Evolutionary aspects of anxiety disorders

John S. Price, D.M.

Danger and harm are avoided by strategic decisions made at all three levels of the triune forebrain: rational (neomammalian), emotional (paleomammalian) and instinctive (reptilian). This applies also to potential harm from conspecifics, which leads to a choice between escalating and de-escalating strategies. Anxiety is a component of de-escalating strategies mediated by the paleomammalian and reptilian forebrains. When the neomammalian (rational) brain fails to deal with the threat of conspecific danger, these more primitive de-escalating strategies may be activated and may present as anxiety disorders. The capacity for concealment of anxiety and other forms of negative affect has also evolved, and excessive concealment may lead to psychopathology by breaking the negative feedback loop of excessive motivation, leading to impaired performance, leading to signals of distress, leading to reduced exhortation to succeed on the part of parents and teachers; this situation is illustrated by a model based on the Yerkes-Dodson law.

Keywords: agoraphobia; anxiety disorders; behavioural ecology; de-escalating strategies; depressive disorders; evolution; triune brain; Yerkes-Dodson law

Author’s affiliation: Department of Psychiatry, South Downs Health NHS Trust, Brighton General Hospital, Brighton BN2 3EW, UK

Address for correspondence: John S. Price, D.M., Odintune Place, Plumpton, BN7 3AN, UK

(e-mail: johnscottprice@hotmail.com)

Acknowledgements

I thank my fellow members of the ASCAP society for exchange of ideas over many years. The ASCAP society (ASCAP may stand for Across Species Comparisons and Psychopathology) is an international organisation of people from various disciplines interested in evolutionary aspects of psychopathology (see www.theascapsociety.net).

Inside the animal's form sits the brain, its work broadly to increase the animal's grip on the world about it, and hardly less the grip of the external world upon the animal.

Sherrington, Rede lecture, 1933.

Modern times are not like the times in which our ancestors evolved. The environment of evolutionary adaptation (EEA) usually refers to the habitat of our immediate ancestors who are thought to have been hunter-gatherers living in bands of about fifty adults, but is really an abstraction which covers all environmental influences going back over three hundred million years to the common ancestor of humans and present-day reptiles. The “mismatch” between now and the EEA is thought to be one cause of psychopathology. “Bad news” is a source of anxiety. We now have daily, or even hourly, access to the bad news of six billion people, more than could be generated by a hunter-gatherer band. Moreover in the EEA bad news was probably discussed and so shared with other group members, whereas modern man tends to watch it or listen to it on his own, or at least without comment. Therefore, as a practicing clinician, I advise all my anxious patients to avoid watching TV news, and I find that many of them have learned the lesson for themselves. They realise that each item of bad news raises their background level of anxiety, and, of course, severely depressed patients may believe that they are personally responsible for the disasters which occur daily around the globe. No one, to my knowledge, has done a controlled trial of “news avoidance” as an item of therapy.

Much has been written about the evolution of anxiety and its disorders.^1-10 Here, rather than repeating familiar arguments, I will try to break some new ground, looking at approaches that may be relevant to research and treatment. I will concentrate on social aspects of anxiety, because non-social anxieties have been well covered, whereas there is still something to say about social anxiety, particularly the relation of social anxiety disorder to generalised anxiety disorder, and the relation of anxiety to depression, and the relation of anxiety and depression to social competition. Evolution is history, and our speculations about how and why certain things evolved cannot be tested directly. As W.H. Auden said, “History is, strictly speaking, the study of questions; the study of answers belongs to anthropology and sociology.” In the case of evolutionary history, answers are also provided by psychology and physiology. Evolutionary speculations are heuristic, in the sense that they may lead to the posing of questions which otherwise would not have been thought of. The proof of the pudding is in the eating.

