Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Objectives: This limited review examines the role of the reticular activating system (RAS), especially the pedunculopontine nucleus (PPN), one site of origin of bottom-up gamma, in the symptoms of bipolar disorder (BD). Methods: The expression of neuronal calcium sensor protein 1 (NCS-1) in the brains of BD patients is increased. It has recently been found that all PPN neurons manifest intrinsic membrane beta/gamma frequency oscillations mediated by high threshold calcium channels, suggesting that it is one source of bottom-up gamma. This review specifically addresses the involvement of these channels in the manifestation of BD. Results: Excess NCS-1 was found to dampen gamma band oscillations in PPN neurons. Lithium, a first line treatment for BD, was found to decrease the effects of NCS-1 on gamma band oscillations in PPN neurons. Moreover, gamma band oscillations appear to epigenetically modulate gene transcription in PPN neurons, providing a new direction for research in BD. Conclusions: This is an area needing much additional research, especially since the dysregulation of calcium channels may help explain many of the disorders of arousal in, elicit unwanted neuroepigenetic modulation in, and point to novel therapeutic avenues for, BD. © 2018 The Authors. Bipolar Disorders Published by John Wiley & Sons Ltd.

Registro:

Documento: Artículo
Título:Bottom-up gamma and bipolar disorder, clinical and neuroepigenetic implications
Autor:Garcia-Rill, E.; D'Onofrio, S.; Mahaffey, S.C.; Bisagno, V.; Urbano, F.J.
Filiación:Center for Translational Neuroscience, University of Arkansas for Medical Sciences, Little Rock, AR, United States
IFIBYNE, CONICET, Universidad de Buenos Aires, Buenos Aires, Argentina
Palabras clave:Arousal; binding; Ca 2+ channels; gamma oscillations; lithium; NCS-1; neuroepigenetics; preconscious awareness; REM sleep; waking
Año:2019
Volumen:21
Número:2
Página de inicio:108
Página de fin:116
DOI: http://dx.doi.org/10.1111/bdi.12735
Título revista:Bipolar Disorders
Título revista abreviado:Bipolar Disord.
ISSN:13985647
CODEN:BDIIA
Registro:http://digital.bl.fcen.uba.ar/collection/paper/document/paper_13985647_v21_n2_p108_GarciaRill

Referencias:

  • Harvey, A.G., Talbot, L.S., Gershon, A., Sleep disturbances in bipolar disorder across the lifespan (2009) Clin Psychol, 16, pp. 256-277
  • Kadrmas, A., Winokur, G., Manic depressive illness and EEG abnormalities (1979) J Clin Psychiatry, 40, pp. 306-307
  • Kupfer, D.J., Foster, F.G., Coble, P., McPartland, R.J., Ulrich, R.F., The application of EEG sleep for the differential diagnosis of affective disorders (1978) Am J Psychiatry, 135, pp. 69-74
  • Kaplan, K.A., Williams, R., Hypersomnia: an overlooked, but not overestimated, sleep disturbance in bipolar disorder (2017) Evid Based Ment Health, 20, p. 59
  • Hegerl, U., Hensch, T., The vigilance regulation model of affective disorders and ADHD (2014) Neurosci Biobehav Rev, 44, pp. 45-57
  • Ng, T.H., Chung, K.F., Ho, F.Y., Yeung, W.F., Yung, K.P., Lam, T.H., Sleep-wake disturbance in interepisode bipolar disorder and high-risk individuals: a systematic review and meta-analysis (2015) Sleep Med Rev, 20, pp. 46-58
  • Geoffroy, P.A., Scott, J., Boudebesse, C., Sleep in patients with remitted bipolar disorders; a meta-analysis of actigraphy studies (2015) Acta Psychiatry Scand, 131, pp. 89-99
  • Olincy, A., Martin, L., Diminished suppression of the P50 auditory evoked potential in bipolar disorder subjects with a history of psychosis (2005) Am J Psychiatry, 162, pp. 43-49
