At least thirteen years were needed to design, set up, and carry out their extensive behavior genetic research plans. Rather than employing the selective breeding frequently used with rats, Scott’s group took advantage of existing breed differences and worked on the assumption that breed differences reflected genetic differences. So, they based their work on five breeds of small dogs that spanned the temperament spectrum: Basenjis, beagles, cocker spaniels, Shetland sheepdogs, and wirehaired terriers.
Although both Scott and Fuller had backgrounds in biology, the neuroscientific and other physiological measures and manipulations that were available in the 1950s were severely limited compared to the research options that are available today. While they did collect some physiological data, they relied largely on diverse objective behavioral tests they designed to expose the dogs to environmental and behavioral challenges that might reveal individual and breed differences. These objective tests mostly allowed for timing or counting specific behavioral responses (rather than relying on subjective ratings by handlers or observers) to over twenty behavioral tests collected throughout the first year of life on large samples of all five breeds. Many of these tests were repeated throughout the dog’s first year of life to quantify developmental changes; this resulted in the administration of over fifty formal tests, plus numerous incidental observations such as whether puppies could learn to hold still when being weighed during weekly health examinations. We refer to many, but not all, of these unique objective tests and behavioral observations in this brief review of their overall study (for a comprehensive summary, see Scott & Fuller, 1965). In a sense, Scott and Fuller devised the first systematic canine emotional-personality tests, which is why we cover it here in some detail.
In addition, two of these breeds, Basenjis and cocker spaniels, were selected for a more complex genetic analysis involving simple crosses of the two breeds, labeled F1s, and crosses of those F1 progeny called F2s (F stands for “filial” or breeding family stock). Back-crosses from F1s to each of these two parent breeds were also completed to check and provide initial verification of any genetic hypotheses. While Scott and Fuller showed that many breed differences could be accounted for by one and two gene models, they surprisingly found that “the vast majority of genetic effects on behavior are highly specific and restricted to one or two situations” (1965, p. 375) rather than cutting across many behavioral traits. This program of research highlighted that trans-situational temperamental variables may be rare and hence difficult to genetically analyze. It is possible that such background traits were emotional ones that are harder to select for than specific behavioral abilities, but Scott and Fuller did not neglect to focus on the emotions of their animals.
One theme running through their work was the similarity of social bonding with conspecifics (members of the same species) and heterospecifics (across other species, including humans), work that highlighted the closely related development of social emotional attachments and place attachments in young puppies. How was this determined? When old enough to maintain body temperature and move about on their own, puppies that were left alone in their home pens emitted loud “distress vocalizations” at a very high rate, signaling their aversion to social isolation. However, they send out even higher rates of distress vocalizations when isolated in a strange place, indicating that distress was amplified when puppies were no longer in a familiar place (Elliot & Scott, 1961). This heightened level of vocalization began tapering off at about eight weeks of age, at the end of what additional research later indicated was the waning of a “critical period” for social attachment (Freedman, King, & Elliot, 1961; Scott, 1958; Scott, Fredericson, & Fuller, 1951). Upon the publication of their book Genetics and the Social Behavior of the Dog (Scott & Fuller, 1965), Scott was invited to be the first Ohio Regent’s Professor of Psychology at Bowling Green State University (BGSU), where the authors of this book worked with Scott in the early 1970s.5
At Scott’s BGSU dog lab, Panksepp’s group discovered that these distress vocalizations were specifically modulated by brain opioids (Panksepp et al., 1978) that had recently been discovered. The key finding was that tiny doses of opioids—namely “feel good” chemistries in the brains of all vertebrates that are naturally very rewarding (indeed addictive, when opioids are concentrated in various drugs)—could reduce separation distress vocalizations in young puppies. Across the late 1970s and 1980s, this led to a research program focused on the identification and description of a separation-distress brain system using direct brain stimulation procedures in guinea pigs and domestic chicks (summarized in Panksepp et al., 1988; Panksepp, 1998a). This research program highlighted a new social emotional system in vertebrates: the PANIC/Sadness system, which contributed substantially to social bonding. In other words, social bonding was partly due to addictive chemistries of the brain, helping explain why the loss of loved ones is so psychologically painful. For the first time a brain social-emotional system had been identified that no one had talked about yet. Parenthetically, at the same time Harry Harlow’s group at University of Wisconsin was demonstrating how emotionally disastrous it was for young rhesus monkeys to live alone (for a poignant summary of that work, see Blum, 2002).
