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 there 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.
Importantly, social dominance selection did not enhance or reduce the other forms of aggressiveness. Indeed, the degree of male red coloration accounted for most of the variation in dominance ability. This suggested that at least in the three-spined stickleback, adult intermale dominance is not closely related to either juvenile aggressiveness or adult territorial aggressiveness.
To summarize, while Bakker (1994) did not elucidate the underlying neurobiological mechanisms of aggressiveness in fish, he provided strong evidence that both juvenile aggressiveness and territorial aggressiveness were strongly influenced by genetic selection, with territorial aggressiveness perhaps being more closely linked to the RAGE/Anger system than juvenile aggression or dominance. While we are not aware of selection studies targeting fish SEEKING or FEAR systems, we would predict that such studies would confirm genetic foundations in fish for those temperament aspects of emotions as well, as has previously been well demonstrated in rodents.
ARE FISH SOCIAL ANIMALS?
Are fish personalities really just defined by SEEKING, RAGE, and FEAR sensitivities, or do fish exhibit social behavior that represents other possible personality dimensions, such as PLAY, as already noted, which may utilize many of the other emotional systems in a nonserious way? Most of the 24,000 species of teleost fish (the vast majority of bony fishes) swim together at times in groups commonly called schools, which biologists refer to as shoals, when the swimming becomes more synchronized (Faucher, Parmentier, Becco, Vandewalle, & Vandewalle, 2010). A key question is whether fish swim in groups because of the same social motivations as mammals—social bonding and separation distress associated with the PANIC/Sadness system—or for some other reason. Some biologists do refer to fish living in social groups (Colleter & Brown, 2011). However, the more common explanation is that shoaling reduces risks of predation, so perhaps reduction of FEAR is the likely emotion underlying shoaling behavior. This hypothesis seems especially reasonable, because shoaling is especially common in prey fish (Budaev, 1997; Ward, Thomas, Hart, & Krause, 2004).
A recent series of studies have argued that western mosquitofish, Gambusia affinis, are social, which may allow their shoaling tendencies to be used as a measure of sociability (Cote, Fogarty, & Sih, 2012). However, these authors measured sociability by placing an individual fish in the middle compartment of a tank with three compartments created by inserting two transparent glass partitions on the opposite ends of a large aquarium. One of the end compartments contained fourteen randomly selected mosquitofish. The compartment at the other end was empty. The authors defined sociability as the amount of time the individual fish spent near the compartment containing the other fish. However, in line with Burns (2008), we would argue this was more of an open field test generating FEAR rather than the separation distress of the PANIC/Sadness emotion, but more definitive conclusions may require the use of medications that are more selective for inhibiting these two systems, namely: benzodiazepines for the FEAR system (Panksepp, 1971), and low doses of opiates for the separation-distress PANIC system (Panksepp et al., 1978).
The Cote group reported that the individual experimental fish showed signs of stress when first introduced to the novel aquarium, as indicated by constant swimming along the sides of the tank, which may be an open-field fear response corresponding to Huntingford’s continuous-swimming fear measure. However, Cote et al. (2012) did not measure this behavior and also did not include any test intended to measure fear in their fish social personality test. So, their “social” fish may have spent more time near the other fish due to fear-induced shoaling, and the researchers provided no clear way of distinguishing shoaling due to social motivation from shoaling resulting from fear.
Cote et al. (2012) did report a weak positive relationship between sociability and boldness, suggesting a tendency for social fish to be less fearful, but unfortunately they used the emergence from a safe place to test for boldness, a test that has been criticized as confounded with exploratory behavior and a poor measure of fear (see Burns, 2008; Reale, Reader, Sol, McDougall, & Dingemanse, 2007).
It may be that mosquitofish exhibit a kind of group behavior that appears social, but the question for neuroevolutionary personality theory is whether this grouping behavior represents a precursor to the mammalian PANIC/Sadness system. Perhaps the most obvious argument against social bonding in fish is that they are so easy to raise in isolation. In fact, the Cote group housed their fish individually in small tanks during their experiments.
