Artículo

Urbano, F.J.; D'Onofrio, S.; Luster, B.; Beck, P.; Hyde, J.; Bisagno, V.; Garcia-Rill, E. "Pedunculopontine nucleus gamma band activity-preconscious awareness, waking, and REM sleep" (2014) Frontiers in Neurology. 5(OCT)
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Abstract:

The pedunculopontine nucleus (PPN) is a major component of the reticular activating system (RAS) that regulates waking and REM sleep, states of high frequency EEG activity. Recently, we described the presence of high threshold, voltage-dependent N- and P/Q-type calcium channels in RAS nuclei that subserve gamma band oscillations in the mesopontine pedunculopontine nucleus (PPN), intralaminar parafascicular nucleus (Pf), and pontine Subcoeruleus nucleus dorsalis (SubCD). Cortical gamma band activity participates in sensory perception, problem solving, and memory. Rather than participating in the temporal binding of sensory events as in the cortex, gamma band activity in the RAS may participate in the processes of preconscious awareness, and provide the essential stream of information for the formulation of many of our actions. That is, the RAS may play an early permissive role in volition. Our latest results suggest that, 1) the manifestation of gamma band activity during waking may employ a separate intracellular pathway compared to that during REM sleep, 2) neuronal calcium sensor (NCS-1) protein, which is over expressed in schizophrenia and bipolar disorder, modulates gamma band oscillations in the PPN in a concentration-dependent manner, 3) leptin, which undergoes resistance in obesity resulting in sleep dysregulation, decreases sodium currents in PPN neurons, accounting for its normal attenuation of waking, and 4) following our discovery of electrical coupling in the RAS, we hypothesize that there are cell clusters within the PPN that may act in concert. These results provide novel information on the mechanisms controlling high frequency activity related to waking and REM sleep by elements of the RAS. © 2014 Urbano, D_onofrio, Luster, Beck, Hyde, Bisagno and Garcia-rill.

Registro:

Documento: Artículo
Título:Pedunculopontine nucleus gamma band activity-preconscious awareness, waking, and REM sleep
Autor:Urbano, F.J.; D'Onofrio, S.; Luster, B.; Beck, P.; Hyde, J.; Bisagno, V.; Garcia-Rill, E.
Filiación:Department of Neurobiology and Developmental Sciences, Center for Translational Neuroscience, University of Arkansas for Medical Sciences, Little Rock, AR, United States
IFIBYNE, ININFA-CONICET-UBA, Argentina
Palabras clave:Bipolar disorder; Calcium/calmodulin-dependent protein kinase II; Cyclic adenosine monophosphate; Leptin; N-and P/Q-type calcium channels; Neuronal calcium sensor; Schizophrenia; calcium channel N type; calcium channel P type; calcium channel Q type; cyclic AMP dependent protein kinase; leptin; neuronal calcium sensor; neuronal calcium sensor 1; unclassified drug; Article; awareness; bipolar disorder; calcium signaling; central nervous system; cognition; consciousness; contingent negative variation; executive function; food intake; free will; gamma rhythm; hallucination; hormonal regulation; human; memory; motor dysfunction; nerve cell network; nonhuman; obesity; oscillation; pedunculopontine tegmental nucleus; perception; preconscious awareness; problem solving; protein expression; REM sleep; reticular activating system; schizophrenia; sleep disorder; sleep waking cycle; slow wave sleep; synaptic transmission; voluntary movement; wakefulness
Año:2014
Volumen:5
Número:OCT
DOI: http://dx.doi.org/10.3389/fneur.2014.00210
Título revista:Frontiers in Neurology
Título revista abreviado:Front. Neurol.
