The Emotional Foundations of Personality
Page 21
CHAPTER 10
Animal Personality Summary
The distinction between emotional attitudes and habits is based on the observed fact that human beings do not always give in to their emotions, even when these have developed into an emotional attitude. . . . Animals on the other hand, do not exhibit any goal-directed actions that are not dictated by emotion or instinct.
—Magda B. Arnold, Emotion and Personality
In the process of natural selection, then, any device that can insert a higher proportion of certain genes into subsequent generations will come to characterize the species.
—Edward O. Wilson, The Morality of the Gene
INTRODUCTION
The first of William McDougall’s two personality principles was to ask whether similar primary instincts and emotions could be observed in humans as well as animals. By “animals,” what McDougall meant were the “higher animals,” namely, mammals. However, if Darwin’s continuity principle is correct, that the characteristics of humans and animals differ by degree and not by kind, then one should be able to trace human emotions and thereby personality characteristics back further than the evolutionary appearance of mammals. One should be able to identify relevant emotions or at least their ancestral glimmerings in our more distant evolutionary relatives as well. So, let us reflect backward in evolutionary time to put our human personalities in perspective, much like medical science, including psychiatry, studies nonhumans as a foundation for understanding human diseases.
At what point in the evolution of the animal kingdom do personality features begin to emerge? How far back in evolutionary time can we identify commonalities with human personalities? Fish are among the earliest vertebrates, meaning they have a spinal cord, along with calcified spinal vertebrae, and a central nervous system. Is it possible, for example, that even fish have personalities, that is, relatively stable personality characteristics that differentiate one fish’s behavior from another’s? Do even lower animals—the invertebrates—have personalities, because they presumably have some rudimentary form of consciousness (Feinberg & Mallatt, 2016)?
Indeed, there are tantalizing hints of consciousness and personality variability even among invertebrates. The nematode Caenorhabditis elegans is a tiny, one-millimeter-long soil-dwelling roundworm whose intimidating biological name is longer than its diminutive body. C. elegans, as its name is usually abbreviated, is widely studied in part because of its simple nervous system that contains only 302 neurons. In a review focused on C. elegans, Mario de Bono and Andres Maricq (2005) pointed out that this primitive creature, evolutionarily separated from humans for perhaps a billion years (Wang, Kumar & Hedges, 1999), contained five neurotransmitters found in vertebrates, including serotonin and dopamine, with dopamine being involved in regulating “a well-described universal foraging strategy” (de Bono & Maricq, 2005, p. 462). Could this be the early suggestion of a SEEKING system motivating this simple creature to search for a meal? Certainly dopamine figures preeminently in the diverse foraging behaviors of all mammals. Even though the discussion of such brain processes is phrased in diverse terms (Panksepp & Moskal, 2008), our preferred moniker for the primary-process manifestation of diverse forms of foraging is the SEEKING system, a universal appetitive mode aroused and directed by brain dopamine, with some of the satisfactions of this universal urge mediated by brain opioids.
Crayfish, a more sophisticated invertebrate species separated from mammals by at least 600 million years, also share neurotransmitters with mammals. Research shows that serotonin can promote aggressive tendencies in crayfish (JB Panksepp & Huber, 2002). Further, both dopamine and morphine function as powerful, possibly addictive, positive reinforcers (JB Panksepp & Huber, 2004; Nathaniel, Panksepp, & Huber, 2009). Could a crayfish’s appetite for dopamine stimulants like amphetamine or cocaine be a clue that it experiences pleasant and unpleasant feelings? Does a developing fondness for morphine mean it subjectively experiences pleasures that guide preferences?
