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Increased visual gamma power in schizoaffective bipolar disorder

Published online by Cambridge University Press:  13 August 2014

J. A. Brealy ,
A. Shaw ,
H. Richardson ,
K. D. Singh ,
S. D. Muthukumaraswamy  and
P. A. Keedwell
J. A. Brealy
Affiliation:
Institute of Psychological Medicine and Clinical Neurosciences, MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University School of Medicine, Hadyn Ellis Building, Cardiff, UK
A. Shaw
Affiliation:
Institute of Psychological Medicine and Clinical Neurosciences, MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University School of Medicine, Hadyn Ellis Building, Cardiff, UK
H. Richardson
Affiliation:
Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Park Place, Cardiff, UK
K. D. Singh
Affiliation:
Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Park Place, Cardiff, UK
S. D. Muthukumaraswamy
Affiliation:
Cardiff University Brain Research Imaging Centre, School of Psychology, Cardiff University, Park Place, Cardiff, UK
P. A. Keedwell*
Affiliation:
Institute of Psychological Medicine and Clinical Neurosciences, MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University School of Medicine, Hadyn Ellis Building, Cardiff, UK
*
*Address for correspondence: Dr P. A. Keedwell, Institute of Psychological Medicine and Clinical Neurosciences, MRC Centre for Neuropsychiatric Genetics and Genomics, Cardiff University School of Medicine, Hadyn Ellis Building, Maindy Road, Cathays, Cardiff CF24 4HQ, UK. (Email: [email protected])
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Abstract

Background.

Electroencephalography and magnetoencephalography (MEG) studies have identified alterations in gamma-band (30–80 Hz) cortical activity in schizophrenia and mood disorders, consistent with neural models of disturbed glutamate (and GABA) neuron influence over cortical pyramidal cells. Genetic evidence suggests specific deficits in GABA-A receptor function in schizoaffective bipolar disorder (SABP), a clinical syndrome with features of both bipolar disorder and schizophrenia. This study investigated gamma oscillations in this under-researched disorder.

Method.

MEG was used to measure induced gamma and evoked responses to a visual grating stimulus, known to be a potent inducer of primary visual gamma oscillations, in 15 individuals with remitted SABP, defined using Research Diagnostic Criteria, and 22 age- and sex-matched healthy controls.

Results.

Individuals with SABP demonstrated increased sustained visual cortical power in the gamma band (t35 = −2.56, p = 0.015) compared to controls. There were no group differences in baseline gamma power, transient or sustained gamma frequency, alpha band responses or pattern onset visual-evoked responses.

Conclusions.

Gamma power is increased in remitted SABP, which reflects an abnormality in the cortical inhibitory-excitatory balance. Although an interaction between gamma power and medication can not be ruled out, there were no group differences in evoked responses or baseline measures. Further work is needed in other clinical populations and at-risk relatives. Pharmaco-magnetoencephalography studies will help to elucidate the specific GABA and glutamate pathways affected.

Keywords

GABAgamma oscillationsglutamatemagnetoencephalographyschizoaffective bipolar disordervisual
Type
Original Articles
Information
Psychological Medicine , Volume 45 , Issue 4 , March 2015 , pp. 783 - 794
Copyright
Copyright © Cambridge University Press 2014 