ISSN:16642295
CAS:cyclic AMP dependent protein kinase
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_16642295_v5_nOCT_p_Urbano

Referencias:

  • Ahima, R.S., Flier, J.S., Leptin (2000) Ann. Rev. Physiol., 62, pp. 413-437
  • Aldabal, L., Bahammam, A.S., Metabolic, endocrine, and immune consequences of sleep deprivation (2011) Open Resp. Med. J., 5, pp. 31-43
  • Balkin, T.J., Braun, A.R., Wesensten, N.J., Jeffries, K., Varga, M., Baldwin, P., Belenky, G., Herscovitch, P., The process of awakening: a PET study of regional brain activity patterns mediating the re-establishment of alertness and consciousness (2002) Brain, 125, pp. 2308-2319
  • Ballanger, B., Lozano, A.M., Moro, E., van Elmeren, T., Hamani, C., Chen, R., Cilia, R., Strafella, A.P., Cerebral blood flow changes induced by pedunculopontine nucleus stimulation in patients with advanced Parkinson's disease: a [(15)O] H2O PET study (2009) Human Brain Map., 30, pp. 3901-3909
  • Beck, P., Mahaffey, S., Urbano, F.J., Garcia-Rill, E., Role of G-proteins in the effects of leptin on pedunculopontine nucleus (PPN) (2013) J. Neurochem., 126, pp. 705-714
  • Beck, P., Odle, A., Wallace-Huitt, T., Skinner, R.D., Garcia-Rill, E., Modafinil increases arousal determined by P13 potential amplitude; an effect blocked by gap junction antagonists (2008) Sleep, 31, pp. 1647-1654
  • Beck, P., Urbano, F.J., Williams, K.D., Garcia-Rill, E., Effects of leptin on pedunculopontine nucleus (PPN) neurons (2013) J. Neural Transm., 120, pp. 1027-1038
  • Bergson, C., Levenson, R., Goldman-Rakic, P., Lidow, M.S., Dopamine receptor-interacting proteins: the Ca2+ connection in dopamine signaling (2003) Trends Pharmacol. Sci., 24, pp. 486-492
  • Boucetta, S., Cisse, Y., Mainville, L., Morales, M., Jones, B.E., Discharge profiles across the sleep-waking cycle of identified cholinergic, GABAergic, and glutamatergic neurons in the pontomesencephalic tegmentum of the rat (2014) J. Neurosci., 34, pp. 4708-4727
  • Brucke, C., Huebl, J., Kempf, F., Krauss, J.K., Yarrow, K., Kupsch, A., Schneider, G.H., Kuhn, A.A., Pallidal gamma activity is correlated to movement amplitude in patients with dystonia (2008) Clin. Neurophysiol., 119 (S1), p. 49
  • Buszaki, G., Neural syntax: cell assemblies, synapsembles, and readers (2010) Neuron, 68, pp. 362-385
  • Capozzo, A., Vitale, F., Mattei, C., Mazzone, P., Scarnati, E., Continuous stimulation of the pedunculopontine tegmental nucleus at 40 Hz affects preparative and executive control in a delayed sensorimotor task and reduces rotational movements induced by apomorphine in the 6-OHDA parkinsonian rat (2014) Behav. Brain Res., 27, pp. 333-342
  • Charpak, S., Paré, D., Llinás, R.R., The entorhinal cortex entrains fast CA1 hippocampal oscillations in the anaesthetized guinea-pig: role of the monosynaptic component of the perforant path (1995) Eur. J. Neurosci., 7, pp. 1548-1557
  • Cheyne, G., Ferrari, P., MEG studies of motor cortex gamma oscillations: evidence for a gamma "fingerprint" in the brain? (2013) Frontiers Human Neurosci., 7, p. #575
  • Chrobak, J.J., Buzsáki, G., Gamma oscillations in the entorhinal cortex of the freely behaving rat (1998) J. Neurosci., 18, pp. 388-398
  • Damasio, A., (2010) Self Comes to Mind: constructing the conscious brain, , New York: Pantheon Books
  • Datta, S., Evidence that REM sleep is controlled by the activation of brain stem pedunculopontine tegmental kainite receptor (2002) J. Neurophysiol., 87, pp. 1790-1798