The existence of these classic brain neurotransmitters in animals genetically separated from humans for many hundreds of millions of years emphasizes the evolutionary similarities we still share with the nervous systems of these ancient creatures, suggesting deep ancestral relationships (Feinberg & Mallatt, 2016). However, the cross-species personality case becomes much more compelling when we start comparing the brains of vertebrates that have nervous systems more similar to our own. Paul MacLean, at the National Institute of Mental Health for nearly thirty years and chief of the Laboratory of Brain Evolution and Behavior, theorized the vertebrate brain had evolved in epochs, with each successive stage basically “layered” (but, of course, still massively interdigitating) with the previous one, yielding a variety of ancestral structures that still exist in the human brain. He called the oldest of these stages the “reptilian brain.” Then, integrated with (but being built “on top of”) the reptilian brain was the “paleomammalian brain,” with features that appeared much later during mammalian evolution and associated with a new social model of living in family groups that distinguished them from reptiles. The most recent evolutionary development in the brain was the “neomammalian cortex” (or simply neocortex) that expanded mammals’ capacity for much more complex learning, memory, and hence more complex decision making and better general adaptation (MacLean, 1990). The neocortex is most extensively developed in humans, although whales and dolphins also have highly developed but structurally somewhat different neocortices (i.e., their neurons are not as distinctly organized into six “layers”).
MacLean argued that the brain structures primarily associated with human emotions were found in the two older, reptilian and paleomammalian brain layers. Although a simplification, if personality is linked to emotions, we can anticipate that reptiles and possibly even their vertebrate ancestors such as fish would also exhibit some recognizable personality characteristics similar to those found in mammals including humans.
So, if fish have personalities, what would we theorize their personality traits to be? Which emotions would we expect to find in these evolutionarily older vertebrates? What are the most primitive emotions, and what evidence would indicate which are the oldest emotions evolutionarily?
Actually, the brain itself can provide answers to these questions. As MacLean realized (and even Darwin recognized), the brain—unlike any other organ in the body—has evolved, with more and more modern specializations on top. Like an archeological site (note the title of the second author’s previous book – The Archaeology of Mind), the further down one digs, the older the neuropsychological materials (i.e., brain functions) one uncovers. We must look toward the more ancient brain regions to find the evolutionarily constructed systems that are critical for the creation of emotions—it is not only reasonable to assume, but the evidence is rather overwhelming, that primal emotionality was created in very deep sub-neocortical brain regions. Indeed, those are the only brain regions where we can evoke a diversity of coherent emotional arousals simply by electrically stimulating specific brain regions (Panksepp, 1982, 1998a). Thus, we here consider the evidence-based fact that emotional arousals (and the affective foundations of personality) are mediated by the archaeologically deeper, more ancient regions of the brain. To the extent that personality is a reflection of one’s emotional strengths and weaknesses, we should be very open to the idea that even fish exhibit temperamental differences in their styles of living and behaving. They too have emotional lives: such brain systems are survival systems—positive ones indicate survival and negative ones potential destruction trajectories—and fish need them as much as we do.
Based on such evolutionary reasoning, the SEEKING emotion is likely to be the oldest of the six primary emotions we focus on to understand personality variability in fish—especially psychobehavioral features such as eagerness and enthusiasm to pursue resources needed for survival, a solid foundation for the other emotions. Equally old should be the RAGE/Anger and FEAR/Anxiety systems.
Is th
ere any credible experimental evidence that fish young exhibit any clear indices of separation-distress PANIC or PLAYfulness? Very little. These are the most recent and perhaps most complex of the basic social emotional-affective action systems. Because fish arose from very early vertebrates that predate reptiles, one might think that fish would not have evolved mammalian-type CARE, PANIC, or PLAY systems and that their temperaments would be characterized by a simpler set of personality traits featuring especially SEEKING, RAGE/Anger, and FEAR/Anxiety, but we must leave open the idea that some aspects of CARE were shuffled into their genetic “cards,” with fathers often having a bigger role than mothers. After a brief review of key fish personality research, we conclude our summary of animal personality dimensions.
FISH PERSONALITY
The stage for a scientific discussion of fish temperament was set by Felicity Ann Huntingford, a psychologist at Oxford University who conducted a classic series of fish studies that tracked multiple fish behaviors across multiple settings and indeed identified three temperament dimensions (Huntingford, 1976) that we think--as already noted--can be related to the SEEKING, RAGE/Anger, and FEAR/Anxiety brain systems (Panksepp, 1998a) as brain evolution principles would have predicted.
