to fear conditioning is an important consideration when exposing it to potential sources of discomfort or stress (e.g., during training or veterinary procedures). For sign-trackers but not goal-trackers, the cues not only predict the aversive event, but may also acquire aversive properties, elicit a strong fear and avoidance responses, and be resistant to extinction. Not much is known about the relationship between ST and fear conditioning, but the same principles that operate in reward learning may apply. How can Sign-tracking be Influenced by the Environment and Training Conditions? Individuals differ in their predisposition to ST behavior, but the specific learning conditions also play a significant role. Even in adult animals, whether ST or GT develops can be modified by changing the environment and training protocol. Decades of laboratory research on ST offers practical information about how to decrease ST behavior in applied animal training. Increasing the delay and distance between the cue and reward reduces sign-tracking Sign-tracking response are more likely to emerge if there is short delay between the cue and reward, and when the cue and reward are physically close or in the same location. Increasing the spatial and temporal separation between the cue and reward leads to a reduction in ST and an increase in GT.[17] Mugging is a common complaint about horses trained with food rewards. Sign-trackers will approach and manipulate any cue associated with food reward, and mugging occurs when a horse approaches and “manipulates” the trainer or, more often, her coat pockets. Mugging may be evidence of ST, which is likely to develop during training if the cue and food are in the same location and if the time delay between them is short. It may be particularly pronounced if the trainer embodies both the cue (holds a clicker in one hand) and food (feeds the horse from the other hand, with treats in a pouch on the person’s waist). In this example the person, the pouch, and the marker combine into a “super-cue” that predicts food. It’s important to recognize that ST is persistent and resistant to extinction (see “Extinction” section below). This means that ST horses will continue to approach and bump the person, even when the she doesn’t have food, because the person has become a motivational magnet. Sign-tracking response are more likely to develop to some cues than others In rats, ST is very common when a moving lever predicts food; animals will approach and manipulate the lever before approaching the food-delivery location. In contrast, when a sound predicts food, rats nearly always show GT and move directly to the food-delivery location. The reasons for this difference are unclear; the different cues are equally effective predictors of food, but only some (the lever) acquire incentive value and can function as a conditioned reinforcer.[18] Using a sound for a cue seems to prevent the development of ST behavior, whereas objects that can be manipulated appear to encourage ST. In training, exactly where clickers fit in isn’t clear; they produce a sound, but are also tangible objects with visual, tactile, and dynamic properties. Most trainers have experienced horses that become focused on and touch (or even lick) the clicker, which suggests that it has acquired incentive value. These ST horses may also be vulnerable to compulsive behavior around the food and clicker, and continue to show a strong motivation for training even when it is no longer pleasurable. At present there is no systematic published research on the development of ST and GT responses with the use of a clicker as the cue. Sign-tracking is resistant to Pavlovian extinction Classically (Pavlovian) conditioned responses to the cue are slower to extinguish in sign-trackers than in goal-trackers.[19] During extinction the cue is repeatedly presented alone without the reward, and the conditioned response to the cue is expected to decrease or disappear. For example, extinction of a clicker-reward association would involve presenting the clicker sound repeatedly, without food, until the animal stops responding to the clicker and no longer expects a treat. Goal-trackers would quickly stop responding to the clicker sound, whereas sign-trackers would continue to respond to the sound. Biased attention to the cue may result in this “persistent and inflexible responding” by sign-trackers during extinction.[20] Resistance to extinction does not seem to occur for cues in instrumental conditioning. [21] An example of a cue (discriminative stimulus) in positive reinforcement training is the verbal command “back”; when the horse steps backward in response to the command, it gets a treat reward. In positive reinforcement training, extinction of the verbal command would be similar for sign-trackers and goal-trackers. Studies show that sign-trackers are also slower to discriminate between reward and no-reward situations, and seem to be attracted to the cue regardless of whether or not it predicts a reward in that situation. For example, a food dish (cue) may predict that the horse will get grain (reward) only when it is in the stall, but not when it is in the barn aisle. Sign-trackers will continue to approach the food dish regardless of its location and whether or not food is available, and are slower than goal-trackers to learn that the dish only predicts food in certain contexts. Pre-exposure to the cue reduces sign-tracking If the animal is familiar with the cue, for example by repeatedly presenting it alone, before it has ever been associated with a reward, ST is inhibited (this is known as latent inhibition). Prior exposure to the cue does not affect the emergence of GT responses directed at the food-delivery location.