  • Datta, S., Desarnaud, F., Protein kinase A in the pedunculopontine tegmental nucleus of rat contributes to regulation of rapid eye movement sleep (2010) J. Neurosci., 30, pp. 12263-12273
  • Data, S., O'Malley, M.W., Patterson, E.H., Calcium/calmodulin kinase II in the pedunculopontine tegmental nucleus modulates the initiation and maintenance of wakefulness (2010) J. Neurosci., 31, pp. 1700-17016
  • Datta, S., Patterson, E.H., Spoley, E.E., Excitation of pedunculopontine tegmental NMDA receptors induces wakefulness and cortical activation in the rat (2001) J. Neurosci. Res., 66, pp. 109-116
  • Datta, S., Siwek, D.F., Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats (2002) J. Neurosci. Res., 70, pp. 79-82
  • Datta, S., Siwek, D.F., Excitation of the brain stem pedunculopontine tegmentum cholinergic cells induce wakefulness and REM sleep (1997) J. Neurophysiol., 77, pp. 2975-2988
  • Datta, S., Spoley, E.E., Patterson, E.H., Microinjection of glutamate into the pedunculopontine tegmentum induces REM sleep and wakefulness in the rat (2001) Amer. J. Physiol. Reg. Integ. Comp. Physiol., 280, pp. R752-R759
  • Deecke, L., Grozinger, B., Kornhuber, H.H., Voluntary finger movement in man: cerebral potentials and theory (1976) Biol. Cyber., 23, pp. 99-119
  • Dellu, F., Mayo, W., Cherkaoui, J., Le Moal, M., Simon, H., Learning disturbances following excitotoxic lesion of cholinergic pedunculo-pontine nucleus in the rat (1991) Brain Res., 544, pp. 126-132
  • Delorme, A., Makeig, S., EEGLAB: an open source toolbox for analysis of single-trial EEG dynamics including independent component analysis (2004) J. Neurosci. Meth., 134, pp. 9-21
  • Dement, W.C., Studies on the effects of REM deprivation in humans and animals (1967) Res. Publ. Assoc. Res. Nerv. Ment. Dis., 43, pp. 456-467
  • Desarnaud, F., Macone, B.W., Datta, S., Activation of extracellular signalregulated kinase signaling in the pedunculopontine tegmental cells is involved in the maintenance of sleep in rats (2011) J. Neurochem., 116, pp. 577-587
  • Dixon, J.B., Dixon, M.E., Anderson, M.L., Schachter, L., O'Brien, P.E., Daytime sleepiness in the obese: not as simple as obstructive sleep apnea (2007) Obesity, 15, pp. 2504-2511
  • D'Onofrio, S., Kezunovic, N., Urbano, F.J., Garcia-Rill, E., Novel treatment for schizophrenia (2013) NIGMS Institutional Development Award meeting, , Washington, DC, June
  • Eckhorn, R., Bauer, R., Jordan, W., Brosch, M., Kruse, W., Munk, M., Reitboeck, H.J., Coherent oscillations: a mechanism of feature linking in the visual system? (1988) Biol. Cyber., 60, pp. 121-130
  • Florio, T., Capozzo, A., Puglielli, E., Pupillo, R., Pizzuti, G., Scarnati, E., The function of the pedunculopontine nucleus in the preparation and execution of an externally- cued bar pressing task in the rat (1999) Behav. Brain Res., 104, pp. 95-104
  • Fujimoto, K., Ikeguchi, K., Yoshida, M., Impaired acquisition, preserved retention and retrieval of avoidance behavior after destruction of pedunculopontine nucleus areas in the rat (1992) Neurosci Res., 13, pp. 43-51
  • Garcia-Rill, E., The basal ganglia and the locomotor regions (1986) Brain Res. Rev., 11, pp. 47-63
  • Garcia-Rill, E., The pedunculopontine nucleus (1991) Prog. Neurobiol., 36, pp. 363-389
  • Garcia-Rill, E., Disorders of the Reticular Activating System (1997) Med. Hypoth., 49, pp. 379-387
  • Garcia-Rill, E., Sleep and arousal states: reticular activating system (2009) New Encyclopedia of Neuroscience, 8, pp. 137-143. , eds. L.R. Squire, F. Bloom, N. Spitzer, F. Gage, T. Albright (Oxford, England: Elsevier)
