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
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
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.