  • Schulze, K.K., Hall, M., McDonald, C., P50 auditory evoked potential suppression in bipolar disorder patients with psychotic features and their unaffected relatives (2007) Biol Psychiatry, 62, pp. 121-128
  • Perry, W., Minassian, A., Feifel, D., Braff, D.L., Sensorimotor gating deficits in bipolar disorder patients with acute psychotic mania (2001) Biol Psychiatry, 50, pp. 418-424
  • Depue, R.A., Arbisi, P., Krauss, S., Seasonal independence of low prolactin concentration and high spontaneous blink rates in unipolar and bipolar II seasonal affective disorder (1990) Arch Gen Psychiatry, 47, pp. 356-364
  • 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
  • Garcia-Rill, E., (2015) Waking and the Reticular Activating System, p. 330. , New York, USA, Academic Press
  • Moruzzi, G., Magoun, H.W., Brain stem reticular formation and activation of the EEG (1949) Electroenceph Clin Neurophysiol, 1, pp. 455-473
  • Watson, R.T., Heilman, K.M., Miller, B.D., Neglect after mesencephalic reticular formation lesions (1974) Neurology, 24, pp. 294-298
  • Vanderwolf, C.H., Are neocortical gamma waves related to consciousness? (2000) Brain Res, 855, pp. 217-224
  • Bastos, A.M., Vezoli, J., Bosman, C.A., Visual areas exert feedforward and feedback through distinct frequency channels (2015) Neuron, 85, pp. 390-340
  • Eckhorn, R., Bauer, R., Jordan, W., Coherent oscillations: a mechanism of feature linking in the visual system? (1988) Biol Cybern, 60, pp. 121-130
  • Gray, C.M., Singer, W., Stimulus-specific neuronal oscillations in orientation columns of cat visual cortex (1989) Proc Natl Acad Sci USA, 86, pp. 1698-1702
  • 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
  • Palva, S., Monto, S., Palva, J.M., Graph properties of synchronized cortical networks during visual working memory maintenance (2009) NeuroImage, 49, pp. 3257-3268
  • Llinas, R.R., Leznik, E., Urbano, F.J., Temporal binding via cortical coincidence detection of specific and nonspecific thalamocortical inputs: a voltage-dependent dye-imaging study in mouse brain slices (2002) Proc Natl Acad Sci USA, 99, pp. 449-454
  • Llinás, R.R., Paré, D., Of dreaming and wakefulness (1991) Neuroscience, 44, pp. 521-535
  • Stam, C.J., van Cappellen van Walsum, A.M., Pijnenburg, Y.A., Berendse, H.W., de Munck, J.C., Scheltens, P., Generalized synchronization of MEG recordings in Alzheimer's disease: evidence for involvement of the gamma band (2002) J Clin Neurophysiol, 19, pp. 562-574
  • Uhlhaas, P.J., Singer, W., High-frequency oscillations and the neurobiology of schizophrenia (2013) Dial Clin Neurosci, 15, pp. 301-313
  • Garcia-Rill, E., Kezunovic, N., D'Onofrio, S., Luster, B., Hyde, J., Gamma band activity in the RAS-intracellular mechanisms (2014) Exp Brain Res, 232, pp. 1509-1522
  • Urbano, F.J., D'Onofrio, S.M., Luster, B.R., Hyde, J.R., Bisagno, V., Garcia-Rill, E., Pedunculopontine nucleus gamma band activity- preconscious awareness, waking, and REM sleep (2014) Front Sleep Chronobiol, 5, p. 210
  • Pedroarena, C., Llinás, R.R., Dendritic calcium conductances generate high-frequency oscillation in thalamocortical neurons (1997) Proc Natl Acad Sci USA, 94, pp. 724-728
  • 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
  • Colgin, L.L., Denninger, T., Fyhn, M., Frequency of gamma oscillations routes flow of information in the hippocampus (2009) Nature, 462, pp. 353-357
  • Bussey, T.J., Muir, J.L., Aggleton, J.P., Functionally dissociating aspects of event memory: the effects of combined perirhinal and postrhinal cortex lesions on object and place memory in the rat (1999) J Neurosci, 19, pp. 495-502
  • Colgin, L.L., Moser, E.I., Gamma oscillations in the hippocampus (2010) Physiology (Bethesda), 25, pp. 319-329
