Skip to main content
SpringerLink
Log in

Gamma band activity in the RAS-intracellular mechanisms

  • Review
  • Published:
Experimental Brain Research Aims and scope Submit manuscript

An Erratum to this article was published on 31 January 2014

Abstract

Gamma band activity participates in sensory perception, problem solving, and memory. This review considers recent evidence showing that cells in the reticular activating system (RAS) exhibit gamma band activity, and describes the intrinsic membrane properties behind such manifestation. Specifically, we discuss how cells in the mesopontine pedunculopontine nucleus, intralaminar parafascicular nucleus, and pontine SubCoeruleus nucleus dorsalis all fire in the gamma band range when maximally activated, but no higher. The mechanisms involve high-threshold, voltage-dependent P/Q-type calcium channels, or sodium-dependent subthreshold oscillations. 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. We address three necessary next steps resulting from these discoveries: an intracellular mechanism responsible for maintaining gamma band activity based on persistent G-protein activation, separate intracellular pathways that differentiate between gamma band activity during waking versus during REM sleep, and an intracellular mechanism responsible for the dysregulation in gamma band activity in schizophrenia. These findings open several promising research avenues that have not been thoroughly explored. What are the effects of sleep or REM sleep deprivation on these RAS mechanisms? Are these mechanisms involved in memory processing during waking and/or during REM sleep? Does gamma band processing differ during waking versus REM sleep after sleep or REM sleep deprivation?

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aserinsky E, Kleitman N (1953) Regularly occurring periods of eye motility, and concomitant phenomena, during sleep. Science 118:273–274

    CAS  PubMed  Google Scholar 

  • Baghdoyan HA, Rodrigo-Angulo ML, McCarley RW, Hobson JA (1987) A neuroanatomical gradient in the pontine tegmentum for the cholinoceptive induction of desynchronized sleep signs. Brain Res 414:245–261

    CAS  PubMed  Google Scholar 

  • Beck P, Odle A, Wallace-Huitt T, Skinner RD, Garcia-Rill E (2008) Modafinil increases arousal determined by P13 potential amplitude: an effect blocked by gap junction antagonists. Sleep 31:1647–1654

    PubMed Central  PubMed  Google Scholar 

  • Berger M, Riemann D (1993) Symposium: normal and abnormal REM sleep regulation: REM sleep in depression—an overview. J Sleep Res 2:211–223

    PubMed  Google Scholar 

  • Bergson C, Levenson R, Goldman-Rakic P, Lidow MS (2003) Dopamine receptor-interacting proteins: the Ca2+ connection in dopamine signaling. Trends Pharmacol Sci 24:486–492

    CAS  PubMed  Google Scholar 

  • Boissard R, Gervasoni D, Schmidt MH, Barbagli B, Fort P, Luppi PH (2002) The rat ponto-medullary network responsible for paradoxical sleep onset and maintenance: a combined microinjection and functional neuroanatomical study. Eur J Neurosci 16:1959–1973

    PubMed  Google Scholar 

  • Braff D, Stone C, Callaway E, Geyer M, Glick I, Bali L (1978) Prestimulus effects on human startle reflex in normal and schizophrenics. Psychophysiology 15:339–343

    CAS  PubMed  Google Scholar 

  • Butler RW, Braff DL, Rausch JL, Jenkins MA, Sprock J, Geyer MA (1990) Physiological evidence of exaggerated startle response in a subgroup of Vietnam veterans with combat-related PTSD. Am J Psychiat 147:1308–1313

    CAS  PubMed  Google Scholar 

  • Caldwell DF, Domino EF (1967) Electroencephalographic and eye movement patterns during sleep in chronic schizophrenic patients. Electroenceph Clin Neurophysiol 22:414–420

    CAS  PubMed  Google Scholar 

  • Coble P, Foster FG, Kupfer DJ (1976) Electroencephalographic sleep diagnosis of primary depression. Arch Gen Psychiat 33:1124–1127

    CAS  PubMed  Google Scholar 

  • Corsi-Cabrera M, Meneses S, Molina E (1987) Correlación Intrahemisférica y Acoplamiento Temporalde la Actividad Eléctrica Cortical Durante la Vigilia, la Etapa II y el Sueño Paradójico en el Hombre. Rev Mex Psicol 4:100–108