Furthermore, touching and contact comfort are key features of the mammalian PANIC/Sadness system, with physical contact providing relief from separation distress (e.g., Panksepp et al., 1980), and fish generally do not touch each other in their shoals, but they may do this indirectly by feeling water-pressure movements from adjacent fish. Fish have a “lateral line” consisting of sensory receptors from head to tail that contain hair cell bundles, which detect water movement and vibrations and enable them to maintain appropriate distances from their shoaling neighbors. Faucher et al. (2010) has shown that after inactivating the lateral line fish cannot maintain a shoal: the distance between their closest neighbor doubles, they have difficulty maintaining their orientation relative to other fish, and they frequently bump into other fish. All shoaling behaviors returned to normal as the hair cell bundles regrew. In support of their findings, Faucher et al. (2010) also cite studies showing that cohesive schooling appears only after the developmental completion of the lateral-line system. Thus, it would seem that the maturation of the fish lateral-line system, which enables fish not to physically touch each other (with touching apparently disrupting their “unity”), sustains highly coordinated shoaling, but no clear social motive for this has yet been identified.
Regarding a potential social emotion underlying shoaling, a computer literature search revealed no reports of social attachments in fish. There were reports of reproductive monogamy in fish, but this seemed mostly driven by dominant female fish competing for limited resources and driving away other female fish (Wong, Munday, Buston, & Jones, 2008), although other reports (Harding, Almany, Houck, & Hixon, 2003) suggest sex-specific aggression by both genders can create similar functional monogamy that has nothing to do with mate loyalty.
A related question is whether fish play; that is, do they have affective rough-and-tumble social PLAY systems in their brains? Gordon Burghardt and Vladimir Dinets of the University of Tennessee, along with James Murphy of the Smithsonian’s National Zoological Park, recently published a report documenting three cichlid fish that independently acquired the behavior of repeatedly hitting a bottom-weighted thermometer sitting on the bottom of the fish’s tank and letting it bounce back, which they argued qualified as object play. The fish lived separately and clearly did not learn the behavior from watching each other (Burghardt et al., 2015). These fish were clearly not playing with each other, and there has yet to be a compelling report of social play in fish. In other words, these play behaviors could be envisioned to arise as examples of object play, perhaps arising from their SEEKING systems. In short, a distinct social PLAY system in fish remains to be demonstrated, that is, affectively positive rough-and-tumble social engagements that are highest in juvenile animals and that taper off dramatically following sexual maturation (Panksepp, et al., 1984).
What about parental CARE tendencies in fish? While most fish species do not provide parental care for their young, there are cases of mouthbrooding (see Grone, Carpenter, Lee, Maruska, & Fernald, 2012 for a biological analysis). There are also cases (mostly of male fish, e.g., sticklebacks and cichlids) defending their nests and guarding their offspring against predators (see Balshine & Sloman, 2011). Although rare, there are also cases of Central American cichlids in which parental fish provide food for their young in the form of skin mucus secretions, and of African cichlids stirring up the lake floor by rapidly beating their pectoral fins to expose bottom-dwelling prey for their young (Ota & Kohda, 2015).
Despite an amazing diversity of parental care activities in fish, an evolutionary analysis of reproductive models in the very large group of ray-finned fishes (class Actinopterygii, a subclass of bony fishes that includes sticklebacks and cichlids) revealed no indication that female-only or biparental care was an outgrowth of a male-only care model or that biparental care has been an evolutionary stepping stone between paternal and maternal care potentially having some neuroevolutionary continuity with mammalian-style maternal parenting. However, the adaptation of females giving live birth (and thereby perhaps a more mammal-like postpartum parental reproductive pattern) has evolved independently at least eight times in ray-finned fish (Mank, Promislow, & Avise, 2005). Accordingly, such species may have antecedents of a primordial CARE system, but at present there are no researched instances of a mammalian-style CARE-type “family feeling” having emerged in fish.
Still, we suspect mammalian-type CARE in fish may have occurred, and if so, it will be most interesting to see if in those cases there are ancestral homologies in the underlying social neurochemistries that would suggest some mammalian-type continuities in fish (e.g., the ancestral variants of oxytocin, such as nine-amino-acid neuropeptides isotocin, mesotocin, and vasotocin. Indeed, it has been shown that isotocin does control paternal care in monogamous cichlid fish (O’Connell, Matthews, & Hofmann, 2012). There is a growing literature that there is some evolutionary CARE continuity from fish to mice and men—but by no means as strong as in women and mammalian mothers in general.
