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 odorants-which 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.

Figure 1.

Filled portions of the arrows under the developmental timeline indicate when the mother of the tested pups ate the flavour-supplemented diet. OR proteins become evident from E12.

Figure 2.

Mean (±s.e.m.) glomerulus volume (µm³), normalized to average weight pup. (a,b) Mothers of ‘control’ pups ate standard flavour chow (light grey bars); mothers of treatment pups ate flavour-supplemented chow (dark grey bars) during gestation, nursing or both. Late nursing mothers ate flavour-supplemented chow for the last 10 days of nursing. Cross-sections of exemplary GFP-tagged glomeruli from each group appear below each bar. Note that there are more OSN axons entering the glomeruli in the treated than the control groups. The scale bar (20 µm) applies to all images.

Figure 3.

Odour exposure elicits odour preferences. Mean (± s.e.m.) proportion of time during a 3 min preference test that pups spent investigating the cherry- and mint-flavoured pellets. Pups that had not been exposed to either flavour showed no preference (grey bars). Pups whose mothers had eaten a flavoured diet (cherry for M71s; mint for M72s) during gestation, nursing or both significantly preferred the flavour their mother ate (dark grey bars) to the novel flavour—mint for M71s; cherry for M72s (light grey bars).