The Emotional Foundations of Personality

by Kenneth L Davis

  Stated differently, a key dilemma in temperament research may be that more complete understandings at the primary-process genetic-neuroscience level are needed to provide solid foundation for all levels of personality development. Such knowledge is essential for understanding the development of higher cognitive capacities. Thus, further work on even lowly domesticated laboratory rats and mice will help provide insights and clearer empirical windows into mammalian minds, as we will discuss from genetic perspectives in the next chapter.

  CHAPTER 9

  Do Rats Have Personalities?

  Of Course They Do!

  Our children from their earliest years must take part in all the more lawful forms of play, for if they are not surrounded with such an atmosphere they can never grow up to be well conducted and virtuous citizens.

  —Plato, The Republic

  LET US START THIS DISCUSSION of personality of our “fellow travelers” with a seemingly outrageous claim: We have learned more about the fundamental neural nature of human emotions (e.g., the subcortical neural circuits and neurochemistries) by studying the brains of laboratory rats than those of human beings. Indeed, the study of their brain emotional systems has proved to be a very effective strategy for the development of new and highly effective antidepressants, one of them from the study of the happy sounds (50 kHz chirps) they make when they play (Burgdorf, Panksepp, & Moskal, 2011; Panksepp, 2015, 2016). And when we breed males and females that show abundant “rat laughter,” we have developed lines of animals that can more easily sustain positive moods and are resistant to depression. On the other hand, when we breed rats that are sourpusses (i.e., laugh very little when they are tickled), they more readily succumb to depression when stressed (Burgdorf et al., 2011; Burgdorf, Colechio, Stanton, & Panksepp, 2017; Burgdorf & Panksepp, 2006; Panksepp, Burgdorf, & Gordon, 2001).

  To raise a controversial point (on which our group has more data than anyone else), we may be learning more about the subcortical fundamentals of our own laughter/joy circuits (and the neural constitution of positive affect) by studying rat brains than those of human beings—we seem to share the same fundamental subcortical circuits for such feelings (Roccaro-Waldmeyer, Babalian, Müller, & Celio, 2016). Of course, all this does not mean rats tell jokes to each other, but they surely have abundant playful fun.

  Indeed, most young laboratory rats are as playful as human children, and indeed, we have learned more about the play circuitry of mammalian brains (but not their jokes) by studying rat brains than human ones. And it looks like our human laughter circuitry arises from the same ancient subcortical brain systems as rats (Burgdorf et al., 2007; Panksepp, 2000b, 2007c). Of course, for most who have not done such studies, these claims may seem outrageous.

  BACKGROUND REFLECTIONS ON LABORATORY RATS (DOMESTICATED RATTUS NORVEGICUS)

  Rats are mammals, but could these little beady-eyed rodents have complex interesting personalities like dogs, chimpanzees, and humans, or is that a fishy proposition (which we will touch on in the next chapter)? That surely depends, in part, on what kind of rats we are talking about. The laboratory rat, which is used extensively in medical and behavioral research, is a highly domesticated animal that has been bred for generations to accept human handling and companionship. While precise numbers are not available, the Federal Research Division of the Library of Congress found as many as 1 million rats were used for research in 2000. Data from the United Kingdom suggested that 414,335 rats were used in 2005 just in that country. These lab animals are purposely bred to be docile and in the laboratory are typically housed individually in separate cages, which has certainly altered their temperaments, perhaps making them almost immune to separation distress (for discussion, see Panksepp, 2003). The lab rat’s wild relative, Rattus norvegicus, the common brown rat, has a major public relations problem but has so far evaded all of the human race’s attempts to exterminate it. This wild relative undoubtedly has more variability in its temperament, but you may be surprised at how much personality even lowly lab rats can display when given the chance.