  • Lang, E.J., Sugihara, I., Llinás, R.R., Olivocerebellar modulation of motor cortex ability to generate vibrissal movements in rat (2006) J Physiol (Lond), 571, pp. 101-120
  • Middleton, S.J., Racca, C., Cunningham, M.O., High-frequency network oscillations in cerebellar cortex (2008) Neuron, 58, pp. 763-774
  • Soteropoulos, D.S., Baker, S.N., Cortico-cerebellar coherence during a precision grip task in the monkey (2006) J Neurophysiol, 95, pp. 1194-1206
  • Timofeev, I., Steriade, M., Fast (mainly 30-100 Hz) oscillations in the cat cerebellothalamic pathway and their synchronization with cortical potentials (1997) J Physiol (Lond), 504, pp. 153-168
  • Lalo, E., Thobois, S., Sharott, A., Patterns of bidirectional communication between cortex and basal ganglia during movement in patients with Parkinson disease (2008) J Neurosci, 28, pp. 3008-3016
  • Cheyne, G., Ferrari, P., MEG studies of motor cortex gamma oscillations: evidence for a gamma “fingerprint” in the brain? (2013) Front Human Neurosci, 7, p. 575
  • Jenkinson, N., Kuhn, A.A., Brown, P., Gamma oscillations in the human basal ganglia (2013) Exp Neurol, 245, pp. 72-76
  • Steriade, M., Paré, D., Datta, S., Oakson, G., Curro, D.R., Different cellular types in mesopontine cholinergic nuclei related to ponto-geniculo-occipital waves (1990) J Neurosci, 10, pp. 2560-2579
  • Kayama, Y., Ohta, M., Jodo, E., Firing of ‘possibly’ cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness (1992) Brain Res, 569, pp. 210-220
  • 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., Stack, E.C., 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 (2009) Neuroscience, 163, pp. 397-414
  • Steriade, M., Datta, S., Pare, D., Oakson, G., Curro Dossi, R.C., Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems (1990) J Neurosci, 10, pp. 2541-2559
  • Fraix, V., Bastin, J., David, O., Pedunculopontine nucleus area oscillations during stance, stepping and freezing in Parkinson's disease (2013) PLoS ONE, 8
  • Goetz, L., Piallat, B., Bhattacharjee, M., Mathieu, H., David, O., Chabardes, S., The primate pedunculopontine nucleus region: towards a dual role in locomotion and waking state (2016) J Neural Transm, 123, pp. 667-678
  • Simon, C., Kezunovic, N., Ye, M., Gamma band unit activity and population responses in the pedunculopontine nucleus (2010) J Neurophysiol, 104, pp. 463-474
  • 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
  • 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
  • Hyde, J.R., 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
  • Luster, B., D'Onofrio, S., Urbano, F.J., Garcia-Rill, E., High-Threshold Ca2 +  channels behind gamma band activity in the pedunculopontine nucleus (PPN) (2015) Physiol Rep, 3
  • Luster, B., Urbano, F.J., Garcia-Rill, E., Intracellular mechanisms modulating gamma band activity in the pedunculopontine nucleus (PPN) (2016) Physiol Rep, 4
  • Garcia-Rill, E., Luster, B., D'Onofrio, S., Mahaffey, S., Bisagno, V., Urbano, F.J., Implications of gamma band activity in the pedunculopontine nucleus (2015) J Neural Transm, 123, pp. 655-665
  • Garcia-Rill, E., Luster, B., Mahaffey, S., Pedunculopontine gamma band activity and development (2015) Brain Sci, 5, pp. 546-567
  • Datta, S., Spoley, E.E., Patterson, E.H., Microinjection of glutamate into the pedunculopontine tegmentum induces REM sleep and wakefulness in the rat (2001) Am J Physiol Reg Integ Comp Physiol, 280, pp. R752-R759
  • Datta, S., Patterson, E.H., Spoley, E.E., Excitation of the pedunculopontine tegmental nmda receptors induces wakefulness and cortical activation in the rat (2002) J Neurosci Res, 66, pp. 109-116
