Watching Molly do cartwheels the other day, I discovered a new psychiatric syndrome: somatopsychosis. It’s a very rare condition and she may be the only sufferer largely due to her terrible parent: me.
Most of us are aware of the miraculous power of our minds over our bodies and the inextricable links between psychological problems and physical problems. At the most basic, feeling physically unwell can make us feel sad about not being able to do things we wanted to do, or anxious that we may have a serious or life-threatening illness. Being a medical student was the worst. Reading lists of symptoms of rare neurological diseases was bound to bring on symptoms of blurred vision, pins and needles and lethargy such that a self-diagnosed brain tumour became a convincing reality. Conversely, when we experience bereavement, adversity or tragedy, we often feel it physically as “heartache” or “headache” or “tiredness” and “sleeplessness”. The term “psychosomatic” is basically a fancy way of saying bodily (somatic) symptoms for which there is a psychological (psycho) basis.
Children are no different and due to their immature abilities to identify and express emotions, their propensity to cite psychological problems as physical ones are more frequent. For children, who may have less understanding that psychological problems stem from the head, the gut is the most frequent organ assigned to physical problems. Children who are worried at school may experience genuine stomach aches or constipation which miraculously remit at the weekends and on holidays. For teenagers and adults, the neurological often (but not always) begins to preside with headaches and migraines becoming more prevalent presentations of psychosomatic symptoms.
Psychosomatic symptoms more commonly arise in children who are less able to understand, identify and report their feelings and emotions. Therefore younger children, and children with learning difficulties and or autistic spectrum disorders are more vulnerable. It may also occur in children where reporting feelings and emotions is not possible, discouraged or seen as a sign of weakness or failure. Often children may have experienced past or current physical problems and therefore have a good understanding of how to solicit help or get their needs met for physical problems. Often parents can contribute to symptoms by their own fears and anxieties about their child’s physical health. This is particularly so if the child has a long standing medical condition or has been unwell in the past. Doctors and health professionals can add their own anxieties “of missing a rare disorder” into the mix with repeated investigations and suggested treatments to help uncover and treat an underlying biological basis to problems, and neglect to consider that the underlying problems may be psychological.
If that is the long established thinking on psychosomatic symptoms, what then is my new disorder of “somatopsychosis”? Well, exactly the reverse: psychological symptoms caused by physical ones. This sounds highly unusual, and indeed, Molly is the only recognised case report of this pathological condition that I have just made up. Here is how it works:
Some doctors, like myself (I hope this is the case and I am not an unusually hard-hearted anomaly), have a skewed sense of pain severity due to our dealings with pain at the very severe end. At times it can border on the down-right unsympathetic: when my husband complains of woozy head and sniffles, it’s most definitely man-flu of no significance and he should take Lemsip, go to bed and quit complaining. When an adult patient complains of pain from a blood test, I sometimes mentally think “Come on – it’s a skin prick – I’ve just sewn someone’s entire arm back on!” and don’t let me get started on people that wince in extreme agony from having a blood pressure taken. I am of course professional, kind and sympathetic to my patients, but I am also human, so I hope you will forgive the occasional internal eye-roll at such “wimpish” behaviour.
Unfortunately for my children, professionalism doesn’t wholly apply at home and although broken legs, cuts that are likely to leave scars and high temperatures are met with the usual heightened maternal anxiety (including vivid nightmares of misaligned bones or fractures that disturb the bone growth plates that only people of medical training contemplate) I admit to a general propensity to a lack of sympathy to minor physical pain. As such poor Molly and D have learnt that a grazed knee will earn a dusting off, a quick wound wash, a hug and a wipe of the tears, but then an expectation that the episode is now over and they are to carry on playing. A bumped knee will unlikely earn more than an “Oh dear, you’ll get a nasty bruise” or sometimes, I admit to even worse: “Well, that’s what you get for charging around without looking where you are going.”
As a child psychiatrist on the other hand, identifying and expressing feelings and emotions are a different kettle of fish. From a young age, both children have been encouraged to talk to me about their internal lives, what has worried them at school and all angles are thoroughly investigated and talked through with utmost attention.
