Mom and apple pie

10 May 2013 by Malcolm Campbell, posted in Biology

“The tie which links mother and child is of such pure and immaculate strength as to be never violated.” Washington Irving (1783-1859)

This weekend, many countries around the world will celebrate Mother’s Day. Countries worldwide, from Brunei to Brazil, Ghana to Greece, Japan to Jamaica, will pay homage to the contribution mothers make in our lives. Other countries celebrate on other days of the year, but the majority will honour motherhood this Sunday.

While motherhood has been around for a while, Mother’s Day is a relatively recent invention. The founding of Mother’s Day is generally attributed to the efforts of Anna Jarvis in the early 20th century. Anna Jarvis was bent on ensuring that the second Sunday of May was set aside for the recognition of one’s mother.

Anna Jarvis was successful in instigating the creation of Mother’s Day, but became dismayed by the commercialisation of the celebration. She felt that her initial notion of properly honouring one’s mother had been trivialised by the mere gifting of a purchased card or candies. She desired something more substantive. In particular, she felt that a written tribute was more aligned with her vision.

I’ve previously written about the incredibly positive influence a mother (and my mother in particular) can have in shaping a person’s life. The tangible things that mothers do to help us progress our lives are plentiful. There are also many less visible things that mothers do that shape our lives. Unwittingly, I had first hand experience with the invisible impact of a mother when my own daughter was an infant.

One morning when my daughter was about 18 months old, with her brother off to pre-school, my daughter and I watched her mom walk away from the house on her way to work. I thought it would be a nice thing to do together, as the start of a father-and-daughter day – “There goes mom, now let’s have some fun!”.

We sat calmly at a second floor window, and watched as her mom gradually disappeared from view. And then things went pear shaped.

As she lost sight of her mom, my daughter burbled out a quiet sob of “mommy”. Within a minute that sob had grown to a full on, continuous wailing stream of “MOMMY! MOMMY! MOMMY!”

I immediately moved into consoling mode – “It’s ok sweetie, we’ll have fun together today” – to no avail. Things that would normally be comforting when her mom was there - back pats, hugs, favourite toys – these had no effect. In fact, I had the distinct impression that any attempt I made at consolation was actually making things worse. The crying seemed much louder, and certainly more pathetic, to the point where I was concerned that the neighbours might think I was engaged in some nefarious form of corporal punishment. A different tack was in order.

Springing into action, I became singer, dancer, clown, whirling dervish, one-man marching band, an ecosystem’s worth of animals – all in a desperate attempt to distract my daughter to get her to stop crying.

Nothing I did would placate her. I was simply not her mother. What she really needed was something that evoked all the positive things she associated with her mother. She needed a whiff of maternal odour.

Perhaps not surprisingly, maternal odour has a profound impact on infant behaviour. This is true across a variety of mammals, including humans, rabbits, mice, rats, dogs and sheep. For example, in newborn mice and rats, maternal odour attracts the neonates to the nipple and induces suckling. This is truly a maternal effect, as the odours of virgin female mice and rats have no effect on the neonates. Remarkably, the suckling-inducing odour is found in the saliva of lactating female mice and rats, and has its effects on the pups within 6-8 hours of birth.

With rabbits, the maternal impact on innate suckling by newborns is pheromone mediated. Pheromones are secreted or excreted molecules that elicit a social response in members of the same species.

Normally, pheromones are perceived through an accessory olfactory system found in mammals, which involves the vomeronasal organ. The vomeronasal organ is located at the base of the nostrils and the roof of the mouth.  The vomeronasal organ is not only physically separated from the main olfactory system in the nose, but it performs a different function in olfaction, namely the detection of pheromones. Neurons in the vomeronasal organ detect pheromones, and transit signals to the brain that shape the perception of other odours, and ultimately change behaviour.

Intriguingly, some experimental evidence suggests that the suckling-inducing pheromone in rabbits is not perceived by the vomeronasal organ. By contrast, the canine version of this pheromone is detected by the vomeronasal organ. In addition, the canine maternal pheromone seems to have effects on dog behaviour that extend beyond infancy.

The canine maternal pheromone has a calming effect on dogs throughout their lifetimes. In fact, a modified version of this pheromone, called dog appeasing pheromone, is an effective treatment of a variety of nervous behaviours in mature dogs, including fear of loud noises, as well as separation anxiety. Separation anxiety can be a particularly acute behavioural problem that some dogs experience when separated from their human companions. Separation anxiety can manifest itself through everything from continuous barking, to floor soiling, to destructive activity. Dog appeasing pheromone can form part of an effective treatment for this particular problem.