  • Datta, S., Evidence that REM sleep is controlled by the activation of brain stem pedunculopontine tegmental kainate receptor (2002) J Neurophysiol, 87, pp. 1790-1798
  • Stea, A., Soomg, T.W., Snutch, T.P., Determinants of PKC-dependent modulation of a family of neuronal Ca2 +  channels (1995) Neuron, 15, pp. 929-940
  • Jiang, X., Lautermilch, N.J., Watari, H., Westenbroek, R.E., Scheuer, T., Caterall, W.A., Modulation of Ca v 2.1 channels by Ca + /calmodulin-dependent kinase II bound to the C-terminal domain (2008) Proc Natl Acad Sci USA, 105, pp. 341-346
  • Castro, S., Falconi, A., Chase, M., Torterolo, P., Coherent neocortical 40-Hz oscillations are not present during REM sleep (2013) Eur J Neurosci, 37, pp. 1330-1339
  • Torterolo, P., Castro-Zaballa, S., Cavelli, M., Chase, M., Falconi, A., Neocortical 40 Hz oscillations during carbachol-induced rapid eye movement sleep and cataplexy (2015) Eur J Neurosci, 281, pp. 318-325
  • Garcia-Rill, E., D'Onofrio, S., Mahaffey, S., Bottom-up gamma: the pedunculopontine nucleus and reticular activating system (2016) Transl Brain Rhythm, 1, pp. 49-53
  • Garcia-Rill, E., Virmani, T., Hyde, J.R., D'Onofrio, S., Mahaffey, S., Arousal and the control of perception and movement (2016) Curr Trends Neurol, 10, pp. 53-64
  • Nakamura, T.Y., Sturm, E., Pountney, D.J., Orenzoff, B., Artman, M., Coetzee, W.A., Developmental expression of NCS1 (frequenin), a regulator of Kv4 K + channels, in mouse heart (2003) Pediatr Res, 53, pp. 554-557
  • Nakamura, T.Y., Jeromin, A., Mikoshiba, K., Wakabayashi, S., Neuronal calcium sensor-1 promotes immature heart function and hypertrophy by enhancing Ca2 +  signals (2011) Circ Res, 109, pp. 512-523
  • Kasri, N.N., Holmes, A.M., Bultynck, G., Regulation of InsP3 receptor activity by neuronal Ca2 + -binding proteins (2004) EMBO J, 23, pp. 312-321
  • Rodrigo, J., Suburo, A.M., Bentura, M.L., Distribution of the inositol 1,4,5-trisphosphate receptor, P400, in adult rat brain (1993) J Comp Neurol, 337, pp. 493-517
  • Hendricks, K.B., Wang, B.Q., Schnieders, E.A., Thorner, J., Yeast homologue of neuronal frequenin is a regulator of phosphatidylinositol-4-OH kinase (1999) Nat Cell Biol, 1, pp. 234-241
  • Rajebhosale, M., Greenwood, S., Vidugiriene, J., Jeromin, A., Hilfiker, S., Phosphatidylinositol 4-OH Kinase is a downstream target of neuronal calcium sensor 1 in enhancing exocytosis in neuroendocrine cells (2003) J Biol Chem, 278, pp. 6075-6084
  • Lian, L.Y., Pandalaneni, S.R., Patel, P., McCue, H.V., Hayesn, L.P., Burgoyne, R.D., Characterisation of the interaction of the C-terminus of the dopamine D2 receptor with neuronal calcium sensor-1 (2011) PLoS ONE, 6
  • Rousset, M., Cens, T., Gavarini, S., Jeromin, A., Charnet, P., Down-regulation of voltage-gated Ca 2+ channels by neuronal calcium sensor-1 is beta subunit-specific (2003) J Biol Chem, 278, pp. 7019-7026
  • Tsujimoto, T., Jeromin, A., Saitoh, N., Roder, J.C., Takahashi, T., Neuronal calcium sensor 1 and activity-dependent facilitation of P/Q-type calcium currents at presynaptic nerve terminals (2002) Science, 295, pp. 2276-2279
  • Weiss, J.L., Archer, D.A., Burgoyne, R.D., NCS-1/frequenin functions in an autocrine pathway regulating Ca2 +  channels in bovine adrenal chromaffin cells (2000) J Biol Chem, 275, pp. 40082-40087
  • Guo, W., Malin, S.A., Johns, D.C., Jeromin, A., Nerbonne, J.M., Modulation of Kv4-encoded K+ currents in the mammalian myocardium by neuronal calcium sensor-1 (2002) J Biol Chem, 277, pp. 26436-26443
  • D'Onofrio, S., Kezunovic, N., Hyde, J.R., Garcia-Rill, E., Modulation of gamma oscillations in the pedunculopontine nucleus (PPN) by neuronal calcium sensor protein-1 (NCS-1): relevance to schizophrenia and bipolar disorder (2015) J Neurophysiol, 113, pp. 709-719