It appears that this table-turning of the usual scenario where parents pay immense attention to physical pain and tend to access less of their children’s internal worlds can have its own unhealthy consequences. Here’s what happened:
Molly: Whee! look at me! I can do really good cartwheels now!
Me: You’d better watch out, doing cartwheels on a slippy rug is not the best idea…
Molly: Ouch! [Blubber, blubber]
Me: I told you so.
Molly: You don’t know what a terrible day I had. Girls were being mean to me at school.
Me: [???? What the hell? Where did that come from?]
I had to suppress a smile as I realised what was happening. Molly subconsciously knew that I wasn’t going to give her sympathy for a bumped bottom, but a potential peer interaction problem would give her the comfort and attention she needed at that time of physical pain.
AAARGHH! I have generated somatopsychosis! At least my early recognition of this oddity has reminded me to be more sympathetic to my children and change my ways. I absolutely don’t want her to subconsciously fabricate mental health problems to gain attention. It does go to show though, the frightening power of our day to day words and actions on our children, and the critical importance of what we DO and DON’T give attention and kindness for.
The media is full of the rise of anti-social behaviour (e.g. violence, aggression, bullying, fighting, lying, stealing, vandalism, fire-setting, drug and alcohol abuse, cruelty to animals) in children and youth offending, but what is the cause of childhood antisocial behaviour and are all anti-social children the same? What is the role of parenting?
Are all anti-social children the same?
There is evidence that not all children with anti-social behaviour are the same. Some children may show a phase of anti-social behaviour in adolescence but this passes and they settle down in adulthood. Far more concerning are children with a life-long tendency to anti-social behaviour. These children tend to be anti-social from a younger age and behaviour is more extreme (e.g. cruelty to animals at age 5 years), but even amongst these children there is evidence of different subgroups. Much research is focused on differentiating groups of anti-social children to see if we can better understand them.
One differentiating factor found is lack of empathy. Empathy is the ability to share someone else’s feelings and experiences by imagining what it would be like to be in that person’s situation. Psychologically speaking, this requires two different types of processes: a “thinking” part: the ability to see things from another person’s point of view; and secondly a “feeling” part: the ability to recognise emotion in others and to feel it in oneself. People without empathy are described as being callous and unemotional. To be anti-social, violent or aggressive is easy if you do not empathise with the victim, so it is no surprise that >90% of children with callous-unemotional traits are involved in some form of anti-social behaviour.
How does empathy affect anti-social behaviour?
Researchers have been interested in children that lack empathy for a while now because of its links to extreme anti-social behaviour, and the definition of “psychopathy/ sociopathy” (this is a criminal justice not mental health term) includes having this lack of empathy. The childhood precursor to this psychopathy label is “callous-unemotional traits” (as it is pretty harsh and pessimistic to label kids as psychopaths), and even this terminology has recently been rebranded as “limited prosocial intent” so that it sounds less pejorative; but this is just semantics, we are essentially talking about the same thing: people that have shallow feelings with lack of empathy and guilt.
My colleague, Essi Viding does research into these traits and wrote a great summary paper (2012), the findings of which I wanted to share as I thought it was fascinating. It turns out that if you study ASBO kids (kids with anti-social behaviour), you will find that 50% of them have these callous-unemotional traits. These children don’t really care about others’ feelings and tend to show no remorse for wrong-doing. It is this group of kids that have the most serious and long lasting problems.
What is the difference then psychologically and biologically between children that commit antisocial behaviour with and without empathy?
In experiments where anti-social kids are hooked up to show responses (for instance heart, skin and eye-tracking monitors or brain scans) to photos/ voice recordings of other people in pain or grief, the children with callous-unemotional traits showed no or reduced physical or brain response. Most people will wince in shared pain if shown pictures or exposed to sounds of others in pain, but these children don’t. When these children were asked to play a game where not following the rules led to punishment, they continued to flaunt the rules and did not seem to learn from punishment. There is biological support for these findings with differences in brain scans in areas of the brain linked to emotion processing and reinforcement learning pathways in callous anti-social children.