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References

Adams, RA, Stephan, KE, Brown, HR, Frith, CD, Friston, KJ (2013). The computational anatomy of psychosis. Front Psychiatry 4, 47.Google Scholar
Addington, D, Addington, J, Schissel, B (1990). A depression rating scale for schizophrenics. Schizophrenia Research 3, 247–251.Google Scholar
Andreasen, NC (1983). The Scale for the Assessment of Negative Symptoms (SANS). University of Iowa: Iowa City.Google Scholar
Andreasen, NC (1984). The Scale for the Assessment of Positive Symptoms (SAPS). University of Iowa: Iowa City.Google Scholar
Andreasen, NC, Endicott, J, Spitzer, RL, Winokur, G (1977). The family history method using diagnostic criteria. Reliability and validity. Archives of General Psychiatry 34, 1229–1235.Google Scholar
Arai, AC, Kessler, M (2007). Pharmacology of ampakine modulators: From AMPA receptors to synapses and behavior. Current Drug Targets 8, 583–602.Google Scholar
Arnal, LH, Giraud, AL (2012). Cortical oscillations and sensory predictions. Trends in Cognitive Science 16, 390–398.Google Scholar
Bartos, M, Vida, I, Jonas, P (2007). Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks. Nature Reviews Neuroscience 8, 45–56.Google Scholar
Breuer, R, Hamshere, ML, Strohmaier, J, Mattheisen, M, Degenhardt, F, Meier, S, Paul, T, O'Donovan, MC, Muhleisen, TW, Schulze, TG, Nothen, MM, Cichon, S, Craddock, N, Rietschel, M (2011). Independent evidence for the selective influence of GABA(A) receptors on one component of the bipolar disorder phenotype. Molecular Psychiatry 16, 587–589.Google Scholar
Buzsaki, G, Wang, XJ (2012). Mechanisms of gamma oscillations. Annual Review of Neuroscience 35, 203–225.Google Scholar
Campbell, AE, Sumner, P, Singh, KD, Muthukumaraswamy, SD (2014). Acute effects of alcohol on stimulus-induced gamma oscillations in human primary visual and motor cortices. Neuropsychopharmacology 39, 2104–2113.Google Scholar
Capogna, M, Pearce, RA (2011). GABA(A,slow): causes and consequences. Trends in Neurosciences 34, 101–112.Google Scholar
Costa, E, Davis, JM, Dong, E, Grayson, DR, Guidotti, A, Tremolizzo, L, Veldic, M (2004). A GABAergic cortical deficit dominates schizophrenia pathophysiology. Critical Reviews in Neurobiology 16, 1–23.Google Scholar
Craddock, N, Jones, L, Jones, IR, Kirov, G, Green, EK, Grozeva, D, Moskvina, V, Nikolov, I, Hamshere, ML, Vukcevic, D, Caesar, S, Gordon-Smith, K, Fraser, C, Russell, E, Norton, N, Breen, G, St Clair, D, Collier, DA, Young, AH, Ferrier, IN, Farmer, A, McGuffin, P, Holmans, PA, Donnelly, P, Owen, MJ, O'Donovan, MC, Wellcome Trust Case Control C (2010). Strong genetic evidence for a selective influence of GABA(A) receptors on a component of the bipolar disorder phenotype (vol. 15, p. 146, 2010). Molecular Psychiatry 15, 1121–1121.Google Scholar
Ethridge, LE, Hamm, JP, Shapiro, JR, Summerfelt, AT, Keedy, SK, Stevens, MC, Pearlson, G, Tamminga, CA, Boutros, NN, Sweeney, JA, Keshavan, MS, Thaker, G, Clementz, BA (2012). Neural activations during auditory oddball processing discriminating schizophrenia and psychotic bipolar disorder. Biological Psychiatry 72, 766–774.Google Scholar
Featherstone, RE, Phillips, JM, Thieu, T, Ehrlichman, RS, Halene, TB, Leiser, SC, Christian, E, Johnson, E, Lerman, C, Siegel, SJ (2012). Nicotine receptor subtype-specific effects on auditory evoked oscillations and potentials. PLoS ONE 7, e39775.Google Scholar
Ferrarelli, F, Sarasso, S, Guller, Y, Riedner, BA, Peterson, MJ, Bellesi, M, Massimini, M, Postle, BR, Tononi, G (2012). Reduced natural oscillatory frequency of frontal thalamocortical circuits in schizophrenia. Archives of General Psychiatry 69, 766–774.Google Scholar