While Panksepp’s (1982, 1998a) remaining primary-process (subcortical) brain emotional systems were worked out in rats and other species, the empirical relationships between the other brain emotion systems and dog behaviors (indirectly evident in Scott and Fuller’s work) still remain to be clarified neuroscientifically. Yet this multigenerational research, spanning the careers of both Scott and Panksepp, highlights the value of how clear animal models for emotions, when combined with direct brain manipulations/understandings, have the power to impact human psychiatric practice (for summaries, see Chapter 18; see also Panksepp, 2015, 2016). The implications of such findings for the understanding of human personality remain to be fully explored, for which we developed the Affective Neuroscience Personality Scales (Davis et al., 2003; Davis & Panksepp, 2011).
Another common social behavior in dogs, enthusiastic tail wagging so common during social interactions, was measured as part of the Jackson Lab project during the research program’s “handling test.” These data showed that Basenjis were less attracted to human handlers and cocker spaniels and beagles were the most attracted. Correspondingly, tail wagging itself appeared two weeks later developmentally in the Basenjis than in cocker spaniels. The difference in appearance of cocker and Basenji tail wagging was highly significant and both differed from the other three breeds, which were intermediate. It was later demonstrated at the BGSU Canine Research Laboratory that tail wagging could also be manipulated in very young and juvenile puppies with opioids and the opioid blocker naloxone (Davis, 1980; Knowles, Conner, & Panksepp, 1989), which like separation distress vocalizations linked canine tail wagging to emotional social bonding/attachments and indirectly to the PANIC/Sadness system.
At Jackson Lab, Scott and Fuller (1965) had also investigated play fighting (also known as rough-and-tumble play) in their dogs. Play fighting with human handlers peaked at about fifteen weeks of age and was also associated with definite breed differences. Among the breeds studied by Scott and Fuller (1965), wirehaired terriers exhibited the most play fighting in response to standard handling tests. Basenjis, Shetland sheepdogs, and beagles played at comparable levels, while cocker spaniels exhibiting considerably less play fighting.
However, the correlation between play fighting and later real fighting between conspecifics (other dogs) was found to be low, suggesting that play fighting was not related to aggressive (RAGE/Anger) sensitivities. Indeed, these distinctions were highlighted in their findings. For example, beagles exhibited a typical high level of play fighting in the handling test (Scott & Fuller, 1965, p. 136) but exhibited the lowest level of serious fighting as observed in dominance tests (p. 155). Cockers showed low play fighting and also low levels of dominance fighting. Wirehaired terriers and Basenjis showed high levels of both play fighting and serious f
ighting, as manifested in “complete dominance” tests. This segregation of real fighting and play fighting likely reflected the activity of two different brain systems, one linked more to the RAGE/Anger system and the retaining of resources such as food, and the other related more to the PLAY system with its social playfulness and positive socialization, distinctions that were evident in many other species (Panksepp, 1998a). While it was not the subject of a primary research project, Scott and Fuller (1965) had already suggested that play fighting reflected a positive social experience, facilitating positive social integration. The relationship between positive affect and playfulness was later empirically confirmed in rats (as described in Chapter 9).
In the general-purpose handling test, Scott and Fuller also measured the avoidance of human handlers, which was interpreted as timidity or fear, likely reflecting the primary FEAR system. Cocker spaniels showed the lowest avoidance of human handlers. Beagles were also less avoidant in the handling test, with the other three breeds exhibiting higher avoidance levels. In addition to being among the most avoidant breeds on the handling test, Shetland sheepdogs were also the poorest performers on the motor-skill and spatial-orientation tests, both of which required climbing, which Scott and Fuller (1965) attributed to shelties being quite fearful of heights.