FISH SUMMARY
While neuroscience-type brain manipulations would be valuable in targeting specific emotions in fish, for purely observational research we would recommend more careful selection of tests to avoid the possible confusion of fearful behavior with various social, aggressive, or exploratory behaviors. Indeed, Reale et al. (2007) have recommended multiple tests of each target behavior (a la Huntingford and Burns) to clarify potential confusions.
In summary, curiosity, anger, and fear, which correspond well with the evolutionarily older SEEKING, RAGE/Anger, and FEAR brain systems, are consistently observed personality dimensions in bony fish, the most evolutionarily ancient class of vertebrates reviewed in this book. So far there is no compelling evidence for well-developed CARE, PANIC, or PLAY systems in fish that would support mammalian-like social behavior. Still, there are hints of evolutionary continuities that we suspect will get ever stronger as more neuroscience research is conducted.
HOMOLOGOUS ANIMAL AND HUMAN PERSONALITY TRAITS: A SUMMARY OVERVIEW
Here we pause to briefly summarize where we have been with this cross-species journey. Some may find it disagreeable to think that humans may share some personality traits with other animals, yet such deep homologies are no longer a surprise to psychiatrists, neuroscientists, and geneticists (e.g., Feinberg & Mallatt, 2016). That fish temperaments may be largely defined by the evolutionarily older SEEKING, RAGE/Anger, and FEAR emotion systems would also have come as no surprise to pioneers like Paul MacLean (1990), who was among the first to describe the numerous homologies across early vertebrate, mammalian, and human brains. With mammalian homologies in mind, MacLean (1990) and Panksepp (1998a) would predict that the more evolutionarily recent social emotion systems—CARE, PANIC/Sadness, and PLAY—would provide many commonalities between rats, dogs, foxes, primates, and humans with each of the six personality-focused primary-emotion BrainMind systems influencing mammalian temperaments, which is exactly what was observed. Rat, dog, and ape temperaments are incredibly complex: anticipating basic rewards, obtaining resources, and sometimes just exploring; defending those resources and life itself when necessary; avoiding danger and physical pain; caring for young and thereby unwittingly transmitting epigenetic adaptations (see Chapter 15); avoiding separation from bonded social mates and from familiar places; and learning to regulate key behaviors through socially interactive and physical play. Each of these systems was apparent in the temperament research of the three mammalian examples we summarized in the past chapters. There are echoes of certain homologies in fish, but relevant neuroscience remains scarce.
In addition, a Conscientiousness factor regulating emotional expression was identified in chimpanzees and brown capuchin monkeys (see Chapter 7), with additional demonstrations likely forthcoming as methodological issues are refined. There was also one more unanticipated possible addition to the temperament of the domestic dog: predatory behavior expressed toward humans (see Chapter 8). This is likely part of the food foraging system and just one of the many possible species-typical predatory expressions of a basic SEEKING urge shared by all vertebrates, for instance, the “quiet biting predatory attack” that can be provoked by deep brain stimulation in both rats and cats (Siegel et al., 1999; Panksepp, 1971; Siegel, 2004). Additional basic research involving the analysis of specific brain systems will be necessary to verify homologous systems in dogs.
