It is also noteworthy that not being “fearful” or “dependent” both loaded on King and Figuerado’s (1997) Dominance dimension rather than the Emotionality dimension, with a third adjective, “aggressive,” splitting its loadings between (high) Dominance and (low) Conscientiousness. In affective neuroscience terms these adjectives would be associated with FEAR, PANIC/Sadness, and RAGE/Anger, respectively. By contrast, in the King and Figueredo study the Emotionality dimension was limited to the more general and less specific terms “stable,” “unemotional,” and not being “excitable,” all resembling the relatively undifferentiated human Big Five Emotional Stability factor. Once again, one is compelled to address the limitations that factor-analytic procedures impose on parsing the workings of the mammalian BrainMind.
PRIMATE SUMMARY
Altogether, these primate studies establish that temperament in the great apes and brown capuchins can be accurately described using rating methods borrowed from human studies and resulting in the same factor-analytically derived dimensions as those derived using human subjects. Having some difficulty replicating an Openness dimension is not surprising given the illusiveness of the smallest of the Big Five factors even in human studies (Goldberg, 1990). More generally, unresolved issues surrounding Conscientiousness and whether it can be systematically monitored in orangutans and primates generally is bound to remain unresolved for some time.
Yet, none of the primate studies reviewed above included a dimension for PANIC/Sadness separation distress (Panksepp, 1998a), perhaps because relevant developmentally important social-isolation challenges were not studied in zoo-reared primates, or because overt SADNESS-related behaviors are rare in zoo environments, as in the death of an infant or social companion. Yet, socially induced comforts of social contact, mediated in part by brain opioid inhibition of the PANIC/Sadness system (Panksepp, Herman, Vilberg, Bishop, & DeEskinazi, 1980; Panksepp, 1981a), supplies the social glue that provides the cohesion observed in the troops of intensely social animals such as chimpanzees and brown capuchin monkeys. Without social bonding, which to a great extent is derived from brain opioid and oxytocinergic inhibition of the PANIC/Sadness system (Panksepp, Normansell, Herman, Bishop, & Crepeau, 1988) and the consequent alleviation of separation distress experiences, we would not likely observe these primate species living in social troops.
Again, it is our view is that primate temperament research (indeed, nonhuman personality research in general) could benefit from a framework for carving this psychological domain into neuroscientifically based basic emotion dimensions. Accordingly, we suggest that a cross-species affective neuroscience provides a new framework for understanding some of the major sources of personality structures across all mammalian species, and thereby may provide a more scientifically meaningful foundation for future progress than the statistical factor-analytic method that has so far been used to classify personality traits.
SUOMI AND MACAQUES’ EARLY EXPERIENCE
Before leaving the primates, we describe how Stephen Suomi’s research on early experience in rhesus macaques illustrates complexities that arise from variations in mothering—namely, expressions of the CARE system—can have on primate personality. Like Scott’s (1962) emphasis on critical periods of development, Suomi studied the behavior of neonates and juveniles, believing that relatively brief early experiences disproportionately influence behavior and temperament throughout the life-span, and showed that early social deprivation could increase emotional reactivity and impulsiveness. Expanding on Harlow’s work with total social deprivation (Harlow, Dodsworth, & Harlow, 1965), Suomi (2006) proceeded to explore a less severe social deprivation model in which rhesus infants were hand-reared for one month and then housed with same-age peers until six months of age. These laboratory hand/peer-reared rhesus monkeys exhibited stable social-emotional deficits, such as low social dominance, little exploration, fewer play bouts, less complex play, and greater adrenocortical and noradrenergic reactions to social separation. In general, these hand/peer-reared monkeys mirrored a “high-reactive” temperament type comprising about 20 percent of rhesus monkeys reared by their mothers in naturalistic settings and also shared characteristics with an “impulsive” type accounting for 5–10 percent of mother-reared rhesus monkeys, with more aggressive social encounters, low social dominance, and low serotonergic functioning (Suomi, 1997).
Research on polymorphisms of the serotonin transporter (5-HTT) gene revealed that hand/peer-reared rhesus monkeys carrying a single “short” allele of the 5-HTT gene were more emotional and distractible, with low attention and visual orientation (Champoux et al., 2002), and showed reduced serotonergic functioning and high levels of aggression (Suomi, 2006). These hand/peer-reared monkeys with a short serotonin transporter allele were also shown to become more aggressive juveniles than mother-reared monkeys with the short allele (Barr et al., 2003). Indeed, rhesus monkeys carrying either one or two short alleles that were mother-reared exhibited normal levels of aggression and serotonin metabolism, similar to rhesus monkeys carrying the long 5-HTT allele (Higley et al.,2000). Thus, typical highly supportive maternal rearing along with normal interactions with peers was able to protect individual monkeys from the effects of the psychopathology-promoting short allele that, like in humans, has more influence on personality when expressed in the context of stressful childhood upbringing (Caspi et al., 2003).
