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Spatial distribution and cognitive correlates of gamma noise power in schizophrenia

Published online by Cambridge University Press:  11 September 2012

Á. Díez ,
V. Suazo ,
P. Casado ,
M. Martín-Loeches  and
V. Molina
Á. Díez
Affiliation:
Basic Psychology, Psychobiology and Methodology Department, School of Psychology, University of Salamanca, Spain Institute of Biomedical Research, Salamanca, Spain
V. Suazo
Affiliation:
Institute of Biomedical Research, Salamanca, Spain Neuroscience Institute of Castilla y León, University of Salamanca, Spain
P. Casado
Affiliation:
UCM-ISCIII Center for Human Evolution and Behavior, Madrid, Spain
M. Martín-Loeches
Affiliation:
UCM-ISCIII Center for Human Evolution and Behavior, Madrid, Spain
V. Molina*
Affiliation:
Institute of Biomedical Research, Salamanca, Spain Psychiatry Service, University Hospital of Valladolid, Spain School of Medicine, University of Valladolid, Spain
*
*Address for correspondence: V. Molina, Ph.D., Psychiatry Service, University Hospital of Valladolid, Avenida Ramón y Cajal, 7, 48005 Valladolid, Spain. (Email: vmolina@med.uva.es)
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Abstract

Background

Brain activity is less organized in patients with schizophrenia than in healthy controls (HC). Noise power (scalp-recorded electroencephalographic activity unlocked to stimuli) may be of use for studying this disorganization.

Method

Fifty-four patients with schizophrenia (29 minimally treated and 25 stable treated), 23 first-degree relatives and 27 HC underwent clinical and cognitive assessments and an electroencephalographic recording during an oddball P300 paradigm to calculate noise power magnitude in the gamma band. We used a principal component analysis (PCA) to determine the factor structure of gamma noise power values across electrodes and the clinical and cognitive correlates of the resulting factors.

Results

The PCA revealed three noise power factors, roughly corresponding to the default mode network (DMN), frontal and occipital regions respectively. Patients showed higher gamma noise power loadings in the first factor when compared to HC and first-degree relatives. In the patients, frontal gamma noise factor scores related significantly and inversely to working memory and problem-solving performance. There were no associations with symptoms.

Conclusions

There is an elevated gamma activity unrelated to task processing over regions coherent with the DMN topography in patients with schizophrenia. The same type of gamma activity over frontal regions is inversely related to performance in tasks with high involvement in these frontal areas. The idea of gamma noise as a possible biological marker for schizophrenia seems promising. Gamma noise might be of use in the study of underlying neurophysiological mechanisms involved in this disease.

Keywords

Default mode networkfirst-degree relativesfrontal regionsproblem solvingpsychosisworking memory
Type
Original Articles
Information
Psychological Medicine , Volume 43 , Issue 6 , June 2013 , pp. 1175 - 1185
Copyright
Copyright © Cambridge University Press 2012 