    Google Scholar 

  • Cox JA, Durussel I, Comte M, Nef P, Lenz SE, Gundelfinger ED (1994) Cation binding and conformational changes in VILIP and two neuron-specific calcium-binding proteins. J Biol Chem 269:32807–32813

    CAS  PubMed  Google Scholar 

  • Cunningham MO, Whittington MA, Bibbig A, Roopun A, LeBeau FE, Vogt A, Monyer H, Buhl EH, Traub RD (2004) A role for fast rhythmic bursting neurons in cortical gamma oscillations in vitro. Proc Natl Acad Sci USA 101:7152–7157

    CAS  PubMed Central  PubMed  Google Scholar 

  • Data S, O’Malley MW, Patterson EH (2010) Calcium/calmodulin kinase II in the pedunculopontine tegmental nucleus modulates the initiation and maintenance of wakefulness. J Neurosci 31:1700–17016

    Google Scholar 

  • Datta S (2002) Evidence that REM sleep is controlled by the activation of brain stem pedunculopontine tegmental kainite receptor. J Neurophysiol 87:1790–1798

    CAS  PubMed  Google Scholar 

  • Datta S, Desarnaud F (2010) Protein kinase A in the pedunculopontine tegmental nucleus of rat contributes to regulation of rapid eye movement sleep. J Neurosci 30:12263–12273

    CAS  PubMed Central  PubMed  Google Scholar 

  • Datta S, Siwek DF (1997) Excitation of the brain stem pedunculopontine tegmentum cholinergic cells induce wakefulness and REM sleep. J Neurophysiol 77:2975–2988

    CAS  PubMed  Google Scholar 

  • Datta S, Siwek DF (2002) Single cell activity patterns of pedunculopontine tegmentum neurons across the sleep-wake cycle in the freely moving rats. J Neurosci Res 70:611–621

    CAS  PubMed  Google Scholar 

  • Datta S, Siwek DF, Patterson EH, Cipolloni PB (1998) Localization of pontine PGO wave generation sites and their anatomical projections in the rat. Synapse 30:409–423

    CAS  PubMed  Google Scholar 

  • Datta S, Patterson EH, Siwek DF (1999) Brainstem afferents of the cholinoceptive pontine wave generation sites in the rat. Sleep Res 2:79–82

    CAS  Google Scholar 

  • Datta S, Patterson EH, Spoley EE (2001a) Excitation of pedunculopontine tegmental NMDA receptors induces wakefulness and cortical activation in the rat. J Neurosci Res 66:109–116

    CAS  PubMed  Google Scholar 

  • Datta S, Spoley EE, Patterson EH (2001b) Microinjection of glutamate into the pedunculopontine tegmentum induces REM sleep and wakefulness in the rat. Am J Physiol Reg Integ Comp Physiol 280:R752–R759

    CAS  Google Scholar 

  • Datta S, Siwek DF, Stack EC (2009) Identification of cholinergic and non-cholinergic neurons in the pons expressing phosphorylated cyclic adenosine monophosphate response element-binding protein as a function of rapid eye movement sleep. Neuroscience 163:397–414

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dement WC (1967) Studies on the effects of REM deprivation in humans and animals. Res Publ Assoc Res Nerv Ment Dis 43:456–467

    Google Scholar 

  • Desarnaud F, Macone BW, Datta S (2011) Activation of extracellular signal-regulated kinase signaling in the pedunculopontine tegmental cells is involved in the maintenance of sleep in rats. J Neurochem 116:577–587

    CAS  PubMed Central  PubMed  Google Scholar 

  • Dickelman S, Born J (2010) The memory function of sleep. Nat Rev Neurosci 11:114–126

    Google Scholar 

  • Eckhorn R, Bauer R, Jordan W, Brosch M, Kruse W, Munk M, Reitboeck HJ (1988) Coherent oscillations: a mechanism of feature linking in the visual system? Biol Cybern 60:121–130

    CAS  PubMed  Google Scholar 

  • Feinberg I, Braun M, Koresko RL, Gottlieb F (1969) Stage 4 sleep in schizophrenia. Arch Gen Psychiat 21:262–266

    CAS  PubMed  Google Scholar 

  • Garcia-Rill E (1997) Disorders of the reticular activating system. Med Hypoth 49:379–387