[22] In clicker training, presenting the clicker sound repeatedly before linking it to a food reward should reduce the incidence of ST and increase GT. If the clicker is introduced and only used during training with food rewards, then ST is more likely to develop. Uncertainty between the cue and reward increases sign-tracking The emergence of ST response is high if the reward follows the cue only some of the time, but only when training begins with partial reinforcement. When training begins with continuous reinforcement and then later adjusts to a partial reinforcement schedule, the incidence ST is low and does not increase. Uncertainty usually refers to training with partial reinforcement, and in most research studies the reward follows the cue half of the time. Certainty refers to continuous reinforcement, and the reward always follows the cue. The effect of uncertainty on the development of ST responses can be dramatic; in one study, when rats were trained with partial reinforcement the proportion of sign-trackers was 90% and goal-trackers was 5%. When rats were trained with continuous reinforcement the proportion of sign-trackers was only 50% and goal-trackers increased to 35%.[23] Uncertainty also refers to variability in the value of the reward, for example if the cue is sometimes followed by a small, low value reward, and at other times by a large, high value reward. ST responses increase with uncertainty, especially when it combines uncertainty in both partial reinforcement and reward value.[24] Environmental enrichment reduces sign-tracking The overwhelming evidence is that environmental enrichment results in a lower incidence of ST.[25] How enrichment interacts with other factors is more complex. For example, in one study, adolescent rats showed less ST behavior than adults, but were more sensitive to food restriction and social isolation. When adolescent rats were placed on a food restricted schedule, ST was higher in socially isolated rats, and GT was higher in pair-housed rats.[26] More research is needed to clarify the complex interactions between enrichment, age, and ST. Take home message Food is commonly used in positive reinforcement training and in desensitization and counter-conditioning behavior modification. An understanding of ST is valuable for animal trainers, particularly those who use clicker-training, because the clicker is a cue specifically introduced to predict a food reward. The goals of this article are to raise awareness of ST, the potential problems linked to ST—including compulsive behavior and resistance to extinction—and suggest ways to reduce ST in order to improve training outcomes and animal welfare. Another goal of this article is to encourage applied research on ST in horses. As a general rule, it’s prudent to be cautious about extrapolating findings from laboratory studies to applied animal training. With respect to ST, many laboratory experiments are set-up to encourage a high incidence of ST and may not represent real-life situations that concern animal trainers and behaviorists. What is needed in horses is a systematic description of ST behavior, identification of contexts that affect the emergence of ST, and recognition of individuals that are at risk for ST responses. References [1] Hearst, E., & Jenkins, H. M. (1974). Sign-tracking: The stimulus–reinforcer relation and directed action. Austin, TX: The Psychonomic Society. As cited in Burns, M., and Domjan, M. (1996) Sign tracking versus goal tracking in the sexual conditioning of male Japanese quail (Coturnix japonica ). Journal of Experimental Psychology: Animal Behavior Processes, Vol 22(3), 297-306). 2 Robinson, T.E., 2009. Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biological Psychiatry 65(10) 869-873. [3] Beckmann, J.S., and Chow, J.J. (2014) Isolating the incentive salience of reward-associated stimuli: value, choice, and persistence. Learning & Memory, 116-127. 4 Boakes, R. A. (1977). Performance on learning to associate a stimulus with positive reinforcement. In H.Davis & H. M. B.Hurwitz (Eds.), Operant-Pavlovian interactions (pp. 67–97). Hillsdale, NJ: Erlbaum. As cited in Burns, M., and Domjan, M. (1996) Sign tracking versus goal tracking in the sexual conditioning of male Japanese quail (Coturnix japonica ). Journal of Experimental Psychology: Animal Behavior Processes, Vol 22(3), 297-306. [5] Nilsson, J., Kristiansen, T.S., Fosseidengen, J.E., Ferno, A, and van den Bos, R. (2008) Sign- and goal-tracking in Atlantic cod (Gadus morhua). Animal Cognition 11(4), 651-659. [6] Anderson, R.I., Bush, P.C., and Spear, L.P. (2013) Environmental manipulations alter age differences in attribution of incentive salience to reward-paired cues. Behavioural Brain Research 257, 83-89 [7] Flagel, S.B., Akil, H., and Robinson, T.E. (2009). Individual