Effects of in utero odorant exposure on neuroanatomical development of the olfactory bulb and odour preferences

Abstract

Human babies and other young mammals prefer food odours and flavours of their mother's diet during pregnancy as well as their mother's individually distinctive odour. Newborn mice also prefer the individual odours of more closely related-even unfamiliar-lactating females. If exposure to in utero odorantswhich include metabolites from the mother's diet and the foetus's genetically determined individual odour-helps shape the neuroanatomical development of the olfactory bulb, this could influence the perception of such biologically important odours that are preferred after birth. We exposed gene-targeted mice during gestation and nursing to odorants that activate GFP-tagged olfactory receptors (ORs) and then measured the effects on the size of tagged glomeruli in the olfactory bulb where axons from olfactory sensory neurons (OSNs) coalesce by OR type. We found significantly larger tagged glomeruli in mice exposed to these activating odorants in amniotic fluid, and later in mother's milk, as well as significant preferences for the activating odour. Larger glomeruli comprising OSNs that respond to consistently encountered odorants should enhance detection and discrimination of these subsequently preferred odours, which in nature would facilitate selection of palatable foods and kin recognition, through similarities in individual odours of relatives.

Models of Intergenerational and Transgenerational Transmission of Risk for Psychopathology in Mice

“…For example, in utero exposure to a maternal diet supplemented with 'cherry' or 'mint' odors results in the descendant F1 generation showing a preference for those odors. Accompanying this behavioral preference was increased volumes in the olfactory bulbs of the glomeruli that process cherry (M71-expressing olfactory sensory neurons and glomeruli) and mint (M72-expressing cells and glomeruli) (Todrank et al, 2011). In other studies, prenatal exposure to cocaine affected the F1 generation's behavior toward cocaine, as well as dopaminergic neurotransmission and stress responsiveness (Malanga et al, 2007;Wang et al, 2013).…”

Extinction reverses olfactory fear-conditioned increases in neuron number and glomerular size

“…Activity-dependent changes are known to occur both during critical periods of development and also in the adult brain, allowing the animal to optimally perform behaviors based on the demands of the surrounding environment. Postmitotic organizational changes, along with activity-dependent plasticity, have been largely implicated in shaping sensory circuits from development through adulthood (1)(2)(3)(4). In particular, the olfactory sensory system of adult mice exhibits functional and neuroanatomical learning-dependent changes following olfactory fear conditioning in adulthood (5)(6)(7).…”

Epigenetic Risk Factors for Diseases: A Transgenerational Perspective

“…Stress in gestating females can alter the offspring's emotional, social, and cognitive abilities (Weinstock 2008 ;Moisiadis and Matthews 2014 ), in part by altering plasma glucocorticoids or androgens. Exposure to specifi c fl avors or odors can also modulate the olfactory system and taste preference in the offspring (Schaal et al 2000 ;Ong and Muhlhausler 2011 ;Todrank et al 2011 ). In certain bird species, females can load antibodies against encountered pathogens into the eggs' yolk, providing protection to their progeny (Frésard et al 2013 ).…”