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Maternal Programming of Defensive Responses 159was seen in adolescent VFD-reared animals. It will be fascinating to see whetherthese traits are then transmitted to the next generation.A critical issue here is that of the effect of environmental adversity on maternalbehavior. One might well wonder how variations in maternal behavior in the ratmaintained in the constancy of laboratory animal housing fit within such a model.Indeed, the variations in pup licking/grooming described above occur in the presenceof a rather stable environment (at least physically). We think that the explanationfor this apparent paradox lies in the relation between anxiety and maternalbehavior (Fleming, 1999; Francis et al., 2000; Meaney, 2001). In humans andlaboratory rats, anxiety predicts maternal sensitivity to pups; indeed, Fleming(1988) argued that among human females, anxiety was the best predictor of maternalsensitivity to her infant. This idea is consistent with several clinical studiessuggesting that environmental stressors alter human parental behavior througheffects on mood and general emotional well-being (see above). Importantly, LowLG-ABN mothers are significantly more fearful than are High LG-ABN dams(Francis et al., 2000).If this idea has merit, then chronic stress, which renders laboratory rats moreanxious, should alter maternal behavior. Female rats exposed to stress during pregnancyshow increased retrieval latencies (Fride et al., 1985; Kinsely et al., 1988;Moore & Power, 1986), a finding that would seem to reflect an effect of stress onmaternal responsivity. Gestational stress in the rat decreases the frequency of puplicking/grooming during lactation (Champagne & Meaney, 2000; Smythe et al.,2004). We examined the effect of such gestational stress on maternal behavior inHigh and Low LG-ABN mothers (Champagne & Meaney, 2006). Females previouslycharacterized as High or Low LG-ABN mothers with their first litter wereexposed to restraint stress during the last half of gestation or to control conditions.Gestational stress decreased the frequency of maternal LG with the secondlitter in the High but not in Low LG-ABN mothers. Thus, a stressfulenvironmental signal during gestation was sufficient to completely reverse the patternof maternal behavior in High LG-ABN mothers. The maternal behavior ofHigh LG-ABN mothers exposed to gestational stress during an earlier pregnancywas indistinguishable from that of Low LG-ABN mothers. And of course theseeffects on maternal behavior are apparent in the development of the offspring. Asadults, the offspring of High LG-ABN/gestationally stressed mothers were comparableto those of Low LG-ABN dams on measures of behavioral and HPA responsesto stress.Effects on offspring in these studies might be associated with classic “prenatalstress” effects, because these animals were in utero during the imposition of thestressor. To address this question, we examined the offspring of a subsequentpregnancy over which time no experimental manipulations were imposed. As itturns out, the effects of gestational stress during the second pregnancy were apparentwith a subsequent, third litter, even in the absence of any further stress.