differences in the attribution of incentive salience to reward-related cues: Implications for addiction. Neuropharmacology 56 (S1), 139-148. [8] Flagel, S.B., Watson, S.J., Akil, H., and Robinson, T.E. (2008) Individual differences in the attribution of incentive salience to a reward-related cue: Influence on cocaine sensitization. Behavioural Brain Research 186(1) 48-56. [9]Tunstall, B.J. and Kearns, D.N. (2015) Sign-tracking predicts increased choice of cocaine over food in rats. Behavioural Brain Research 281, 222-228. [10] Flagel, S.B., Watson, S.J., Akil, H., and Robinson, T.E. (2008) Individual differences in the attribution of incentive salience to a reward-related cue: Influence on cocaine sensitization. Behavioural Brain Research 186(1) 48-56. [11] Litt, A., Khan, U., and Shiv, B. (2010) Lusting while loathing: Parallel counterdriving of wanting and liking. Psychological Science 21(1), 118-125. [12] Fleming, A. (2015) The science of craving. The Economist: The Intelligent Life (May/June) http://www.intelligentlifemagazine.com/content/features/wanting-versus-liking?https%3A%2F%2Fwww.socialflow.com%2Fpublish#?fsrc=scn/fb/te/bl/ed/100socialflow=science+of+craving [13] Fleming, A. (2015) The science of craving. The Economist: The Intelligent Life (May/June) http://www.intelligentlifemagazine.com/content/features/wanting-versus-liking?https%3A%2F%2Fwww.socialflow.com%2Fpublish#?fsrc=scn/fb/te/bl/ed/100socialflow=science+of+craving [14] Morrow, JD, Saunders, BT, Maren, S, and Robinson, TE. 2015. Sign tracking to an appetitive cue predicts incubation of conditioned fear in rats. Behavioural Brain Research 276, 59-66. [15] Morrow, JD, Saunders, BT, Maren, S, and Robinson, TE. 2015. Sign tracking to an appetitive cue predicts incubation of conditioned fear in rats. Behavioural Brain Research 276, 59-66. [16] Tomie, A., Lincks, M., Nadarajah, S.D., and Pohorecky, L.A., (2012). Pairings of lever and food induce Pavlovian conditioned approach of sign-tracking and goal-tracking in C57BL/6 mice. Behavioural Brain Research 226(2), 571-578. [17] Silva, F.J., Silva, K.M., and Pear, J.J. (1992) Sign- versus goal-tracking: Effects of conditioned-stimulus-to-unconditioned-stimulus distance. Journal of the Experimental Analysis of Behavior 57(1), 17-31. [18] Beckmann, J.S., and Chow, J.J. (2014) Isolating the incentive salience of reward-associated stimuli: value, choice, and persistence. Learning & Memory, 116-127. [19] Ahrens, A.M., Singer, B.F, Fitzpatrick, C.J., Morow, J.D., and Robinson, T.E., (2015) Rats that sign-track are resistant to Pavlovian but not instrumental extinction. Behavioural Brain Research July 30, 2015 [20] Ahrens, A.M., Singer, B.F., Fitzpatrick, C.J., Morrow, J.D, and Robinson, T.E. (2015) Rats that sign-track are resistant to Pavlovian but not to instrumental extinction. Behavioural Brain Research, July 30 (update ref) [21] Ahrens, A.M., Singer, B.F., Fitzpatrick, C.J., Morrow, J.D, and Robinson, T.E. (2015) Rats that sign-track are resistant to Pavlovian but not to instrumental extinction. Behavioural Brain Research, July 30 (update ref) [22] Boughner, R.L., and Papini, M.R., (2003) Appetitive latent inhibition in rats: Now you see it (sign tracking), now you don't (goal tracking). Learning & Behavior 31(4), 387-392. [23] Robinson, M.J.F., Anselme, P., Suchomel, K., and Berridge, K.C. (2015) Amphetamine-induced sensitization and reward uncertainty similarly enhance incentive salience for conditioned cues. Behavioral Neuroscience 129(4), 502-511 [24] Anselme, P., Robinson, M.J.F., and Berridge, K.C., (2013) Reward uncertainty enhances incentive salience attribution as sign-tracking. Behavioural Brain Research 238, 53-261 [25] Beckmann, J.S. and Bardo, M.T. (2012) Environmental enrichment reduces attribution of incentive salience to a food-associated stimulus. Behavioural Brain Research 226, 331—334. [26] Anderson, R.I., Bush, P.C., and Spear, L.P. (2013) Environmental manipulations alter age differences in attribution of incentive salience to reward-paired cues. Behavioural Brain Research 257, 83-89. by Robin Foster, PhD, CAAB Certified Applied Animal Behaviorist  Canine behavior problems rooted in fear and anxiety are some of the most common complaints presented to veterinarians, applied animal behaviorists, and trainers. Anxiety-based problems are difficult to treat, and in both people and animals there can be an unexpected increase in fear in the absence of any negative experiences. Behavior modification to treat anxiety typically involves desensitization; the dog is exposed to the feared stimulus without anything bad happening and without triggering fight or flight responses, such as barking, lunging, or balking. In theory repeated exposure--especially when paired with a pleasurable event like a treat (counter-conditioning)--should lead to a decrease and ultimate extinction of the fear and reactivity. But in reality fear-based behavior problems are notoriously resistant to extinction and in some cases may even get worse. For example, suppose your dog becomes alert and shows signs of stress when he spots another dog on the other side of the street, and nothing bad happens. In theory this neutral (or even positive) experience should reduce your dog’s fear and anxiety, but maybe it persists or gets worse. Why?! There are many possible reasons, but one that is rarely discussed in dog training circles is a well-known phenomenon called incubation. In the late 1960s European personality psychologist Hans Eysenck introduced the concept of incubation. He used this term because in both humans and animals fear often seems to incubate, or intensify, in the absence of any experience. Several studies published over the last half-century have confirmed that four key factors account for fear incubation and resistance to extinction.