In contrast, the anti-social children with empathy showed the same aversive responses as children not involved in anti-social behaviour to pictures and sounds of pain and grief, and learnt quickly from punishment. However when they are shown threatening faces, they over-respond with emotion and when they are shown neutral and ambiguous facial expressions, they identified them as being threatening. Brain scans back up these differences. The anti-social children with empathy tended to have abnormal amygdala development. This is the area of the brain involved in fear and anxiety processing. These anti-social children have normal empathy but have a heightened awareness of threat, which explains why they perceive neutral faces as threatening. In a world where everyone is viewed as threatening, hostile or an enemy, it can make sense to be combative, aggressive and violent. This is that bully in the playground that says “Are you looking at me?” – when you weren’t even looking at them.
Genetic studies have also supported this divide, finding that there is strong inheritance of callous nature, whereas anti-social behaviour without callousness was not inherited but generated by environmental factors such as harsh or inadequate parenting, or an interplay between these environmental factors and genes associated with anxiety or heightened emotion.
Finally, it has also been found that the children in the different groups respond differently to parenting strategies. Punishment and traditional sanction-based strategies (time-out, withdrawal of privileges) works well for empathic anti-social children, but has no effect on callous children. Callous children only respond to positive reinforcement (praise) and rewards.
What causes anti-social behaviour?
This type of evidence has led to different theoretical models for two groups of children involved in anti-social behaviour.
Group 1: Genetic predisposition. Antisocial and callous kids: these children are thought to lack empathy as they do not find other people’s distress aversive and because they fail to be able to learn from punishment. It is easy to be aggressive and cruel if you are unable to feel guilt and if the suffering of others doesn’t bother you. It is easy to continue to behave in this way life-long if you are unable to learn from punishment. These difficulties are often inherited in brain structure.
Group 2: Environmental Causation: Anti-social but not callous kids: these children have abnormal socialisation because they have a heightened sense of threat, and view the world as hostile towards them. They exhibit aggression and cruelty as a result of living in unstable and threatening environments which has shaped their brains and psychology to respond in this way as a means of coping and survival. Their anti-social behaviour is often in the context of a peer group within which there is support and empathy.
What has this got to do with parenting?
Whether we like it or not, parents are the first line defence against anti-social behaviour in society. By better understanding the causes of anti-social behaviour and by understanding our children, we can best adapt our parenting to prevent our children becoming anti-social. Although children in group 1 with genetic predisposition are the more difficult to help, they can be supported by fostering self-esteem. They will respond better to motivation to act in a pro-social way, rather than harsh punishment which will not deter them. Anti-social behaviour in children with empathy can be prevented by strong loving families that place appropriate boundaries and sanctions. For these children, wider society has a great role to play in generating or preventing anti-social behaviour, as tolerant, peaceful and accepting societies can offer protection whilst violent, unstable and alienating societies can fuel them.
Anti-social behaviour in children with and without callous-unemotional traits. Viding et al. (2012) Journal of the Royal Society of Medicine. 195-200.
This is the last of the How to improve your child’s success before they are even born series. See Part 1, Part 2 and Part 3. OK, its pretty heavy going on the science, but if you really want to understand anxiety then its worth a read.
Most people are aware that stress and anxiety are not good for pregnant mothers. Even in 400 B.C., Hippocrates espoused the influence of emotions on pregnancy outcomes, leading to a plethora of literary dramas old and new where stress has caused the leading lady to miscarry or go into premature labour. More recently though, following Barker’s theories of foetal adaptation to the mother’s womb environment (see my post How to improve your child’s success before they are even born: Part 3), scientists have found that a mother’s anxiety in pregnancy can influence psychological and behavioural outcomes of her developing foetus over and above those caused by premature delivery. There is now a well-established literature base linking mother’s anxiety in pregnancy to several psychological and psychiatric outcomes in children, including: anxiety, attention deficit hyperactivity disorder (ADHD), cognitive problems, changes in temperament, aggression, conduct problems and even schizophrenia (Beydoun & Saftlas, 2008; Talge et al. 2007; Van den Bergh et al., 2005).
