Parental olfactory experience influences behavior and neural structure in subsequent generations

Abstract

Using olfactory molecular specificity, we examined the inheritance of parental traumatic exposure, a phenomenon that has been frequently observed, but not understood. We subjected F0 mice to odor fear conditioning before conception and found that subsequently conceived F1 and F2 generations had an increased behavioral sensitivity to the F0-conditioned odor, but not to other odors. When an odor (acetophenone) that activates a known odorant receptor (Olfr151) was used to condition F0 mice, the behavioral sensitivity of the F1 and F2 generations to acetophenone was complemented by an enhanced neuroanatomical representation of the Olfr151 pathway. Bisulfite sequencing of sperm DNA from conditioned F0 males and F1 naive offspring revealed CpG hypomethylation in the Olfr151 gene. In addition, in vitro fertilization, F2 inheritance and cross-fostering revealed that these transgenerational effects are inherited via parental gametes. Our findings provide a framework for addressing how environmental information may be inherited transgenerationally at behavioral, neuroanatomical and epigenetic levels.

Effect of high fat diet on paternal sperm histone distribution and male offspring liver gene expression

“…17 A diet poor in folate induced DNA methylation changes in the sperm and alterations of gene expression in the placenta. 47 Using odor-induced fear conditioning in male mice, it was found that offspring also had enhanced sensitivity to the same odor, which was associated with hypomethylation at a specific olfactory receptor gene 48 . Induction of a pre-diabetic state in fathers (feeding a high fat diet in combination with streptozotocin injection) altered pancreatic gene expression pattern in male offspring.…”

Extracellular RNA is transported from one generation to the next in Caenorhabditis elegans

“…Molecules that can cross generational boundaries can cause apparent intergenerational effects. Exposure to some chemicals can cause multigenerational effects in mammals [e.g., endocrine disruptors (45) or odors (46)]. Examination of how many generations the molecules used to trigger a response persist within an animal could inform mechanisms underlying multigenerational effects.…”

L’expérience sensorielle et nutritionnelle des parents et leur état métabolique orientent le comportement alimentaire de leur descendance

“…En ce qui concerne les macronutriments, la consommation de protéines et de lipides chez des enfants de 10 ans est corrélée à la consommation de ces mêmes nutriments par leur mère pendant la grossesse [24]. Bien qu'encore limités et partiels, ces résultats soulignent la possibilité de traces stables de l'expérience chimiosensorielle précoce chez génome des spermatozoïdes du gène Olfr151 codant les récepteurs olfactifs M71 [37]. Enfin, le comportement alimentaire est indissociable des rythmes circadiens et des horloges internes (cérébrale, tissulaire) correspondant à des systèmes moléculaires complexes sensibles aux apports éner-gétiques.…”