Generalised anxiety disorder (GAD)

Here is an example of how contemplation of the EEA may generate ideas. A team from the University of British Columbia construed GAD as an unsuccessful search for safety.¹¹ They addressed “three distinctive features of generalised anxiety disorder (GAD): the undue persistence of the anxiety and worry; the excessive generality of the anxiety, and the lacklustre response of GAD to cognitive therapy procedures…People with GAD persist in multiple, persistent searches for safety, but they seldom succeed in achieving lasting satisfaction.” The big question is, “Where does safety come from?” This becomes clear if we imagine that during part of the EEA human beings went through a stage of living in hierarchically organised groups, much as most monkeys and apes do today. In such a group, most rewards are dependent on the animal’s social rank, and the only means of social advancement is to rise in rank. An ambitious chimpanzee challenges the animal who ranks above, who probably resists the challenge, and a ritualised fight ensues – which may last on and off for many months, until either the challenger gives up, or the higher ranking animal is deposed. The two then undergo what primatologist deWaal has called “conditional reconciliation” - they kiss and hug and make up, but with the understanding that the deposed animal is now subordinate; this means that the subordinate animal has to behave submissively to an animal he may have dominated for some years.^12-14 If we consider the state of mind of the deposed animal after he has been beaten but before he has reconciled, we can see the need for some reorganisation of goals and attitudes: we have suggested that depressed mood may help the animal to give up the goal of retaining his high rank, and reconcile him to his inferior social position.¹⁵ But the depression does not help him to reconcile with his supplanter. Here there is a role for generalised anxiety, with its frantic search for safety. There is only one source of safety in the chimpanzee world, and that is from the victorious animal, and so the deposed animal turns to the victor for reassurance and protection, and is so needful of safety that he accepts the terms of the conditional reconciliation, and his gratitude for the relief of anxiety overcomes his resentment at being deposed. In this hypothetical situation we can see how depression and anxiety can work together to achieve what has been called “functional agonism.”¹⁶

Such a scenario has been reported in a street-corner gang¹⁷ which is probably the nearest that human society gets to a chimpanzee group. But most human social life is infinitely complex and the simple situation of the chimpanzee or the human gang cannot be discerned. From the research point of view, our ideas stress the importance of the work carried out by Paul Gilbert and his colleagues in Derby, UK,¹⁸ and others,¹⁹ into the relation between depressed and anxious mood and submissive behaviour. And from the treatment point of view, we endorse the approach of Interpersonal Psychotherapy (IPT) which explores current conflicts in the lives of patients.²⁰ Unresolved rebellions against parents and other powerful people should be explored. Also, given that in human society it is often the group as a whole, rather than individuals, who exercise power, the patient’s relations with “authority” should be examined, and, for instance, any questionable self-assertion should be avoided, such as submitting inflated expense accounts or massaged tax returns. This is similar to the suggestion of David Buss²¹ that anxiety helps to prevent unattractive, incompetent or deviant people from being excluded from their group; anxiety may not make people more attractive and competent, but it can make them less deviant, and it can help to reconcile unattractive group members to a more subordinate role in which they may be better tolerated.

One cannot help noticing that in a Christian country, many of the population submit to a powerful figure every week, confessing their sins, going through a ritual not unlike the conditional reconciliation of the chimpanzee. And one recalls that C.S.Lewis, in The Problem of Pain, concluded that the function of mental pain is to reconcile man to God. Lewis, having experienced severe depression, concluded that man is so proud and arrogant that to achieve submission even this degree of mental pain is required. Submission to a cult leader and his beliefs, or to a psychotherapist and his theories, may achieve a similar result.

In summary, I have suggested that depression and anxiety work synergistically together to promote functional agonism, whereby rank differences are maintained and rank reversals are achieved without group disruption. Depression prevents rebellion and generalised anxiety promotes reconciliation, so that a hierarchy based on reassurance, gratitude and respect can replace either social chaos or a hierarchy based on intimidation. Groups with such “hedonic” hierarchies are likely to outcompete groups with agonistic hierarchies, so that the effect of selection between groups will be added to the individual advantage of the anxious person (avoiding punishment or exclusion by a more powerful person or by the group as a whole) and these advantages have presumably, during the course of evolution, outweighed the disadvantage of giving up the resources which are the rewards of high social rank. This synergistic action of depression and anxiety is compatible with the finding of extensive comorbidity between anxiety states and depressive disorders^22-25, and with the finding that the genetic predisposition to major depression is indistinguishable from the predisposition to generalised anxiety disorder (GAD).²²