Another case of fear affecting test performance was on the trailing test that required dogs to track a scent down a series of branching boards leading to a fish treat. All breeds did well except the wirehaired terriers and Basenjis. However, the poor performance of Basenjis was due a “fear reaction to the apparatus” (Scott & Fuller, 1965 p. 247) and refusal to cross the board trail. Basenjis were not afraid of heights like the shelties and were skilled climbers, but their cautious reaction to the strange apparatus interfered with their scores on the motor-skills test and was another example of the highly specific nature of many instinctive fears.
The leash training test measured the tendency of juvenile puppies to adapt to being on the leash or to fight this restraint. Scott and Fuller noted that “Basenjis were outstanding in their vigorous resistance to the restraint of a collar and lead” (1965 p. 209). The heritability for fighting the restraint of the leash was estimated from 0.45 to 0.77 (with 1.0 reflecting perfect heritability). Leash fighting with juvenile puppies may be a good model reflecting the RAGE/Anger system in action, which responds to physical restraint possibly based on an evolutionary adaptation to being captured by a predator (Panksepp, 1998a). Similarly, when placed in the restrictive Pavlov stand for the reactivity test (similar to that used by Ivan Pavlov for his classic studies on canine classical conditioning of salivation), Basenjis also exhibited a strong tendency to bite. While Basenjis showed the highest and cockers the lowest percentage of biting in the Pavlov stand at all ages, the differences became greater with each successive trial. By fifty-one weeks, 83 percent of Basenjis and only 7 percent of cocker spaniels were biting the restraint. Hence, the marked personality differences between aggressiveness and fighting across species—with Basenjis and cocker spaniels being respectively at the high and low extremes—demonstrating hereditary influences from puppyhood through early adulthood, potentially in the responsivity of the RAGE/Anger system.
Scott and Fuller’s (1965) overall emotional reactivity test was administered at seventeen, thirty-four, and fifty-one weeks of age, during which each dog was restrained in a Pavlov stand and subjected to ten stressful episodes with eighteen behavioral and physiological measures. Cocker spaniels showed the lowest overall reactivity scores, and Scott and Fuller interpreted the reactivity test as a measure of inhibitory training. They related the cocker’s relatively calm performance during this test to the breed’s historic capacity to respond to threats, especially hand motions, by ceasing all activity for a moment with no signs of emotional disturbance. This conclusion was further supported by the Jackson Lab’s weekly medical checkup procedures, during which puppies, in order to be weighed, were trained to remain quiet for one minute by the handler holding his or her hands near the animal but attempting not to touch the puppy standing on the scale. By fourteen weeks of age, 80 percent of cocker spaniel puppies would remain quietly on the scale for one minute, which was more than twice the percentage for any other breed. In wirehaired terriers, also the most reactive and least inhibited breed at fifty-one weeks on the reactivity test, only 10 percent of the puppies could quietly remain on the scale for one minute. It is tempting to associate the cocker’s capacity for inhibition as a cross-species form of the human Big Five Conscientiousness trait, which has been thought to represent the cortical regulation of subcortically based primary traits (Davis & Panksepp, 2011) and which in Chapter 7 was identified in chimpanzees and brown capuchin monkeys but has otherwise been difficult to identify in nonhumans.
Shetland sheepdogs showed slightly lower levels of inhibition than cocker spaniels during the reactivity test at all three ages. By contrast, wirehaired terriers, beagles, and Basenjis were consistently much more reactive and less inhibited than cockers and shelties. Like cockers, shelties were less reactive and more easily inhibited in the Pavlov stand, but in contrast to cockers, shelties exhibited high levels of fearfulness in other tests, as noted previously. In fact, among cockers, beagles, shelties, and Basenjis, all four combinations of high and low inhibition (on the reactivity test) and with high and low fear (on the human handler test) were exhibited, suggesting that inhibition training (low reactivity) and fearfulness (high avoidance) segregate independently genetically, as illustrated in Table 8.1.
Table 8.1. Segregation of Fear and Reactivity Across Four Dog Breeds
Fear and Avoidance Reactivity
Low High
High Shetland sheepdogs Basenjis
Low Cocker spaniels Beagles
Adapted from findings reported in Scott & Fuller (1965).