In another example of the influence of mothering on temperament, rhesus infants bred to be either highly emotionally reactive or normally reactive were cross-fostered to well-experienced mothers selected because they were either highly nurturing or normally nurturing. The high-reactive infants reared by the highly nurturing mothers exhibited more exploration and less psychological disturbance during weaning than all other combinations. When moved into larger social groups, these high-reactive monkeys reared by the very nurturant mothers also attained top positions in the dominance hierarchy, with high-reactive monkeys fostered to normally nurturing mothers moving to the bottom of the hierarchy. Furthermore, highly reactive females reared by the highly nurturing mothers exhibited the maternal style of the foster mothers (Suomi, 1997). Such nature-nurture complexities demonstrate the dynamic character of the BrainMind that seemingly defies simple explanations. It will be interesting to learn the extent to which these maternal-gene interactions influencing temperaments of these rhesus monkeys are related to socially induced epigenetic (i.e., gene expression intensity) changes as found by Michael Meaney’s ( 2010) work with rats—more on that subject in Chapter 15.
PRIMATE SUMMARY WITH A HUMAN PERSPECTIVE
One of the themes running through the personality/temperament literature is the predominance of factor analysis as the tool of choice for identifying basic personality traits. Beginning with Raymond Cattell (1943) and the eventual emergence of the Big Five human temperament factors, personality theory has become captivated by statistically derived “latent” factors, and animal temperament research has fallen in step. Our colleague and mentor John Paul Scott often repeated that statistics in psychology were just tools for determining the intensities and patterns of experimental/behavioral effects, as opposed to a way of identifying the biological sources of those effects. Perhaps we need to think of factor analysis as just a tool that, may have been more valuable during the “black box” era of psychology and is now superseded by the current explosion of neuroscience approaches that allow us to peer inside the brain and directly manipulate brain functions, such as basic emotional networks, which we have advocated to be major contributors to human and animal temperamental variability.
Early in the twentieth century, Walter Hess was a pioneer in providing temperament research with improved tools to directly observe the naturally evolved “factors” within the brain (for complete summary, see Hess 1957). Notably, if one can stimulate the subcortical brain in a particular anatomical location with a tiny and relatively crude input, and consistently observe the same coherent output, and repeat the process across ma
ny animals, and attain the same results, one can be confident that the input has activated an organized brain system worth investigating. By pursuing such research during the modern era, Jaak Panksepp (1971, 1998a, 2005) continued such lines of research and documented seven subcortical primary-process (innate) emotion systems in the brain: that he labeled SEEKING, RAGE/Anger, FEAR, LUST, CARE, separation-induced PANIC/Sadness, and PLAY, of which six (excluding LUST) are here advanced as most relevant for personality/temperament research. Using tools that Hess pioneered, each of these brain emotional states evoked with subcortical electrical stimulation are considered primal foundations for our core emotional feelings—instinctual emotional-feeling systems that are critical tools for living and perhaps the formation of personality traits.
But how can we know nonspeaking animals have any feelings at all? This Pandora’s box—the mystery of valenced experiences—was opened up in the middle of the twentieth century by two groups of investigators (Olds & Milner, 1954; Delgado, Roberts & Miller, 1954) using deep brain stimulation (DBS) to simply inquire whether one can obtain rewarding or punishing effects from such brain arousals. Jim Olds found powerfully rewarding sites in many regions below the neocortex (animals would voluntarily turn on the DBS), but not in the top of the brain that controls our sensory perceptions and thoughts. Delgado and colleagues found other sites that were punishing—animals would turn off the DBS applied to other nearby brain regions. Such effects have been found in all mammals, indeed, all vertebrates that have been studied (Wauquier & Rolls, 1976).
The working hypothesis is that such DBS studies empirically define brain systems that feel “good” and “bad” in various ways—they help define how various positively or negatively valenced states of mind arise from subcortical brain activities. Now more recent neuroscience tools are also available for further investigations, including optogenetics (light stimulation of the brain) and DREADD (designer receptors exclusively activated by designer drugs).
Thus, there is currently strong anatomical, pharmacological, and physiological evidence for these seven defined emotion systems in all mammalian brains. Several of these emotions have evolutionarily older roots (SEEKING, RAGE/Anger, and FEAR), which are evident in all vertebrates. But three (CARING, PANIC/Sadness, and PLAY) seem to be much more developed in mammalian brains. Each of these emotional systems can be aroused with DBS, and although they can operate independently, they surely interact with each ther in yet undetermined ways, as well as with a variety of higher BrainMind functions (secondary-level learning and tertiary-level thought processes) to increase the overall adaptiveness (survival ability) by interacting with diverse higher BrainMind processes (for fuller descriptions, see Panksepp, 1998a, 2005, 2010b, 2011a; Panksepp & Biven, 2012).