    CAS  Google Scholar 

  • Garcia-Rill E, Biedermann JA, Chambers T, Karson CN (1995) Mesopontine neurons in schizophrenia. Neuroscience 66:321–335

    CAS  PubMed  Google Scholar 

  • Garcia-Rill E, Kobayashi T, Good C (2003) The developmental decrease in REM sleep. Thal Rel Syst 46:1–17

    Google Scholar 

  • Garcia-Rill E, Heister DS, Ye M, Charlesworth A, Hayar A (2007) Electrical coupling: novel mechanism for sleep-wake control. Sleep 30:1405–1414

    PubMed Central  PubMed  Google Scholar 

  • Garcia-Rill E, Charlesworth A, Heister DA, Ye M, Hayar A (2008) The developmental decrease in REM sleep: the role of transmitters and electrical coupling. Sleep 31:1–18

    Google Scholar 

  • Garcia-Rill E, Kezunovic N, Hyde J, Beck P, Urbano FJ (2013) Coherence and frequency in the reticular activating system (RAS). Sleep Med Rev 17:227–238

    PubMed  Google Scholar 

  • Gibson JR, Beierlein M, Connors BW (1999) Two networks of electrically coupled inhibitory neurons in neocortex. Nature 402:75–79

    CAS  PubMed  Google Scholar 

  • Gray CM, Singer W (1989) Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex. Proc Natl Acad Sci USA 86:1698–1702

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gujar N, McDonald A, Nishida M, Walker MP (2011) A role for REM sleep in recalibrating the sensitivity of the human brain to specific emotions. Cereb Cortex 21:115–123

    PubMed Central  PubMed  Google Scholar 

  • Hasler BP, Insana SP, James JA, Germain A (2013) Evening-type veterans report worse lifetime posttraumatic stress symptoms and greater brainstem activity across wakefulness and REM sleep. Biol Psychiat 94:255–262

    Google Scholar 

  • Heister DS, Hayar A, Charlesworth A, Yates C, Zhou Y, Garcia-Rill E (2007) Evidence for electrical coupling in the SubCoeruleus (SubC) nucleus. J Neurophysiol 97:3142–3147

    PubMed Central  PubMed  Google Scholar 

  • Herlitze S, Garcia DE, Mackie K, Hille B, Scheuer T, Catterall WA (1996) Modulation of Ca2+ channels by G-protein beta gamma subunits. Nature 380:258–262

    CAS  PubMed  Google Scholar 

  • Hyde J, Kezunovic N, Urbano FJ, Garcia-Rill E (2013a) Visualization of fast calcium oscillations in the parafascicular nucleus. Pflügers Archiv 465:1327–1340

    CAS  PubMed  Google Scholar 

  • Hyde J, Kezunovic N, Urbano FJ, Garcia-Rill E (2013b) Spatiotemporal properties of high speed calcium oscillations in the pedunculopontine nucleus. J Appl Physiol 115:1402–1414

    CAS  PubMed  Google Scholar 

  • Ikeda SR (1996) Voltage-dependent modulation of N-type calcium channels by G-protein beta gamma subunits. Nature 380:255–258

    CAS  PubMed  Google Scholar 

  • Jones EG (2007) Calcium channels in higher-level brain function. Proc Natl Acad Sci USA 14:17903–17904

    Google Scholar 

  • Jus K, Bouchard M, Jus A, Villeneuve A, Lachance R (1973) Sleep EEG studies in untreated long-term schizophrenic patients. Arch Gen Psychiat 29:286–290

    Google Scholar 

  • Kammermeier PJ, Ruiz-Velasco V, Ikeda SR (2000) A voltage-independent calcium current inhibitory pathway activated by muscarinic agonists in rat sympathetic neurons requires both Gαq/11 and Gβγ. J Neurosci 20:5623–5629

    CAS  PubMed  Google Scholar 

  • Kane JM, D’Souza DC, Patkar AA, Youakim JM, Tiller JM, Yang R, Keefe RS (2010) Armodafinil as adjunctive therapy in adults with cognitive deficits associated with schizophrenia: a 4-week, double-blind, placebo-controlled study. J Clin Psychiat 71:1475–1481