  • D'Onofrio, S., Urbano, F.J., Messias, E., Garcia-Rill, E., Lithium decreases the effects of neuronal calcium sensor protein 1 in pedunculopontine neurons (2016) Physiol Rep, 4
  • Handley, M.T., Lian, L.Y., Haynes, L.P., Burgoyne, R.D., Structural and functional deficits in a neuronal calcium sensor-1 mutant identified in a case of autistic spectrum disorder (2010) PLoS ONE, 5
  • Leboyer, M., Kupfer, D.J., Bipolar disorder; new perspectives in health care and prevention (2010) J Clin Psychiatry, 71, pp. 1689-1695
  • Goldberg, J.F., Chengappa, K.N., Identifying and treating cognitive impairment in bipolar disorder (2009) Bipolar Disord, 11, pp. 123-137
  • Bora, E., Yucel, M., Pantelis, C., Cognitive endophenotypes of bipolar disorder: a meta-analysis of neuropsychological deficits in euthymic patients and their first-degree relatives (2009) J Affect Disord, 113, pp. 108-120
  • 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 USA, 100, pp. 313-317
  • Brown, K.M., Tracy, D.K., Lithium: the pharmacodynamics actions of the amazing ion (2012) Ther Adv Psychopharmacol, 3, pp. 163-176
  • Schlecker, C., Boehmerle, W., Jeromin, A., Neuronal calcium sensor-1 enhancement of InsP3 receptor activity is inhibited by therapeutic levels of Li + (2006) J Clin Invest, 116, pp. 16668-16674
  • Cadet, J.L., Epigenetics of stress, addiction, and resilience: therapeutic implications (2016) Mol Neurobiol, 53, pp. 545-560
  • Haberland, M., Montgomery, R.L., Olson, E.N., The many roles of histone deacetylases in development and physiology: implications for disease and therapy (2009) Nat Rev Genet, 10, pp. 32-42
  • Didonna, A., Opal, P., The promise and perils of HDAC inhibitors in neurodegeneration (2015) Ann Clin Transl Neurol, 2, pp. 79-101
  • Subramanian, S., Bates, S.E., Wright, J.J., Espinoza-Delgado, I., Piekarz, R.L., Clinical toxicities of histone deacetylase inhibitors (2010) Pharmaceuticals (Basel), 3, pp. 2751-2767
  • Urbano, F.J., Bisagno, V., Mahaffey, S., Garcia-Rill, E., Class II histone deacetylases require P/Q-type Ca 2+ channels and CaMKII to maintain gamma oscillations in the pedunculopontine nucleus (2018) Sci Rep, 8, p. 13156
  • Kezunovic, N., Hyde, J., Simon, C., Urbano, F.J., Williams, D.K., Garcia-Rill, E., Gamma band activity in the developing parafascicular nucleus (Pf) (2012) J Neurophysiol, 107, pp. 772-784
  • Hyde, J., Kezunovic, N., Urbano, F.J., Garcia-Rill, E., Visualization of fast calcium oscillations in the parafascicular nucleus (2013) Pflugers Arch, 465, pp. 1327-1340

Citas:

---------- APA ----------
Garcia-Rill, E., D'Onofrio, S., Mahaffey, S.C., Bisagno, V. & Urbano, F.J. (2019) . Bottom-up gamma and bipolar disorder, clinical and neuroepigenetic implications. Bipolar Disorders, 21(2), 108-116.
http://dx.doi.org/10.1111/bdi.12735
---------- CHICAGO ----------
Garcia-Rill, E., D'Onofrio, S., Mahaffey, S.C., Bisagno, V., Urbano, F.J. "Bottom-up gamma and bipolar disorder, clinical and neuroepigenetic implications" . Bipolar Disorders 21, no. 2 (2019) : 108-116.
http://dx.doi.org/10.1111/bdi.12735
---------- MLA ----------
Garcia-Rill, E., D'Onofrio, S., Mahaffey, S.C., Bisagno, V., Urbano, F.J. "Bottom-up gamma and bipolar disorder, clinical and neuroepigenetic implications" . Bipolar Disorders, vol. 21, no. 2, 2019, pp. 108-116.
http://dx.doi.org/10.1111/bdi.12735
---------- VANCOUVER ----------
Garcia-Rill, E., D'Onofrio, S., Mahaffey, S.C., Bisagno, V., Urbano, F.J. Bottom-up gamma and bipolar disorder, clinical and neuroepigenetic implications. Bipolar Disord. 2019;21(2):108-116.
http://dx.doi.org/10.1111/bdi.12735