The first two factors are nearly impossible to control and behaviorists are often trying to manage the consequences of their effects on fear and reactivity. The third and fourth factors come into play during behavior modification and should be taken into consideration when using exposure methods to treat fear and anxiety. Recent studies of incubation have focused on the brain and have found a link between an individual’s vulnerability to incubation and low levels of a substance called brain-derived neurotrophic factor (BDNF). One study showed that fear was extinguished equally quickly in animals with low and normal levels of BDNF, but that fear was more likely to reappear in animals with low BDNF after just one bad experience following fear extinction (this is called renewal). There are two take-home points for behaviorists and trainers. First, owners should be made aware that the treatment for fear and anxiety will generally take longer and may be vulnerable to relapse in animals with a neurotic/introverted temperament or a history of trauma. Second, behavior modification recommendations should emphasize long exposures to weak triggers. In my experience many failed desensitization efforts are a direct result of violation of these two conditions. For example, letting another dog approach and greet a fearful dog is too intense! Quick retreats at the first sight of an approaching dog is too brief! Letting your dog watch another dog from a distance and for a long time (until he loses interest is best) will produce the most effective results in most cases. I have used the example of dog-dog reactivity, but the same principles apply to any fear-based behavior issue. References
Eysenck H. 1968. A theory of the incubation of anxiety/fear responses. Behaviour Research and Therapy 6(3):309-321. Pickens C, Theberge F. 2014. Blockade of CB1 receptors prevents retention of extinction but does not increase low preincubated conditioned fear in the fear incubation procedure. Behavioural Pharmacology. 25(1):23-31. by Robin Foster, PhD, CAAB  The first time that my young English setter visited the stable where I board horses he was overjoyed at the freedom to explore new sights, smells, and (yuck) tastes. After thoroughly investigating the horse stalls and chicken coop, his attention shifted to the horses themselves. As he ducked under the electric fence bordering the pasture, he let out an agonized yelp as his back touched the hot wire. He streaked toward me, tail tucked and eyes wide, and for the rest of the day he never strayed from my side. That electric jolt was probably the first pain he had ever experienced.
On a different occasion at the barn (never a dull moment!) as I was saddling my mare for a lazy summer afternoon trail ride, we were interrupted by the sound of thundering hoofs. Galloping up the lane was my friend Ann’s horse . . . without its rider! As soon as the horse reached a grassy spot near the barn, she stopped abruptly, let out a big sigh of relief, dropped her head and started grazing. Apparently a tractor had frightened the horse, who shied and bolted for home leaving Ann behind—dirty, annoyed, and luckily only a little bruised. What do these incidents have in common? The most obvious similarity is that in both cases the frightened animals ran away from danger. A somewhat less obvious similarity is that both animals also ran towards safety. I served as a safety cue for my dog, and the familiar farm was a safety cue for the horse. Importantly, the animals felt immediately relieved and relaxed in the the presence of the safety cue. The power of safety signals to inhibit fear and avoidance, and to promote relief and relaxation, was established decades ago in laboratory studies with rodents. The vast majority of behavior issues experienced by domestic animals are based in fear and anxiety, but safety signal training is not typically included in behavior modification protocols. In a review article currently in press in the Journal of Veterinary Behavior, Paul McGreevy et al. highlight the importance of safety needs in motivating in animal learning and the potential for safety signal training as a tool in the treatment of fear and anxiety in animals. Causes of fear and anxiety-based behavioral problems Some fears are learned through painful, unpleasant, or traumatic experiences. In animals we rarely know what the bad experience was, but by watching closely we can usually identify the stimuli or situations that the animal perceives as threatening and that may have been associated with the bad experience. In social animals, some fears may be learned by observing others reacting fearfully toward the danger cue. And some fears, such as wariness of unfamiliar individuals