Social anxiety disorder

I have suggested above that GAD plays a part in managing the organisation of a social hierarchy, and promotes reconciliation with a successful rival. Thus it is concerned with social change. Social anxiety disorder is also concerned with avoiding harm from conspecifics, but is concerned with social homeostasis. The difference is one between anxious mood and anxious emotion. An emotion is directed at an object, and is sensitive to changes in the object, whereas a mood is unfocussed or self-focussed, and is unaffected by changes in the environment.²⁶ It is likely that emotions and moods are mediated by different levels of the brain, and in order to illustrate this I will use Paul MacLean’s model of the triune brain,^27,28 suggesting that depressed emotion and anxious emotion are mediated by the paleomammalian forebrain, whereas depressed mood and anxious mood are mediated by reptilian forebrain.

A triune mind in a triune brain

In order to comprehend clearly the human response to danger, and to see anxiety in the context of all the mechanisms deployed in the avoidance of danger, it is necessary to invoke the concept of the triune mind.^29,30 The idea that the mind consists of two or more relatively independent entities has been around at least since the time of Plato.³¹ It has been most pithily expressed by Pascal in his aphorism, “The heart has its reasons which the reason knows nothing of.” Ancient Eastern philosophers, whose ideas were largely promulgated in the West by Gurdjieff, used the metaphor of the cart, horse and driver.³⁰ The driver represented Reason, or the rational mind, but he had only limited control over the horse, who represented the emotional mind (located in the heart), who in turn had limited control of the cart, representing the instinctive mind, located by some in the gut. Plato likened the three minds to different organs of state.³¹

The work of the evolutionary neuroanatomist Paul MacLean has given support to the idea of the triune mind by his demonstration of a triune brain²⁷. Prior to MacLean, it was thought that over the course of evolution the brain had gradually grown in size, with the later additions on the whole controlling the earlier parts, largely by inhibition. MacLean pointed out that the forebrain had grown in three distinct stages, leaving three “central processing assemblies” which relatively independently respond to changes in the environment. Firstly, the reptilian forebrain evolved from the fish and amphibian brains and concerned itself, as far as social relations went, with the courtship of the opposite sex, and competition with the same sex by means of agonistic behaviour. This brain is present in all reptiles, birds and mammals, and in humans it occupies the basal ganglia or corpus striatum. Then, instead of a homogeneous accretion of additional brain volume, there developed a “paleomammalian brain” which dealt with mammalian social life, the family, the parent/offspring bond, and such social matters as were not part of reptilian social life. This brain is situated in the limbic system. And not only did it deal with mammalian matters, but it also dealt, in a mammalian way, with those problems which had been faced by reptiles and were also faced by mammals, such as the avoidance of danger, the courtship of the opposite sex and competition with the same sex; but, at the same time, the reptilian brain continued to deal with the same old problems in its old reptilian way. In higher mammals there developed the neomammalian brain which subserves what we recognise as rational thought and decision-making, and it brings these capacities to bear not only on modern problems such as technology and litigation, but also on the older problems which are addressed by the reptilian and paleomammalian brains such as avoidance of danger, courtship and competition. This neomammalian brain is situated in the neocortex.

Thus we have three brains dealing with the same problems, and to some extent they co-operate, but also to some extent they act independently. They have different sources of information, they make different executive decisions, and they have different representations in awareness. This is quite a surprising situation, one that would not have been predicted, say, by an engineer accustomed to designing robots. The most surprising thing is that the rational brain, which appears to be the most sophisticated thinking machine ever to have evolved, has so little control over the two lower brains. The driver is not in control of the horse or the cart. It would have been easy for such control to have evolved, so the fact that it has not evolved suggests that there is some advantage in having one or more relatively independent lower “central processing assemblies”. In the case of danger avoidance, there is some advantage in speed of reaction, so that avoidance occurs rapidly before the more sophisticated, but slower, neomammalian brain can take action. But there is also a sense in which the lower brain “knows better”, having sources of information not available to the higher brain. This seems to be particularly true in the case of avoiding danger from conspecifics. In competitive relations with conspecifics, a decision frequently has to be made between escalation (fighting harder) and de-escalation (fleeing or submitting) and this decision appears to be made, relatively independently, by each of the three brains, sometimes sequentially, sometimes simultaneously (Table 1).