    Google Scholar 

  • Kane JM, Yang R, Youakim JM (2012) Adjunctive armodafinil for negative symptoms in adults with schizophrenia: a double-blind, placebo-controlled study. Schizophr Res 135:116–122

    PubMed  Google Scholar 

  • Kezunovic K, Simon C, Hyde J, Smith K, Beck P, Odle A, Garcia-Rill E (2010) Arousal from slices to humans: translational studies on sleep-wake control. Transl Neurosci 1:2–8

    Google Scholar 

  • Kezunovic N, Urbano FJ, Simon C, Hyde J, Smith K, Garcia-Rill E (2011) Mechanism behind gamma band activity in the pedunculopontine nucleus (PPN). Eur J Neurosci 34:404–415

    PubMed Central  PubMed  Google Scholar 

  • Kezunovic N, Hyde J, Simon C, Urbano FJ, Garcia-Rill E (2012) Gamma band activity in the developing parafascicular nucleus (Pf). J Neurophysiol 107:772–784

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kezunovic N, Hyde J, Goitia B, Bisagno V, Urbano FJ, Garcia-Rill E (2013) Muscarinic modulation of high frequency activity in the pedunculopontine nucleus (PPN). Frontiers Neurol: Sleep and Chronobiol 4:176. doi:10.3389/fneur.2013.00176

    Google Scholar 

  • Kirov R, Uebel H, Albrecht B, Banachewski T, Yordanova J, Rothenberg A (2012) Attention-deficit/hyperactivity disorder (ADHD) and adaptation night as determinants of sleep patterns in children. Eur Child Adolesc Psychiat 21:681–690

    Google Scholar 

  • Koh PO, Undie AS, Kabbani N, Levenson R, Goldman-Rakic P, Lidow MS (2003) Up-regulation of neuronal calcium sensor-1 (NCS-1) in the prefrontal cortex of schizophrenic and bipolar patients. Proc Natl Acad Sci USA 100:313–317

    CAS  PubMed Central  PubMed  Google Scholar 

  • Krupfer DL (1976) REM latency: a psychobiologic marker for primary depressive disease. Biol Psychiat 11:159–174

    Google Scholar 

  • Leonard CS, Llinas R (1994) Serotonergic and cholinergic inhibition of mesopontine cholinergic neurons controlling REM sleep: an in vitro electrophysiological study. Neuroscience 59:309–330

    CAS  PubMed  Google Scholar 

  • Llinas RR (1988) The intrinsic electrophysiological properties of mammalian neurons: insights into central nervous system function. Science 242:1654–1664

    CAS  PubMed  Google Scholar 

  • Llinás RR, Steriade M (2006) Bursting of thalamic neurons and states of vigilance. J Neurophysiol 95:3297–3308

    PubMed  Google Scholar 

  • Llinas RR, Grace AA, Yarom Y (1991) In vitro neurons in mammalian cortical layer 4 exhibit intrinsic oscillatory activity in the 10- to 50-Hz frequency range. Proc Natl Acad Sci USA 88:897–901

    CAS  PubMed Central  PubMed  Google Scholar 

  • Llinas RR, Leznik E, Urbano FJ (2002) Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices. Proc Natl Acad Sci USA 99:449–454

    CAS  PubMed Central  PubMed  Google Scholar 

  • Llinas RR, Soonwook C, Urbano FJ, Hee-Sup S (2007) γ-Band deficiency and abnormal thalamocortical activity in P/Q-type channel mutant mice. Proc Natl Acad Sci USA 104:17819–17824

    CAS  PubMed Central  PubMed  Google Scholar 

  • Luebke JI, McCarley RW, Greene RW (1993) Inhibitory action of muscarinic agonists on neurons in the rat laterodorsal tegmental nucleus in vitro. J Neurosci 70:2128–2135

    CAS  Google Scholar 

  • Mamelak AN, Hobson JA (1989) Dream bizarreness as the cognitive correlate of altered neuronal brain in REM sleep. J Cog Neurosci 1:201–222

    CAS  Google Scholar 

  • Manni R, Terzaghi M, Ratti PL, Repetto A, Zangaglia R, Pacchetti C (2011) Hallucinations and REM sleep behavior disorder in Parkinson’s disease: dream imagery intrusions and other hypotheses. Consc Cgn 20:1021–1026

