Neuroendocrine control of maternal behaviour in birds
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Date
29/06/2019Author
Aleksandrova, Yana
Metadata
Abstract
Maternal behaviour in humans and animals promotes the survival and future
success of offspring. It is mainly controlled by the brain behaviour network in
the hypothalamus. The behavioural and physiological changes which occur
when an animal ‘becomes maternal’ are significant and include the cessation
of reproductive behaviours and often a modulation of the stress response,
energy balance and aggression. While the mammalian maternal brain has
been extensively studied, much less is known in birds. This PhD project
aimed to investigate the peptides and neuroendocrine pathways which
govern the onset and maintenance of avian maternal care.
In the mammalian brain, maternal behaviour and other social behaviours are
regulated by the nonapeptides oxytocin and vasopressin, which are also
involved in the stress response and water balance. The oxytocin and
vasopressin orthologues in birds and reptiles, called mesotocin and
vasotocin, are very similar in structure and perform similar roles. However,
very few studies have focussed on their involvement in maternal care. In the
experiments presented in this thesis, it was found that mesotocin mRNA
expression was higher in the paraventricular nucleus (PVN) of hens rearing
chicks than in laying hens as early as the first day of rearing, suggesting the
involvement of mesotocin in rearing in the chicken. In a subdivision of the
lateral bed nucleus of the stria terminalis (BnSTl), mesotocin mRNA
expression was lower during incubation, compared to laying and rearing,
while vasotocin mRNA expression was lower in both incubating hens and
hens on the first day of rearing, compared to layers. This differed from the
expected results, as data from previous studies suggested that mesotocin in
the medial BnST (BnSTm) of birds promoted maternal behaviour. Even
though, to the knowledge of the author, the lateral sector of this nucleus had
not been separately examined in this context prior to this project, results
were expected to be similar, as the medial and lateral BnST are closely
related and often examined together. It was speculated that the changes in
the BnSTl which were observed could be connected to a possible decrease
in social interactions in chickens during incubation. Incubating hens very
rarely leave the nest and actively discourage others from approaching it. This
could theoretically lead to fewer interactions with their conspecifics.
However, no formal measurement of sociality and social interactions was
performed during this project and, since the chickens in the relevant
experiment were housed in pairs with both birds often entering incubation at
roughly the same time, it would have been difficult to judge what their
behaviour would have been if the rest of the flock had been present. A
measurement of social interaction should be included in further experiments
investigating the significance of nonapeptide changes in the BnSTl during
incubation.
With regards to vasotocin, it was speculated that the lower mRNA expression
during incubation in the BnSTl could be related to an attenuated stress
response in maternal birds. This suggestion was based on previous studies
in other avian and mammalian species which have shown that parental
animals can have lower responsiveness to stress. However, the stress
response was not measured in this study and future work is necessary to
determine whether it is indeed attenuated in the chicken under these
conditions.
In order for maternal behaviour to take place, sexual behaviours need to be
inhibited. Gonadal steroids, which control sexual behaviours, have been
shown to interact with nonapeptides in the brains of mammals and birds, but
these interactions are complex, context-dependent and not fully understood.
The results of this project showed that acute treatment with certain sex
steroids after a period of priming was capable of significantly increasing the
expression of mesotocin or vasotocin mRNA in specific areas of the brain
behaviour network. In both the PVN and BnSTl, testosterone but not its
metabolite estradiol increased mesotocin expression, suggesting that the
action of testosterone on mesotocin was direct. Vasotocin expression was
increased only in the BnSTl by both testosterone and estradiol, suggesting
that the action of testosterone on vasotocin in this brain area was likely
achieved through estradiol, following the aromatisation of testosterone.
Gonadotropin inhibitory hormone (GnIH) is produced in the hypothalamus
and has a strong inhibitory effect on the reproductive axis. GnIH shows
significant changes throughout the reproductive cycle in the brains of both
mammals and birds. After examining the changes in GnIH throughout the
hen reproductive cycle, it was found that hens on the fourteenth day of
incubation had a significantly higher number of GnIH-immunoreactive cells in
the PVN compared to laying hens. These results were in agreement with
previous findings and suggested that GnIH may be involved in
downregulating reproductive behaviours during incubation.
