In the last two decades the study of
grooming has become the subject of extensive
research, primarily because of its usefulness in
modelling hierarchical motor control and because
grooming is structurally organized in a variety
of movements that can be analysed for
identifying rules that govern behavioural
sequencing. This approach may provide insights
into the way the central nervous system controls
chains of rhythmical movements. In addition,
grooming can be produced easily by either novel
environments or water immersion, which makes it
possible to record many bouts of grooming for
long periods.
A variety of evidence suggests that grooming
in a number of vertebrate and invertebrate
species is centrally organized, and that rodents
groom in a cephalo-caudal progression which
resembles the order in which grooming actions
appear in developing animals. The biological
significance of grooming is still not clear,
although studies indicate that it represents a
de-arousal mechanism serving homeostasis,
and is generally considered to be a motor
pattern with adaptive functions beyond the
simple care of fur.
Most ethological studies regarding grooming
have been concerned with the analysis of its
temporal patterning, mainly by the use of two
methods: serial dependence and hierarchical
analysis models, the latter appear to explain
the patterning of grooming better than the
former. Detailed studies in mammals, insects,
and birds have led to the suggestion that
grooming is hierarchically organized, that
grooming movements cluster into anterior and
posterior groups according to body regions, and
that the transition between grooming acts
appears to follow specific rules such as
perseverance and reciprocity.
These studies reveal that many features
of grooming are common to several species, and
that grooming appeared very early in the
evolution of animals. However, some
quantitative aspects of grooming may vary from
one species to another, even within species. For
example, Fentress (1968) found that duration of
grooming differed between two species of voles
after exposure to an overhead moving object,
suggesting varying "optimal arousal" levels
amongst species. Moreover, face grooming
frequency was distinct between two strains of
mice. Berridge (1990) found a similarity in the
patterning of grooming among several species of
rodents. The small differences in duration of
single elements were attributed to phenotypical
(allometric control) or genotypical
(phylogenetic relatedness) aspects. There is
also evidence that aspects, such as grooming
bout length, are distinct in species of American
squirrels, and that these differences may be
attributed to ecological factors, which have
rarely been considered in grooming
analysis.
Grooming and other types of behaviour,
particularly yawning, are elicited by
intracerebroventricularly injected neuropeptides
suggesting that both behaviour patterns share
some of the neural mechanisms involved in their
generation. Yawning, like grooming. is a current
behaviour in many species and has gained the
attention of many investigators. Contrary to
grooming, yawning seems to be an arousal
mechanism that serves to preserve
wakefulness. It has been suggested, however,
that yawning and preening, which is the avian
equivalent of grooming, are comfort patterns
that are related to each other, either
motivationally or functionally. In humans,
yawning has been considered as a stereotyped
action pattern associated with sleeping and
waking. Little is known, however, of what
function yawning may serve or what environmental
circumstances modulate its rate. There is no
further information about the relationship
between grooming and yawning, probably because
in contrast with grooming, yawning can not be
elicited by environ mental manipulations, but
only by the adrninistration of drugs. This makes
it difficult to carry out experiments to assess
which environmental conditions modulate yawning
rates and its relation to other types of
behaviour such as grooming.
In this paper we present a comparative
analysis of grooming in two sublines of
Sprague-Dawley rats
selectively bred for high- (HY) and lowyawning
(LY) frequency. The main advantage of using
these two strains of rats is that it allows us
to assess the effect that yawning has on the
structure of behaviour patterns that are
sensitive to environmental manipulations. Our
study focuses mainly on quantitative aspects of
grooming structure, and because in preliminary
observations we detected that HY rats were more
active than LY rats, we also included open field
tests, which are commonly used for measuring
behaviour believed to be involved in emotional
reactivity. Besides ease of performance, some of
the open field measured behaviour patterns are
sensitive to genetic and experimental
manipulations which reinforce their ecological
validity.[...]