Animals stressed in pregnancy give birth to anxious baby animals
The first evidence for this came from animal studies. Researchers found that rats and monkeys exposed to stress in pregnancy produced offspring that had long-term difficulties with attention, motor behaviour, aggression, memory and showed “hyper-vigilant behaviour” (Van den Bergh et al., 2005). Hyper-vigilant behaviour in animals is a proxy for human anxiety. It incorporates being alert to potential threat with corresponding changes in body systems to prepare to respond to threat. Think about how you would have felt travelling to work on the underground the day after the 7/7 London bombings of 2005, and this is probably a good picture of human “hyper-vigilant” state. Darting eyes on the look-out for suspicious bags with no owner, or people with over-sized back packs, slight tension in muscles, slightly increased heart rate and breathing rate, a little bit more perspiration than usual and if someone were to pop a balloon behind you, you’d probably have been ready to run. Hyper-vigilance is a good thing if you are in a stressful situation. It has served me well on many a walk home from the night-bus stop. If you are continually hyper-vigilant or hyper-vigilant in non-threatening situations like social situations or on aeroplanes; it can be very problematic and is called “anxiety”.
In animals it is easy to experiment and find out what is happening, you can wire animals up to measure muscle tension, heart rates and perspiration fairly unobtrusively. Even better, you can take blood samples and measure the levels of “stress hormone” cortisol. By doing these experiments, scientists have been studying the various effects of maternal stress on animal offspring and among several suspected effects, they have found pretty conclusively that in animals stress in pregnancy causes changes in the development of the foetal stress regulation system, the Hypothalamic-Pituitary-Axis (HPA) re-setting it to be on heightened alert.
How does the body deal with stress? What goes wrong to cause anxiety? – an analogy
What is the HPA-axis? The HPA axis is a collection of parts of the body that communicate by hormones to regulate certain bodily responses, including the stress response. In its function to regulate stress-response, it works pretty much like the emergency fire service. When you see a fire, you pick up the phone and dial 999. This puts you through to a national call centre, where you are asked which emergency service you would like. Once they realise that it is the fire service you need, they contact the regional fire control centre which contacts your local fire brigade which sends out an engine to where you are. The firemen hopefully put out the fire and call back the fire brigade centre to report that the job is done, which then feeds this information back regionally so that the case can be closed. Alternatively, if the fire has gotten out of hand, they can report regionally or nationally depending on the extent of the fire to request more engines to help.
The hypothalamus (a region in the brain) is the national call centre. When the eyes see threat, they alert the hypothalamus. This lets the brain’s pituitary gland, (regional fire control centre) know that there is a threat and a stress response is required. The pituitary communicates with the kidneys (local fire brigade), which then provides the stress response: the steroid hormone cortisol (fire engine). The fire engine goes out to sort the problem. Cortisol does this by going to the heart and making it pump harder, it goes to the lungs and makes it breathe quicker, it goes to the sweat glands and makes them produce sweat, it goes to the muscles and makes them tense and ready for action. All so that you can either fight or flee the threat.
If a city undergoes a heat wave and there is an increased propensity to fires starting and burning out of control. The fire service would probably request more resources on standby and be on heightened alert to send out more engines. More engines than needed might be sent out to small fires to ensure that they did not catch and turn into large fires. This is precautionary and helpful in the short term, but is an over-reaction if continued long term, beyond the time of realistic threat. The same thing happens to our body’s emergency response system. If there is a history of heightened stress, the body responds by increasing the base level of cortisol in the blood stream and increasing the amount of cortisol released in response to stress. This is not a problem if there is continued threat, but if the situation calms down and the body does not down regulate its stress-response system, the result is persistent anxiety.
In animals at least, it has been shown that the animals themselves do not need to have been exposed to stress for their bodies to be placed on heightened alert, they merely have to be exposed to their mother’s heightened alert system in the womb. Thus in animal experiments, giving pregnant mothers injections of cortisol equivalent substances can cause their children to have higher base levels of cortisol and heightened cortisol response when they are born and with continued effect into adult life (Van den Bergh et al., 2005). These animals went on to display a range of long-term behavioural and cognitive impairments. This can be thought of as part of Barker’s hypothesized foetal programming whereby the foetus exposed to high levels of maternal stress hormone predicts a hostile environment and prepares itself by adapting its HPA-axis to best cope with impending fight for survival. Where the resulting environment is actually not that stressful; the HPA-axis is now not working properly and leads to a range of problems.
