Abstract
BackgroundThere are lingering concerns about caffeine consumption during pregnancy or the early postnatal period, partly because there may be long-lasting behavioral changes after caffeine exposure early in life.Methodology/Principal FindingsWe show that pregnant wild type (WT) mice given modest doses of caffeine (0.3 g/l in drinking water) gave birth to offspring that as adults exhibited increased locomotor activity in an open field. The offspring also responded to cocaine challenge with greater locomotor activity than mice not perinatally exposed to caffeine. We performed the same behavioral experiments on mice heterozygous for adenosine A1 receptor gene (A1RHz). In these mice signaling via adenosine A1 receptors is reduced to about the same degree as after modest consumption of caffeine. A1RHz mice had a behavioral profile similar to WT mice perinatally exposed to caffeine. Furthermore, it appeared that the mother's genotype, not offspring's, was critical for behavioral changes in adult offspring. Thus, if the mother partially lacked A1 receptors the offspring displayed more hyperactivity and responded more strongly to cocaine stimulation as adults than did mice of a WT mother, regardless of their genotype. This indicates that long-term behavioral alterations in the offspring result from the maternal effect of caffeine, and not a direct effect on fetus. WT offspring from WT mother but having a A1R Hz grandmother preserved higher locomotor response to cocaine.Conclusions/SignificanceWe suggest that perinatal caffeine, by acting on adenosine A1 receptors in the mother, causes long-lasting behavioral changes in the offspring that even manifest themselves in the second generation.
Highlights
Caffeine (1,3,7-trimethylxanthine) is a widely consumed psychoactive substance that is readily available through several dietary products
Conclusions/Significance: We suggest that perinatal caffeine, by acting on adenosine A1 receptors in the mother, causes long-lasting behavioral changes in the offspring that even manifest themselves in the second generation
We found that some effects of perinatal exposure to caffeine were mimicked in mice heterozygous for adenosine A1 receptors, which have half the normal number of such receptors
Summary
Caffeine (1,3,7-trimethylxanthine) is a widely consumed psychoactive substance that is readily available through several dietary products (coffee, tea, cocoa beverages and chocolate bars). Human and animal studies have shown that high caffeine intake represents a risk for adverse pregnancy outcomes and teratological consequences in offspring [4,5]. There are many animal studies on the effect of caffeine intake by dams, and often rather high doses of this substance (.50 mg/kg) have been studied. At low to moderate doses (50 to 300 mg, i.e. 1 to 3 cups of coffee), caffeine induces a central stimulation in humans, eliciting feelings of wellbeing, alertness, energy and ability to concentrate. The subjective effects induced by caffeine at higher doses (300 to 800 mg) are characterized by negative feelings such as anxiety, nervousness and insomnia, a condition sometimes referred to as ‘‘caffeinism’’ [6]. There are lingering concerns about caffeine consumption during pregnancy or the early postnatal period, partly because there may be long-lasting behavioral changes after caffeine exposure early in life
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