Scott and Fuller (1965) described maternal care of puppies but only indirectly touched on the CARE system by frequently hypothesizing maternal effects, including maternal effects on aggressiveness, which have now been shown in rats (Parent & Meaney, 2008), as discussed in Chapter 9. Also, Scott and Fuller (1965) decided not to study investigative behavior, even though the investigative system was one of Scott’s nine categories of behavior systems (Scott, 1958, 1972). Exploratory/investigative behavior, to monitor the status of what would relate to the primary SEEKING system, was judged to require too much space, given its relationship to hunting in the dog, and would have been too difficult to study experimentally in the field.
With a behavior genetics approach to behavior, these pioneers broadly sampled what we would view as the affective neuroscience temperament dimensions, which, for example, included demonstrations of the importance of distress vocalizations that would later be linked to Panksepp’s PANIC/Sadness system. Their research also included carefully measured individual differences in the PLAYfulness, FEAR, and RAGE/Anger systems. One might also consider cocker spaniel (and to a lesser extent sheltie) inhibition as a nonhuman candidate for the Big Five dimension of Conscientiousness and the regulation of emotion. Scott and Fuller’s discussion of what we would interpret as the SEEKING and CARE systems rounded out a rather complete treatment of the mammalian personality domain. In a highly objective study that predated modern neuroscience, Scott and Fuller impressively documented what Panksepp was identifying as primary mammalian emotion systems. Once again, a comprehensive analysis of mammalian behavior provided a set of traits that have been reported with remarkable consistency starting with Darwin and leading through so many other contributors to neuroscientifically documented blue ribbon emotions of affective neuroscience (Panksepp, 1981, 1982, 1998a; Panksepp & Biven, 2012). Scott and Fuller’s work invites further research exploring the empirical relationships between their many observations and these brain emotion systems underlying dog behavior. In addition, their work set the stage for later dog testing, which we now selectively review.
More Canine Assessments
Scott and Fuller’s work inspired subsequent b
ehavioral dog testing. We begin with studies on dogs tested using canine behavior questionnaires and then briefly review behavioral tests for dogs in military work and one study on pets in a rescue shelter. We reserve for the second part of this chapter research on the quality of social attachments in dogs, followed by a brief review of puppy testing research on selecting guide dogs for the blind (Pfaffenberger, Scott, Fuller, Ginsburg, & Bielfelt, 1976) and police dogs, all with the goal of comparing the breadth of canine personality dimensions to Panksepp’s six primary emotions related to human emotional personality issues.
Swedish Working Dog Association Studies
Svartberg and Forkman (2002) studied personalities of pet dogs using data from a dog behavior rating questionnaire developed by the Swedish Working Dog Association called the Dog Mentality Assessment (DMA). The DMA was developed mainly for dog breeders, but it became a popular general assessment with owners as well that has resulted in a massive database containing over 15,000 pet dogs from 164 breeds. The DMA evaluates dogs interacting with a familiar handler in response to ten separate subtests measuring thirty-three behavioral variables, which measure a dog’s reactions to strangers, opportunities to play with a human, reactions to prey-like objects, and several potentially fearful and aggression-inducing situations. From the forty-seven most popular breeds, Svartberg and Forkman randomly selected 1,175 adult dogs that averaged about two years of age.
An exploratory factor analysis on their large dataset yielded five latent dimensions: Playfulness, Curiosity/Fearlessness, Chase Proneness (including following and grabbing behavior), Sociability, and Aggressiveness (including threat displays and attacks). The Chase Proneness factor included ratings from only a single test, and the researchers tentatively interpreted it as predatory behavior, which based on rat research (discussed in Chapter 9) would align it with Panksepp’s SEEKING system. Although unpublished, some work was done in Scott’s BGSU dog lab examining predatory responses of puppies to small papier-mâché animal models with rudimentary limbs and heads, which also suggested the possibility of studying canine predatory behavior as a distinct temperamental dimension.
The Emotional Foundations of Personality Page 16