Who cares about animals? What about humans?
Stressing humans to study anxiety is rather unethical. Shockingly, it used to be allowed and “Little Albert” is a classic case in psychology literature. Little Albert was a 9 month old boy who was not afraid of rats and was given a rat to play with. A dastardly psychologist John B. Watson wanted to see if it was possible to cause a phobia of rats. Every time little Albert touched the rat, a man stood behind him and banged a piece of metal with a hammer making a loud noise scaring little Albert. Needless to say, after a while of this, Albert became afraid of rats and stopped going near them, proving it is possible to induce a phobia. No wonder experimental psychology has a bad name!
These days, we are thankfully not allowed to do such things, but it does mean that extrapolating work from animal studies into humans is harder. We have to rely on stress that occurs naturally in the lives of pregnant women rather than purposefully causing stress in order to study its effects on offspring. Natural and man-made disasters have been used to study the effects of anxiety in pregnancy.
Studies of children who were in the womb of mothers affected by 9/11 showed that these children were born with lower birth weights even though they were born at term, compared to children conceived following 9/11 (Berkowitz et al., 2003). Infants whose mothers were pregnant during the 1998 Canadian ice storm that led to electricity and water shortages for up to 5 weeks scored lower on mental development indices and tests of language development compared to other children, even after taking into account birth complications, birth weight, prematurity and post-natal depression (La Plante et al., 2004).
It is not just extreme stress such as a national disaster that can cause effects. Studies have also used questionnaires asking pregnant mothers about their levels of stress at varying times in their pregnancy and then studied their children at varying ages from newborn to adolescence. In general the link between maternal stress and impaired offspring outcome is borne out, sometimes even with a direct dose-response effect (Beydoun & Saftlas, 2008; Talge et al. 2007; Van den Bergh et al., 2005). Results from different studies vary as each study is different in terms of the stress they are measuring (some studies ask for work stress, bereavement, marital stress, criticism from partners, or just how anxious you feel), the time in pregnancy the stress occurs (studies vary in studying stress in the first, second or third trimester), and the outcome and age of children they are studying (some studies look at language and development in the first year, others look at ADHD symptoms in childhood and yet others look for anxiety and conduct problems in adolescence). Despite this, the majority consensus of all the studies is that there is a significant negative effect of maternal pre-natal anxiety which can have lasting effect. In this way, it is not just your DNA that is biologically influencing your child’s outcome, but environment, via biological mechanisms.This is epigenetics, the new buzz in child psychiatry research.
Interesting finer details
The theory regarding differences in timing effects is that this relates to timing of brain development. Throughout pregnancy the developing foetal brain goes from a neural tube to a baby’s brain which is a complicated journey. Different parts of the brain are forming throughout the 40 weeks, and the effects of insult to the brain at a particular period in pregnancy will depend on the part of the brain that is forming at that time. So for instance, a brain insult (such as anxiety) occurring at the time that the language centres in the brain are forming may lead to language deficits down the line. It is known that the links between pre-natal anxiety and schizophrenia are related only to stress that occurs in the first trimester (Khashan et al., 2008), whilst maternal anxiety experienced in the third trimester is more likely to cause offspring anxiety (O’Connor et al., 2002). Even more interestingly, there appear to be differential effects depending on the gender of the developing foetus, females more likely to develop anxiety, males more likely to be affected by attention, cognitive problems and aggressive tendencies! There is strong evidence for this in animal models and supportive evidence for this from human studies (Glover 2011; Glover & Hill, 2012)
The reason for these different gender outcomes has been thought about from an evolutionary perspective. Historically the female role in species survival in animals and humans has been to bear children and look after them, the male role has been to protect and provide resources. Different skills are required for these different roles. Thus, in a hostile environment, it pays for the mother to be fertile to ensure succession and hyper-vigilant to prey and threat. It pays for the father to go and explore new territory for food and shelter, to take risks to achieve this and to be aggressive enough to fight others for territory and food. In this context, the effect of stress in generating anxiety in females and cognitive impairment and aggression in males can be understood. Hey, in an Armageddon situation I think we would all want rough and tough Bruce Willis at our side not intellectual Stephen Fry.