  • Garcia-Rill, E., Charlesworth, A., Heister, D.A., Ye, M., Hayar, A., The developmental decrease in REM sleep: the role of transmitters and electrical coupling (2008) Sleep, 31, pp. 1-18
  • Garcia-Rill, E., Heister, D.S., Ye, M., Charlesworth, A., Hayar, A., Electrical coupling: novel mechanism for sleep-wake control (2007) Sleep, 30, pp. 1405-1414
  • Garcia-Rill, E., Hyde, J., Kezunovic, N., Urbano, F.J., Petersen, E., The physiology of the pedunculopontine nucleus- implications for deep brain stimulation (2014) J. Neural. Transm., , In Press
  • Garcia-Rill, E., Kezunovic, N., D'Onofrio, S., Luster, B., Hyde, J., Bisagno, V., Urbano, F.J., Gamma band activity in the RAS- intracellular mechanisms (2014) Exptl. Brain Res., 232, pp. 1509-1522
  • Garcia-Rill, E., Kezunovic, N., Hyde, J., Beck, P., Urbano, F.J., Coherence and frequency in the reticular activating system (RAS) (2013) Sleep Med. Rev., 17, pp. 227-238
  • Garcia-Rill, E., Skinner, R.D., The sleep state-dependent P50 midlatency auditory evoked potential (2001) Sleep Medicine, pp. 697-704. , eds. T.L. Lee-Chiong, M.A. Carskadon, S.J. Sateia (Philadelphia, PA: Hanley & Belfus)
  • Gray, C.M., Singer, W., Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex (1989) Proc. Nat. Acad.Sci., 86, pp. 1698-1702
  • Hallett, M., Volitional control of movement: the physiology of free will (2007) Clin. Neurophysiol., 118, pp. 1179-1192
  • Heister, D.S., Hayar, A., Charlesworth, A., Yates, C., Zhou, Y., Garcia-Rill, E., Evidence for electrical coupling in the SubCoeruleus (SubC) nucleus (2007) J. Neurophysiol., 97, pp. 3142-3147
  • Hermann, C.S., Human EEG responses to 1-100 Hz flicker: response phenomena (2001) Exp. Brain Res., 137, pp. 346-353
  • Hernandez-Chan, N.G., Gongora-Alfaro, J.L., Alvarez-Cervera, F.J., Solis-Rodriguez, F.A., Heredia-Lopez, F.J., Arankowsky-Sandoval, G., Quinolinic acid lesions of the pedunculopontine nucleus impair architecture, but not locomotion, exploration, emotionality or working memory in the rat (2011) Behav. Brain Res., 225, pp. 482-490
  • Hyde, J., Kezunovic, N., Urbano, F.J., Garcia-Rill, E., Spatiotemporal properties of high speed calcium oscillations in the pedunculopontine nucleus (2013) J. Appl. Physiol., 115, pp. 1402-1414
  • Hyde, J., Kezunovic, N., Urbano, F.J., Garcia-Rill, E., Visualization of fast calcium oscillations in the parafascicular nucleus (2013) J. Eur. Physiol. (Pflug Arch), 465, pp. 1327-1340
  • Jenkinson, N., Kuhn, A.A., Brown, P., Gamma oscillations in the human basal ganglia (2013) Exp. Neurol., 245, pp. 72-76
  • Jones, E.G., Calcium channels in higher-level brain function (2007) Proc. Nat. Acad. Sci., 14, pp. 17903-17904
  • Keating, G.L., Winn, P., Examination of the role of the pedunculopontine tegmental nucleus in radial maze tasks with or without a delay (2002) Neurosci., 112, pp. 687-696
  • Kezunovic, N., Hyde, J., Goitia, B., Bisagno, V., Urbano, F.J., Garcia-Rill, E., Muscarinic modulation of high frequency activity in the pedunculopontine nucleus (PPN) (2013) Frontiers Neurol. Sleep Chronobiol., 4 (176), pp. 1-13
  • Kezunovic, N., Hyde, J., Simon, C., Urbano, F.J., Garcia-Rill, E., Gamma band activity in the developing parafascicular nucleus (Pf) (2012) J. Neurophysiol., 107, pp. 772-784
  • Kezunovic, N., Simon, C., Hyde, J., Smith, K., Beck, P., Odle, A., Garcia-Rill, E., Arousal from slices to humans: Translational studies on sleep-wake control (2010) Transl. Neurosci., 1, pp. 2-8