For humans, we thought it would be useful to have a personality test that attempts to evaluate the primary-process emotional reactivities of our own species—based upon brain emotional systems that have long been evident from cross-species affective neuroscience research (Panksepp, 1982, 1998a). As already summarized, our initial attempt to move in that direction generated a set of evolutionarily defined psychological test scales to tap into each of the primary affective brain systems except LUST (as already noted, omitted to avoid introducing unwanted “guarded” response biases) in the hope of promoting neuroscientifically anchored systematics in the field (Davis et al., 2003). Indeed, each of the six scales monitoring these basic emotional factors—from primordial SEEKING, RAGE/Anger, and FEAR to more socially sophisticated CARE, PANIC/Sadness, and PLAY—correlated highly with various Big Five dimensions except for Conscientiousness. Conscientiousness did not clearly represent any of the primary emotions, suggesting that it may be better envisioned as a cognitive rather than an affective factor, perhaps one representing higher cognitive brain functions regulating the expression of emotions, increasing behavioral sophistication, and adaptability. This idea could shed light on why Scott and Fuller (1965) found that cocker spaniels were so capable of inhibiting their emotional reactions to stressful events and suggests cockers might provide a reasonable animal model for studying an elementary form of Conscientiousness. That Conscientiousness so far has been psychometrically measured only in chimpanzees and brown capuchin monkeys suggests that Conscientiousness requires a well-developed neocortex (for an alternate view on rat prefrontal cortex, see Uylings & van Eden, 1990; for a rat model of orbital prefrontal cortex inhibition of aggressive behavior discussed in Chapter 7, see de Bruin, 1990). Even more dramatically, Frans de Waal (2009) has illuminated complex social emotions, including empathy and compassion, in our primate cousins, which may suggest other novel scales for higher anthropoid social emotions will eventually be needed.
Davis et al. (2003) showed that in humans PLAY correlated positively with Extraversion, CARE correlated positively with Agreeableness but negatively with RAGE/Anger, and SEEKING correlated positively with Openness to Experience. However, they also pointed out a basic flaw with the factor-analytically derived Big Five: RAGE/Anger, FEAR, and PANIC/Sadness all correlated negatively with Emotional Stability/low Neuroticism. Indeed, half a century ago, Walter Hess (1957b) recognized that RAGE and FEAR were two distinct primal emotions (although he did not use our primary-process terminology). MacLean (1990) also recognized that RAGE and FEAR had been major temperament dimensions for probably well over 500 million years (i.e., before the Cambrian explosion of new species), predating the evolutionary appearance of fish and agreeing with RAGE/Anger and FEAR being observable distinct personality dimensions in Huntingford’s (1976) fish research. However, along with PANIC/Sadness, the Big Five lumps together all three negatively valenced emotions, which figure so prominently in psychopathology, or at best relegates them to blends or facets rather than according them the primary temperament status that is apparent in the brain of every mammal. So using the six primary emotion brain systems as a template, Davis et al. (2003; refined in Davis & Panksepp, 2011) constructed the Affective Neuroscience Personality Scales (ANPS), which was conceptualized largely as a human research tool capable of situating human subjects in primary-process affective space but that could also usefully be adapted for the study of other species. However, such a jump would be too large for many academic psychologists.
Thus, the scientific study of emotions remains a contentious topic, and the existence of emotional experiences in animals is still more controversial than it should be (for full review, see Panksepp & Biven, 2012; Panksepp, Lane, Solms, & Smith, 2017). There is also a disconnect in what scientists who work with animals claim and what intelligent nonscientists who live with animals believe. To evaluate where the latter stand on such issues, Paul Morris and colleagues from the University of Portsmouth in the United Kingdom surveyed 907 animal owners’ beliefs about the existence of potential emotions in the animals they deal with on a daily basis (Morris, Doe, & Godsell, 2008). The results were striking. The vast majority of these respondents, including 337 dog owners and 272 cat owners, believed their companion animals experienced primary emotions such as anger, fear, surprise, joy/happiness, sadness, anxiety, and curiosity, and a smaller but substantial number of owners also believed the animals had what might be deemed derived emotions, such empathy, shame, pride, grief, guilt, jealousy, and embarrassment. In support of their view, consider that artificial activation of all subcortical emotional systems discussed in this book can serve as rewards and punishments in various learning tasks. Indeed, it is highly likely that the time-honored behavioristic concepts such as “reward” and “punishment” derive the capacity to mold learned behaviors because the various affective changes of brains were designed, in evolution, to guide learning (Panksepp, 1998a, 2005, 2010b, 2011a).
