aversive shock by either pressing a lever during the warning
signal or during the shock itself, the total length of stomach
wall erosions was much smaller than in the yoked partner,
which received exactly the same number of shocks, but
could not control them. Also, when a feedback tone was
given after each correct avoidance–escape response, the
amount of gastric ulceration was further reduced. However,
when brief punishment shock was given to the avoidance–
escape and yoked animals whenever an avoidance–escape
was made, then the avoidance–escape group showed more
severe ulcer formation than the yoked partners. Further, in
the absence of informational feedback, a positive correlation
was observed between the number of active coping
attempts and the amount of gastric ulceration.
In line with these results is an observation in Roman high
avoidance (RHA) and Roman low avoidance (RLA) rats,
which can be considered to represent the proactive and
reactive coping style, respectively. It was shown that RHA
rats, after stress of food-deprivation for five days, had more
stomach lesions than RLA rats [52]. A negative correlation
between attack latency in the intruder test and gastric
ulceration induced by restraint-in-water stress [53], also
suggests that animals that prefer a proactive coping style
are more vulnerable to the formation of ulcers during
uncontrollable stress. In rat colonies, dominant animals
that are usually representatives of the proactive coping
style are reported to develop stomach wall erosions when
they have lost their leading position (social outcast) after
frequent attacks by other colony members [15].
Another example of a possible relationship between
behavioral coping characteristics and pathology has been
found in veal calves. It was shown that veal calves fed
only with milk developed tongue-playing as a stereotypy
[54]. However, not all calves did this with the same intensity.
Those calves that developed a lot of oral stereotypies
showed less stomach wall ulcers when slaughtered at 20
weeks of age. However, calves that did not develop
tongue-playing, all had such ulcers at the same slaughter
age [54]. Recently these results were confirmed in a larger
study involving 300 veal calves (van Reenen et al., in
preparation). Also in tethered breeding sows that were
housed individually, two separate groups could be distinguished:
some cows spent up to 80% of their active time in
this behavior while others hardly developed stereotypies.
Surprisingly, the sows that showed less initial resistance
in the back-test were the ones to develop high levels of
stereotypy later on [55]. Recently, it was shown that high
levels of stereotypies are associated with a reduced sympathetic
activation caused by the chronic stress of tethering as
was shown by a decrease in heart rate during bouts of stereotyped
behavior. In this view, stereotypies help the animal to
cope with the adverse situation of tethering [56].
There is increasing evidence that individual animals that
adopt the proactive or reactive coping style differ in
sensitivity of the dopaminergic system and consequently
they may differ in vulnerability to the development of
stereotypies. For instance, in mice, the dopamine receptor
agonist apomorphine produced a greater enhancement of
stereotyped behavior in proactive coping animals than in
reactive coping animals, suggesting that proactive coping
animals may be associated with a more sensitive dopaminergic
system [57]. Similar correlations were found in rat
lines previously selected for high and low expression of
stereotyped behavior (gnawing) in response to apomorphine.
The apomorphine-susceptible rats showed more
proactive coping behavior (fleeing), whereas the apomorphine-
unsusceptible rats showed more reactive behavior
(freezing) in reaction to an open-field [58]. A similar relation
between coping style and stereotypy has been demonstrated
in pigs. Individual proactive (high resistant) and
reactive (low resistant) coping pigs can be distinguished
in the back-test in which the reaction to manual restraint
is measured [59]. Recently it was shown that the high-resistant
pigs have a higher oral stereotypic response (snout
contact-fixation with floor) to apomorphine as compared
to low-resistant pigs [60]. Thus, also in pigs there is a relationship
between coping style, sensitivity of the dopaminergic
system and development of stereotypies. Moreover, it
has been shown that the dopaminergic-sensitivity factor, i.e.
the latency to initiate stereotypic gnawing induced by
apomorphine, also predicted ulcerogenic vulnerability [61].
The underlying mechanism of increased vulnerability of
proactive coping animals to develop stereotypies is not well
understood. Here it is hypothesized that altered HPA-axis
regulation plays a crucial role in the development of stereotypies.
In farm animals it has been suggested that stereotypies
are performed to lower the state of arousal and anxiety
and to lower corticosteroid levels; however, not all studies
show this correlation [62]. A possible explanation for the
conflicting data may be the differential effects of corticosteroid
hormones at the stage when the stereotypy starts to
develop and at the stage when a full-blown stereotypy
continues to exist. It is hypothesized that stress levels of
corticosteroids may enhance the acquisition and expression
of stereotypies, whereas an already developed stereotypy
may reduce corticosteroid levels. This is supported by the
following two examples in rodents. First, amphetamine activates
dopamine pathways and induces stereotyped behavior
(e.g. gnawing) that can be potentiated by high levels of
corticosterone [63]. This suggests that brain glucocorticoid
receptors are involved. Moreover, corticosteroids sensitize
the dopaminergic system, probably through binding to the
glucocorticoid receptors [64]. Second, dopamine-depleting
lesions of the caudate-putamen are associated with a reduction
in stereotyped behavior but an enhanced corticosterone
response [65]. Thus, glucocorticoids via glucocorticoid
receptors may play an important role in the sensitization
of the dopaminergic system. Interestingly, apomorphinesusceptible
rats do differ in glucocorticoid receptor and
mineralocorticoid receptor expression in different brain
nuclei and have higher (and more prolonged) plasma
ACTH and total plasma corticosterone responses than