More about voles


Further reply to A. Randrup & G. Sorenson


ASCAP (somewhere)


I am impressed by the great variation in hierarchical behaviour both within  and between species, such that in some hierarchies to be subordinate gives  rise to no problems, whereas in others the subordinate role seems to be one  of continuous terror and humiliation. In your own work with bank voles  (1), you found that an enriched environment greatly reduced the "putting  down" of subordinates by high ranking voles; but even in the enriched  environment there was one tyrant who persecuted the subordinate for no  apparent reason, and in the pernicious environment some hierarchies were  peaceful. In many species the unprovoked bullying of subordinates is  enough to induce a state of learned helplessness - no electrified grid is  necessary in these species. In some species there are physiological  effects in subordinates which seem an important part of their adaptation;   inhibition of sex change in certain fish, adoption of juvenile colouring in  lizards, inhibition of ovulation in mice and some New World monkeys;  we do  not know the mechanisms of these changes, nor whether they are related to  the central nervous mechanisms responsible for psychogenic death. Nor do  we know whether hypertension and other causes of psychogenic death are  entirely mediated by the increased secretion of corticosteroids and/or  catecholamines which are recognised accompaniments of subordinate status. Research on subordination has a long way to go;  at present it seems to be  mainly motivated by cadiologists, gastroenterologists, nephrologists and  more recently immunologists;  only in Denmark is it realised that  psychological problems may intervene between aversive social experiences  and serious physical disease.

   I would agree with you that subordination is not pathogenic in itself:   only in certain circumstances. These circumstances would seem to be:


1. If the environment is unfavourable so that agonistic interactions are  increased.

2. If the higher ranking individual is a bully or lacks the social skill  to accept submission.

3. If the individual lacks the social skill to submit adequately (or does  not wish to submit) or lacks other skills for coping with subordination  such as the stereotypies in your voles.

  It might clarify things if we reserved the term submission for voluntary  acceptance of subordination, in contrast to its involuntary depressive  counterpart, which could be called depressive yielding. The title of my  essay was confusing, suggesting that depression masquerading as physical  illness was a metaphor of submission, whereas, being totallly involuntary,  it should not have come into the category of submission at all. The title  should have been "Metaphors of yielding."  If you submit voluntarily, you  do not need to undergo depressive yielding.


Report from the Institute of Zoology in London


After writing the above, I attended a meeting of the Association for the  Study of Animal Behaviour at the London Zoo. The subject was "Neural and  Endocrine Mechanisms in the Control of Behaviour."  Three of the talks were  relevant to the above discussion and I would like to share with you my  somewhat patchy memory of them.

   Norbert Sachser from Bayreuth in Germany described his work on captive  colonies of guinea pigs. Two dozen mixed sexed animals kept in a 12 metre  square enclosure develop a stable social structure in which there is social 

asymmetry among the males but not among the females. About three males  become territorial males, relating to half a dozen females;  each  territorial male has two or three satellite males, who each relate to two  or three only of the territorial male's females. Other males occupy the  space between the territories and do not relate to any females. There is  little fighting and the territorial males do not try to mate with each  other's females, even if they stray onto their territories. There is no  difference in adrenal cortical or medullary function or in testosterone  levels between the three categories of males.

   If two strange males are caged together with a strange female, the  outcome depends on the social history of the males. If they have been  brought up with other males, there is a day or two of intense fighting and  then one submits and becomes a satellite male, and the fighting stops. If  the two males have been brought up with females only, the fighting goes on  and the loser dies, not of wounds but of metabolic disorder;  it seems that  the losing male has never learned to submit. Without this learning  experience, the guinea pigs are like those of von Holst's losing tree  shrews who hid away and died;  with learning, the guinea pigs did much  better as the adrenomedullary function of the losers returned to normal,  unlike that of the other category of losing shrews who became uneasy  subordinates. It seems that some animals like the wolf and the rhesus  monkey have an innate capacity for submission, others like the guinea pig  have the capacity to learn submission, others like the tree shrew and the  male patas monkey lack the capacity to learn submission. This no doubt  reflects social structure during evolution. The wolf always lived in  groups, the tree shrew always lived in territorial pairs, the guinea pig  had a more flexible social structure. John Crook once said: "Ecology 

determines social structure which determines personality."