or novel objects, can emerge without experience through evolved or artificially selected genetic predispositions. A threatening stimulus or “danger cue” can trigger a progressive series of defensive reactions that include freezing, fleeing, and fighting. These behaviors are usually undesirable in a companion or working animal, but persist because fear is physically uncomfortable and the defensive reactions are effective at both reducing the fear and removing the threat. Animals with fear-based problems seem to get worse over time, possibly because, by reacting sooner, they minimize their exposure to the danger cue. Behavior modification for fear-based behaviors Owners often put off seeking professional help until their fearful animals do something unacceptable or experience veterinary problems associated with chronic anxiety. Behavior modification, sometimes in conjunction with anti-anxiety medication like fluoxetine or alprazolam, has proven very effective for reducing fear emotions and avoidance behaviors. The most common techniques for treating behavior problems rooted in fear and anxiety are classical counter-conditioning (CCC), operant counter-conditioning (OCC), and extinction, which includes a method of exposure and response prevention (ERP). Safety signal training is rarely employed. These techniques modify emotions and behavior through different mechanisms. CCC changes the meaning of the danger cue by pairing it with a high value treat (or other attractive stimulus). The animal begins to expect something good in the presence of the danger cue, and the fear is inhibited. Once the emotion is under control appropriate behaviors are much easier to train. OCC reduces the unwanted behavior by rewarding a different acceptable behavior when the danger cue is present, either using a high value treat (positive reinforcement) or by removing the danger cue (negative reinforcement). For example, when the danger cue is present (a stranger is approaching) and the dog looks up at the handler instead of lunging, looking up would be rewarded with a treat or by moving away from the danger cue. The logic behind OCC is that if the animal’s behavior is relaxed, calm emotions will follow. In practice CCC and OCC are typically used together. Extinction involves repeatedly presenting the danger cue without anything bad happening, and eventually the animal will learn that the danger cue does not predict danger. In theory, extinction seems like a simple technique but it is fraught with practical challenges. Extinction requires long exposures to the danger cue because brief exposures can increase fear through a process called incubation. To get the longer exposure may require physically preventing the animal from running away, barking, and lunging (ERP), which in practice is challenging at best, and may pose welfare and safety issues. Flooding is an extinction technique that exposes an animal to a high intensity of the danger cue until the animal relaxes (or stops trying to escape). Flooding can be effective, but it must be used selectively and cautiously. As an example of how flooding can backfire, I consulted on a case involving an Arabian horse that spooked at white plastic bags and had tossed his rider several times. Several months before I started working with the horse, a different trainer had recommended a flooding procedure: the horse was confined to his stall with 50 white bags with the idea that he would eventually get used to them. But instead the horse started whinnying and pacing frantically for about 5 minutes, and then kicked through the stall door and ran off. Not only was he hard to catch afterward, from that point forward he was even more fearful of white bags and refused to set foot into his stall. External inhibitors of fear and anxiety It’s important to distinguish safety signals from external inhibitors, which are things in the animal’s environment that help reduce fear or anxiety without any training. For example, background noise like an electric fan can reduce a dog’s anxiety about fireworks, and the presence of a calm mare can inhibit a young foal’s fear of humans. When the external inhibitor is another animal, it may be considered a form of social facilitation. As an example, I was assisting at a clinic where one rider was trying quite unsuccessfully to convince her horse to walk through an obstacle called a “car wash”, which is a wall of streamers. Pushing and pulling the 1200 pound animal was pointless, and the horse was not interested in carrots, so we recruited an experienced horse to demonstrate. After two or three passes closely following the relaxed leader through the streamers, the previously fearful horse willingly and leisurely walked through the car wash alone. As an important practical note, an anxious leader would have produced the opposite effect and increased the horse’s fear and avoidance of the obstacle. Training safety signals Safety cues are learned through experience by signaling the absence of a bad event or aversive stimulus. They are powerful inhibitors of fear and avoidance, and can override undesirable responses triggered by danger cues. This property makes safety signal training a promising addition to behavior modification protocols for treating fear-based problems in