Activity of Midbrain Reticular Formation and Neocortex during the Progression of Human Non-Rapid Eye Movement Sleep

To clarify the neural correlates and brain activity during the progression of human non-rapid eye movement (NREM) sleep, we examined the absolute regional cerebral blood flow (rCBF) during light and deep NREM sleep and during wakefulness in normal humans using positron emission tomography with H215O. Relative changes in rCBF during light and deep NREM sleep in comparison to the rCBF during wakefulness were also analyzed. During light NREM sleep, the rCBF in the midbrain, in contrast to that in the pons and thalamic nuclei, did not decrease when compared to that during wakefulness, whereas rCBF decreased in the left medial frontal gyrus, left inferior frontal gyrus, and left inferior parietal gyrus of the neocortex. During deep NREM sleep, the rCBF in the midbrain tegmentum decreased, and there was a marked and bilateral decrease in the rCBF in all neocortical regions except for the perirolandic areas and the occipital lobe. There have been three groups of brain structures, each representing one type of deactivation during the progression of NREM sleep. The activity of the midbrain reticular formation is maintained during light NREM sleep and therefore represents a key distinguishing characteristic between light and deep NREM sleep. Selective deactivation of heteromodal association cortices, including those related to language, occurs with increasingly deep NREM sleep, which supports the recent theory that sleep is not a global, but it is a local process of the brain.

[1]  R. Llinás,et al.  Of dreaming and wakefulness , 1991, Neuroscience.

[2]  B. Gulyás,et al.  Activation by Attention of the Human Reticular Formation and Thalamic Intralaminar Nuclei , 1996, Science.

[3]  M. Raichle,et al.  Brain blood flow measured with intravenous H2(15)O. I. Theory and error analysis. , 1983, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[4]  W. Obrist,et al.  Human cerebral blood flow during sleep and waking. , 1973, Journal of applied physiology.

[5]  F. Sakai,et al.  Normal human sleep: Regional cerebral hemodynamics , 1980, Annals of neurology.

[6]  N. Lassen,et al.  Cerebral O2 metabolism and cerebral blood flow in humans during deep and rapid-eye-movement sleep. , 1991, Journal of applied physiology.

[7]  Alan C. Evans,et al.  Regional Cerebral Blood Flow Changes as a Function of Delta and Spindle Activity during Slow Wave Sleep in Humans , 1997, Journal of Neuroscience.

[8]  T. Ogawa,et al.  Electrophysiology of ascending, possibly cholinergic neurons in the rat laterodorsal tegmental nucleus: comparison with monoamine neurons , 1987, Neuroscience Letters.

[9]  W. Mendelson,et al.  Human Sleep: Research and Clinical Care , 1987 .

[10]  D. J. Mullaney,et al.  Automatic sleep/wake identification from wrist activity. , 1992, Sleep.

[11]  G V RUSSELL The brainstem reticular formation. , 1957, Texas reports on biology and medicine.

[12]  J C Mazziotta,et al.  Tomographic mapping of human cerebral metabolism: Sensory deprivation , 1982, Annals of neurology.

[13]  M. Torrens Co-Planar Stereotaxic Atlas of the Human Brain—3-Dimensional Proportional System: An Approach to Cerebral Imaging, J. Talairach, P. Tournoux. Georg Thieme Verlag, New York (1988), 122 pp., 130 figs. DM 268 , 1990 .

[14]  D. Contreras,et al.  The slow (< 1 Hz) oscillation in reticular thalamic and thalamocortical neurons: scenario of sleep rhythm generation in interacting thalamic and neocortical networks , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  B. Jacobs,et al.  Structure and function of the brain serotonin system. , 1992, Physiological reviews.

[16]  W. B. Knowles,et al.  Behavioral and EEG changes following chronic brain stem lesions in the cat. , 1950, Electroencephalography and clinical neurophysiology.

[17]  A. Braun,et al.  Regional cerebral blood flow throughout the sleep-wake cycle. An H2(15)O PET study. , 1997, Brain : a journal of neurology.

[18]  M. Steriade,et al.  Brainstem Control of Wakefulness and Sleep , 1990, Springer US.

[19]  Larry L. Butcher,et al.  Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain , 1986, Brain Research Bulletin.

[20]  O. Lindvall,et al.  The adrenergic innervation of the rat thalamus as revealed by the glyoxylic acid fluorescence method , 1974, The Journal of comparative neurology.

[21]  K. Kitahama,et al.  Neurotoxic lesion of the mesencephalic reticular formation and/or the posterior hypothalamus does not alter waking in the cat , 1991, Brain Research.

[22]  Christian Degueldre,et al.  Functional Neuroanatomy of Human Slow Wave Sleep , 1997, The Journal of Neuroscience.

[23]  N. Kleitman,et al.  Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. , 1953, Science.

[24]  Karl J. Friston,et al.  Comparing Functional (PET) Images: The Assessment of Significant Change , 1991, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[25]  M. Mintun,et al.  Brain blood flow measured with intravenous H2(15)O. II. Implementation and validation. , 1983, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[26]  J. Krueger,et al.  A neuronal group theory of sleep function , 1993, Journal of sleep research.

[27]  G. Moruzzi,et al.  Brain stem reticular formation and activation of the EEG. , 1949, Electroencephalography and clinical neurophysiology.

[28]  M. Mesulam,et al.  Central cholinergic pathways in the rat: An overview based on an alternative nomenclature (Ch1–Ch6) , 1983, Neuroscience.

[29]  H. Craig Heller,et al.  Restoration of brain energy metabolism as the function of sleep , 1995, Progress in Neurobiology.

[30]  Lars Olson,et al.  Ascending Monoamine Neurons to the Telencephalon and Diencephalon , 1966 .

[31]  B. E. Jones,et al.  Paradoxical sleep and its chemical/structural substrates in the brain , 1991, Neuroscience.

[32]  E. Wolpert A Manual of Standardized Terminology, Techniques and Scoring System for Sleep Stages of Human Subjects. , 1969 .

[33]  T. Sejnowski,et al.  Thalamocortical oscillations in the sleeping and aroused brain. , 1993, Science.

[34]  Karl J. Friston,et al.  Statistical parametric maps in functional imaging: A general linear approach , 1994 .