(Table 1 about here)

Since anxiety may be a component of the de-escalation response, it is necessary to say something about escalation and de-escalation, which are familiar concepts in ethology³² and behavioural ecology,³³ but have not yet been clearly formulated in psychology.

Escalation and de-escalation

For over three hundred million years, competition between members of the same sex has taken the form of agonistic behaviour, and, from observation of countless species of existing mammals and reptiles, ethnologists have pointed out that this behaviour is ritualised, in the sense that it obeys certain rules. One of these rules is that each individual has a limit in the punishment he is able to receive before switching from escalation to de-escalation. Another rule is that when one contestant submits, the winner exercises mercy and does not take advantage of any submissive posture adopted by the loser.

In a contest, there is usually mutual signalling of Resource-Holding Potential (RHP) which is an estimate of fighting capacity, and if there is a significant difference in RHP between two contestants, the one with less RHP usually backs off before any engagement starts. Or, if the contest occurs on a territory owned by one contestant, there is a convention that the owner of the territory wins. If territory is not an issue, and RHP is equal, a fight ensues, which may escalate through several stages of fighting behaviour, such as the roaring of stags,³⁴ which is followed by parallel walking, which is followed by locking horns. Each contestant is giving out punishment to the other, and receiving punishment in return. When does one of them give up? This interesting value has been honed by hundreds of million years of evolution, but for simplicity’s sake can be expressed in terms of “punishment units received”, a value which is determined partly by the animal’s motivation (the value to the animal of what is being fought over, a quantity known as Resource Value), partly by ontogenetic experience, and partly by heredity.³⁵ Assuming the resource to be of equal value to both contestants, and their life experience to have been equivalent, the deciding factor, according to behavioural ecologists, is either genetically determined or randomised according to a genetically determined schedule, and the contestant with the greater capacity to endure punishment before submitting is said to adopt a hawk strategy, while the contestant with the lesser capacity, and who therefore submits, is said to adopt a dove strategy. Adopting reasonable parameters, a mixture of hawk and dove strategies is evolutionarily stable³⁶ (whether the mixture is between individuals or within individuals on different occasions does not matter). Hawk and dove are graded characters, so that in any contest, an individual is likely to be confronted with an opponent who is either more hawkish or less hawkish than himself, and this is why contests can be resolved without injurious fighting, and why ritual agonistic behaviour has become such a widespread means of distributing resources such as territory and social rank between individuals.

Escalation and de-escalation at three brain levels

Decisions to escalate or de-escalate take place either simultaneously or consecutively at all three levels of the triune brain (Table 1). At the rational, or neomammalian level, the decision is made consciously and voluntarily either to fight harder or to back off; when backing off, the appeasement display may take the form of a graciously worded apology, or a flowery speech of submission. At the emotional or limbic level, escalation takes the form of anger, indignation and the exhilaration of combat, with its associated bodily changes; de-escalation at this level may recruit the dysphoric emotions of anxiety and the sense of being chastened. Also, since this level involves the rules of group membership and prestige competition, guilt and shame also play roles so the appeasement display typically consists of weeping, blushing, and protestations of repentance (Table 2). At the instinctive level, we hypothesize that escalation in the reptilian brain takes the form of elevated mood, giving the individual a prolonged increase in energy, optimism, self-confidence and heightened sociability all of which function to recruit allies. Conversely, de-escalation at the instinctive level takes the form of depressed mood and may include the unfocused anxiety of GAD, the fatigue of chronic fatigue syndrome, and the physical disabilities of somatisation disorder37. The appeasement display at this level communicates this impairment and disability to any rival or to society as a whole. Parenthetically, when directed at friends and allies, the appeasement display takes the form of a distress signal, sending the message, “I am sick, care for me, and do not send me into the arena to fight on your behalf”.38 
 