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References

Almeida, PR, Vieira, JB, Silveira, C, Ferreira-Santos, F, Chaves, PL, Barbosa, F, Marques-Teixeira, J (2011). Exploring the dynamics of P300 amplitude in patients with schizophrenia. International Journal of Psychophysiology 81, 159–168.CrossRefGoogle ScholarPubMed
Barr, MS, Farzan, F, Tran, LC, Chen, R, Fitzgerald, PB, Daskalakis, ZJ (2010). Evidence for excessive frontal evoked gamma oscillatory activity in schizophrenia during working memory. Schizophrenia Research 121, 146–152.CrossRefGoogle ScholarPubMed
Bledowski, C, Prvulovic, D, Hoechstetter, K, Scherg, M, Wibral, M, Goebel, R, Linden, DE (2004). Localizing P300 generators in visual target and distractor processing: a combined event-related potential and functional magnetic resonance imaging study. Journal of Neuroscience 24, 9353–9360.CrossRefGoogle ScholarPubMed
BrainVision (2006). BrainVision Analyzer. User Manual, pp. 55–56. Brain Products GmbH: Munich, Germany.Google Scholar
Broyd, SJ, Demanuele, C, Debener, S, Helps, SK, James, CJ, Sonuga-Barke, EJ (2009). Default-mode brain dysfunction in mental disorders: a systematic review. Neuroscience and Biobehavioral Reviews 33, 279–296.CrossRefGoogle ScholarPubMed
Buzsáki, G (2006 a). Diversity of cortical functions: inhibition. In Rhythms of the Brain, pp. 61–79. Oxford University Press: New York.CrossRefGoogle Scholar
Buzsáki, G (2006 b). The gamma buzz: gluing by oscillations in the waking brain. In Rhythms of the Brain, pp. 231–261. Oxford University Press: New York.CrossRefGoogle Scholar
Doesburg, SM, Roggeveen, AB, Kitajo, K, Ward, LM (2008). Large-scale gamma-band phase synchronization and selective attention. Cerebral Cortex 18, 386–396.CrossRefGoogle ScholarPubMed
Eichele, T, Debener, S, Calhoun, VD, Specht, K, Engel, AK, Hugdahl, K, von Cramon, DY, Ullsperger, M (2008). Prediction of human errors by maladaptive changes in event-related brain networks. Proceedings of the National Academy of Sciences USA 105, 6173–6178.CrossRefGoogle ScholarPubMed
Ford, JM, Roach, BJ, Faustman, WO, Mathalon, DH (2008). Out-of-synch and out-of-sorts: dysfunction of motor-sensory communication in schizophrenia. Biological Psychiatry 63, 736–743.CrossRefGoogle ScholarPubMed
Gandal, MJ, Edgar, JC, Klook, K, Siegel, SJ (2011). Gamma synchrony: towards a translational biomarker for the treatment-resistant symptoms of schizophrenia. Neuropharmacology 62, 1504–1518.CrossRefGoogle ScholarPubMed
Gonzalez-Burgos, G, Lewis, DA (2012). NMDA receptor hypofunction, parvalbumin-positive neurons and cortical gamma oscillations in schizophrenia. Schizophrenia Bulletin. Published online: 21 February 2012. doi:10.1093/schbul/sbs010.CrossRefGoogle ScholarPubMed
Hill, K, Mann, L, Laws, KR, Stephenson, CM, Nimmo-Smith, I, McKenna, PJ (2004). Hypofrontality in schizophrenia: a meta-analysis of functional imaging studies. Acta Psychiatrica Scandinavica 110, 243–256.CrossRefGoogle ScholarPubMed
Jensen, O, Kaiser, J, Lachaux, JP (2007). Human gamma-frequency oscillations associated with attention and memory. Trends in Neurosciences 30, 317–324.CrossRefGoogle ScholarPubMed
Kay, SR, Fiszbein, A, Opler, LA (1987). The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophrenia Bulletin 13, 261–276.CrossRefGoogle ScholarPubMed
Lakatos, P, Chen, CM, O'Connell, MN, Mills, A, Schroeder, CE (2007). Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53, 279–292.CrossRefGoogle ScholarPubMed
Lewis, DA, Hashimoto, T, Volk, DW (2005). Cortical inhibitory neurons and schizophrenia. Nature Reviews Neuroscience 6, 312–324.CrossRefGoogle ScholarPubMed