    Google Scholar 

  • Maquet P, Peters JM, Aerts J, Delfiore G, Degueldre C, Luxen A, Franck G (1966) Functional neuroanatomy of human rapid-eye-movement sleep and dreaming. Nature 383:163–166

    Google Scholar 

  • Martone ME, Edelmann VM, Ellisman MH, Nef P (1999) Cellular and subcellular distribution of the calcium-binding protein in the central nervous system of the rat. Cell Tissue Res 295:395–407

    CAS  PubMed  Google Scholar 

  • Mavanji V, Ulloor J, Saha S, Datta S (2004) Neurotoxic lesions of phasic pontine-wave generator cells impair retention of 2-way active avoidance memory. Sleep 27:1282–1292

    PubMed  Google Scholar 

  • Mitler MM, Dement WC (1974) Cataplectic-like behavior in cats after micro-injections of carbachol in pontine reticular formation. Brain Res 68:335–343

    CAS  PubMed Central  PubMed  Google Scholar 

  • Morgan PT, Pace-Schott E, Pittman B, Stickgold R, Malison RT (2010) Normalizing effect of modafinil on sleep in chronic cocaine users. Am J Psychiat 167:331–340

    PubMed  Google Scholar 

  • Moruzzi G, Magoun HW (1949) Brainstem reticular formation and activation. Electroenceph Clin Neurophysiol 1:455–473

    CAS  PubMed  Google Scholar 

  • Nakamura TY, Jeromin A, Mikoshiba K, Wakabayashi S (2011) Neuronal calcium sensor-1 promotes immature heart function and hypertrophy by enhancing Ca2+ signals. Circ Res 109:512–523

    CAS  PubMed  Google Scholar 

  • Ozerdem A, Guntenkin B, Atagun I, Turp B (2011) Reduced long distance gamma (28–48 Hz) coherence in euthymic patients with bipolar disorder. J Affect Disord 132:325–332

    PubMed  Google Scholar 

  • Palva S, Monto S, Palva JM (2009) Graph properties of synchronized cortical networks during visual working memory maintenance. Neuroimage 49:3257–3268

    PubMed  Google Scholar 

  • Pan CY, Jeromin A, Lundstrom K, Yoo SH, Roder J, Fox AP (2002) Alterations in exocytosis induced by neuronal Ca+2 sensor-1 in bovine chromaffin cells. J Neurosci 22:2427–2433

    CAS  PubMed  Google Scholar 

  • Panckeri KA, Schotland HM, Pack AI, Hendricks JC (1996) Modafinil decreases hypersomnolence in the English bulldog, a natural animal model of sleep-disordered breathing. Sleep 19:626–631

    CAS  PubMed  Google Scholar 

  • Pedroarena C, Llinás RR (1997) Dendritic calcium conductances generate high-frequency oscillation in thalamocortical neurons. Proc Natl Acad Sci USA 94:724–728

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pillai V, Kalmbach DA, Ciesla JA (2011) A meta-analysis of electroencephalographic sleep in depression: evidence for genetic markers. Biol Psychiat 70:912–919

    PubMed  Google Scholar 

  • Ribary U, Ioannides AA, Singh KD, Hasson R, Bolton JP, Lado F, Mogilner A, Llinás RR (1991) Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. Proc Natl Acad Sci USA 88:11037–11041

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rieman D, Spiegelhalder K, Nissen C, Hirscher V, Baglioni C, Feige B (2012) REM sleep instability: a new pathway for insomnia? Pharmacopsychiat 45:167–176

    Google Scholar 

  • Roffwarg HP, Muzio JN, Dement WC (1966) Ontogenetic development of the human sleep-dream cycle. Science 152:604–619

    CAS  PubMed  Google Scholar 

  • Ross RJ, Ball WA, Sullivan KA, Caraff SN (1989) Sleep disturbance as the hallmark of posttraumatic stress disorder. Am J Psychiat 146:697–707

    CAS  PubMed  Google Scholar 

  • Sallese M, Iacovelli L, Cumashi A, Capobianco L (2000) Regulation of G protein-coupled receptor kinase subtypes by calcium sensor proteins. Biochim Biophys Acta 1498:112–121