  • Kezunovic, N., Urbano, F.J., Simon, C., Hyde, J., Smith, K., Garcia-Rill, E., Mechanism behind gamma band activity in the pedunculopontine nucleus (PPN) (2011) Eur. J. Neurosci., 34, pp. 404-415
  • Kimura, T., Pignatelli, M., Suh, J., Kohara, K., Yoshiki, A., Abe, K., Tonegawa, S., Island cells control temporal association memory (2014) Science, 343, pp. 896-901
  • Koh, P.O., Undie, A.S., Kabbani, N., Levenson, R., Goldman-Rakic, P., Lidow, M.S., Up-regulation of neuronal calcium sensor-1 (NCS-1) in the prefrontal cortex of schizophrenic and bipolar patients (2003) Proc. Natl. Acad. Sci., 100, pp. 313-317
  • Lalo, E., Thobois, S., Sharott, A., Polo, G., Mertens, P., Pogosyan, A., Patterns of bidirectional communication between cortex and basal ganglia during movement in patients with Pakinson disease (2008) J. Neurosci., 28, pp. 3008-3016
  • Lang, E.J., Sugihara, I., Llinás, R.R., Olivocerebellar modulation of motor cortex ability to generate vibrissal movements in rat (2006) J. Physiol., 571, pp. 101-120
  • Leri, F., Franklin, K.B., Learning impairments caused by lesions to the pedunculopontine tegmental nucleus: an artifact of anxiety? (1998) Brain Res., 807, pp. 187-192
  • Libet, B., Do we have free will? (1999) J. Consc. Studies, 9, pp. 47-57
  • Libet, B., Gleason, C.A., Wright, E.W., Pearl, D.K., Time of conscious intention to act in relation to onset of cerebral activity (readiness-potential). The unconscious initiation of a freely voluntary act. (1983) Brain, 106, pp. 623-642
  • Litvak, V., Eusebio, A., Jha, A., Oosterveld, R., Barnes, G., Foltynie, T., Movement-related changes in local and long-range synchronization in Parkinson's disease revealed by simultaneous magnetoencephalography and intracranial recordings (2012) J. Neurosci., 32, pp. 10541-10553
  • Llinas, R.R., Grace, A.A., Yarom, Y., In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range (1991) Proc. Nat. Acad. Sci., 88, pp. 897-901
  • Mena-Segovia, J., Sims, H.M., Magill, P.J., Bolam, J.P., Cholinergic brainstem neurons modulate cortical gamma band activity during slow oscillations (2008) J. Physiol., 586, pp. 2947-2960
  • Middleton, S.J., Racca, C., Cunningham, M.O., Traub, R.D., Monyer, H., Knöpfel, T., Schofield, I.S., Whittington, M.A., High-frequency network oscillations in cerebellar cortex (2008) Neuron, 58, pp. 763-774
  • Miyazato, H., Skinner, R.D., Garcia-Rill, E., Neurochemical modulation of the P13 midlatency auditory evoked potential in the rat (1999) Neurosci., 92, pp. 911-920
  • Morgan, P.T., Pace-Schott, E., Pittman, B., Stickgold, R., Malison, R.T., Normalizing effect of modafinil on sleep in chronic cocaine users (2010) Amer. J. Psychiat., 167, pp. 331-340
  • Muldoon, A.F., Soltesz, I., Cossart, R., Spatially clustered neuronal assemblies comprise the microstructure of synchrony in chronically epileptic networks (2013) Proc. Nat. Acad. Sci., 110, pp. 3567-3572
  • Narici, L., Romani, G.L., Neuromagnetic investigation of synchronized spontaneous activity (1989) Brain Topog., 2, pp. 19-30
  • Ozerdem, A., Guntenkin, B., Atagun, I., Turp, B., Basar, E., Reduced long distance gamma (28-48 Hz) coherence in euthymic patients with bipolar disorder (2011) J. Affect. Disord., 132, pp. 325-332
  • Palva, S., Monto, S., Palva, J.M., Graph properties of synchronized cortical networks during visual working memory maintenance (2009) Neuroimage, 49, pp. 3257-3268