Lewis, DA, Sweet, RA (2009). Schizophrenia from a neural circuitry perspective: advancing toward rational pharmacological therapies. Journal of Clinical Investigation 119, 706–716.CrossRefGoogle ScholarPubMed
Light, GA, Hsu, JL, Hsieh, MH, Meyer-Gomes, K, Sprock, J, Swerdlow, NR, Braff, DL (2006). Gamma band oscillations reveal neural network cortical coherence dysfunction in schizophrenia patients. Biological Psychiatry 60, 1231–1240.CrossRefGoogle ScholarPubMed
Manoach, DS (2003). Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Schizophrenia Research 60, 285–298.CrossRefGoogle ScholarPubMed
Möcks, J, Kohler, W, Gasser, T, Pham, DT (1988). Novel approaches to the problem of latency jitter. Psychophysiology 25, 217–226.CrossRefGoogle Scholar
Niessing, J, Ebisch, B, Schmidt, KE, Niessing, M, Singer, W, Galuske, RA (2005). Hemodynamic signals correlate tightly with synchronized gamma oscillations. Science 309, 948–951.CrossRefGoogle ScholarPubMed
Ongur, D, Lundy, M, Greenhouse, I, Shinn, AK, Menon, V, Cohen, BM, Renshaw, PF (2010). Default mode network abnormalities in bipolar disorder and schizophrenia. Psychiatry Research 183, 59–68.CrossRefGoogle ScholarPubMed
Phillips, WA, Silverstein, SM (2003). Convergence of biological and psychological perspectives on cognitive coordination in schizophrenia. Behavioral and Brain Sciences 26, 65–82.CrossRefGoogle ScholarPubMed
Pomarol-Clotet, E, Salvador, R, Sarro, S, Gomar, J, Vila, F, Martinez, A, Guerrero, A, Ortiz-Gil, J, Sans-Sansa, B, Capdevila, A, Cebamanos, JM, McKenna, PJ (2008). Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network? Psychological Medicine 38, 1185–1193.CrossRefGoogle ScholarPubMed
Raichle, ME, MacLeod, AM, Snyder, AZ, Powers, WJ, Gusnard, DA, Shulman, GL (2001). A default mode of brain function. Proceedings of the National Academy of Sciences USA 98, 676–682.CrossRefGoogle ScholarPubMed
Raichle, ME, Snyder, AZ (2007). A default mode of brain function: a brief history of an evolving idea. NeuroImage 37, 1083–1090.CrossRefGoogle ScholarPubMed
Rutishauser, U, Ross, IB, Mamelak, AN, Schuman, EM (2010). Human memory strength is predicted by theta-frequency phase-locking of single neurons. Nature 464, 903–907.CrossRefGoogle ScholarPubMed
Rutter, L, Carver, FW, Holroyd, T, Nadar, SR, Mitchell-Francis, J, Apud, J, Weinberger, D, Coppola, R (2009). Magnetoencephalographic gamma power reduction in patients with schizophrenia during resting condition. Human Brain Mapping 30, 3254–3264.CrossRefGoogle ScholarPubMed
Scheeringa, R, Fries, P, Petersson, KM, Oostenveld, R, Grothe, I, Norris, DG, Hagoort, P, Bastiaansen, MC (2011). Neuronal dynamics underlying high- and low-frequency EEG oscillations contribute independently to the human BOLD signal. Neuron 69, 572–583.CrossRefGoogle Scholar
Segarra, N, Bernardo, M, Gutierrez, F, Justicia, A, Fernadez-Egea, E, Allas, M, Safont, G, Contreras, F, Gascon, J, Soler-Insa, PA, Menchon, JM, Junque, C, Keefe, RS (2011). Spanish validation of the Brief Assessment in Cognition in Schizophrenia (BACS) in patients with schizophrenia and healthy controls. European Psychiatry 26, 69–73.CrossRefGoogle ScholarPubMed
Singer, W (1993). Synchronization of cortical activity and its putative role in information processing and learning. Annual Review of Physiology 55, 349–374.CrossRefGoogle ScholarPubMed
Singer, W (1999). Neuronal synchrony: a versatile code for the definition of relations? Neuron 24, 49–65.CrossRefGoogle ScholarPubMed