In animal models it has also been found that stressed out female rats reach sexual maturity earlier, are sexually active earlier, have more offspring but invest less time in the care of each (Meaney, 2007). We have to remember we are talking about rats here, but in humans there is evidence that a harsh early environment (poverty, neglect, abuse) can lead to precocious puberty. You can draw any other rat-human parallels yourself.
The astute amongst you, might be complaining that this is all hogwash and that so many things might be confounding the picture. A confounder is something that can be related to both the purported cause and the outcome. The main ones affecting our current scenario are things like poverty, post-natal depression and maternal educational level. One could argue that a deprived, uneducated mother prone to depression is more likely to experience stress during pregnancy and more likely to have difficulty raising children, thereby causing the psychological deficits seen in their offspring in childhood and adolescence. In animal studies, this is easy to exclude, the new born pups or monkeys are cross fostered so that the mother stressed in pregnancy is replaced once the baby is born by an unstressed mother. Results remain. It is not possible to do this with humans.
In the majority of human studies, known and suspected confounders (social class, post-natal depression, maternal education to name a few) were measured and significant results remained even when these confounders were taken into account. What about the effect of genetics? It is possible to argue that a mother genetically predisposed to anxiety is likely to be anxious in pregnancy and to pass on anxiety genes thereby causing offspring to be anxious. You can see how hard it is to prove anything in science, yet clever research designs continue to come up to try and get to the answers. In a master-stroke of research design now possible due to the frequency of in-vitro fertilisation, Rice (2010) compared, in a cohort of IVF children, the association between prenatal stress and child outcome in those who were genetically related to the mother with those who were not (i.e. receiving egg donation). They found there was an association between mother’s stress in pregnancy and child’s symptoms of anxiety and conduct disorder even in the unrelated mothers.
How does this relate to you and me?
So, how to prevent anxiety in pregnancy? For me, I was smug reaching pregnancy having achieved a stable, loving relationship, stable financial and employment situation and having lived child-free life to the full. I felt I was ready to face pregnancy and motherhood in the best position that I could be in to avoid anxiety. There would have been nothing to stop a loved one being run over by a bus or being faced with infertility problems or illness but, at least the readily controllable variables were answered for.
Things can’t always go as planned though! Typical of most pregnant ladies, the thought of a new bald addition to the family somehow provokes the mental image of bald addition being placed into a beautiful, white cot with pressed linen sheets in a light and bright nursery attached to a south-facing home with wooden floors, modern furniture and period features. Hence in the first trimester of pregnancy Banker and I embarked on a 10 month process of flat hunting, flat offers, flat rejections, flat offer accepted, flat exchange of contracts, flat completion delay, eviction from rental and 2 weeks of homelessness, worldly goods in storage and 2 week enforced holiday in France to avoid sleeping on the street, flat completion, moving in, moving out, flat total remodelling and renovation, all of which no doubt sent the cortisol flying through my placenta!
Here biology and scientific literature come to the rescue again. Thankfully, like all natural miracles, the pregnant body seems to do all it can to protect itself and its prize. It is well known that in the third trimester of pregnancy and for a period post-natally the body dumbs itself right down (Henry & Rendell, 2007). Having for many years prized myself on my amazing memory and lauded it over my husband who seems to have been born with the happy disposition of the forgetful, I became just the same. Misplacing things left, right and centre, but instead of fretting and panicking, just sitting back and saying “Ah, sod it”. During my last week at work, I merrily typed away at a patient’s report only to re-read it to find that it was gobbledegook! Evolutionarily this dumbing down particularly affecting memory impairment is likely to protect against the harmful effects of third trimester anxiety, as well as to help block out the trauma of childbirth so that we become willing victims for another round!