In contrast to rabbits and dogs, the mouse suckling scent is not attributable to a simple pheromone. In fact, for mice, mom smells like a complex mixture of volatile compounds. Mice lacking the vomeronasal organ are still able to find the nipple and suckle, while those that lack the ability to smell normal odours can’t.

Like other mammals, human infants are also responsive to maternal odours. Maternal odour induces both innate breast searching and suckling behaviour in neonates. Beyond this, like their canine counterparts, human maternal odour has a calming influence on human neonates, and can be used to reduce crying. In fact, it is so effective at reducing crying that it has been suggested for that purpose in hospital maternity wards.

Importantly, maternal odour seems to reduce infant discomfort during some hospital procedures, including obtaining blood samples through heel pricking. In the presence of maternal odour, neonates were less likely to grimace or cry when a blood sample was taken, in comparison to when the sample was taken in the absence of maternal odour.

Remarkably, it may not be the maternal odour per se, but the familiarity of the odour that has this placating effect. To whit, some of the effects of maternal odour can be mimicked using a chemical, vanillin. As you might suspect based on its name, vanillin is the plant-derived volatile compound that gives vanilla its distinct scent. The odour of vanillin can also reduce the pain experienced by neonates when they receive a heel prick, provided they have smelled the vanillin not long after birth.

In fact, prenatal exposure to an odour may be every bit as important for building comfort with a particular odour as post-natal exposure. For a variety of mammals, from dogs to humans, when pregnant mothers consumed the odour compounds found in anise, but not vanillin, their newborn offspring showed preference for anise. By contrast, the neonates of mothers who had not consumed either anise nor vanillin had no preference for one or the other, and sometimes even a slight aversion for anise.

This is all to say that what your mom ate while you were in utero impacts your odour preferences. The odours you were exposed to, either directly or indirectly, in these early stages of your existence shaped the comfort, or lack thereof, you experience in the presence of particular odours. The comfort provided by mom and apple pie may all be about mom – her odour, and the odour preferences she set you up with.

There’s an important point to be made about odour preference, and odour-induced comfort relative to maternity. That is, both preference and comfort are very much positive perceptions. It is telling that the default perception mode is positive when it is associated with a maternal origin. Just as nothing beats a maternal touch, it may be that nothing beats a maternally-associated odour as well.

In the case of my daughter, it may be that odour won the day. In her inconsolable state, I lay her down on her mom’s pillow. Within seconds, or so it seemed, she was restored to her normal calm self. I assumed she was simply exhausted by the crying, but it is more likely that she was comforted by the scent of a wonderful mother.

References:

Arteaga L et al. (2013) Smell, Suck, Survive: Chemical Signals and Suckling in the Rabbit, Cat, and Dog.  Chemical Signals in Vertebrates 12: 51-59

Goubet N et al. (2007) Familiarity breeds content? Soothing effect of a familiar odor on full-term newborns. Journal of Developmental & Behavioral Pediatrics 28: 189-194

Kim YM et al. (2010) Efficacy of dog-appeasing pheromone (DAP) for ameliorating separation-related behavioral signs in hospitalized dogs. The Canadian Veterinary Journal 51: 380-384

Logan DW et al. (2012) Learned recognition of maternal signature odors mediates the first suckling episode in mice. Current Biology 22: 907-909

Patris B et al. (2013) Suckling Odours in Rats and Mice: Biological Substrates that Guide Newborns to the Nipple. Chemical Signals in Vertebrates 12: 77-85

Rattaz C et al. (2005) The calming effect of a familiar odor on full-term newborns. Journal of Developmental & Behavioral Pediatrics 26: 86-92

Schaal B et al. (2000) Human foetuses learn odours from their pregnant mother’s diet. Chemical senses 25: 729-737

Siracusa C et al. (2010) Effect of a synthetic appeasing pheromone on behavioral, neuroendocrine, immune, and acute-phase perioperative stress responses in dogs. Journal of the American Veterinary Medical Association 237: 673-681

Wells DL & Hepper PG (2006) Prenatal olfactory learning in the domestic dog. Animal behaviour 72: 681-686

Images: All photographs by Malcolm M. Campbell.

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