    CAS  PubMed  Google Scholar 

  • Sanford LD, Morrison AR, Mann GL, Harris JS, Yoo L, Ross RJ (1994) Sleep patterning and behaviour in cats with pontine lesions creating REM without atonia. J Sleep Res 3:233–240

    PubMed  Google Scholar 

  • Schredl M, Paul F, Reinhard I, Ebner-Priemer UW, Schmahl C, Bohus M (2012) Sleep and dreaming in patients with borderline personality disorder: a polysomnographic study. Psychiat Res 200:430–436

    Google Scholar 

  • Semba K, Fibiger HC (1992) Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro- and antero-grade transport and immunohistochemical study. J Comp Neurol 323:387–410

    CAS  PubMed  Google Scholar 

  • Shalev AY, Orr SP, Per T, Schreiber S, Pitman RK (1992) Physiologic responses to loud tones in Israeli patients with posttraumatic stress disorder. Arch Gen Psychiat 49:870–875

    CAS  PubMed  Google Scholar 

  • Simon C, Kezunovic N, Ye M, Hyde J, Hayar A, Williams DK, Garcia-Rill E (2010) Gamma band unit and population responses in the pedunculopontine nucleus. J Neurophysiol 104:463–474

    CAS  PubMed Central  PubMed  Google Scholar 

  • Simon C, Kezunovic N, Williams DK, Urbano FJ, Garcia-Rill E (2011) Cholinergic and glutamatergic agonists induce gamma frequency activity in dorsal subcoeruleus nucleus neurons. Am J Physiol Cell Physiol 301:C327–C335

    CAS  PubMed Central  PubMed  Google Scholar 

  • Simor P, Horvath K, Ujma PP, Gombos F, Bodizs R (2013) Fluctuations between sleep and wakefulness: wake-like features indicated by increased EEG alpha power during different stages in nightmare disorder. Biol Psychiat 94:592–600

    Google Scholar 

  • Singer W (1993) Synchronization of cortical activity and its putative role in information processing and learning. Annu Rev Physiol 55:349–374

    CAS  PubMed  Google Scholar 

  • Spencer KM, Nestor PG, Niznikiewicz MA, Salisbury DF (2003) Abnormal neural synchrony in schizophrenia. J Neurosci 23:7407–7411

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stam CJ, van Cappellen van Walsum AM, Pijnenburg YA, Berendse HW, de Munck JC, Scheltens P, van Dijk BW (2002) Generalized synchronization of MEG recordings in Alzheimer’s disease: evidence for involvement of the gamma band. J Clin Neurophysiol 19:562–574

  • Steriade M (1999) Cellular substrates of oscillations in corticothalamic systems during states of vigilance. In: Lydic R, Baghdoyan HA (eds) Handbook of behavioral state control. Cellular and molecular mechanisms. CRC Press, New York, pp 327–347

    Google Scholar 

  • Steriade M, Llinás RR (1988) The functional states of the thalamus and the associated neuronal interplay. Physiol Rev 68:649–742

    CAS  PubMed  Google Scholar 

  • Taverna E, Francolini M, Jeromin A, Hilfiker S, Roder J, Rosa P (2002) Neuronal calcium sensor 1 and phosphatidylinositol 4-OH kinase beta interact in neuronal cells and are translocated to membranes during nucleotide-evoked exocytosis. J Cell Sci 115:3909–3922

    CAS  PubMed  Google Scholar 

  • Torres KCL, Souza BR, Miranda DM, Sampiao AM, Nicolato R, Neves FS (2009) Expression of neuronal calcium sensor-1 (NCS-1) is decreased in leukocytes of schizophrenia and bipolar disorder patients. Prog Neuro-Pharmacol Biol Psychiat 33:229–234

    CAS  Google Scholar 

  • Tsujimoto T, Jeromin A, Satoh N, Roder JC, Takahashi T (2002) Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals. Science 295:2276–2279

    CAS  PubMed  Google Scholar 

  • Uhlhaas PJ, Singer W (2010) Abnormal neural oscillations and synchrony in schizophrenia. Nat Rev Neurosci 11:100–113

    CAS  PubMed  Google Scholar 

  • Urbano FJ, Leznik E, Llinas R (2007) Modafinil enhances thalamocortical activity by increasing neuronal electrotonic coupling. Proc Natl Acad Sci USA 104:12554–12559