The fish species she studied was the three-spined stickleback, Gasterosteus aculeatus, a commonly studied small freshwater fish that is native to some inland waters of Europe. Huntingford thought this species was a good candidate for studying temperament or personality because she had noticed that different individual sticklebacks naturally exhibited marked differences in behavior. Her strategy was to observe the fish in different experimental situations that might highlight their personality strengths and weaknesses. She basically gave each stickleback a behavioral personality test designed for fish (not unlike Scott and Fuller’s approach with dogs), which required careful attention to a variety of distinct behaviors.
Huntingford first tested male sticklebacks during various stages of their nest-building and breeding cycle and found some fish consistently exhibited more aggression (defined as lunges and bites) throughout the breeding cycle. Individual patterns of lunges and bites occurred regardless of whether the intruder was a member of their own stickleback species or an unrelated species. Likewise, there were individual differences in curiosity (defined as amount of time facing an intruder). Importantly, these aggressive and curious tendencies were independent of each other; that is, fish that exhibited more aggressive behavior were not necessarily the same ones that were more curious.
To further investigate these behaviors, Huntingford also gave two additional tests to male sticklebacks in their nonbreeding phase. The first test measured their behavior in the presence of a predator fish, a young pike that had been fed to satiation just before the experiment, which had the advantage of getting the stickleback’s reaction to one of its natural predators while minimizing the danger of being eaten. In this test, in addition to getting measures of apparently curious investigative behaviors, Huntingford was also able to statistically identify what she initially called “bold” behavior characterized by a lack of timidity.
The second test compared observations of sticklebacks in their home aquarium versus two different strange aquaria. One of the strange aquaria was bare of plants or other objects. Both strange aquaria were intended to function as “open field” tests, which have been used for years to measure fear in rodents. Indeed, both of the strange aquaria disturbed the fish, as indicated by less “jerky” (typical) swimming, more “still” moments (freezing), which were broken by “continuous” (faster escape) swimming, and more “spine raising” (defensive reaction).
When she statistically compared all of her tests across her subjects, she found that the fish that were least disturbed (least fearful) in the strange tanks were also the most aggressive breeding-nest defenders. Likewise, the fish that were the least timid in the predator-pike test were also the most aggressive in the reproductive tests. She concluded that the main dimension she had observed was “fearfulness,” which had inhibited aggressiveness against breeding nest invaders as well as “boldness” in the pike test. In her words, “This fearfulness might be suppressing the response to a predator and to a conspecific [other three-spined stickleback intruders] to a similar extent” (Huntingford, 1976, p. 256). However, she also noted that aggression and fear had varied independently in her experiments, as did curiosity and fear. In the end, she concluded that she was observing an element of fearful inhibition in each of her experiments, which had influenced the overall behavior of her fish.
Altogether, Huntingford reported three distinct behavioral dimensions that aligned with the three evolutionarily older affective emotions: the most prominent was fear, which corresponded with the FEAR/Anxiety system of mammalian affective neuroscience; aggression, which we would hypothesize corresponded to the well-documented RAGE/Anger system in several mammalian systems (especially cats and rats); and her curiosity factor lined up with the affective neuroscience SEEKING system. Importantly, as with all dynamic creatures, she observed these emotions interacting with each other, with fear reducing the levels of aggression (RAGE/Anger) and decreasing exploratory activity (SEEKING).
Using multiple fish personality tests and measuring a variety of behaviors, Huntingford used classical psychological multitrait-multimethod technique (Campbell & Fiske 1959) to identify three personality dimensions, thus being consistent with our prediction that fish personalities, compared to mammalian personalities, would be more restricted to (but not necessarily limited to) the most evolutionarily ancient primary-process emotional action systems: SEEKING, RAGE/Anger, and FEAR/Anxiety. She also confirmed one of McDougall’s observations, that fear was the great inhibitor of behavior. We await research evaluating whether the three emotional-personality dimensions of fish are controlled by some of the same neurochemistries of mammalian neural systems, including, we are willing to predict, those of primates.