Gonzalez-Burgos, G, Hashimoto, T, Lewis, DA (2010). Alterations of cortical GABA neurons and network oscillations in schizophrenia. Current Psychiatry Reports 12, 335–344.Google Scholar
Grützner, C, Wibral, M, Sun, L, Rivolta, D, Singer, W, Maurer, K, Uhlhaas, PJ (2013). Deficits in high- (>60 Hz) gamma-band oscillations during visual processing in schizophrenia. Frontiers in Human Neuroscience 7, 88.60+Hz)+gamma-band+oscillations+during+visual+processing+in+schizophrenia.+Frontiers+in+Human+Neuroscience+7,+88.>Google Scholar
Haenschel, C, Linden, D (2011). Exploring intermediate phenotypes with EEG: working memory dysfunction in schizophrenia. Behavioural Brain Research 216, 481–495.Google Scholar
Hall, MH, Spencer, KM, Schulze, K, McDonald, C, Kalidindi, S, Kravariti, E, Kane, F, Murray, RM, Bramon, E, Sham, P, Rijsdijk, F (2011). The genetic and environmental influences of event-related gamma oscillations on bipolar disorder. Bipolar Disorders 13, 260–271.Google Scholar
Harrow, M, Grossman, LS, Herbener, ES, Davies, EW (2000). Ten-year outcome: patients with schizoaffective disorders, schizophrenia, affective disorders and mood-incongruent psychotic symptoms. British Journal of Psychiatry 177, 421–426.Google Scholar
Hashimoto, T, Volk, DW, Eggan, SM, Mirnics, K, Pierri, JN, Sun, ZX, Sampson, AR, Lewis, DA (2003). Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia. Journal of Neuroscience 23, 6315–6326.Google Scholar
Homayoun, H, Moghaddam, B (2007). NMDA receptor hypofunction produces opposite effects on prefrontal cortex interneurons and pyramidal neurons. Journal of Neuroscience 27, 11496–11500.Google Scholar
Hong, LE, Summerfelt, A, McMahon, R, Adami, H, Francis, G, Elliott, A, Buchanan, RW, Thaker, GK (2004). Evoked gamma band synchronization and the liability for schizophrenia. Schizophrenia Research 70, 293–302.Google Scholar
Hoogenboom, N, Schoffelen, JM, Oostenveld, R, Parkes, LM, Fries, P (2006). Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 29, 764–773.Google Scholar
Janssen, B, Weinmann, S, Berger, M, Gaebel, W (2004). Validation of polypharmacy process measures in inpatient schizophrenia care. Schizophrenia Bulletin 30, 1023–1033.Google Scholar
Jia, XX, Xing, DJ, Kohn, A (2013). No consistent relationship between gamma power and peak frequency in macaque primary visual cortex. Journal of Neuroscience 33, 17–21.Google Scholar
Jones, NC, Reddy, M, Anderson, P, Salzberg, MR, O'Brien, TJ, Pinault, D (2012). Acute administration of typical and atypical antipsychotics reduces EEG gamma power, but only the preclinical compound LY379268 reduces the ketamine-induced rise in gamma power. International Journal of Neuropsychopharmacology 15, 657–668.Google Scholar
Kirov, G, Pocklington, AJ, Holmans, P, Ivanov, D, Ikeda, M, Ruderfer, D, Moran, J, Chambert, K, Toncheva, D, Georgieva, L, Grozeva, D, Fjodorova, M, Wollerton, R, Rees, E, Nikolov, I, van de Lagemaat, LN, Bayés, A, Fernandez, E, Olason, PI, Böttcher, Y, Komiyama, NH, Collins, MO, Choudhary, J, Stefansson, K, Stefansson, H, Grant, SG, Purcell, S, Sklar, P, O'Donovan, MC, Owen, MJ (2012). De novo CNV analysis implicates specific abnormalities of postsynaptic signalling complexes in the pathogenesis of schizophrenia. Molecular Psychiatry 17, 142–153.Google Scholar
Kissler, J, Muller, MM, Fehr, T, Rockstroh, B, Elbert, T (2000). MEG gamma band activity in schizophrenia patients smd healthy subjects in a mental arithmetic task and at rest. Clinical Neurophysiology 111, 2079–2087.Google Scholar
Kwon, JS, O'Donnell, BF, Wallenstein, GV, Greene, RW, Hirayasu, Y, Nestor, PG, Hasselmo, ME, Potts, GF, Shenton, ME, McCarley, RW (1999). Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. Archives of General Psychiatry 56, 1001–1005.Google Scholar