Much of the rest of this book is devoted to relating these ancestral emotional powers of the BrainMind to the fundamental personality infrastructures of human brains. However, we will first summarize work on the personality variability in dogs and rats—with less and less known as we progress down the phylogenetic “ladder.” (Ladder is a misnomer—no such ladder exists, just the genetic diversification of species, because it is difficult to identify a common vertebrate ancestor that survived the last mass extinction event, namely, the last of the big die-offs of the last 500 million years—the most relevant one for mammals being the Cretaceous-Paleogene extinction event, which occurred approximately 66 million years ago.) Nevertheless, the animal and human personality complexities will undoubtedly remain poorly understood until we are able to align the major constitutional temperamental factors studied by monitoring the linguistic-questioning/answering functions of human brains with the natural (evolved) emotional/affective functions of vertebrate (especially mammalian) brains.
CHAPTER 8
The Special Case of Our Canine Companions
Besides love and sympathy, animals exhibit other qualities connected with the social instincts, which in us would be called moral; and I agree with [Louis] Agassiz . . . that dogs possess something very like a conscience.
Dogs possess some power of self-command, and this does not appear to be wholly the result of fear.
—Charles Darwin, The Descent of Man
THIS CHAPTER SHIFTS from our closest evolutionary relative to man’s best friend, animals that have been our companions for at least 18,000 years, predating the emergence of agriculture (Thalmann et al., 2013). It is possible that our symbiotic relationship with wolves was the gateway to ultimate domestication, which led to further selection of prosocial traits (Coppinger & Coppinger, 2001; Feuerbacher & Wynne, 2012). From a Darwinian continuity perspective, a key question is how the basic temperaments of dogs may be close to traits we value in humans, while perhaps being less complex than those of chimpanzees.
Methodologies in dog personality research involve more laboratory-type measurements of dogs’ responses to standard challenges, in contrast to what must necessarily be more naturalistic observational research with chimpanzees. Might using these behavioral test batteries, as opposed the observer rating approach, lead to different conclusions? The extent to which temperament findings in dogs and chimpanzees remain similar, despite shifting from more flexible observer rating studies to more laboratory-type challenges, will strengthen the evolutionary case for similar, even homologous (evolutionarily related) emotional foundations of mammalian personalities. We spend a bit more time on dogs than on monkeys and rats because dogs figure so heavily in issues of human-animal companionship. Dogs are, after all, “man’s best friend,” although they may not see it quite that way. Thus, we divide this chapter into two parts: first we describe Scott and Fuller’s behavior genetic studies and related work that followed, and then we discuss work on quantifying socialization, including examples of puppy testing and a long-term project domesticating another canine, the fox.
With dogs, the personality discussion may move into more familiar territory for most readers, because most folks have lived with a dog or even several dogs at some point in their lives. Certainly, those who have had canine companions would agree that dogs have personalities that reflect stable behavioral and emotional characteristics that differentiate their dogs from other dogs. Of course, due to selective breeding started many centuries ago, we now have an enormous variety of dogs available for comparisons. Indeed, the American Kennel Club registers 175 different breeds, with many manifesting distinct behavioral-temperament differences. While we recognize that there are many passionate cat lovers as well, there has been much less research on cat personalities than on dogs (Gartner & Weiss, 2013). Hence, here we have selected domestic dogs, as a unique mammalian species that probably exhibits diverse genetically based personality traits both across and within subspecies, many of them arising from selective breeding for certain behavioral/psychological characteristics across the last few centuries. More important, our long historical relationship with dogs was based on the fact that we developed a symbiotic relationship long before the agricultural revolution, going back to a time when humans were still hunter-gatherers, starting perhaps some 40,000 years ago, during the peak of the last glacial period, with gradually increasing breeding of canine companions for specific utilitarian traits. As noted by Leslie Irvine (2004), “Selective cross-breeding has been done since antiquity, but it really accelerated during the 19th century.” Still, it was another century before humans became interested in the scientific analysis of canine personalities, which had been pragmatically crafted to serve human needs across the past few centuries (Serpell, 1995).
ASSESSING CANINE BEHAVIOR AND PERSONALITY
Scott and Fuller: Social Behavior of the Dog
The classic work of John Paul Scott and John L. Fuller (1965), at the Jackson Memorial Laboratory in Bar Harbor, Maine, set a high quality standard for any future temperament research in dogs. J. P.Scott was recruited in 1946 to initiate a large-scale project in dog behavior genetics at the Jackson Lab. In collaboration with Fuller, Scott set out to fill a void in our understanding of the inf
luence of heredity upon behavior, a subject that was not popular in the zeitgeist following World War II, with the residue of German genetic fantasies, such as Übermensch, fresh in people’s minds. Overall, Scott and Fuller’s work still highlights both the difficulties and promises of large-scale temperament studies in complex domestic animals, a body of work that remains to be equaled.
The Emotional Foundations of Personality Page 15