animals. Safety signals can be trained using two different techniques: discrimination and backward conditioning. In general, when the safety cue is present nothing bad happens (and a lot of good things may happen!). The most practical application of safety signal discrimination training is the “A+/B-/AB-” model; “A” is the danger cue, “B” is the safety cue, “+” is the presence of the aversive, and “-“ is the absence of the aversive. We can use the case of a dog that is fearful of strangers to illustrate the training protocol. First, let’s assume that the dog had some sort of bad experience with a stranger in the past (“A+”) and now reacts by lunging and barking at strangers. In safety signal training the dog learns that when the safety cue—usually its owner, but it could be a toy or a clicker sound—is present nothing bad ever happens (“B-”), even when a stranger is also present (“AB-”). In real-life situations we assume that the fear conditioning event (“A+”) already happened and do not need to repeat it during safety signal training! It’s also important to avoid pairing the safety cue with unpleasant stimuli or events, especially early in training (this is yet another reason against using punitive and dominance training methods, especially with a new pet). Some techniques currently used to treat fear-based behaviors may be effective in part by creating safety signals through discrimination training. For example, in Grisha Stewart’s Behavioral Adjustment Training (BAT), the handler exposes a dog to the threatening stimulus (danger cue) at a safe distance, where the dog is attentive and alert but not fearful. Because there is prolonged exposure to the danger cue and nothing bad happens when both the danger cue and handler are present, the handler may become a conditioned safety signal. Safety signals may also be learned through backward conditioning. In this process, the safety cue appears immediately after the aversive is removed and predicts a period of respite from the threat. Backward conditioning is more common in real-life experiences than in training, but it may play a role in negative reinforcement training. For example, a horseback rider typically applies leg pressure to get the horse to move forward or speed up. When the horse responds correctly the rider releases the pressure (negative reinforcement) and will often say, “Yes!” or “Good girl!” Because the verbal cue occurs immediately after the pressure is removed and it predicts a respite from the pressure, it may become a safety signal through backward conditioning. Safety signals can be anything: a click! or a special word; a bandana or vest; a location; or a familiar animal or person. Owners often become safety cues for their pets. For example, I was on a recent follow-up consultation for an Australian shepherd that was fearful and aggressive toward visitors in the home. The owners had set up a spacious designated dog area, and in general he seemed content being confined there. During the consultation we wanted to see if the dog would be comfortable in this space when a visitor was present, which would give the owners the “luxury” of finally being able to invite friends to their home. Interestingly, when I was present in the home the dog was comfortable in the designated dog area only when one of the owners stayed with him, and he was distraught when the owner left to join us in an adjacent room. This suggests that the owner, but not the space, had become a conditioned safety signal. The up-side to this story is that when an owner serves as safety signal, it is evidence of a strong trusting relationship between the animal and human. Why all the fuss about safety signals? In addition to their value at inhibiting fear and avoidance, safety cues possess the following properties that make them particularly appealing for behavior modification: 1) Once learned, it is very difficult to retrain the safety signal as a danger signal; 2) Safety signals can ease the effects of environmental and social stressors; 3) Safety cues possess rewarding qualities and seem to act as antidepressants; 4) In the presence of safety signals, animals tend to engage in naturally rewarding behaviors like exploration, eating, and social interactions; in contrast, danger signals inhibit these behaviors and fearful animals do not value food or social attention; 5) Safety signals inhibit new fear conditioning; and 6) The ability of safety cues to inhibit fear and anxiety is generalized across situations. A fascinating discovery is that these properties of safety signals do not apply to people with PTSD, who cannot learn to discriminate between safety and danger cues. This unique impairment can be used to diagnose fears having a traumatic origin; it is not known if the same impaired learning is seen in animals that have a history of trauma, but it would be an important clinical finding. References Christianson, JP, Fernando, ABP, Kazama, AM, Javanovic, T, Ostroff, LE, and Sangha, S. 2012. Inhibition of fear by learned safety signals: A mini symposium review. The Journal of Neuroscience 32: 14118-14124. McGreevy, P, Henshall, C, Starling, M, McLean, A, and Boakes, R. 2014. The importance of safety signals in animal handling and training. Journal of Veterinary Behavior (in press) |