  • Panckeri, K.A., Schotland, H.M., Pack, A.I., Hendricks, J.C., Modafinil decreases hypersomnolence in the English bulldog, a natural animal model of sleep disordered breathing (1996) Sleep, 19, pp. 626-631
  • Petrovic, J., Lazic, K., Ciric, J., Kalauzi, A., Saponjic, J., Topography of the sleep/wake states related EEG microstructure and transitions structure differentiates the functionally distinct cholinergic innervation disorders in rat (2013) Behav. Brain Res., 256, pp. 108-118
  • Philips, S., Takeda, Y., Greater frontal-parietal synchrony at low gamma-band frequencies for inefficient then efficient visual search in human EEG (2009) Int. J. Psychophysiol., 73, pp. 350-354
  • Plante, D.T., Winkelman, J.W., Sleep disturbance in bipolar disorder: therapeutic implications (2008) Am. J. Psychiatry., 165 (7), pp. 830-843
  • Rager, G., Singer, W., The response of cat visual cortex to flicker stimuli of variable frequency (1998) Eur. J. Neurosci., 10, pp. 1856-1877
  • Ray, S., Naumann, R., Burgalossi, A., Tang, O., Schmitt, H., Brecht, M., Gridlayout and theta-modulation of layer 2 pyramidal neurons in medial entorhinal cortex (2014) Science, 343, pp. 891-896
  • Reese, N.B., Garcia-Rill, E., Skinner, R.D., The pedunculopontine nucleusauditory input, arousal and pathophysiology (1995) Prog. Neurobiol., 47, pp. 105-133
  • Reese, N.B., Garcia-Rill, E., Skinner, R.D., Auditory input to the pedunculopontine nucleus I. Evoked potentials. (1995) Brain Res. Bull., 37, pp. 247-255
  • Reese, N.B., Garcia-Rill, E., Skinner, R.D., Auditory input to the pedunculopontine nucleus II. Unit responses. (1995) Brain Res. Bull., 37, pp. 257-264
  • Ros, H., Magill, P.J., Moss, J., Bolam, J.P., Mena-Segovia, J., Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states (2010) Neurosci., 170, pp. 78-91
  • Rosanova, M., Casali, A., Bellina, V., Resta, F., Mariotti, M., Massimini, M., Natural frequencies of human corticothalamic circuits (2009) J. Neurosci., 29, pp. 7679-7685
  • Sakai, K., El Mansari, M., Jouvet, M., Inhibition by carbachol microinjections of presumptive cholinergic PGO-on neurons in freely moving cats (1990) Brain Res., 527, pp. 213-223
  • Satorra-Marín, N., Homs-Ormo, S., Arévalo-García, R., Morgado-Bernal, I., Coll-Andreu, M., Effects of pre-training pedunculopontine tegmental nucleus lesions on delayed matching- and non-matching-to-position in a T-maze in rats (2005) Behav. Brain Res., 160, pp. 115-124
  • Shik, M.L., Severin, F.V., Orlovskii, G.N., Control of walking and running by means of electric stimulation of the midbrain (1966) Biofizika, 11, pp. 659-666
  • Shouse, M.N., Siegel, J., Pontine regulation of REM sleep components in cats: integrity of the pedunculopontine tegmentum (PPT) is important for phasic events but unnecessary for atonia during REM sleep (1992) Brain Res., 571, pp. 50-63
  • Simon, C., Kezunovic, N., Williams, D.K., Urbano, F.J., Garcia-Rill, E., Cholinergic and glutamatergic agonists induce gamma frequency activity in dorsal subcoeruleus nucleus neurons (2011) Amer. J. Physiol. Cell Physiol., 301, pp. C327-C335
  • Simon, C., Kezunovic, N., Ye, M., Hyde, J., Hayar, A., Williams, D.K., Garcia-Rill, E., Gamma band unit and population responses in the pedunculopontine nucleus (2010) J. Neurophysiol., 104, pp. 463-474
  • Singer, W., Synchronization of cortical activity and its putative role in information processing and learning (1993) Ann. Rev. Physiol., 55, pp. 349-374