Prestige competition overtakes agonistic competition
 
Methods of competition have become more complex over the course of evolution. Group living lengthened the duration of contests, so that even in apes a struggle for dominance may take several months to be resolved. And, instead of fleeing, as happens in territorial species, the loser could remain in the group with the winner of the contest, and this gave rise to appeasement or submissive behaviour, which reflects the capacity to live in a subordinate social role. Anxiety and fear of the dominant individual, together with relatively low self-esteem and lowered mood, enabled the social hierarchy to maintain stability, and prevent rebellion. At some stage in evolution, this stabilising anxiety gave rise to a new way of relating to a higher-ranking individual: respect. The leaders of the group made themselves attractive to the group members instead of (or in addition to) intimidating them. Social rank was then determined by the choice of the group rather than by agonistic dyadic encounters. The new self-concept of Social Attention Holding Power began to replace RHP, as group members evaluated themselves according to their power to attract interest and investment (such as votes or other forms of political support).39 Related to SAHP is the concept of prestige, which is the extent to which the group is prepared to invest in the individual. Prestige competition was added to, but did not entirely replace, agonistic competition.40
 
 (Table 2 about here)
The capacity for escalation and de-escalation appears to have survived the switch to prestige competition, but takes different forms, at least at the upper two forebrain levels (Table 2). At the highest level, pursuit of goals replaces the decision to attack, so that escalation consists in the adoption of new goals, and de-escalation consist of giving up goals. The goals are usually ones that lead to prestige, if achieved. Also, on social occasions, escalation takes the form of self-assertion, such as standing up to speak, and promoting one’s own goals, whereas de-escalation takes the form of self-effacement, and allowing other people’s goals to take precedence in the group.
At the emotional level, escalation is less dramatic than the anger of agonistic competition; it takes the form of exhilaration, enthusiasm and self-confidence. De-escalation reflects the fact that punishment comes from the group rather than from a dominant individual, so there is social anxiety, guilt and shame. This is an appeasement display to the group, expressing contrition for breaking group rules, or for failing to come up to group standards.
At the instinctive, reptilian level of the forebrain, little seems to have changed, and elevation of mood represents escalation, whereas depression of mood, together with the anxious mood of GAD, represents de-escalation. However, the information which leads to the activation of the strategy set is clearly different. Instead of measuring punishment received from the rival, the reptilian brain in some way monitors social standing in the group, and is sensitive to group approbation and disapprobation, to comparison of self with other group members, and with one’s own aspirations, and to the knowledge of having failed the group in some way and the likelihood of being found out.
The manifestations of escalation and de-escalation at the three brain levels are shown for agonistic competition in Table 1 and for prestige competition in Table 2.

The importance of attachment, equality and co-operation

We³⁸ have been accused of emphasising the competitiveness of human life at the expense of co-operation, equality and affiliation. We certainly do not deny the importance of affiliation, and we respect the enormous contribution of John Bowlby who first introduced the idea of attachment and separation into psychiatry, and also his reliance on data from comparative ethology; nor do we deny that a lot of psychopathology derives from the loss of attachments, from death, rejection, infidelity or boredom.

Even the threat of the death of a spouse may cause both anxiety and depression. Also, it seems likely, both from research and experience in the clinic, that adverse experience with parents in early childhood, leading to insecure attachment, and also failure to integrate successfully with the peer-group in adolescence, can predispose to psychiatric disorder in later life.¹ And basic research on the way these early adversities alter brain function is important.⁴¹

From the evolutionary point of view, however, we think that the roots of depression and anxiety go back further than the evolution of attachment, at least back to the common human and reptilian ancestor, who very likely shared with most present day reptiles the complete absence of attachment, or family life, or even pair-bonding, and in whom relations with the opposite sex were restricted to courtship and with the same sex to ritual agonistic behaviour. When attachment evolved, it had a profound effect on ranking behaviour, and even in monkeys, let alone apes, rank depends on kinship and alliances, so that the loss of a powerful patron was probably the best predictor of a fall in rank.^42,43 Depression and anxiety following loss thus represent a pre-emptive mood change to adjust the individual to lower status. (This does not apply to the emotion of grief which is likely to have other functions.)