    CAS  PubMed Central  PubMed  Google Scholar 

  • Urbano FJ, Kezunovic N, Hyde J, Simon C, Beck P, Garcia-Rill E (2013) Gamma band activity in the reticular activating system (RAS). Front Neurol: Sleep Chronobiol 3(6):1–16

    Google Scholar 

  • Vanderwolf CH (2000a) What is the significance of gamma wave activity in the pyriform cortex? Brain Res 877:125–133

    CAS  PubMed  Google Scholar 

  • Vanderwolf CH (2000b) Are neocortical gamma waves related to consciousness? Brain Res 855:217–224

    CAS  PubMed  Google Scholar 

  • Vogel GW (1975) A review of REM sleep deprivation. Arch Gen Psychiat 32:749–761

    CAS  PubMed  Google Scholar 

  • Vogel GW, Feng P, Kinney GG (2000) Ontogeny of REM sleep in rats: possible implications for endogenous depression. Physiol Behav 68:453–461

    CAS  PubMed  Google Scholar 

  • Voss U, Holzmann R, Tuin I, Hobson JA (2009) Lucid dreaming: a state of consciousness with features of both waking and non-lucid dreaming. Sleep 32:1191–1200

    PubMed Central  PubMed  Google Scholar 

  • Walker MP (2009) The role of sleep in cognition and emotion. Ann N Y Acad Sci 1156:168–197

    PubMed  Google Scholar 

  • Watson RT, Heilman KM, Miller BD (1974) Neglect after mesencephalic reticular formation lesions. Neurology 24:294–298

    CAS  PubMed  Google Scholar 

  • Weiss JL, Hui H, Burgoyne RD (2010) Neuronal calcium sensor-1 regulation of calcium channels, secretion, and neuronal outgrowth. Cell Mol Neurobiol 30:1283–1292

    CAS  PubMed  Google Scholar 

  • Whittington MA, Traub RD, Jefferys JG (1995) Synchronized oscillations in interneuron networks driven by metabotropic glutamate receptor activation. Nature 373:612–615

    CAS  PubMed  Google Scholar 

  • Ye M, Hayar A, Strotman B, Garcia-Rill E (2010) Cholinergic modulation of fast inhibitory and excitatory transmission to pedunculopontine thalamic projecting neurons. J Neurophysiol 103:2417–2432

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zarcone V, Azumi K, Dement W, Gulevich G, Kraemer H, Pivik R (1975) REM phase deprivation and schizophrenia. Arch Gen Psychiat 32:1431–1436

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by NIH award R01 NS020246 and by core facilities of the Center for Translational Neuroscience supported by NIH award P20 GM103425 to Dr. Garcia-Rill. In addition, this work was supported by grants from FONCYT-Agencia Nacional de Promoción Científica y Tecnológica; BID 1728 OC.AR. PICT 2008-2019 and PICT-2012-1769 (to Dr. Urbano), and CONICET- PIP 2011-2013-11420100100072 and PICT-2012-0924 (to Dr. Bisagno).

Author information

Authors and Affiliations

  1. Department of Neurobiology and Developmental Sciences, Center for Translational Neuroscience, University of Arkansas for Medical Sciences, Slot 847, 4301 West Markham St., Little Rock, AR, 72205, USA

    E. Garcia-Rill, N. Kezunovic, S. D’Onofrio, B. Luster & J. Hyde

  2. IFIBYNE, CONICET-UBA, Buenos Aires, Argentina

    V. Bisagno & F. J. Urbano

  3. ININFA, CONICET-UBA, Buenos Aires, Argentina

    V. Bisagno & F. J. Urbano

Authors
  1. E. Garcia-Rill
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. N. Kezunovic
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. S. D’Onofrio
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. B. Luster
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Hyde
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. V. Bisagno
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. F. J. Urbano
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to E. Garcia-Rill.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Garcia-Rill, E., Kezunovic, N., D’Onofrio, S. et al. Gamma band activity in the RAS-intracellular mechanisms. Exp Brain Res 232, 1509–1522 (2014). https://doi.org/10.1007/s00221-013-3794-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00221-013-3794-8

Keywords

Search

Navigation