Developmental comparison of sleep EEG power spectral patterns in infants at low and high risk for sudden death

Abstract Power spectral density measured from central cortical EEG recordings during sleep was compared in two groups of 20 infants each at intervals between 1 week and 6 months of age. One group consisted of siblings of infants who had previously died of the sudden infant death syndrome, as determined by history and autopsy report (sibling group). The second group was made up of age, sex and socioeconomically matched infants with no familial history of sudden infant death (control group). All-night, 12 h polygraphic recordings were obtained and classified into sleep and waking states according to established scoring criteria. Left and right bipolar central cortical EEG tracings for continuous 10 min periods were sampled during the first, middle and last quiet sleep (QS) and active sleep (AS) epochs of the night. Sequential 16 sec segments of sampled EEG data were digitized, subjected to FFT, corrected, transformed and sorted in terms of power into adjacent 4 c/sec bands between 0 and 19 c/sec. Statistical evaluation was focused on sample, age and group differences in both QS and AS. Sample effects were noted in both groups and in relation to both sleep states. During QS a consistent increase in power focused at 4–11 c/sec was observed in the first epoch of the night after 8 weeks of age. This emergent ‘time-of-night’ difference was more generalized in left hemisphere and more pronounced at 8 weeks in the sibling group. Evidence cited suggested that this effect could be mediated by a maturing circadian modulation of other physiological systems. Sample effects during AS were present at 1 week and disappeared after 16 weeks of age. This effect, which consisted of a generalized increase in EEG power during the final AS epoch of the night, was observed more extensively over the right hemisphere and was comparable in both groups. Characteristic changes in power occurred within specific frequency bands as a function of age in both groups. During QS primary increments in power were noted in the 0–3 and 12–15 c/sec,bands, the latter preceded by a postnatal decrease. The largest developmental increase in power observed was at 12–15 c/sec, and appeared between 4–8 weeks in siblings and 8–12 weeks in controls. Since this frequency band is associated with the EEG spindle pattern during QS, observed changes were interpreted in terms of the maturation of established thalamocortical substrates for this pattern. Power spectral density changes in AS were minimal, except for the 4–7 c/sec band, which showed changes indicative of a distinctive maturation in certain elements of the EEG frequency spectrum studied here. In quiet sleep differential functions were noted for bands corresponding to the so-called delta (0–3 c/sec) and theta (4–7 c/sec) frequencies labeled initially by Davis et al. (1938). Changes in higher frequency bands were less independent and appeared to be primarily focused in the 12–15 c/sec (sigma) range. In fact, the greatest change registered with age in any frequency band during QS was at 12–15 c/sec, corresponding functionally to the appearance of spindle activity in the sleep EEG. Spectral density changes during active sleep were generally less remarkable, with one exception. Activity at 4–7 c/sec showed a dynamic developmental sequence, similar in many respects to that seen in the 12–15 c/sec band during QS. The similarity between developmental patterns at 12–15 c/sec during QS and 4–7 c/sec in AS is worthy of note. Numerous findings have attributed rhythmic EEG activity in sensorimotor cortex to intrinsic thalamocortical circuits in the somatosensory system. When rhythmic activity is present a ‘gated’ or oscillatory discharge is thought to result from the absence of movement and the corresponding stability of somatosensory afferent discharge (for review see Creutzfeldt 1974). The parallel development of these two rhythmic frequencies in the two different sleep states suggests that both are dependent upon the maturation of similar or perhaps identical thalamocortical connections. Moreover, their presence in either sleep stage may signal a common condition of somatosensory ‘stability’. The different frequencies manifested under this condition could be a result of established differences in thalamic and cortical excitability during the two sleep states. Virtually every EEG power spectral measure obtained in the present study indicated that changes occurred earlier in the sibling group. This outcome was confirmed by both orthogonal and rate-of-change statistical analyses. In relation to the primary developmental characteristics outlined above, the difference can best be described as a 1 month advance in normal developmental sequencing. Several frequency components which peaked or stabilized at 12 weeks of age in the control group did so at 8 weeks in the siblings, particularly in left hemisphere data. Additionally, the key rhythmic EEG frequencies in sleep, namely 12–15 c/sec during QS and 4–7 c/sec in AS, both showed advanced patterns of maturation in the sibling group. The sample effects described above also emerged earlier in the sibling group, at least during QS. This finding is consistent with evidence indicating an earlier circadian effect on autonomic patterns during QS in these infants (Hoppenbrouwers et al. 1980a; Hoppenbrouwers 1981) and supports the conclusion that the EEG sample effect in QS was related to circadian influences. Finally, it should be noted that a new set of changes was documented in siblings between 16 and 24 weeks of age, after a period of relative stability starting at 8 weeks. Control infants showed stability only after 12 weeks of age and generally failed to demonstrate this later shift. Collectively, these findings suggest that central nervous system maturational sequences are accelerated in siblings of SIDS infants. There are several possible explanations for such a conclusion. First, numerous studies have suggested that risk for SIDS is associated with a mild chronic hypoxia beginning early in life and leading to a number of adaptive physiological responses (for review see McGinty and Sterman 1980). The high-risk sibling group studied here showed elevated respiratory and cardiac rates in all states, a greatly reduced incidence of apnea and a variety of other characteristics consistent with this interpretation (Hoppenbrouwers et al. 1980b; Harper et al. 1978, 1981). It is possible that factors directly or indirectly associated with this adaptation result in an acceleration of CNS development. Animal studies have shown clearly that CNS maturation can be altered by both behavioral and similar to those seen for 12–15 c/sec activity in QS. This similarity suggested maturation of a common or parallel substrate. Characteristic changes during AS also appeared earlier in siblings than controls. The observed advance in the appearance of many key developmental features of the sleep EEG among siblings was attributed to accelerated CNS maturation in this group. It was suggested that this acceleration could result either as an adaptive response to a suspected congenial, mild hypoxia in siblings or as a consequence of altered parenting in families who had experienced a sudden infant death.