Overnight changes in the slope of sleep slow waves during infancy.

STUDY OBJECTIVES Slow wave activity (SWA, 0.5-4.5 Hz) is a well-established marker for sleep pressure in adults. Recent studies have shown that increasing sleep pressure is reflected by an increased synchronized firing pattern of cortical neurons, which can be measured by the slope of sleep slow waves. Thus we aimed at investigating whether the slope of sleep slow waves might provide an alternative marker to study the homeostatic regulation of sleep during early human development. DESIGN All-night sleep electroencephalography (EEG) was recorded longitudinally at 2, 4, 6, and 9 months after birth. SETTING Home recording. PATIENTS OR PARTICIPANTS 11 healthy full-term infants (5 male, 6 female). INTERVENTIONS None. MEASUREMENTS AND RESULTS The slope of sleep slow waves increased with age. At all ages the slope decreased from the first to the last hour of non rapid-eye-movement (NREM) sleep, even when controlling for amplitude differences (P < 0.002). The decrease of the slope was also present in the cycle-by-cycle time course across the night (P < 0.001) at the age of 6 months when the alternating pattern of low-delta activity (0.75-1.75 Hz) is most prominent. Moreover, we found distinct topographical differences exhibiting the steepest slope over the occipital cortex. CONCLUSIONS The results suggest an age-dependent increase in synchronization of cortical activity during infancy, which might be due to increasing synaptogenesis. Previous studies have shown that during early postnatal development synaptogenesis is most pronounced over the occipital cortex, which could explain why the steepest slope was found in the occipital derivation. Our results provide evidence that the homeostatic regulation of sleep develops early in human infants.

[1]  Giulio Tononi,et al.  Characteristics of sleep slow waves in children and adolescents. , 2010, Sleep.

[2]  M. Steriade,et al.  Natural waking and sleep states: a view from inside neocortical neurons. , 2001, Journal of neurophysiology.

[3]  G. Tononi,et al.  Sleep function and synaptic homeostasis. , 2006, Sleep medicine reviews.

[4]  G. Tononi,et al.  Molecular and electrophysiological evidence for net synaptic potentiation in wake and depression in sleep , 2008, Nature Neuroscience.

[5]  M. Steriade,et al.  A novel slow (< 1 Hz) oscillation of neocortical neurons in vivo: depolarizing and hyperpolarizing components , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[6]  H. Bastuji,et al.  Sleep ontogenesis revisited: a longitudinal 24-hour home polygraphic study on 15 normal infants during the first two years of life. , 1997, Sleep.

[7]  Giorgio F. Gilestro,et al.  Widespread Changes in Synaptic Markers as a Function of Sleep and Wakefulness in Drosophila , 2009, Science.

[8]  P. Achermann,et al.  Mathematical models of sleep regulation. , 2003, Frontiers in bioscience : a journal and virtual library.

[9]  Sean L. Hill,et al.  Sleep homeostasis and cortical synchronization: I. Modeling the effects of synaptic strength on sleep slow waves. , 2007, Sleep.

[10]  A. Borbély,et al.  Sleep regulation in rats during early development. , 1990, The American journal of physiology.

[11]  T. Anders,et al.  Developmental course of nighttime sleep-wake patterns in full-term and premature infants during the first year of life. I. , 1985, Sleep.

[12]  M. Sterman,et al.  Quantitative analysis of infant EEG development during quiet sleep. , 1977, Electroencephalography and clinical neurophysiology.

[13]  Marcello Massimini,et al.  Sleep homeostasis and cortical synchronization: III. A high-density EEG study of sleep slow waves in humans. , 2007, Sleep.

[14]  P. Achermann,et al.  Development of the nocturnal sleep electroencephalogram in human infants. , 2004, American journal of physiology. Regulatory, integrative and comparative physiology.

[15]  O Benoit,et al.  Nocturnal sleep organization during the first months of life. , 1982, Electroencephalography and clinical neurophysiology.

[16]  P. Achermann,et al.  Slow oscillations in human non‐rapid eye movement sleep electroencephalogram: effects of increased sleep pressure , 2010, Journal of sleep research.

[17]  H Schulz,et al.  The distribution of slow-wave sleep across the night: a comparison for infants, children, and adults. , 1991, Sleep.

[18]  P. Huttenlocher,et al.  Regional differences in synaptogenesis in human cerebral cortex , 1997, The Journal of comparative neurology.

[19]  P. Huttenlocher Morphometric study of human cerebral cortex development , 1990, Neuropsychologia.

[20]  G. Tononi,et al.  Local sleep in awake rats , 2011, Nature.

[21]  P. Achermann,et al.  Exposure to pulsed high‐frequency electromagnetic field during waking affects human sleep EEG , 2000, Neuroreport.

[22]  Sean L. Hill,et al.  The Sleep Slow Oscillation as a Traveling Wave , 2004, The Journal of Neuroscience.

[23]  A. Borbély A two process model of sleep regulation. , 1982, Human neurobiology.

[24]  Giulio Tononi,et al.  Sleep and Synaptic Homeostasis: Structural Evidence in Drosophila , 2011, Science.

[25]  Jakob Heinzle,et al.  Impaired slow wave sleep downscaling in encephalopathy with status epilepticus during sleep (ESES) , 2011, Clinical Neurophysiology.

[26]  G. Tononi,et al.  Cortical Firing and Sleep Homeostasis , 2009, Neuron.

[27]  G. Tononi,et al.  Sleep homeostasis and cortical synchronization: II. A local field potential study of sleep slow waves in the rat. , 2007, Sleep.

[28]  Post-natal development of sleep organization in man: speculations on the emergence of the ‘S process’ , 1992, Neurophysiologie Clinique/Clinical Neurophysiology.

[29]  P. Salzarulo,et al.  Sleep states development in the first year of life assessed through 24-h recordings. , 1982, Early human development.

[30]  P. Achermann,et al.  Development of the 24-h rest-activity pattern in human infants. , 2006, Infant behavior & development.

[31]  C. Guilleminault,et al.  Development of sleep-wake patterns and non-rapid eye movement sleep stages during the first six months of life in normal infants. , 1982, Pediatrics.