The Standard Social Science Model portrays human ancestors as independent, egalitarian people, much like present day hunter-gatherers.¹ The inequalities and competitiveness of the developed world were seen as recent cultural pathologies. It followed from this view that anxiety, depression and other psychopathologies could not have evolved in the context of social competition. However, this cultural view greatly underestimates the power of culture to transform society. Stevens and I have pointed out that humans have a powerful capacity to undergo a sudden and radical change of belief system, and to indoctrinate others into that new belief.⁴⁴ It only takes a single prophet to look around at his competitive society, in which success is considered good and to be rewarded, and to pronounce “Success is bad and should be punished”, for a new society to arise in which, as in present day Kalahari Bushmen, success and ostentation are ridiculed, and an atmosphere of “counterdominance” prevails.⁴⁵ Thus we should expect groups of our ancestors to be wildly culturally divergent, along many dimensions of variation, but the dimension of equality/inequality was likely to be a popular one. And it only takes a message of three words (“success is bad” or “success is good”) to transform the entire way of life. But, although the message is short, it is a uniquely human one. There is no way in which a chimpanzee group could switch from one ideology to another (even though environmental conditions such as food supply have a large effect on the competitiveness of chimpanzee groups). In summary, we are saying that our ancestors had the capacity to live in both equality and inequality, and they had available, if needed, the behavioural mechanisms such as depression and anxiety which made cohesive group life possible in conditions of inequality.

Implications

In painting this evolutionary scenario of affective disorders, I have passed the white light of escalation/de-escalation theory through the prism of triune brain theory, and revealed a triptych of three central processing assemblies operating relatively independently in the forebrain and each of them responding to the fortunes and misfortunes of social competition, subserving what Darwin described as intrasexual selection.⁴⁶ The implication for both research and treatment are fairly clear.

Research into defeat in experimental animals has largely been initiated and financed by specialities in general medicine, because defeat, especially when escape is blocked, causes high blood pressure, renal failure and gastrointestinal ulcers, but now it is at last being realised that these defeated animals, so distressed that their bodily organs are diseased, also suffer from some psychological upset, and that subordinate animals may suffer from depression.^47,48 It is now nearly twenty years since McGuire and his colleagues^49, reported alterations in blood serotonin associated with hierarchical position in vervet monkeys, a finding which is counterintuitive since the majority of the body’s serotonin resides in the gastrointestinal tract, but in spite of this evident breakthrough, their findings have not to my knowledge been repeated by other laboratories, let alone extended. There is a pressing need for an all-out sociophysiological assault on the mechanisms of hierarchical behaviour.^50,51

In relation to treatment, it is clear that if the rational level of the brain can sort out the problems of social competition that the individual encounters, there is no need for the more primitive levels to introduce their uncomfortable solutions, any more than it is necessary for a cold individual to shiver when he has the alternatives of putting on more clothes, turning on the central heating, or migrating to the tropics. The object is to replace unconscious behavioural strategies with conscious, rational ones.⁵² This has implications for the time a therapist spends sorting out real life conflicts, as opposed to ventilating emotions and arguing the patient out of depressive thinking. Also, it illustrates to the therapist how he inevitably enters the patient’s hierarchical world, to exercise influence which may be benign or otherwise.

Depression is more common than elevation of mood, and this reflects the fact that submission has been a more useful evolutionary tool than fighting to the death. Some individuals have easily triggered submissive responses,⁵³ on the “smoke detector” principle that several false alarms are better than one burning, and there is likely to be considerable genetic variation in this trait of dysthymia,⁵⁴ which appears also to be sensitised by adverse experience in childhood. This realisation is important for parents, educationists, and those concerned with primary prevention.

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