Discussion:
High- and low-yawning Sprague-Dawley rats
differ in many open field and induced-grooming
behaviour patterns. This finding is consistent
with inbred selection studies revealing that
genetic influences are ubiquitous for animal
behaviour. The results of the open field test
show that HY rats are more active than LY rats,
indicating that they are less emotionally
reactive than the latter. This suggestion is
supported by the fact that both groups of rats
varied with respect to ambulation, and to a
lesser extent, defecation, the two most reliable
parameters in open field tests, and in
accordance to current open field behaviour
interpretations. We conclude that the inbred
selection carried out on HY and LY rats appears
to parallel a low and high level, respectively,
of emotional reactivity, and from this we can
predict the existence of an inverse
correlation between yawning frequency and
emotional reactivity. With the present
results we cannot confirm the above-mentioned
hypothesis, in part because we did not record
yawns and in part because the open field test
lasted only 15 min, which is a short period for
yawning behaviour to appear. A corroboration of
this is the suggestion that yawning might
signal the termination of a stressful situation
instead of being present throughout it.
Although we did not find any significant
difference in open field grooming behaviour, it
is possible that the continuous sampling method
we used, was not appropriate to detect
differences in grooming between the two groups
of rats, or that the difference between the
groups was in time engaged in behaviour other
than grooming. These results agree with the
suggestion that in open field tests, grooming
does not seem to be related to indexes of
emotional reactivity.
The analysis of water immersion-induced
grooming revealed that LY rats include more
movements than HY rats in their grooming
sequences. This overall difference indicates
that LY rats perform longer sequences of
grooming, and that they also spend more time in
each sequence of grooming. Of course, it might
be that both HY and LY rats spend the same time
in each sequence of grooming, but with LY rats
performing the task more quickly than HY rats.
Our initial suggestion, however, is supported by
the analysis of grooming transitions, which
indicated that LY rats execute more transitions
between grooming acts. Our results partially
parallel those of other studies suggesting
quantitative differences in grooming behaviour
between different strains of mice or rats.
Despite the quantitative differences in grooming
between HY and LY rats, both groups of rats
groom according to a cephalocaudal progression,
as bas been found by other authors. It should be
noted that this progression also implies that
animals use more acts for grooming their facial
than caudal part. Therefore. there is a
cephalo-caudal progression not only of order but
also of number of grooming movements.
Correspondence analysis revealed that
grooming acts, in both HY and LY rats, are
hierarchically organized. This complex structure
instead of a serial dependence of grooming acts
has been found by other authors and appears to
be a common feature in many species. The
functional implications of this structure have
not been clarified, although it might be that in
terms of costs and benefits it is more
advantageous for an animal to groom by
recruiting several movements and directing them
to specific areas than to groom by executing a
chain of single movements. which would require a
repetitive 'coming and going' mechanism
investing more time and losing efficiency of
grooming. HY and LY rats also groom according to
precise rules: the transitions between grooming
acts depend on anatomical proximity, whereas
their clustering which is the main
characteristic of a hierarchical organization.
requires not onl~ the recruitnient of a number
of acts but also certain degree of transitional
reciprocity between them. This implies thai
clustering of grooming acts does not necessarily
have to be related to anatomical regions as has
been suggested. For instance. our results
indicate that elustering of facial acts include
mouth-sides, which is a movement directed to the
trunk, anatomically far and distinct from the
facial area.
The present study also detected a
quantitative and organizational 'polarization'
of grooming movements between HY and LY rats. LY
rats perform more clustered facial acts. whereas
HY rats engaged in more clustered caudal acts.
This distinct 'syntax' of grooming indicates a
lunetional and neurophysiological
différence between both groups of rats.
If this suggestion is correct it would indicate
that the central nervous system commands
grooming movements in a distinct way for HY and
LY rats. maybe by emphasizing the action of
certain neural structures and inhibiting others.
Also it might be that two neural subsystems
exist for controlling facial and caudal
grooming.
For instance, patterns of locomotion based
on rhythmic movements have been studied in a
number of lower vertebrate groups, revealing an
alternation of muscular activity between head
and tail portions that might be determined
centrally. The findings relating to the
polarization of grooming behaviour between HY
and LY rats opens new possibilities for studying
the underlying neural mechanisms that control
grooming organization. Whether this polarization
is related to a functional significance is not
yet clear, but it is likely that differences in
grooming between HY and LY rats are associated
with other behavioural traits. Concerning this,
results in our laboratory indicate that
spontaneous and pharmacologically-induced
yawning in HY rats is positively correlated with
penile erections. Thus. the 'excessive' caudal
grooming of the HY subline may be related to
sexual function, a conclusion reached by Moore
& Rogers (1984). showing that self-grooming
in young male rats contributes to the maturation
of genitalia. Similarly, the fact that LY rats
have a higher number of body shakes suggests
that this behaviour has an adaptive function. By
performing it repeatedly, animals rid their fur
of a great quantity of water. Accordingly, we
predict that LY rats would dry their body fur in
less time. which is consistent with the finding
that they engage in less caudal grooming.
