Abstract
Hormonal transitions across the menstrual cycle may modulate human reward processing and reinforcement learning, but previous results were contradictory. Studies assessed relatively small samples (n < 30) and exclusively used within-subject designs to compare women in hormonally distinct menstrual cycle phases. This increased the risk of sporadic findings and results may have been disproportionally affected by expectancy effects. Also, replication studies are widely missing, which currently precludes any reliable inferences. The present study was intended as a conceptual replication of a previous study [(1), Neuropsychologia 84; n = 15]. There, we had observed a reduction in avoidance learning capacity when women were in the high estradiol state of the late follicular phase as compared to the mid luteal phase with enhanced progesterone influence. These results conformed to the idea that estradiol and progesterone may antagonistically modulate dopaminergic transmission as a dopamine agonist and antagonist, respectively. Heightened progesterone in the luteal phase thereby supported the ability to learn from the negative outcomes of one's actions, while the follicular rise in estradiol interfered with this capacity. Here, we re-examined the above described within-subject difference between the follicular and the luteal phase in a between-subjects design. Seventy-five women were tested once with a probabilistic feedback learning task, while being either in the follicular (36 women) or luteal phase (39 women), and were compared for phase-related differences in behavior. Secondly, we combined the new data with data from three previous studies from our laboratory that used the same task and menstrual cycle phases. This meta-analysis included only data from the first test day, free of any biasing expectancy effects. Both analyses demonstrated the consistency of the decline in avoidance learning in the follicular relative to the luteal phase. We also showed that this decline reliably occurred in all of the included samples. Altogether, these results provide evidence for the consistency of a behavioral difference and its apparent association with a transient change in hormonal state that occurs in the natural menstrual cycle. Our findings may also open new avenues for the development of reliable between-subjects test protocols in menstrual cycle research.
Highlights
There is an ongoing debate about whether menstrual cycle phase related differences in the concentrations of estradiol and progesterone significantly affect human reinforcement learning and reward seeking behavior as well as the associated neural processes
Most studies in this domain were largely underpowered [n < 30; average sample size = 17 women; (3)] and replication studies are currently lacking. It is unclear whether previous observations in humans were a product of the prevailing publication bias in the cognitive sciences or whether they reflected the relatively strong effects of estradiol and progesterone in the mesocorticolimbic dopamine system that are suggested by animal studies
In female rodents estradiol acts as natural dopamine agonist, which promotes the sensitivity for reward and interferes with the ability to avoid actions that lead to an undesired outcome (4, 5)
Summary
There is an ongoing debate about whether menstrual cycle phase related differences in the concentrations of estradiol and progesterone significantly affect human reinforcement learning and reward seeking behavior as well as the associated neural processes. In line with the rodent evidence, the neuroimaging study by Diekhof and Ratnayake (1) found that women showed a reduced ability to learn from negative feedback in the high estradiol state of the late follicular phase compared to the mid luteal phase, in which progesterone reached its cyclic maximum. Their results were based on the data of 15 young women, who were repeatedly tested. This can be accomplished by testing a larger repetition sample with the same experimental setup as used in the first study [in our example this would have been equivalent to a within-subject design applied to a bigger sample; see Schmidt (13) for discussion and overview]
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