  • Steriade, M., Curro Dossi, R., Pare, D., Oakson, G., Fast oscillations (20-40 Hz) in thalamocortical systems and their potentiation by mesopontine cholinergic nuclei in the cat (1991) Proc. Nat. Acad. Sci., 88, pp. 4396-4400
  • Steriade, M., Paré, D., Datta, S., Oakson, G., Curro Dossi, R., Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves (1990) J. Neurosci., 10, pp. 2560-2579
  • Steriade, M., Datta, S., Pare, D., Oakson, G., Curro Dossi, R., Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems (1990) J. Neurosci., 10, pp. 2541-2559
  • Uhlhaas, P.J., Singer, W., Abnormal neural oscillations and synchrony in schizophrenia (2010) Nat. Rev. Neurosci., 11, pp. 100-113
  • Spiegel, K., Knutson, K., Leproult, R., Tasali, E., Van Cauter, E., Sleep loss: a novel risk factor for insulin resistance and Type 2 diabetes (2005) J. App. Physiol., 99, pp. 2008-2019
  • Taheri, S., Lin, L., Austin, D., Young, T., Mignot, E., Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index (2004) PLoS Med., 1 (3), p. e62
  • Torres, K.C.L., Souza, B.R., Miranda, D.M., Sampiao, A.M., Nicolato, R., Neves, E., Expression of neuronal calcium sensor-1 (NCS-1) is decreased in leukocytes of schizophrenia and bipolar disorder patients (2009) Prog. Neuro-Pharmacol. Biol. Psychiat., 33, pp. 229-234
  • Trottenberg, T., Fogelson, N., Kuhn, A.A., Kivi, A., Kupsch, A., Schneider, G.H., Brown, P., Subthalamic gamma activity in patients with Parkinson's disease (2006) Exp. Neurol., 200, pp. 56-65
  • Urbano, F.J., Leznik, E., Llinas, R.R., Modafinil enhances thalamocortical activity by increasing neuronal electrotonic coupling (2007) Proc. Nat. Acad. Sci., 104, pp. 12554-12559
  • Urbano, F.J., Kezunovic, N., Hyde, J., Simon, C., Beck, P., Garcia-Rill, E., Gamma band activity in the reticular activating system (RAS) (2012) Frontiers Neurol.; Sleep Chronobiol., 3 (6), pp. 1-16
  • Vgontzas, A.N., Bixler, E.O., Tan, T.L., Kantner, D., Martin, L.F., Kales, A., Obesity without sleep apnea is associated with daytime sleepiness (1998) Arch. Inter. Med., 158, pp. 1333-1337
  • Voss, U., Holzmann, R., Tuin, I., Hobson, J.A., Lucid dreaming: a state of consciousness with features of both waking and non-lucid dreaming (2009) Sleep, 32, pp. 1191-1200
  • Wang, H.L., Morales, M., Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat (2009) Eur. J. Neurosci., 29, pp. 340-358

Citas:

---------- APA ----------
Urbano, F.J., D'Onofrio, S., Luster, B., Beck, P., Hyde, J., Bisagno, V. & Garcia-Rill, E. (2014) . Pedunculopontine nucleus gamma band activity-preconscious awareness, waking, and REM sleep. Frontiers in Neurology, 5(OCT).
http://dx.doi.org/10.3389/fneur.2014.00210
---------- CHICAGO ----------
Urbano, F.J., D'Onofrio, S., Luster, B., Beck, P., Hyde, J., Bisagno, V., et al. "Pedunculopontine nucleus gamma band activity-preconscious awareness, waking, and REM sleep" . Frontiers in Neurology 5, no. OCT (2014).
http://dx.doi.org/10.3389/fneur.2014.00210
---------- MLA ----------
Urbano, F.J., D'Onofrio, S., Luster, B., Beck, P., Hyde, J., Bisagno, V., et al. "Pedunculopontine nucleus gamma band activity-preconscious awareness, waking, and REM sleep" . Frontiers in Neurology, vol. 5, no. OCT, 2014.
http://dx.doi.org/10.3389/fneur.2014.00210
---------- VANCOUVER ----------
Urbano, F.J., D'Onofrio, S., Luster, B., Beck, P., Hyde, J., Bisagno, V., et al. Pedunculopontine nucleus gamma band activity-preconscious awareness, waking, and REM sleep. Front. Neurol. 2014;5(OCT).
http://dx.doi.org/10.3389/fneur.2014.00210