While more research is needed in the PANIC/Sadness-related personality differences of dogs, future attachment style research between humans and dogs might benefit from measuring specific canine appropriate social contact behaviors, such as tail wagging and face licking (e.g., Davis, 1980; Knowles et al., 1989), that could add objectivity as well as add qualitative richness to the descriptions of initial social contact the dogs made with either the owner or stranger. However, it would be especially important to include measures of separation distress vocalizations to assess the activation of the specific PANIC/Sadness system, which is characterized by a form of separation anxiety that is distinct from the anxiety generated by the FEAR system (Davis, Gurski, & Scott, 1977; Panksepp, 1998a).
An interesting new approach to detecting separation distress affect and possibly attachment style is the cognitive bias test model. This test is based on the assumption that in ambiguous situations individuals experiencing negative emotions will make more negative (pessimistic) judgments and individuals experiencing positive emotions will make more positive (optimistic) judgments, which has been confirmed in several species, including humans (Mendl, Burman, Parker, & Paul, 2009). Indeed, dogs (9 to 108 months of age) that exhibited higher levels of behaviors related to social separation distress when left alone made more pessimistic-like responses to ambiguous stimuli than dogs exhibiting less social separation distress (Mendl et al., 2010), which we would interpret as validating an animal model of the distressful PANIC/Sadness emotion biasing behavioral choices in a negative direction, and further suggest that it may be subcortical “affective bias” that is influencing these behavioral choices.
Puppy Testing Predictions
Another interesting question that arises from a discussion of early socialization is whether one can tell from examining a puppy what kind of personality it will have when it matures. This is an important question if one is deciding whether to expend the resources required to train a dog for police work or to become a guide dog for the blind. However, families also invest a great deal of money, time, and effort into raising a puppy and often would like some assurance that their new pet is going to remain a welcome addition rather than a burden to the family. This goes doubly so for selecting service companion dogs that are trained to assist medically impaired individuals, including psychiatrically challenged soldiers returning from difficult tours of duty.
While there are critics of puppy testing, especially at six to seven weeks or earlier (Riemer, Müller, Virányi, Huber, & Range, 2014; Wilsson & Sundgren, 1998), there are three validation studies with consistently positive results. These three studies all involve predicting puppies’ aptitudes for later training either as guide dogs for the blind or as police dogs in the latter two studies. The guide dog study was an outgrowth of Scott’s collaboration with Clarence Pfaffenberger, who was trying to reduce the number of dogs that had to be trained to produce a working Seeing Eye dog, because when the program started it could successfully train only 30 percent of its guide dog candidates. A series of thirteen behavioral tests was introduced for puppies from eight to twelve weeks of age, which included many of the kinds of tests Scott and Fuller had used in the Jackson Lab research program. A total of 239 puppies were tested and trained as guide dogs: those that were judged to have failed the tests (n = 33), those that had performed poorly (n = 18), and those that had passed (n = 188). Including puppies they thought could not be successfully trained was important to have sufficient variation in the sample to clearly show that better test results actually were related to better training results.
Four tests best predicted future success as guide dogs: the come test, the fetch test, the heel test, and the footing-crossing test. The use of these four tests improved training success rates to 60 percent, with those puppies failing the test succeeding only 20 percent of the time (Scott & Bielfelt, 1976). The first three tests could be easily conducted outdoors by a new puppy buyer. The come test involved walking a good distance away from the puppy, squatting down facing the puppy, and calling out “come puppy” while clapping or using its name (if it has one). The best result is when the puppy comes immediately. Poorer results are when the puppy has to be coaxed repeatedly or does not come at all. In the fetch test, the handler shows the puppy a small rubber ball while trying to get the puppy excited before throwing the ball several feet away and calling “puppy fetch” in a lively voice. The handler continues clapping and encouraging the puppy. The best result is when the puppy retrieves the ball to the handler immediately. For the heel test, if the puppy has never been on a leash, the puppy can be carried a short way from a familiar place, put on the leash, and encouraged to walk back on the left side of a right-handed handler. Otherwise, the puppy can be put on leash and walked away from the familiar place. The puppy can run slightly ahead of the handler, and the session is not turned into an obedience lesson. The issue (i.e., test result) is whether the puppy cooperates with the handler or fights the leash. These first three tests assess whether the puppy is motivated to interact with a human handler and, in the case of heeling on a leash, whether that extends to tolerating some physical restriction. The footing-crossing test involves a puppy being led over a patch of metal and a shallow curb. Observers rated whether the puppies were alert to these differences in their footing, which would be useful later as guide dogs.
