Abstract
Defective arousal mechanisms are viewed as contributory to sleep hypopnea disorders and sudden infant death syndrome. Sighs (i.e. augmented breaths) as well as startles have not traditionally been viewed as arousal-related phenomena in infants. We hypothesized that, if sighs and starles are the initial event in a sequential arousal process, then they might be associated with specific EEG activity changes, because activation of the arousal-related ascending reticular activating system can suppress thalamus-generated σ spindle oscillations. We studied spontaneous sighs and startles and those elicited by briefly occluding the infants face mask airway in 12 normal infants (age 10-19 wk) during non-rapid eye movement sleep. We recorded EEG (C3-P3), ECG, O2 saturation, diaphragmatic electromyography, limb electromyography, and video of the infant. The startle intensity was scored on a scale of 0 to 3 based on video recorded movements. Sleep spindle periodicity was analyzed by using a threshold over a compressed spectral band array. Spontaneous sighs and sleep startles were immediately followed by an interspindle interval prolongation from (mean ± SEM) 8.0 ± 0.16 s (control period) to 17.9 ± 1.45 s after spontaneous sighs, to 23.8 ± 1.26 s after spontaneous sighs accompanied by startles and to 26.5 ± 1.45 s after occlusion-related sighs and startles. Furthermore, the intensity of occlusion-evoked startles was positively correlated with the interspindle interval prolongation (p < 0.01). We conclude that spontaneous as well as evoked sighs and startles are immediately followed by a transient sleep spindle suppression. This phenomenon indicates a close linkage between sighs, startles, and reticular formation-related arousal mechanisms.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
Abbreviations
- SIDS:
-
sudden infant death syndrome
- REM:
-
rapid eye movement sleep
- N-REM:
-
nonrapid eye movement sleep
- EMG:
-
electromyogram
- RE:
-
reticular
References
Kahn A, Picard E, Blum D 1986 Auditory arousal threshold of normal and near-miss SIDS infants. Dev Med Child Neurol 28: 299–302
Hunt C 1981 Abnormal hypercarbic and hypoxic sleep arousal responses in near-miss SIDS infants. Pediatr Res 15: 1462–1464
Task Force of the American Sleep Disorders Association 1992 EEG arousals: scoring rules and examples. A preliminary report from the sleep disorders atlas. Sleep 15: 174–184
Rees K, Spence PS, Earis JE, Calverly MA 1995 Arousal responses from apneic events during non-rapid-eye-movement sleep. Am J Crit Care Med 152: 1062–1021
McNamara F, Issa FG, Sullivan CE 1996 Arousal pattern following central and obstructive breathing abnormalities in infants and children. J Appl Physiol 81: 2651–2657
Wulbrand H, Zezschwitz HG, Bentele KHP 1995 Submental and diaphragmatic muscle activity during and at resolution of mixed and obstructive apneas and cardiorespiratory arousal in preterm infants. Pediatr Res 38: 298–305
Morgrass MA, Ducharme FM, Brouillette RT 1994 Movement/arousals. Am J Respir Crit Care Med 150: 1690–1696
Lijowska A, Reed NW, Chiodini M, Thach BT 1997 Sequential arousal behaviour in infants in asphyxial sleep environments. J Appl Physiol 83: 219–228
Wulbrand H, McNamara F, Thach BT 1997 Occurrence of arousal related reflexes, sigh and startle, during airway occlusion in infants. Am J Respir Crit Care Med 155: A13
Munk MHJ, Roelfsma PR, König P, Engel AK, Singer W 1996 Role of reticular activation in the modulation of intracortical synchronization. Science 272: 271–274
Steriade M, Amzica F, Contreras D 1996 Synchronization of fast (30-40 Hz) spontaneous cortical rhythms during brain activation. J Neurosci 16: 392–417
Steriade M, Llinás R 1988 The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68: 649–742
Lenard HG 1970 The development of sleep spindles in the EEG during the first two years of life. Neuropediatrie 1: 264–276
Metcalf DR 1970 Sleep spindle ontogenesis. Neuropediatrie 1: 428–433
Anders T, Emde R, Parmalee A 1971 A manual of Standardized Terminology, Technology, and Criteria for Scoring of States of Sleep and Wakefulness in Newborn Infants. UCLA Brain Information Service/ BRI Publications Office, Los Angeles, pp 11–124.
Fisch BJ 1991 Spehlmann's EEG Primer. 2nd Ed. Elsevier, Amsterdam, p 129
Fisch BJ 1991 Spehlmann's EEG Primer. 2nd Ed. Elsevier, Amsterdam, p 231
Hunt NE 1986 Phase Retrieval and Zero Crossings. Kluwer Academic Publishers, Boston, pp 54–65.