Indeed, there is overwhelming objective scientific evidence that various basic emotions are fundamental powers of the BrainMind, in both humans and other animals, and we would suggest they are of critical importance for understanding the foundations of human temperament. Cross-species affective neuroscience has the potential for scientifically mapping out the continuity of the emotional BrainMind in subcortical-limbic circuits of all vertebrate brains, as it already has for understanding various psychiatric disorders (Panksepp, 2005, 2015, 2016). We suspect that when we structure our human temperamental measures in terms of primary-process emotional issues, many of the higher aspects of personality may become easier to analyze. However, in seeking a comprehensive story, we should not forget that the higher regions of the brain are more plastic than the lower regions, and that there are environmentally relevant susceptibility factors that are not yet well understood, perhaps the most subtle of all being that the degree of environmentally induced plasticity may itself be heritable (i.e., epigenetics, discussed in Chapter 15). Clearly, such issues will never be well understood in humans unless we have corresponding animal models to study the underlying neurobiological details. We will understand our own fundamental (evolved) emotional systems and the feelings they generate largely through cross-species research, rather than just human research. This said, our neocortical expansions and capacity to speak allow us to have abundant thoughts that no other species has yet had. But little of that would exist without our grand ancestral voices and evolved primary-process affective heritage.
To summarize, working backward from this chapter through the previous three chapters, we have identified ancient neurochemistries spanning a billion years of animal evolution that humans share with the nematode C. elegans and have explored evidence for mammalian emotional commonalities with fish—originating perhaps 600–400 million years ago—in the SEEKING, RAGE/Anger, and FEAR emotional action systems, with glimmers of even some commonalities in our CARE system neurochemistries. Further, these ancient neural “survival systems” are still retained in the mammalian emotional affective BrainMind makeup, along with fuller elaborations of various social emotions, especially CARE, PANIC/Grief/Sadness, and PLAY. Each of these emotional affective systems is an ancestral guide for living and learning and “speak” to us in the oldest of experienced languages: They feel like something. That is, these inborn affective qualia, originating from survival systems that evolutionarily precede verbal language and are so often difficult to describe in words, each has a positive or negative valence about them that informs us about our survival paths and probabilities. Pleasant affects like the joy of CARE in nurturing infants encourage us to maintain our evolutionary-survival trajectories. Unpleasant affects like FEAR tell us we may be in danger and urge us to stop or to run—to freeze or flee—while automatically teaching us to avoid such situations in the future (via yet poorly understood “Laws of Affect” that control learning and memory formation).
These raw subjective feelings are one of life’s great mysteries. No one yet knows precisely how subcortical brain networks generate such affective states of mind. We do know that they are experienced by many classes of animals, and most certainly all mammals, because they change how these animals, including humans, behave both in the moment and by altering life trajectories as they spontaneously result in learning. Animals learn to avoid the unpleasant affects and work for more of the pleasant affects. However, that these affects are experienced does not necessarily mean animals are consciously “aware” of them. They probably do not cognitively dwell on such states of mind as much as humans do, partly because of our capacity to think and speak. It is widely believed that brain cortex is required to generate conscious awareness of an affect as a kind of symbolic re-representation. Yet, as we study animals with more complex cortical development—as their cerebral cortex more closely approximates the human neocortex (especially the other anthropoid apes)—it becomes more likely that they do experience some kind of higher conscious awareness of their own affects. However, without being able to communicate with verbal language, it is difficult to know the level of any other species’ actual experience, although there are tantalizing hints in animals from jackdaws to chimpanzees of some level of cognitive awareness (Bekoff, 2007; de Waal, 2009; Feinberg & Mallatt, 2016).
In any case, the increased encephalization of the brain, as perhaps best seen in chimpanzees, allows for more nuanced behavior and feelings and social learning. The expansion of the neocortex seems to allow for greater emotional regulation, as seen in the conscientiousness of chimpanzees and brown capuchin monkeys, as well as increased social sophistication, as seen in the reports of chimpanzee political alliances and examples of moral behavior. Of course, the apex of neocortical development occurs in humans. However, it is our position that even the most complex refinements and subtleties of human behavior and principles rest on the foundational values for living inherited in the form of our ancient subcortical emotional affects and their ancestral voices that speak to us in the most primal language: the spontaneous affective language of what it feels like to be alive—to experience life.