Further, there was a caveat in the maternal anxiety literature! In a review of the literature, Vivette Glover (2011), a fellow North West London resident, describes studies selecting only well-off middle to upper class women in stable circumstances. They found that in this group mild stress in pregnancy had a beneficial influence on child outcome with better mental and physical development of the children and a similar trend for IQ. The suggestion is that in this group of women, a small amount of pre-natal stress may actually enhance foetal brain development. This inverted-U shaped dose-response effect is typical of anxiety and you will be familiar with the idea that a small amount of anxiety helps you sharpen your attention to perform on stage or in an exam, but too much anxiety can cripple your efforts. If Big Sis wins the Nobel Prize, I’ll be remembering to send a bottle of bubbly to my builders for the aptly timed “mild” stress!
References and Influences:
Beydoun H, Saftlas AF. Physical and mental health outcomes of prenatal maternal stress in human and animal studies: a review of recent evidence (2008). Paediatric and Perinatal Epidemiology, 22, 438–466.
Talge, N.M., Neal, C., Glover, V. and the Early Stress, Translational Research and Prevention Science Network: Fetal and Neonatal Experience on Child and Adolescent Mental Health (2007). Antenatal maternal stress and long-term effects on child neurodevelopment: how and why? Journal of Child Psychology and Psychiatry, 48, 245–261.
Van den Bergh, B.R.H., Mulder, E.J.H., Mennesa, M. & Glover, V. (2005). Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neuroscience and Biobehavioral Reviews, 29, 237–258.
Berkowitz, G.S., Wolff, M.S., Janevic, T.M., Holzman,I.R., Yehuda, R., & Landrigan, P.J. (2003). The World Trade Center disaster and intrauterine growth restriction. Journal of the American Medical Association, 290, 595–596.
LaPlante, D. P., Barr, R.G., Brunet, A., Du Fort, G.G., Meaney, M.J., Saucier, J.F., Zelazo, P.R., & King, S. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatric Research, 56, 400–410.
Khashan, A.S., Abel, K.M., McNamee, R., Pedersen, M.G.,Webb, R.T., Baker, P.N., et al. (2008). Higher risk of offspring schizophrenia following antenatal maternal exposure to severe adverse life events. Archives of General Psychiatry, 65, 146–152.
O’Connor, T.G., Heron, J., Golding, J., Beveridge, M., & Glover, V. (2002b). Maternal antenatal anxiety and children’s behavioural/emotional problems at 4 years. Report from the Avon Longitudinal Study of Parents and Children. British Journal of Psychiatry, 180, 502–508.
Glover, V. (2011). Annual Research Review: Prenatal stress and the origins of psychopathology: an evolutionary perspective. Journal of Child Psychology and Psychiatry 52, p 356–367.
Glover, V. & Hill, J. (2012). Sex differences in the programming effects of prenatal stress on psychopathology and stress responses: An evolutionary perspective. Physiology & Behavior 106 (2012) 736–740.
Meaney, M.J. (2007). Environmental programming of phenotypic diversity in female reproductive strategies. Advances in Genetics, 59, 173–215.
Rice, F., Harold, G.T., Boivin, J., van den Bree, M., Hay, D.F., & Thapar, A. (2010). The links between prenatal stress and offspring development and psychopathology: Disentangling environmental and inherited influences. Psychological Medicine, 40, 335–345.
Henry, J.D. & Rendell, P.G. (2007). A review of the impact of pregnancy on memory function. Journal of clinical and experimental neuropsychology, 29 (8), 793–803.
 Interestingly, there appears to be an evolutionarily hard-wired biological predisposition to phobia development to things which are traditionally harmful. Thus, it is easy to induce a phobia for things like rodents, snakes and spiders but very difficult to induce a phobia to cars, guns and knives which are more likely to be a threat in the modern age.
 A dose-response effect is an effect whereby the greater dose of something purported to cause a particular effect, will cause a greater effect. For example, if sun exposure is linked to tanned skin, a dose response effect would mean that more sun exposure leads to a deeper tan. Finding a dose-response effect is good (but not necessarily definitive) evidence that a causal link exists.