Sohal, VS, Zhang, F, Yizhar, O, Deisseroth, K (2009). Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698–702.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Spreng, RN, Mar, RA, Kim, AS (2009). The common neural basis of autobiographical memory, prospection, navigation, theory of mind, and the default mode: a quantitative meta-analysis. Journal of Cognitive Neuroscience 21, 489–510.CrossRefGoogle Scholar
Suazo, V, Diez, A, Martin, C, Ballesteros, A, Casado, P, Martin-Loeches, M, Molina, V (2012). Elevated noise power in the gamma band related to negative symptoms and memory deficit in schizophrenia. Progress in Neuro-Psychopharmacology and Biological Psychiatry 38, 270–275.CrossRefGoogle ScholarPubMed
Tallon-Baudry, C, Bertrand, O, Peronnet, F, Pernier, J (1998). Induced gamma-band activity during the delay of a visual short-term memory task in humans. Journal of Neuroscience 18, 4244–4254.CrossRefGoogle ScholarPubMed
Teale, P, Collins, D, Maharajh, K, Rojas, DC, Kronberg, E, Reite, M (2008). Cortical source estimates of gamma band amplitude and phase are different in schizophrenia. NeuroImage 42, 1481–1489.CrossRefGoogle ScholarPubMed
Uhlhaas, PJ, Pipa, G, Lima, B, Melloni, L, Neuenschwander, S, Nikolic, D, Singer, W (2009). Neural synchrony in cortical networks: history, concept and current status. Frontiers in Integrative Neuroscience 3, 17.CrossRefGoogle ScholarPubMed
Uhlhaas, PJ, Singer, W (2006). Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron 52, 155–168.CrossRefGoogle ScholarPubMed
Uhlhaas, PJ, Singer, W (2010). Abnormal neural oscillations and synchrony in schizophrenia. Nature Reviews Neuroscience 11, 100–113.CrossRefGoogle ScholarPubMed
Venables, NC, Bernat, EM, Sponheim, SR (2009). Genetic and disorder-specific aspects of resting state EEG abnormalities in schizophrenia. Schizophrenia Bulletin 35, 826–839.CrossRefGoogle ScholarPubMed
Wechsler, D (1997). Wechsler Adult Intelligence Scale, 3rd edn.The Psychological Corporation: San Antonio, TX.Google Scholar
Weisbrod, M, Hill, H, Niethammer, R, Sauer, H (1999). Genetic influence on auditory information processing in schizophrenia: P300 in monozygotic twins. Biological Psychiatry 46, 721–725.CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S, Thermenos, HW, Milanovic, S, Tsuang, MT, Faraone, SV, McCarley, RW, Shenton, ME, Green, AI, Nieto-Castanon, A, LaViolette, P, Wojcik, J, Gabrieli, JD, Seidman, LJ (2009). Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proceedings of the National Academy of Sciences USA 106, 1279–1284.CrossRefGoogle ScholarPubMed
Winterer, G, Coppola, R, Goldberg, TE, Egan, MF, Jones, DW, Sanchez, CE, Weinberger, DR (2004). Prefrontal broadband noise, working memory, and genetic risk for schizophrenia. American Journal of Psychiatry 161, 490–500.CrossRefGoogle ScholarPubMed
Winterer, G, Ziller, M, Dorn, H, Frick, K, Mulert, C, Dahhan, N, Herrmann, WM, Coppola, R (1999). Cortical activation, signal-to-noise ratio and stochastic resonance during information processing in man. Clinical Neurophysiology 110, 1193–1203.CrossRefGoogle ScholarPubMed
Winterer, G, Ziller, M, Dorn, H, Frick, K, Mulert, C, Wuebben, Y, Herrmann, WM, Coppola, R (2000). Schizophrenia: reduced signal-to-noise ratio and impaired phase-locking during information processing. Clinical Neurophysiology 111, 837–849.CrossRefGoogle ScholarPubMed
Zhou, Y, Liang, M, Tian, L, Wang, K, Hao, Y, Liu, H, Liu, Z, Jiang, T (2007). Functional disintegration in paranoid schizophrenia using resting-state fMRI. Schizophrenia Research 97, 194–205.CrossRefGoogle ScholarPubMed
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