  One of the main advantages of laboratory rats (and mice) is their combination of docility, fecundity, rapid maturation, and all the organs and all the brain systems that humans have (but in miniature, of course). Because many writers, including Darwin, have noted that being able to selectively breed for a behavior characteristic is strong evidence of its genetic basis, rodents’ capacity for rapid multiplication has often made them subjects of a great diversity of selective breeding efforts. Much of what is known about rat personality comes from breeding for extreme emotional traits, and several such focused projects working with single emotions are reviewed in this chapter, in contrast to the types of projects seen with primates and dogs that attempt to assess a broad array of the animals’ personalities.

  The abundance of behavioral emotional research in laboratory rats (and mice) has yielded clear evidence for the heritability of more affective temperamental traits in warm-blooded mammals than have ever been demonstrated in cold-blooded vertebrates such as fish (see Chapter 10). The inheritance of the evolutionarily older RAGE/Anger and FEAR brain systems has been demonstrated multiple times in so-called gene knockout strains of mice (which have specific genes selectively inactivated) where elevations of both of these traits are evident (Crawley, 2007). Here, we focus on research using lab rats, which has confirmed the evolutionarily more ancient biologically endowed emotions of SEEKING, RAGE/Anger, and FEAR, as well as the socially oriented emotional systems of LUST, CARE/Maternal nurturing, and PLAYfulness, but perhaps less so for PANIC/Sadness (separation distress, which may have been selected against during domestication, because it was desirable for behavioral research to have animals living alone, one to a small cage; Panksepp, 2003). Most of these emotional systems are easily studied in laboratory rodents, and accordingly, we would argue they have been evolutionarily layered onto rodent personalities, which may serve as neuroscientific models for the study of the fundamentals of most primary emotional feelings. Such work may enable in-depth studies of the neural foundations of mammalian temperaments, which we believe further support a biological foundation for the primary affective traits that account for a great deal of human personality differences.

  SELECTIVE BREEDING AND THE FEAR SYSTEM

  Selective breeding is nothing new in the biopsychological world. There were several early research programs of behavioral selection for temperamental fear in rodents. Calvin Hall, who spent most of his career at Western Reserve University, devised what he called a strange (i.e., novel), open-field situation, which provoked rat emotionality or excitability, or what we would label fear (Hall, 1934a). He used his new open-field test to select for and breed high and low fear strains of rats (Hall, 1941). Interestingly, Hall received his Ph.D. at the University of California, Berkeley working with Edward Tolman and Robert Tryon. At that time, Tryon was in the process of selectively breeding his maze “bright” and “dull” strains of rats to demonstrate the influence of genetics on learning processes in an era dominated by behaviorist learning theory, which emphasized that environmental rather than genetic differences controlled individual behavior differences. (Of course genetics was in its “fetal,” preinfancy in those days.) Thus, it is not surprising that Hall used his open-field device so successfully to selectively breed high and low fear strains.

  He placed rats in a brightly lit, eight-foot-diameter, round box that rats found stressful, because it was a strange, bright place with nowhere for a normally nocturnal prey animal to hide. He mated the male and female rats that showed the most emotional defecation and urination in the open-field test, to create a high fear line of rats, and the male and female rats showing the lowest stress-induced eliminative behaviors, yielding a low fear line (Hall, 1934b). Following this procedure for each subsequent generation, Hall found gradually increasing fear differences between the two strains during eight generations of selective breeding.

  A more recent program used the elevated plus-maze to selective
ly breed rats for high anxiety-related behavior (HAB) and low anxiety behavior (LAB; Liebsch, Montkowski, Holsboer, & Landgraf, 1998). The elevated plus-maze was designed to elicit a rat’s innate fears of open and elevated spaces. It is usually elevated about two feet from the floor and has two four-inch wide crossing arms constructed in the shape of a plus sign. One of the arms is completely open with no sides. The other arm has walls on all sides except in the center where the two arms cross, that is, a center area allowing entry into the walled or open parts of the maze. The enclosed arm is usually dark and the open arm brightly lit, which also addresses the nocturnal rat’s natural preference for dark places. Typically, all rats explore the parts of the maze with walls with the more fearful animals avoiding the open arm with no walls.