The first of the two police dog studies was conducted in South Africa (Slabbert & Odendaal, 1999). They gave 167 young German shepherd puppies eight behavioral tests and later recorded whether the puppies passed a 103-day training course, which had to be completed by two years of age. Most of their objective tests were completed by twelve weeks of age, and three of those were most predictive of later successful training. The first was the obstacle test, a variation of the guide dog come test, in which puppies at eight weeks of age had to go through a large pipe (five feet long and two feet in diameter) and climb over stairs about eighteen inches high to reach a handler who called them. A fetch test, similar to the guide dog test, examined whether a puppy at eight weeks retrieved a small toy to its handler and was a strong predictor of later training success. At twelve weeks a startle test subjected each puppy to a stranger jumping out from behind a wall in front of the puppy. Puppies that made no effort to run away received the highest scores. A fourth test, another stranger test that the puppies received much later at six and nine months, involved a stranger provoking the puppies by striking them firmly but gently with a rag. If the dog bit the rag and held on, it received a high score; if it showed fear it received a low score. These tests were able to identify 91.7 percent of the successful dogs and 81.7 percent of the unsuccessful dogs.
The second of the police dog studies comes from the Czech Republic (Svobodová, Vápeník, Pinc, & Bartoš, 2008). In the Czech study, 206 German shepherd dogs were given ten tests and weighed at seven weeks of age. Interestingly, the strongest predictor of whether a puppy would later pass certification was its weight at seven weeks, which the authors attributed to a general preference of police to use large dogs. However, among the behavioral measures, the strongest predictors were the puppy’s willingness to chase, catch, and fetch a tennis ball and whether a puppy would bite and fight a rag being drawn away from it, which the authors collectively labeled “attitude to predation.” Although a weaker predictor, in three of the ten tests the puppies were exposed to loud distracting noises. Puppies that showed the most fear received the lowest scores; those that exhibited less fear and even showed exploratory interest in the noise receiver higher scores. Lastly, there was evidence that the more the puppy approached the tester in a friendly way, the more likely the puppy would later be successfully certified for police work.
All three of these studies aimed to identify dogs that could be trained to perform complex tasks. One finding all three studies have in common was a puppy fetching at an early age, which was strongly related to later training success. Scott and Bielfelt (1976) found that retrieving at later ages was not as predictive, because ev
entually almost all dogs in their sample could learn to fetch. However, the willingness at seven or eight weeks to fetch may indicate intense prosocial motivation that can carry into a dog’s adult life and facilitate its trainability to work closely with humans. While there may be a predatory SEEKING element that energizes the chasing component of fetching, there also seems to be a strong social motivation to interact with the handler that could indicate a sensitive PANIC/Sadness or PLAY system, which makes the ensuing contact with the handler very motivating as well. Along these lines, the guide dog study and the South African study found strong evidence that a puppy’s willingness and motivation to come to a human handler at eight weeks was also a strong predictor of later trainability, which could be related to the extent of human interactions in the Czech study, all of which support the idea that, in the dogs that excelled in their training, already as young puppies the PANIC/Sadness system had established a strong motivation to maintain contact with humans.