Lewis, DA, Curley, AA, Glausier, JR, Volk, DW (2012). Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia. Trends in Neurosciences 35, 57–67.Google Scholar
Liu, TY, Hsieh, JC, Chen, YS, Tu, PC, Su, TP, Chen, LF (2012). Different patterns of abnormal gamma oscillatory activity in unipolar and bipolar disorder patients during an implicit emotion task. Neuropsychologia 50, 1514–1520.Google Scholar
Maris, E, Oostenveld, R (2007). Nonparametric statistical testing of EEG- and MEG-data. Journal of Neuroscience Methods 164, 177–190.Google Scholar
Martucci, L, Wong, AH, De Luca, V, Likhodi, O, Wong, GW, King, N, Kennedy, JL (2006). N-methyl-D-aspartate receptor NR2B subunit gene GRIN2B in schizophrenia and bipolar disorder: polymorphisms and mRNA levels. Schizophrenia Research 84, 214–221.Google Scholar
Minzenberg, MJ, Firl, AJ, Yoon, JH, Gomes, GC, Reinking, C, Carter, CS (2010). Gamma oscillatory power is impaired during cognitive control independent of medication status in first-episode schizophrenia. Neuropsychopharmacology 35, 2590–2599.Google Scholar
Mulert, C, Kirsch, V, Pascual-Marqui, R, McCarley, RW, Spencer, KM (2011). Long-range synchrony of gamma oscillations and auditory hallucination symptoms in schizophrenia. International Journal of Psychophysiology 79, 55–63.Google Scholar
Muthukumaraswamy, SD, Edden, RAE, Jones, DK, Swettenham, JB, Singh, KD (2009). Resting GABA concentration predicts peak gamma frequency and fMRI amplitude in response to visual stimulation in humans. Proceedings of the National Academy of Sciences USA 106, 8356–8361.Google Scholar
Muthukumaraswamy, SD, Myers, JF, Wilson, SJ, Nutt, DJ, Hamandi, K, Lingford-Hughes, A, Singh, KD (2013). Elevating endogenous GABA levels with GAT-1 blockade modulates evoked but not induced responses in human visual cortex. Neuropsychopharmacology 1, 1–8.Google Scholar
Muthukumaraswamy, SD, Singh, KD, Swettenham, JB, Jones, DK (2010). Visual gamma oscillations and evoked responses: variability, repeatability and structural MRI correlates. NeuroImage 49, 3349–3357.Google Scholar
Nichols, TE, Holmes, AP (2002). Nonparametric permutation tests for functional neuroimaging: a primer with examples. Human Brain Mapping 15, 1–25.Google Scholar
O'Donnell, BF, Hetrick, WP, Vohs, JL, Krishnan, GP, Carroll, CA, Shekhar, A (2004). Neural synchronization deficits to auditory stimulation in bipolar disorder. Neuroreport 15, 1369–1372.Google Scholar
Oke, OO, Magony, A, Anver, H, Ward, PD, Jiruska, P, Jefferys, JGR, Vreugdenhil, M (2010). High-frequency gamma oscillations coexist with low-frequency gamma oscillations in the rat visual cortex in vitro. European Journal of Neuroscience 31, 1435–1445.Google Scholar
Perry, G, Brindley, LM, Muthukumaraswamy, SD, Singh, KD, Hamandi, K (2014). Evidence for increased visual gamma responses in photosensitive epilepsy. Epilepsy Research 108, 1076–1086.Google Scholar
Reite, M, Teale, P, Collins, D, Rojas, DC (2010). Schizoaffective disorder – A possible MEG auditory evoked field biomarker. Psychiatry Research – Neuroimaging 182, 284–286.Google Scholar
Riečanský, I, Kašpárek, T, Rehulová, J, Katina, S, Přikryl, R (2010). Aberrant EEG responses to gamma-frequency visual stimulation in schizophrenia. Schizophrenia Research 124, 101–109.Google Scholar
Robinson, SE (2004). Localization of event-related activity by SAM(erf). Neurology & Clinical Neurophysiology 2004, 109.Google Scholar
Robinson, SE, Vrba, J (1999). Functional neuroimaging by syntheticaperture magnetometry (SAM). In Recent Advances in Biomagnetism (ed. Yoshimoto, T., Kotani, M., Kuriki, S., Karibe, H. and Nakasato, N.), pp. 302–305. Tohoku University Press: Sendai, Japan.Google Scholar
