Behavioral State Organization in Human Term Fetuses: Evidence of Relatively Tight Control of State Cycling

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Abstract
Repeated alterations in episodes of quiet sleep (QS) and active sleep (AS) is a basic feature of behavioral state organization in human fetuses. Activation of the reticular formation (RF) is important in the transition from QS to AS, and intrinsic changes in central nervous system (CNS) activity govern RF activation. Vibroacoustic stimulation (VAS) can alter RF activation and thus delay the occurrence of QS. We hypothesize that if intrinsic RF activation in human fetuses is greatest just after entering AS and is decreasing as an AS-to-QS transition is approached, then fetuses ought to be in an active period longer if stimulated just after entering AS than if stimulated closer to an AS-to-QS transition. The purpose of this study was to test this hypothesis. We examined 87 normal human fetuses between 37 and 41 weeks of gestation. Behavioral states were assigned based on fetal heart rate pattern and the presence or absence of fetal eye and gross body movements. All fetuses were observed to enter AS before being randomized to a particular group. After remaining in AS for 3 min, the fetus either was not stimulated (N = 30), received a single 1-s VAS after 3-5 min of AS (N = 30), or received a single 1-s VAS after 44-46 min of AS (N = 27). Heart rate and eye and body movements were monitored continuously until the fetus either returned to QS and remained in that state for 3 min or did not return to QS within 60 min. All 57 fetuses who were stimulated in AS responded to VAS with gross body movement and an increase in heart rate, indicating that there was no effect of prestimulus state duration on the sensitivity to VAS. Fetuses stimulated after 3-5 min of AS behaved similarly to fetuses who had entered AS spontaneously. However, fetuses who were stimulated after being in AS for 44-46 min remained in an active period for a significantly shorter length of time following VAS than fetuses who either had been in AS for 3-5 min before VAS (19.6 min versus 36.4 min, P = 0.0001) or had entered AS spontaneously (19.6 min versus 44-2 min, P = 0.0001). When we included our results from a previous study examining state organization following VAS delivered in QS, we found that stimulation of the fetus around the time of a spontaneous AS-to-QS transition elicited a significantly different behavioral response than VAS delivered around the time of a spontaneous QS-to-AS transition: regardless of whether fetuses were in AS or QS at the time of stimulation, fetuses who were stimulated in close proximity to an AS-to-QS transition returned to QS sooner than fetuses who were stimulated closer to a QS-to-AS transition (18.7 min versus 37.2 min, P = 0.0001). We conclude that underlying changes in CNS activity, which continue to occur in the absence of overt behavioral changes, place relatively strict requirements on the amount of AS and QS during fetal life.

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