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The Journal of Neuroscience, July 29, 2009, 29(30):9481-9489; doi:10.1523/JNEUROSCI.1428-09.2009

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Neurobiology of Disease
Cortical Oscillatory Activity Is Critical for Working Memory as Revealed by Deficits in Early-Onset Schizophrenia

Corinna Haenschel,^1,2,3 Robert A. Bittner,^1,2,4 James Waltz,⁵ Fabian Haertling,⁶ Michael Wibral,⁴ Wolf Singer,² David E. J. Linden,³ and Eugenio Rodriguez^2,7

¹Laboratory for Neurophysiology and Neuroimaging, Department of Psychiatry, Johann Wolfgang Goethe University, 60590 Frankfurt, Germany, ²Max Planck Institute for Brain Research, 60528 Frankfurt, Germany, ³School of Psychology, Bangor University, Gwynedd LL57 2AS, United Kingdom, ⁴Brain Imaging Center, 60528 Frankfurt, Germany, ⁵University of Maryland School of Medicine, Baltimore, Maryland 21228, ⁶Department of Child and Adolescent Psychiatry, Johann Wolfgang Goethe University, 60528 Frankfurt, Germany, and ⁷Pontificia Universidad Católica de Chile, Escuela de Psicología, 7820436 Macul, Santiago, Chile

Correspondence should be addressed to Corinna Haenschel, School of Psychology, Adeilad Brigantia, Bangor University, Gwynedd LL57 2AS, UK. Email: c.haenschel{at}bangor.ac.uk

Impairments in working memory (WM) are a core cognitive deficit in schizophrenia. Neurophysiological models suggest that deficits during WM maintenance in schizophrenia may be explained by abnormalities in the GABAergic system, which will lead to deficits in high-frequency oscillations. However, it is not yet clear which of the three WM phases (encoding, maintenance, retrieval) are affected by dysfunctional oscillatory activity. We investigated the relationship between impairments in oscillatory activity in a broad frequency range (3–100 Hz) and WM load in the different phases of WM in 14 patients with early-onset schizophrenia and 14 matched control participants using a delayed matching to sample paradigm.

During encoding, successful memorization was predicted by evoked theta, alpha, and beta oscillatory activity in controls. Patients showed severe reductions in the evoked activity in these frequency bands. During early WM maintenance, patients showed a comparable WM load-dependent increase in induced alpha and gamma activity to controls. In contrast, during the later maintenance phase, patients showed a shift in the peak of induced gamma activity to the lower WM load conditions. Finally, induced theta and gamma activity were reduced in patients during retrieval.

Our findings suggest that the WM deficit in schizophrenia is associated with impaired oscillatory activity during all phases of the task and that the cortical storage system reaches its capacity limit at lower loads. Inability to maintain oscillatory activity in specific frequency bands could thus result in the information overload that may underlie both cognitive deficits and psychopathological symptoms of schizophrenia.

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Received March 24, 2009; revised June 3, 2009; accepted June 15, 2009.

Correspondence should be addressed to Corinna Haenschel, School of Psychology, Adeilad Brigantia, Bangor University, Gwynedd LL57 2AS, UK. Email: c.haenschel{at}bangor.ac.uk

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