Saxena, N, Muthukumaraswamy, SD, Diukova, A, Singh, K, Hall, J, Wise, R (2013). Enhanced stimulus-induced gamma activity in humans during propofol-induced sedation. PLoS ONE 8, e57685.Google Scholar
Schulz, SB, Heidmann, KE, Mike, A, Klaft, ZJ, Heinemann, U, Gerevich, Z (2012). First and second generation antipsychotics influence hippocampal gamma oscillations by interactions with 5-HT3 and D-3 receptors. British Journal of Pharmacology 167, 1480–1491.Google Scholar
Sheehan, DV, Lecrubier, Y, Sheehan, KH, Amorim, P, Janavs, J, Weiller, E, Hergueta, T, Baker, R, Dunbar, GC (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. Journal of Clinical Psychiatry 59, 22–33.Google Scholar
Spaak, E, Bonnefond, M, Maier, A, Leopold, DA, Jensen, O (2012). Layer-specific entrainment of gamma-band neural activity by the alpha rhythm in monkey visual cortex. Current Biology 22, 2313–2318.Google Scholar
Spencer, KM (2009). The functional consequences of cortical circuit abnormalities on gamma oscillations in schizophrenia: insights from computational modeling. Frontiers in Human Neuroscience 3, 33.Google Scholar
Spencer, KM (2012). Baseline gamma power during auditory steady-state stimulation in schizophrenia. Frontiers in Human Neuroscience 5, 190.Google Scholar
Spencer, KM, Nestor, PG, Perlmutter, R, Niznikiewicz, MA, Klump, MC, Frumin, M, Shenton, ME, McCarley, RW (2004). Neural synchrony indexes disordered perception and cognition in schizophrenia. Proceedings of the National Academy of Sciences of the United States of America 101, 17288–17293.Google Scholar
Spencer, KM, Niznikiewicz, MA, Nestor, PG, Shenton, ME, McCarley, RW (2009). Left auditory cortex gamma synchronization and auditory hallucination symptoms in schizophrenia. BMC Neuroscience 10, 85.Google Scholar
Spencer, KM, Niznikiewicz, MA, Shenton, ME, McCarley, RW (2008). Sensory-evoked gamma oscillations in chronic schizophrenia. Biological Psychiatry 63, 744–747.Google Scholar
Spitzer, RL, Endicott, J, Robins, E (1978). Research diagnostic criteria: rationale and reliability. Archives of General Psychiatry 35, 773–782.Google Scholar
Stone, JM, Dietrich, C, Edden, R, Mehta, MA, De Simoni, S, Reed, LJ, Krystal, JH, Nutt, D, Barker, GJ (2012). Ketamine effects on brain GABA and glutamate levels with 1H-MRS: relationship to ketamine-induced psychopathology. Molecular Psychiatry 17, 664–665.Google Scholar
Thompson, M, Weickert, CS, Wyatt, E, Webster, MJ (2009). Decreased glutamic acid decarboxylase(67) mRNA expression in multiple brain areas of patients with schizophrenia and mood disorders. Journal of Psychiatric Research 43, 970–977.Google Scholar
Uhlhaas, PJ, Linden, DEJ, Singer, W, Haenschel, C, Lindner, M, Maurer, K, Rodriguez, E (2006). Dysfunctional long-range coordination of neural activity during Gestalt perception in schizophrenia. Journal of Neuroscience 26, 8168–8175.Google Scholar
Vrba, J, Robinson, SE (2001). Signal processing in magnetoencephalography. Methods 25, 249–271.Google Scholar
Wood, J, Kim, Y, Moghaddam, B (2012). Disruption of Prefrontal Cortex Large Scale Neuronal Activity by Different Classes of Psychotomimetic Drugs. Journal of Neuroscience 32, 3022–3031.Google Scholar
Woods, SW (2003). Chlorpromazine equivalent doses for the newer atypical antipsychotics. Journal of Clinical Psychiatry 64, 663–667.Google Scholar
Wynn, JK, Light, GA, Breitmeyer, B, Nuechterlein, KH, Green, MF (2005). Event-related gamma activity in schizophrenia patients during a visual backward-masking task. American Journal of Psychiatry 162, 2330–2336.Google Scholar
Young, RC, Biggs, JT, Ziegler, VE, Meyer, DA (1978). A rating scale for mania: reliability, validity and sensitivity. British Journal of Psychiatry 133, 429–435.Google Scholar