Changes in Maternal Behaviour in Response to Hormonal Regulation

Maternal Behaviour
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Dam nursing pup offspring. Source: Rogers, 2013

During pregnancy, the maternal brain undergoes significant changes as a result of hormonal regulation. In response to these changes postpartum, behavioural manifestations of said regulation are produced and are shown to have even further effects in offspring [1][5][7][10]. Studies in animal/human relationship models between mothers and offspring help deepen our understanding of behaviour versus brain plasticity.

1.a Maternal behaviour in animal models

Traits commonly associated with postpartum maternal care are [3-4][6-10]:

  • Maternal aggression against intruders
  • Pup retrieval
  • Nursing position
  • Licking and grooming

Vasopressin, oxytocin, prolactin, and corticotrophin releasing hormone (CRH) are among the most studied hormones that cause behavioural changes. These
hormonal-influences have been implicated in changes of maternal care and aggression within mouse models studying innate anxiety.

1.a.I. Vasopressin

A variant experiment for testing aggressiveness
For maternal defence testing, covariants such as reproductive state
and pup influence are introduced (Bosch et al., 2010c). Source: JoVEJournalVideo, 2014

Vasopressin is the most reviewed in recent studies of maternal behaviour. Its up-regulation has been seen to increase a mother’s aggression when against an intruder in the presence of her pups [4]. Within the central amygdala, vasopressin release is said to increase in response to the presence of an intruder within high anxiety bred (HAB) lactating mice. Due to an increase of vasopressin, attack frequency against an intruder increases as well as a reduction in latency occurs between consecutive attacks. This shows that although a lactating dam’s innate anxiety may be high, these mice are able to disregard natural fear responses in order to protect their pups from danger. Introducing an antagonist for vasopressin suppresses maternal aggression causing attack frequency to decrease. Synthetic vasopressin provided to low anxiety bred mice (LAB) on V1a receptors (intracerebroventricular injection) causes an increase in aggression which is normally not seen. This argues that vasopressin indeed has a causal link with maternal care and aggression.

Other areas of the limbic system and local structures have been seen to an up-regulate neurohormones during the lactation period as well. Naturally the response of behaviours vary alongside the site release/binding occurs at [3-4][6-10].

In the bed nucleus of the strial terminalis (BNST), increased vasopressin expression also occurs during the lactation period of female mice [3]. This correlates with results previously discussed with the central amygdala (i.e increased attack frequency during the maternal defence test) but also accounts for reduced anxiety during open arm tests when mice are exposed to V1a receptor antagonist infusions. In the medial preoptic area (MPOA) vasopressin binding was found to increase during mother-pup feeding. Desensitizing the nipples and allowing them to sensitize throughout feeding showed a trend in which vasopressin binding in the MPOA region decreased and increased in response to the test.

1.a.II. Oxytocin

Oxytocin regulation has been overshadowed by vasopressin in recent years as a regulator of maternal care. It is up-regulated during the lactation period alongside vasopressin and other neurohormones [3].

There have been several contrasting papers as to whether or not oxytocin has a direct effect on maternal care or not. In one study, it was found that oxytocin binding increased during the lactation period in the MPOA, although it did not seem to have any effect on changes in pup licking and grooming or nursing position. In a later study, oxytocin from the MPOA was thought to influence pup licking and grooming through projections directed towards the nucleus accumbens [9]. High dopamine levels correlated strongly with high licking and grooming activity and were shown to be suppressed when oxytocin antagonists were applied. Oxytocin has been studied in pair bonding extensively but is still juvenile in its understanding of effects on maternal care in animal models

1.a.III. Prolactin

Prolactin regulation is important during the lactation period as well. In recent studies, prolactin is seen to up-regulate in the subventricular zone of the hypothalamus [6]. It is thought to be used as a facilitator of neural genesis which in turn stimulates the growth of olfactory neurons. These olfactory inputs in turn send projections to the amygdala and MPOA as well but further research on this pathway has not been established yet.

Pup odors are novel stimuli to a mother’s post-partum level of maternal care. When a prolactin antagonist such as bromocriptine is applied to pregnant mother dams, under stressful conditions these mothers experience longer latency for maternal care due to their increased anxiety. This includes sitting away from their pups and infrequently checking up on them compared to control variables, indicating a loss of quality care.

Prolactin has also been theorized to have effects on hippocampal memory in which the hormone maintains cell survival during stressful situations.

1.a.IV. Corticotrophin-Releasing Factor

Arched Back Nursing in Long-Evans rats
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Arched Back Nursing (ABN) is the most active position
a dam can take during feeding. It denotes a high level
of maternal care (Bosch and Neumann, 2012). Source: Meaney and Zyf, (2005)

Corticotrophin-releasing factor (CRF) is an essential hormone involved in normal stress responses [8]. In one study it was found that introducing an agonist for CRF receptors:

- Impaired arched back nursing
- Reduced maternal aggression

An antagonist such as D-Phenylalanine:

- Decreases innate anxiety (remaining on open arms in an elevated plus maze)

During the lactation period, CRF release from the paraventricular nucleus of the hypothalamus is suppressed as an additional response for maternal care. Although, in said previous study a contrasting position was noted in which CRF remained high within a stream of high anxiety bred mice and was working independent of reproductive state. To account for why lactating mice in this stream did not suppress CRF effects, it has been suggested that vasopressin/oxytocin is able to compensate for the negative activity.

Maternal motivation such as pup retrieval is found to be unaffected possibly due to a deficiency of a CRF receptor or associated binding protein.