In the police studies, quiet biting (as opposed to angry noisy biting) likely reflects increased emphasis on SEEKING-based predatory behavior (with angry noisy biting more likely reflecting dispositions toward RAGE/Anger). In puppies, an aptitude for this capacity may be promoted and stimulated by taunting the puppy with a rag. This predatory (SEEKING) feature was also highlighted in the military dog training study cited above. In police or military work, biting hard and holding the bite to subdue a human target is an important tool, which the officer-handler must be able to turn on and off with commands given to the dog.
Having a less sensitive FEAR system seems to be an important affective dimension for such working dogs as well. Being able to tolerate being startled by loud noises or not being afraid of loud noises in general was a consistent predictor of future success as a police dog. Lastly, the puppy’s willingness to tolerate restraint as measured by the guide dog heeling test may be a good proxy for a less sensitive RAGE/Anger system, which along with the puppy’s willingness to please a human handler is an obvious requirement of all guide dog work. However, it would be surprising if this simple test were not equally effective in predicting training success in police and military working dogs.
In summary, both brain emotion network analysis and modern genetic profiling will allow investigators to have better anchored measures of emotional temperament than was available in previous eras. With ready access to modern genetic tools, such work is likely to be a major focus of future inquiries. Such analyses may already be coupled to the most remarkable canine selection study ever conducted, as described next.
The Fox Domestication Project
About fifty years ago, a selection project aimed at domesticating the Russian silver fox (Vulpes vulpes) was initiated to explore the domestication process in mammals. Starting with a population of silver foxes that had been farm bred for about fifty years (starting in the early twentieth century), foxes displaying the weakest fear and aggressive responses were selected to begin a line of potentially tame foxes (Trut, Oskina, & Kharlamova, 2009). Subsequent generations were subjected to attempted touching, petting, and hand feeding, and less than 10 percent of the pups exhibiting the most tameness were selected as parents for the next generation. After three generations of such selection, “aggressive and fear avoidance responses were eliminated from the experimental population” (p. 351). In the fourth generation, spontaneous tail wagging in response to humans was observed. In the sixth generation, 4 out of 213 fox pups emerged that eagerly sought human contact and wagged, whined, and licked faces like domestic dogs. The frequency of such pups increased to 17.9 percent by the 10th generation, 35 percent by the 20th generation, and 49 percent in the 30th generation. Reduced reactivity of the FEAR system seemed to have been closely involved in selection for tameness in the silver fox, because the age at which fear was first seen was shifted to about 4 months in the tame line from about 45 days in the unselected line (Trut et al., 2009). Of course, it is likely that sensitivities of PANIC/Sadness, PLAY, RAGE/Anger, SEEKING, and perhaps even CARE were also involved (as discussed further below), but without in depth neuroscience work, such issues will remain empirically unresolved.
A second line of silver foxes was selected for aggressiveness toward humans, and it was discovered that the tame and aggressive lines always exhibited different vocalizations toward humans: Tame foxes produced “cackles” and “pants,” and the aggressive line “coughs” and “snorts” (Gogoleva, Volodin, Volodina, Kharlamova, & Trut, 2010). When foxes from the same lines were observed together in pairs, despite directional testing for generations, tame foxes retained their capacity for agonistic behavior and vocalizations toward other foxes and aggressive foxes retained their capacity for affiliative behavior and vocalization, suggesting the genetic independence and complexity of these emotional systems.