  In the Liebsch et al. (1998) breeding program, rats with less activity in the open arms (fewer entries and less time spent in the fear-provoking arms) were selected and bred to create the HAB line, and those with more activity in the open arms became the parents in the LAB line. Other tests showed that HAB animals spent less time in the center of an open field, thus validating that the HAB line experienced more fear than LAB animals in an open-field test. HAB animals also struggled less when first exposed to a forced swim test, which further suggested a possible depressive tendency in the HAB line (Liebsch et al., 1998).

  Cross-fostering on these lines failed to reveal any maternal developmental influences (Wigger, Loerscher, Weissenbacher, Holsboer, & Landgraf, 2001), and crossbred F1 and F2 hybrids were intermediate to the pure HAB and LAB lines on all plus-maze fear measures, both findings consistent with genetic inheritance. We would note that human families sometimes naturally produce such crossbreeding results. That is, sometimes a person with a high fear phenotype marries a person with a low fear phenotype, and on average the couple produces children with intermediate fear sensitivities, although with the complex FEAR system, some children may track closer to the high or low fear sensitivity parent.

  Interestingly, at ten days of age HAB rat pups also emitted more 40-kHz vocalizations than did LAB pups (Wigger et al., 2001). It would be relevant to determine whether these HAB rats also emitted more adult 22-kHz alarm calls, which would clearly indicate more negative affect as adults (more on rat vocalization later). Further confirming evidence included higher levels of stress indicators such as ACTH, corticosterone, and prolactin in HAB versus LAB male rats, especially when exposed to the plus-maze with no access to the enclosed arm.

  Treatment for seven weeks with the SSRI antidepressant drug paroxetine (Paxil) also brought the active struggle time of the HAB rats in the forced swim test up to the level of the LAB rats (Landgraf & Wigger, 2002), which again suggested a possible depressive component in the HAB line. However, more specifically targeting fear levels, injections of the anti-anxiety drug diazepam (marketed as Valium), a highly effective antianxiety medication in the benzodiazepine group, increased the percentage of time spent in the plus-maze open arms twenty-fold in HAB rats (with a less dramatic increase of 2.5-fold in LAB animals) and increased the speed to enter the open arm sevenfold in HAB rats (only twofold in LAB line). While fear in the HAB line was dramatically relieved by diazepam, even after many generations of selection the LAB line apparently also retained the capacity to experience fear, because they also responded less fearfully after the diazepam treatment. The fact that even the LAB line continued to experience fear suggests that a potent deeply engrained FEAR system exists in the brain. Indeed, Panksepp (1971) and others have demonstrated that a powerful flight response can be evoked by stimulating specific regions in the hypothalamus, and animals given a chance will turn off the brain stimulation that activates such FEAR responses. That after the diazepam the LAB rats still experienced FEAR/Anxiety suggests that the FEAR system is likely to remain an adaptive tool for living in all mammals, regardless of their personality profiles, because it has been so essential for survival. Although highly elevated levels of fear may become maladaptive in domestic environments, presumably such systems can become overactive or sensitized not only by genetic background but also by life experiences, leading, for example, to humans developing chronic anxiety/fear disorders that may need psychiatric treatments (e.g., with benzodiazepines).

  CONSPECIFIC FIGHTING AND THE RAGE/ANGER SYSTEM

  Even though rats have been domesticated for lab use for many generations, these animals retain a functional RAGE/Anger system and a corresponding capacity to become aggressive. However, in discussing anger, one must be careful to define the targeted behavior. While there are no selection studies based on fighting in highly domesticated lab rats, Panksepp (1971), using precise electrical stimulation of the brain, showed that like cats (Flynn, 1976; Hess, 1957b; Siegel, 2004) rats possess two separate brain systems capable of provoking an attack. One of these systems, for predatory attack, is characterized by a “quiet” systematic pursuit of mice, followed by a focused nape attack bite typically associated with predation, a behavioral trait rats commonly exhibit toward mice (Albert & Walsh, 1984). The other attack system is associated with defending resources and escaping physical restraint, such as might be experienced when caught by a predator. This latter type of “affective” attack behavior has been labeled the RAGE/Anger system (Panksepp, 1998a) and probably has evolutionary origins in the earliest vertebrates. In contrast, the predatory behavior is not generated by the RAGE/Anger system but is part of the general-process SEEKING system, which is essential for the search for food and all other resources needed for survival. Hence, what many think of as “bloodthirsty” hunting of prey is basically just finding a meal and has little to do with interpersonal violence.