1.a.V. Further effects on offspring

Influences of maternal care on offspring have been studied as well. Maternal separation from offspring has been seen to increase levels of aggressiveness in developing mice. Studies show that maternal separation induces more aggressive forms of play fighting in juvenile developing mice [10]. Using maternal separation as an early life stressor, play fighting which is a normal aspect of development in juvenile mice enhances when mice are bred under these conditions. Nape attacks increase between treated mice versus unknown intruders, similar to a maternal defence test. As a result of this, significant correlations of increased plasma corticosterone and vasopressin have been noted to up-regulate only during maternal separation. CRH does not increase collectively with corticosterone when maternal separation is induced but it is up-regulated during play fighting. This suggests that maternal separation induces effects on the hypothalamic-pituitary system at an early level before CRH can be induced. A similar study also suggests that hormone release is region specific as well as time dependent [7]. It was shown that maternal separation interfered with vasopressin and oxytocin receptor binding in several different regions as well as occurring at specific ages of development.

Play fighting in young mice
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Most attack positions involve the nape of the neck.
Source: S. M. Pellis, V. C. Pellis, and D. A. Dewsbury, (1989)

V1a-R binding decrease:

  • Piriform cortex – adolescence and adult age
  • Lateral septum – juvenile age
  • Dentate gyrus of hippocampus – adolescence

Oytocin receptor binding:

a) Decrease:

  • Agranular cortex – adolescence
  • Lateral septum – adult age
  • Caudate putamen – adult age

B) Increase:

  • Medial preoptic area (MPOA) – adolescence
  • Ventromedial hypothalamus – adult age

1.b In human models

During the lactation period, humans have been seen to exhibit similar effects to their animal counterparts in relation to maternal behaviour. In 2011, Holbrook measured the level of aggression in breast feeding women versus formula feeding women and nulliparous women [5]. The study showed that when posed a competitive challenge that not necessarily involved the safety of children, breast feeding women showed a higher level of activity during testing. Women who formula fed or had no significant other were indistinguishable from each other giving strong evidence that aggression is independent of motherhood and is specific to lactation periods. Breast feeding women also had the lowest blood pressure overall between the groups when they themselves were confronted with an aggressive encounter similar to a maternal defence test. The study was limited however due to the inability to test hormone manipulation in vivo, thus no causative effect was deduced.

Further studies show the lasting effects of maternal behaviour on offspring. Bartz et. al found that inducing oxytocin changes nasally into adult males stimulated memories tracing back to whether or not maternal closeness was felt during their childhood [1]. A correlation appeared in which high attachment anxiety compared with low oxytocin levels and low attachment anxiety with high oxytocin levels. Subjects described having a closer feeling with their mothers and being cared for when exposed to a higher dose of oxytocin and arguably the same vice versa. Important to note is that the induced changes did not affect how the person felt at the current time which rules out the possibility of memory alteration. It is hypothesized that oxytocin acts as a primer for memory pathways, which in turn strengthens memories that are closely related to an individual’s own personal ideals and beliefs at the time.

For studies on post-partum-depression (PDD), click on the hyperlink.

1. Bartz, J. A., Zaki, J., Ochsner, K. N., Bolger, N., Kolevzon, A., Ludwig, N., et al. (2010). Effects of oxytocin on recollections of maternal care and closeness. Proceedings of the National Academy of Sciences, 107(50), 21371-21375.
2. Bosch, O. J., & Neumann, I. D. (2012). Both oxytocin and vasopressin are mediators of maternal care and aggression in rodents: from central release to sites of action.., 61, 293-303.
3. Bosch, O. J., Pfortsch, J., Beiderbeck, D. I., Landgraf, R., & Neumann, I. D. (2010). Maternal Behaviour is Associated with Vasopressin Release in the Medial Preoptic Area and Bed Nucleus of the Stria Terminalis in the Rat. Journal of Neuroendocrinology, 22(5), 420-429.
4. Bosch, O. J., & Neumann, I. D. (2010). Vasopressin released within the central amygdala promotes maternal aggression. European Journal of Neuroscience, 31(5), 883-891.
5. Hanh-Holbrook, J., Holt-Lunstad, J., Holbrook, C., Coyne, S. M., & Lawson, E. T. (2011). Maternal Defense: Breast Feeding Increases Aggression by Reducing Stress. Association for Psychological Science, 22, 1288-1295.
6. Larsen, C. M., & Grattan, D. R. (2010). Prolactin-Induced Mitogenesis in the Subventricular Zone of the Maternal Brain during Early Pregnancy Is Essential for Normal Postpartum Behavioral Responses in the Mother. Endocrinology, 151(8), 3805-3814.
7. Lukas, M., Bredewold, R., Neumann, I., & Veenema, A. (2010). Maternal separation interferes with developmental changes in brain vasopressin and oxytocin receptor binding in male rats. Neuropharmacology, 58(1), 78-87.
8. Klampfl, S. M., Neumann, I. D., & Bosch, O. J. (2013). Reduced brain corticotrophin-releasing factor receptor activation is required for adequate maternal care and maternal aggression in lactating rats. European Journal of Neuroscience, 38, 2742-2750.
9. Shahrokh, D. K., Zhang, T. Y., Diorio, J., Gratton, A., & Meaney, M. J. (2010). Oxytocin-Dopamine Interactions Mediate Variations In Maternal Behavior In The Rat. Endocrinology, 151(5), 2276-2286.
10. Veenema, A. H., & Neumann, I. D. (2009). Maternal separation enhances offensive play-fighting, basal corticosterone and hypothalamic vasopressin mRNA expression in juvenile male rats. Psychoneuroendocrinology, 34(3), 463-467.

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