The hormone prolactin is involved in maternal care in mammals and birds
and it is important in incubation and rearing. It is known to be controlled by
the dopaminergic system through the D1 dopamine receptor (D1, D1R),
which promotes, and the D2 dopamine receptor (D2, D2R), which inhibits its
expression. In this project, quantitative polymerase chain reaction (qPCR)
was used to measure prolactin and D2 mRNA in the pituitary glands of hens
throughout the reproductive cycle, from laying eggs through to the first day of
rearing chicks. No changes in mRNA expression for either prolactin or D2
were observed, suggesting that changes in their mRNA expression in the
pituitary gland are not crucial for the display of incubation and rearing. It is
possible that other mechanisms contribute strongly to the increase in plasma
prolactin during incubation.
Apart from controlling prolactin, dopamine is also involved in maternal and
other social behaviours, such as sexual behaviour, social approach, social
attachment, social dominance and aggression. Other monoamines, including
serotonin (5-hydroxytryptamine, 5-HT), noradrenaline and adrenaline have
also been implicated in social interactions, including aggression and
maternal behaviour. All of these monoamines are present in the raphe
nucleus but, to the author’s knowledge, the changes in their concentrations
in this brain area throughout the reproductive cycle from egg-laying through
to chick-rearing had not been characterised in birds prior to this project.
Liquid chromatography - mass spectrometry (LC-MS) was used to examine
the concentrations of monoamines in the raphe nucleus of the female
chicken throughout the reproductive cycle and test the hypothesis that they
might be involved in maternal care in this species. No differences were found
between groups for any of the examined monoamines, which included
adrenaline, noradrenaline, dopamine, 5-HT, the dopamine precursor
dihydroxyphenylacetic acid (DOPAC), the 5-HT precursor tryptophan and
tryptophan’s metabolite hydroxyanthranilic acid.
These results do not provide any evidence that monoamines in the raphe
nucleus play a role in incubation or rearing in the chicken. However, as only
monoamine content rather than release was measured, a role mediated by
differences in release cannot be excluded. In addition, limitations of the
experimental procedure mean that results from this experiment should be
interpreted with caution.
Many animals display negative responses to the young of their species when
not in a maternal state but habituation to young individuals can often alter
these behaviours and produce a maternal response. The display of maternal
care induces c-fos (an immediate early gene, marker of neuronal activation)
expression in brain areas controlling the behaviour. The effects of social
stimulation with chicks vs adults were tested in Japanese quail. The change
of species from chicken was necessary due to unforeseen issues at the
Roslin Institute Poultry Unit which led to the loss of the existing colony of
maternal chickens. Unfortunately, despite many efforts, the colony could not
be replaced in time for the aforementioned experiment to be conducted on
the original species of choice. Japanese quail were the best replacement
species the author had access to. While they rarely incubate eggs in
captivity, they do display rearing behaviour, in addition to also being
precocial, like the chicken, and having physiology and brain organisation
similar to chickens.
It was found that adult female Japanese quail habituated to chicks for 6 days
spent significantly more time in close proximity to novel chicks compared to
novel adult individuals and stimulation with chicks caused greater c-fos
expression than stimulation with a novel adult in a brain area related to
maternal and other social behaviours (the PVN) and, surprisingly, an area
related to sexual behaviour (the nucleus of the commisurae pallii, nCPa).
What type of cells were activated remains unclear and sexual behaviour was
not tested for. In contrast, c-fos expression was lower in the group presented
with chicks in the raphe nucleus – an area known to be involved in maternal
behaviour, as well as stress. It can be speculated that, after habituation,
chicks may have induced the beginning of maternal behaviour in females
(and therefore higher activation in PVN neurones). They may have also
presented a less stressful stimulus than a new adult (inducing less activation
in the raphe nucleus). However, full maternal behaviour was not observed
within the scope of this experiment and stress was not measured. Therefore,
further studies are necessary to examine the significance of these brain
areas in interactions with chicks, including determining what type of
neurones were being activated.
This thesis presents an overview of the changes throughout the reproductive
cycle in some major hormones of the brain behaviour network and examines
their possible roles in maternal behaviour through specific brain nuclei. It
provides evidence for the involvement of the mesotocin/vasotocin and GnIH
systems in the control of maternal care in birds and sheds more light on the
complex relationship between sex steroids and the brain nonapeptides. The
findings presented here contribute to the areas of neuroscience, physiology,
developmental biology and endocrinology.