  Anger is an important temperament dimension, which has received more attention in animal temperament studies than in humans, especially because the Big Five personality model has relegated anger to either a “blend” or “facet” of Emotional Stability or the opposite of Agreeableness in a kind of “love-hate” dimension, rather than a separate primary personality dimension. This may also partly reflect the fact that most humans have been trained to regulate negative anger tendencies so that they rarely manifest as clearly as in animal models. However, just like the domesticated rats (which typically show little anger), humans certainly retain a powerful capacity for anger, which is all too frequently expressed in cases of domestic violence on the “full-blown” end of the anger dimension and with irritation and impatience on the more “toned-down” end.

  One contribution of animal temperament research could be to help gain a better understanding of the basic brain processes underlying this primary-process emotional-temperament dimension as manifested in human personalities, which could also lead to enhanced recognition of the often hidden role of anger and milder forms of irritability in human conflict. The animal work can help pinpoint the underlying neurochemical factors that promote anger, which can lead to medicines to control this potentially dangerous aspect of human personalities. For example, as derived from animal work, antagonists of the brain neuropeptide synaptic transmitter (Substance P) that mediates animal RAGE may be helpful in regulating excessive anger/violence in human beings.

  MATERNAL NURTURANCE AND THE CARE SYSTEM

  A very distinctive dimension of mammalian temperament is caring for young. Michael Meaney’s group has studied maternal behavior in rats and found substantial individual differences in how rat mothers treated their newborns during their first week of life (Champagne, Francis, Mar, & Meaney, 2003). These maternal caregiving differences included the frequency and skill exhibited when licking, grooming, and nursing their neonatal pups. Remarkably, these researchers also found that individual differences in rat maternal care affected fear responses of their offspring as measured by open-field tests, amount eaten in a novel cage, and behavioral changes following a physical restraint tests. Specifically, offspring reared by mothers exhibiting less neonatal licking, grooming, and “arched-back nursing” (LG-ABN) showed increased hypothalamic-pituitary-adrenal responses to these stressors compared
to offspring receiving more LG-ABN (Liu et al., 1997; Caldji et al., 1998). Cross-fostering experiments in which the rat pups of less attentive rat mothers were raised by more attentive rat mothers (Francis, Diorio, Liu, & Meaney, 1999) showed that high levels of LG-ABN decreased stress reactivity in the cross-fostered offspring, confirming that this stress resistance was indeed imparted by the effective mothering the rat pups had received. Furthermore, these maternal effects were passed from one generation of females to the next. That is, females born to less effective mothers but raised by more nurturant mothers became more effective mothers themselves. These researchers also showed that humans handling the pups of low LG-ABN mothers—more or less simulating the increased maternal stimulation—produced females whose later maternal behavior as adults was not different from those raised by high LG-ABN mothers and who exhibited increased LG-ABN toward their own neonatal pups.

  In this landmark article, Meaney’s research group concluded they had demonstrated nongenomic transmission of significant individual differences of rat maternal behavior and stress reactivity (Francis et al., 1999). In other words, somehow this nurturing-evoked stress resistance was being passed on to the next generation. Subsequent research (Weaver et al., 2004) demonstrated that these epigenetic effects (more on this in Chapter 15) were the result of reduced DNA methylation in the offspring of high LG-ABN mothers. Reduced DNA methylation meant that the DNA itself was not changed, but its configuration was changed in a way that altered gene expression. Furthermore, cross-fostering could reverse the inherited genetic effect and produce a methylation pattern associated with the rearing mother (Weaver et al., 2004).