   One finding in the guinea pig work deserves special mention. When two  strange group-reared animals are matched in a fight, the first clue to the  outcome of the fight is a huge increase in adrenocortical activity in the  eventual loser;  at the same time the winner-to-be and the female make  mutual courtship gestures;  both these changes occur before there is any  differentiation in the agonistic behaviour of the two males. This suggests  at least two possibilities. One is that the winner-to-be is emitting an  olfactory agonistic signal. The other is that the corticosteroid response  to the stress of fighting is part of a feed-back loop which triggers the  decision to lose in the eventual loser;  this would fit in with the ideas  of Leshner (2) and his findings that adrenalectomised mice show delayed  losing, and normal mice injected with ACTH or cortisone show exaggerated  losing behaviour.

   The other two relevant talks concerned the social suppression of  ovulation. Dave Abbott, recently moved from the London Zoo to Wisconsin  Primate Centre, described his work on the marmoset. In a group of  marmosets there are separate male and female linear hierarchies, and only  the alpha male and female mate. The subordinate females have low serum LH  and undeveloped ovaries. The mechanism that blocks sexual development is a  scent emitted by the alpha female, as anosmic subordinate females ovulate  normally (unless they have been subordinate for a long time). Subordinate  females with apparatus that administered intermittent subcutaneous doses of  gonadotrophin releasing hormone also ovulated normally.

   Chris Faulkes of the Institute of Zoology described his work on captive  naked mole rats, in which the situation seems to be very similar to the  marmoset, except that it has not been shown conclusively that the 

suppression is effected by a scent from the alpha female. The degree of  suppression is prodigious:  one "queen" may suppress a hundred subordinate  females for as long as fifteen years;  the junior subordinates dig tunnels  and collect roots and tubers which they bring back to the queen in the nest  chamber;  the senior subordinates protect the colony from snakes and other  predators. In the subordinate females the preoptic area of the  hypothalamus is loaded with gonadotrophin releasing hormone (more so even  than the alpha female) but it is not released.

   I think the guinea pig, the marmoset and the mole rat are instructive  examples of subordinate behaviour but I do not think they offer promising  animal models of human depression. Human depression has a long time scale  and a momentum of its own once it has started;  in all the cases described  above the subordinate animals return to normal as soon as they can get away  from the dominant animals. Male guinea pigs whose sexual behaviour has  been suppressed for many months start mating within minutes when put on  their own with a female. And the female marmosets start ovulating straight  away. The suppressed males have motile sperms - this is necessary because  it takes six weeks to manufacture a sperm, whereas ovulation can occur  quickly enough to allow fertilisation from a mating occurring immediately  after release from suppression;  in this way a suppressed couple which  suddenly obtains a territory can achieve a fertile mating without delay. Unlike depression, these rodent forms of subordination are mediated by  olfaction, and the subordination depends on the continued presence of the  olfactory stimulus;  this seems to be true of rodent subordination  generally. In "depressed" dogs and vervet monkeys the behavioural change  is not contingent on the continued presence of a dominant animal. Also, 

the strategy is different in the two cases:  the subordinate rodent is  waiting to get away, and alert for the opportunity to do so. The human  undergoing depressive yielding is learning to adjust to an unfavourable  social situation (lowered social status) and is not alert about anything. My guess is that vertebrates have only one mechanism for making a long-term  behavioural response to an unfavourable situation;  rodents have used this  for responding to unfavourable weather;  primates, and possibly other  orders, have used it for responding to social adversity. But I am probably  wrong, and even if the guess were correct, I think this work on rodent  agonistic behaviour is of great importance for a science of social  behaviour basic to the study of psychopathology, and we should add our  psychiatric voice to the cardiologists and reproductive physiologists who  are supporting it.


1. Sorenson, G. (1987) Stereotyped behaviour, hyperaggressiveness and  "tyrannic" hierarchy induced in bank voles (Clethrionomys glareolus) by a  restricted cage milieu. Progress in Neuro-psychopharmacology and  Biological Psychiatry, 11, 9-21.


2. Leshner, A.I. (1983) The hormonal responses to competition and their  behavioral significance. In Hormones and Aggressive Behavior Ed. by  B.B.Svare. New York:  Plenum Press.