From video tapes of the foxes during standard tests, 311 measures of physical activities such as position in the cage, body postures, ear position, and sounds were reduced to fifty key behaviors. The first principal component (a statistical clustering) of this reduced set of behaviors provided an objective measure that accounted for 48.4 percent of the variance (a statistical measure of overall percent relatedness or how well findings are explained by the chosen measures). This first principal component distinguished the aggressive and unselected lines from the tame line, as well as the F1 backcross to tame foxes, with the F1 line (tame line bred with aggressive line) being intermediate (Kukekova et al., 2008), clearly demonstrating the genetic differences between the tame and aggressive lines. While no specific genetic hypotheses were offered, one must assume that many genes and brain systems must be involved considering that the proportion of foxes that could be characterized as tame almost tripled from the 10th to the 30th generation. In addition to the FEAR and RAGE/Anger systems that were selected against in the tame parent line, it is likely that the PANIC/Sadness social bonding system was selected for as well, because tail wags and face licking in response to humans—both of which are known to increase in response to opioid blockers increasing PANIC/Sadness sensitivity (Davis, 1980; Knowles et al., 1989)—amazingly emerged in the fourth and sixth generations of this remarkable selection project.
CANINE SUMMARY
In canines, many of the descriptive details of social bonding and separation-induced distress have been documented (Scott & Fuller, 1965), the C-BARQ (Hsu & Serpell, 2003) has provided a “separation-related behavior” trait scale for dogs, and Topal et al. (1998) has developed a new test of social attachment. However, fuller understanding of sensitivity to separation distress as a temperament dimension in dogs and of the range of social bonding/dependence in dogs extending to pathological separation-related behavior (Mendl et al., 2010), and their genetic and neural underpinnings, will require much additional research. Clearly, better linking the social separation experience to the mammalian brain’s PANIC/Sadness system (Panksepp, 1998a) and the underlying brain and genetic mechanisms is needed to explore the canine model for separation-induced pathology in humans.
While foxes may naturally be less intensely social than dogs and wolves, the silver fox domestication project has shown that foxes possess the genetic basis for pronounced positive social motivation, including heterospecific bonding with humans. The counter suggestion that domesticated dogs have retained predatory tendencies, which are expressed toward humans, may provide insight into another pathological dimension of canine behavior in relation to humans. Although this has yet to be studied, one might start with breeds that have been found to be extra aggressive to humans historically, such as pit bulls (Sacks et al., 2000) and potentially determine whether predatory SEEKING and/or RAGE/Anger are responsible for their aggressiveness.
Another area that is once again highlighted in dog research is the confounding of fear and exploration. FEAR and SEEKING (Panksepp, 1998a) are two ancient but distinct brain emotion systems, which may often interact as animals negotiate their environments. Indeed, all the primary emotional networks tend to overlap in lower regi
ons of the brain, such as hypothalamus and midbrain periaqueductal gray, providing many opportunities for interactions. However, a temperament profile must allow for FEAR and SEEKING to vary independently; for instance, low exploratory tendencies do not automatically imply high levels of fear. A solid understanding of temperament requires the use of models that can better distinguish the anticipatory dopaminergic SEEKING system from the danger-oriented benzodiazepine-receptor-regulated FEAR system.
Overall, the key dilemma in temperament research is that there are no generally accepted experimental strategies to decode the neural nature of primary-process emotions in human subjects. A study of such brain systems in animals may eventually provide us with a causal neuroscience understanding of what it means for the mammalian/human to experience distinct affective feelings, but the primal neural mechanisms of affect simply cannot be deciphered through human research. There are at least seven emotional command networks as determined by distinct instinctual tendencies aroused by localized deep (subcortical) brain stimulation. Three of the positive affective systems, LUST, CARE, and PLAY, are all heavily dependent on the foundational influence of the general enthusiasm-promoting power of the SEEKING system, which may participate in all types of affective sentience (Panksepp, 1998a; Panksepp & Biven, 2012). However, these four as well as the three affectively negative ones (RAGE/Anger, FEAR, and PANIC/Sadness) all provide the motivation (i.e., unconditioned responses) for various kinds of learning (i.e., secondary processes) and surely higher cognitive (tertiary) processes that are very hard to systematically evaluate in animal models but that, in combination, surely guide higher cognitive-affective decision making and states of mind. Most dog owners (including Darwin) believe that their pets exhibit these higher cognitive capacities, which are so difficult to study rigorously in nonhumans.
The Emotional Foundations of Personality Page 18