REPLICATION AND TERMINOLOGY CONCERNS IN FISH PERSONALITY RESEARCH
To address testing and terminology concerns regarding fear and curiosity in fish temperament research, James Burns (2008) used guppies (Poecilia reticulata) and multiple measures of all tests to determine the reliability and validity of three common fish “personality” tests: an open field test (being placed in a large, unfamiliar aquarium), an emergence test (latency to leave a safe place), and a novel object test (latency to approach novel objects). Burns’s (2008) data supported the use of open-field freezing as a measure of fear but cast doubt on the emergence test as a measure of fear (which may better reflect SEEKING). Still, none of the novel object measures correlated with any open field measure, which suggested that the open-field test in fish should currently be reserved as a measure of fear in fish rather than a measure of exploratory/investigatory behaviors. In any event, Burns confirmed Huntingford’s findings, as well as our conclusion that the SEEKING and FEAR systems should be carefully separated in personality research. Burns also declared that “I take shyness-boldness to be the same as fearfulness” (Burns, 2008, pp. 344–45), a conclusion also reached by other researchers (Budaev, 1997; Warren & Callaghan, 1975, 1976). We especially appreciate the willingness of Huntingford to use affective descriptors, which was not scientifically fashionable in those days.
Aggressiveness was the second of Huntingford’s (1976) personality dimensions that corresponded to one of the affective neuroscience primary emotions studied in fish (but note that the necessary brain research remains to be done). However, in a real tour de force, Theo Bakker (1994) conducted a classic behavior genetic dissection of aggressiveness and the RAGE/Anger system in three-spined sticklebacks, Gasterosteus aculeatus, the same species studied by Huntingford. Being able to selectively breed for a trait is strong evidence for the existence of biological underpinnings. Bakker started with a natural, unselected population of freshwater sticklebacks and selectively bred multiple lines of males and females for high or low juvenile aggression, high or low territorial aggression, and high or
low social dominance. His test for juvenile and territorial aggression consisted of presenting each fish with an opponent in a glass tube placed in its tank and observing acts of biting and bumping at the opponent. Juvenile aggressive tests were conducted when the fish were in their young juvenile stage of development. Territorial aggressive tests were conducted when the fish were in their mature reproductive stage. Another key feature of his triple high/low selection process was testing each generation of each line with all three aggression tests to determine how the different forms of aggression were segregating genetically.
Bakker found that selection for reduced juvenile and territorial aggression yielded significant differences from control lines of fish in both males and females after only a single generation, with larger differences observed through the third generation. However, breeding lines selected for enhanced aggression failed to produce a significant divergence from the control lines except for adult females, which yielded high and low differences in territorial fighting only after the third generation. These results suggested that there was insufficient genetic variation in Bakker’s initial population to further enhance male aggressiveness, which would be consistent with the male stickleback’s very aggressive reputation. Alternatively, natural selection may have already maximized juvenile and territorial aggression traits (especially in males) before the beginning of experimental selection. In any event, dominance selection was based on dominance contests between two fish in neutral tanks and produced divergence by the third generation, in which high dominance males dominated low-dominance males in 19 out of 24 contests.
Comparing correlations of the different aggression tests across selection lines revealed that selecting for juvenile aggressiveness in one line and adult female aggressiveness in a second line produced very similar juvenile and female aggressiveness in both lines, suggesting that both forms of aggression were affected by the same genes. However, correlations between juvenile and territorial aggression in male selection lines were not as strong, “suggesting that in males juvenile aggressiveness is only partly governed by the same genetic factors as territorial aggressiveness” (Bakker, 1994, p. 155). In short, selecting for reduced levels of juvenile aggressiveness did not potently influence male territorial aggression. Thus, juvenile aggressiveness may actually be an ancestral very early form of play fighting (as in many mammals) or perhaps a rather “pure” representation of the RAGE/Anger system also reflected in territorial behavior in mature males during breeding season, but including additional factors perhaps related to overall reproductive fitness.