Therefore, LY rats would direct most of their
grooming behaviour towards facial instead of
caudal areas. This suggestion is consistent with
the results of correspondence analysis of LY
rats that indicate that body shakes and pauses
are closely related, with the latter serving as
transitional elements between facial and caudal
grooming.
The hierarchical organization of grooming of
HY and LY rats also agrees with predictions
derived from the decision-making hypothesis of
Dawkins & Dawkins (1973). HY and LY rats
'decision points' different Dawkins 1973) mainly
at the transition between facial and caudal
grooming. Alternatives of drying distinct parts
of the body may be partially determined at the
level of these decisions points; mouth abdomen
for HY and pauses for LY rats. Although the
structure of grooming behaviour of HY and LY
rats appears to have a strong influence from the
central nervous system. it is also clear that
external factors are involved in their
initiation and termination. In our experiments,
we wet the rats, eliciting the initiation of a
natural sequencing of groommg, which rats
execute to dry their fur quickly and efficiently
because body temperature may drop. Efficient
drying requires a continuous flow of information
between the peripheral and central nervous
system. But once such goal-directed behaviour
bas been displayed, feedback mechanisms should
either switch to other areas of activity or stop
ongoing activity. We would expect that with warm
water, rats also exhibit a natural sequence of
grooming, but complete their drying in less
time. It remains, however, to be discovered
which parts of the central nervous system
command these decisions. Recently, Berridge
& Wishaw (1992) showed that neuronal
structures like the striatum are involved in the
control of the serial order of grooming.
Therefore, HY and LY rats may have endogenous
modifications in the basal ganglia imposed by
selection, and that may explain some of the
differences in grooming sequences that we have
found. Although grooming appears to depend to a
large extent on the influence of the central
nervous system, evidence suggests that it is
also under the control of postural facilitation,
feedback mechanisms, allometric control, and as
our results suggest, strain-specific functional
and neurophysiological aspects.
A crucial question is whether yawning,
grooming and emotional behaviour are
related. Our results show that along with a
high or low frequency of yawning, there are
other traits that altogther separate HY and LY
rats. A possibility is that all these
differences are only side-products of the inbred
selection and that the behavioural heterogeneity
we found between both groups of animals is a
mechanism evolved against homozygocity which
might be disadvantageous for a population. In
this context, small genetic changes may cause
behavioural differences of great importance in
the speciation of animals. A second alternative
is that these differences represent the
separation of behavioural systems, a concept
that makes it possible to explain that a number
of behaviour patterns are related either
functionally or motivationally. The behavioural
system we detected resembles that reported by
Delius (1988). When gulls were disturbed by an
external stimulus, they exhibited a sequence of
behaviour patterns that included preening,
yawning and sleeping, suggesting that when there
is a change in the ongoing arousal level,
animals display a set of behaviour patterns
leading to restore the previous state of
arousal. In mammals, yawning has been
associated with transitions between waking and
sleeping, and after exposure to stressful
situations whereas grooming is believed to be
involved in decreasing an enhanced arousal.
Therefore, both types of behaviour seem to be
associated with changes of ongoing arousal. It
might be that the selection carried out on HY
and LY rats also separated those types of
behaviour that are associated with specifical
thresholds of arousal. Because of the obvious
advantages of having a high yawning strain, the
majority of the studies in our laboratory have
focused on them, and preliminary results have
revealed that HY rats in a novel environment,
other than an open field cage, show increased
grooming followed by yawning and sleeping
(unpublished data), confirming the observation
of Delius (1988). Further results are necessary
to confirrn these hypotheses, but we believe
that with this initial approach, new insights
are gained about yawning, grooming and their
relationship.
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