Experience-induced fetal plasticity: the effect of gestational ethanol exposure on the behavioral and neurophysiologic olfactory response to ethanol odor in early postnatal and adult rats

Abstract

Human fetal ethanol exposure is strongly associated with ethanol avidity during adolescence. Evidence that intrauterine olfactory experience influences chemosensory-guided postnatal behaviors suggests that an altered response to ethanol odor resulting from fetal exposure may contribute to later abuse risk. Using behavioral and neurophysiological methods, the authors tested whether ethanol exposure via the dam's diet resulted in an altered responsiveness to ethanol odor in infant and adult rats. Compared with controls, (a) fetal exposure tuned the neurophysiologic response of the olfactory epithelium to ethanol odor at some expense to its responsiveness to other odorants in infantile rats--this effect was absent in adults; (b) the neural effect in infantile rats was paralleled by an altered behavioral response to ethanol odor that was specific to this odorant--this effect was also absent in adults; and (c) a significant component of the infantile behavioral effect was attributable to ethanol's effect on the olfactory neural modality. These data provide evidence for an important relationship between prenatal ethanol experience and postnatal behavioral responsiveness to the drug that is modulated or determined by olfactory function.

Figure 1

Behavioral response to ethanol odor at Postnatal Day 15. The figure illustrates the concentration response curves for ethanol odor, showing the mean (± SE) reflexive sniffing index values as a function of relative odorant stimulus concentration and maternal treatment group (Steps 1, 2, 4, 8, and 16 refer to odorant concentrations of 3.125 × 10⁻³, 6.25 × 10⁻³, 1.25 × 10⁻², 2.5 × 10⁻², and 5 × 10⁻² of vapor saturation at 20 °C, respectively). ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.

Figure 2

Reflexive sniffing index values averaged across ethanol odorant concentrations as a function of sex and maternal treatment. The values represent the mean (± SE) reflexive sniffing index values. ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.

Figure 3

Behavioral response to ethylacetoacetate odor at Postnatal Day 15. The figure illustrates the concentration response curves for ethylacetoacetate odor, showing the mean (± SE) reflexive sniffing index values as a function of relative odorant stimulus concentration (Steps 1, 2, 4, 8, and 16 refer to odorant concentrations of 7.81 × 10⁻⁴, 1.56 × 10⁻³, 3.125 × 10⁻³, 6.25 × 10⁻³, and 1.25 × 10⁻² of vapor saturation at 10 °C, respectively). ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.

Figure 4

Behavioral response to ethanol odor at Postnatal Day 90. The figure illustrates the concentration response curves for ethanol odor, showing the mean (± SE) reflexive sniffing index values as a function of relative odorant stimulus concentration and maternal treatment group (Steps 1, 2, 4, 8, and 16 refer to odorant concentrations of 3.125 × 10⁻³, 6.25 × 10⁻³, 1.25 × 10⁻², 2.5 × 10⁻², and 5 × 10⁻² of vapor saturation at 20 °C, respectively). ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.

Figure 5

Behavioral response to ethylacetoacetate odor at Postnatal Day 90. The figure illustrates the concentration response curves for ethylacetoacetate odor, showing the mean (± SE) reflexive sniffing index values as a function of relative odorant stimulus concentration (Steps 1, 2, 4, 8, and 16 refer to odorant concentrations of 7.81 × 10⁻⁴, 1.56 × 10⁻³, 3.125 × 10⁻³, 6.25 × 10⁻³, and 1.25 × 10⁻² of vapor saturation at 10 °C, respectively). ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.

Figure 6

Relative neural response as a function of odorant and maternal treatment group for the Postnatal Day 15 group. The figure illustrates the mean (± SE) index values for the neural response index. EA = ethylacetoacetate; CA = carvone; HEP = heptanal; E = ethanol; PROA = propyl acetate; ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.

Figure 7

Composite color scale enhanced surface plots for the turbinate mucosa for each maternal treatment group in response to ethylacetoacetate (EA), carvone (CA), heptanal (HEP), ethanol (E), and propyl acetate (PROA). The height of the z-axis corresponds to a change in response for a given odorant at a particular pixel compared with the standard, amyl acetate, for that pixel after the entire array of responses have been equilibrated to a value of 100%. Black-and-white panel (upper left corner) illustrates the turbinate mucosa and the orientation of the response panels. A = anterior; D = Dorsal; ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.

Figure 8

Relative neural response as a function of odorant and maternal treatment group for the Postnatal Day 90 group. The figure illustrates the mean (± SE) index values for the neural response index. EA = ethylacetoacetate; CA = carvone; HEP = heptanal; E = ethanol; PROA = propyl acetate; ET = fetal-ethanol-exposed rats; PF = pair-fed rats; CH = chow-fed rats.