Pfurtscheller G 1993 Special uses of EEG computer analysis in clinical environment In: Niedermeyer E, Lopes da Silva F (eds) Electroencephalography. Basic Principles, Clinical Applications, and Related Fields. 3rd Ed. Williams & Wilkins, Baltimore, pp 1125–1133
Thach BT, Taeusch W 1976 Sighing in newborn infants: role of inflation-augmenting reflex. J Appl Physiol 41: 502–507
Volpe J 1995 Neurology of the Newborn. 3rd Ed. WB Saunders, Philadelphia, p 106
Hunt W 1936 Studies of the startle pattern. II. Bodily pattern. J Psychol 2: 207–213
McGraw 1937 M The Moro reflex. Am J Dis Child 54: 240–251
Hu B, Steriade M, Deschénes 1989 The effects of brainstem peribrachial stimulation on reticular thalamic neurons: the blockage of spindle waves. Neuroscience 31: 1–12
Moruzzi and Magoun 1949 Brain stem reticular formation and activation of the EEG. EEG Clin Neurophysiol 1: 455–743
Steriade M, McCormick DA, Sejnowski TJ 1993 Thalamocortical oscillations in the sleeping and aroused brain. Science 262: 679–685
Steriade M, Jones EG, Llinás RR 1990 Thalamic Oscillations and Signalling. John Wiley & Sons, New York, pp 299–306.
Sofroniew MV, Consolazione A, Eckenstein F, Cuello AC 1985 Cholinergic projections from the midbrain and pons to the thalamus in the rat, identified by combined retrograde tracing and choline acetyltransferase immunohistochemistry. Brain Res 329: 213–223
McCormick DA, Wang Z 1991 Serotonin and noradrenaline excite GABAergic neurones of the guinea pig thalamic reticular nucleus and the cat perigeniculate nucleus. J Physiol 442: 235–255
Steriade M, McCarley RW 1990 Brainstem Control of Wakefulness and Sleep. Plenum Press, New York, p 223
Steriade M, Llinás R 1988 The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68: 649–742
Steriade M, Amzica F 1996 Intracortical and corticothalamic coherency of fast spontaneous oscillations. Proc Natl Acad Sci USA 93: 2533–2538
Garg M, Kurzner SI, Bautista D, Keens TG 1988 Hypoxic arousal responses in infants with bronchopulmonary dysplasia. Pediatrics 82: 52–63
Davidson Ward SL, Nickerson BG, van der Hal A, Rodriguez AM, Jacobs RA, Keens TG 1986 Absent hypoxic and hypercapnic arousal responses in children with myelomeningocele and apnea. Pediatrics 78: 44–50
Sullivan CE, Murphy E, Kozar LF, Phillipson EA 1978 Waking and ventilatory responses to laryngeal stimulation in sleeping dogs. J Appl Physiol 45: 681–689
Wulbrand H, Bentele K 1993 EEG-suppression following augmented breaths during apnea. Pediatr Res 36: 62A( abstr)
Orem J Trotter RH 1993 Medullary respiratory neuronal activity during augmented breaths in intact unanaesthetized cats. J Appl Physiol 74: 761–769
Poe GR, Kristensen MP, Rector DM, Harper RM 1996 Hippocampal activity during transient respiratory events in the freely behaving cat. Neuroscience 72: 39–48
Wolff P 1966 The causes, controls, and organisation of behaviour in the neonate. Psychological Issues, Vol. V, No. 1, Monogr. 17. International University Press, New York, pp 13–20.
Prechtl HRF, Nolte R 1980 The motor behaviour of the preterm infant. In: Prechtl HRF (ed) The Continuity of Pre- and Postnatal Behaviour. Oxford Blackwell Ltd, Oxford, UK, pp 10–57.
Brown P 1995 Physiology of startle phenomenon. Adv Neurol 67: 273–287
Edinger L, Fisher B 1913 Ein Mensch ohne Grosshirn. Pflugers Archiv 152: 535–562
Bullock TH 1984 Comparative neuroethology of startle, rapid escape, and giant fiber-mediated response. In: Eaton RC (ed) Neural Mechanisms of Startle Behaviour. Plenum Press, New York, pp 1–13.
Davis M 1984 The mammalian startle response. In: Eaton RC (ed) Neural Mechanisms of Startle Behaviour. Plenum Press, New York, pp 287–351.
Coons S, Guilleminault C 1985 Motility and arousals in near miss sudden infant death syndrome. J Pediatr 107: 728–732
Kahn A, Groswasser J, Rebuffat E, Sottiaux M, Blum D, Foerster M, Franco P, Bochner A, Alexander M, Bachy A, Richard P, Verghote M, LePolain D, Wayenberg JL 1992 Sleep and cardiorespiratory characteristics of infant victims of sudden death: a prospective case-control study Sleep 15: 287–292
Schechtmann VL, Harper RM, Wilson AJ, Southall DP 1992 Sleep state organization in normal infants and victims of the sudden infant death syndrome. Pediatrics 89: 865–870
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Wulbrand, H., McNamara, F. & Thach, B. Suppression of σ Spindle Electroencephalographic Activity as a Measure of Transient Arousal after Spontaneous and Occlusion-Evoked Sighs and Startles. Pediatr Res 44, 767–773 (1998). https://doi.org/10.1203/00006450-199811000-00021
Received:
Accepted:
Issue date:
DOI: https://doi.org/10.1203/00006450-199811000-00021
This article is cited by
-
How to score arousals in preterm infants?
Wiener Klinische Wochenschrift (2003)


