Proximate causes and consequences of intergenerational influences of salient sensory experience.

Abstract

Salient sensory environments experienced by a parental generation can exert intergenerational influences on offspring, including offspring not conceived at the time of the parental experience. While these data provide an exciting new perspective on biological inheritance, questions remain about causes and consequences of intergenerational influences of salient sensory experience. We have previously shown that exposing male mice to a salient olfactory experience like olfactory fear conditioning results in offspring demonstrating a sensitivity to the odor used to condition the paternal generation and possessing an enhanced neuroanatomical representation for that odor. In this study, we first injected RNA extracted from sperm of male mice that underwent olfactory fear conditioning into naive single cell zygotes and found that both male and female adults that develop from these embryos have increased sensitivity and enhanced neuroanatomical representation for the odor (Odor A) with which the paternal male had been conditioned. Next, we found that female, but not male offspring sired by males conditioned with Odor A show enhanced freezing when presented with Odor A after being exposed to a sub-threshold olfactory fear conditioning protocol that consisted of only a single Odor A + shock pairing. Our data provide evidence that RNA found in the paternal germline after exposure to salient sensory experiences can contribute to intergenerational influences of such experiences, and that such intergenerational influences confer an element of adaptation to the filial generation. In so doing, our work suggests that some causes (sperm RNA) and consequences (behavioral flexibility) of intergenerational influences of parental experiences are conserved across experiences as diverse as stressors, dietary manipulations, and sensory experiences.