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      High-frequency oscillations and the neurobiology of schizophrenia

      research-article
      , PhD * , MD; PhD
      Dialogues in Clinical Neuroscience
      Les Laboratoires Servier
      oscillations, gamma, synchrony, cognition, schizophrenia, neurobiology

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          Abstract

          Neural oscillations at low- and high-frequency ranges are a fundamental feature of large-scale networks. Recent evidence has indicated that schizophrenia is associated with abnormal amplitude and synchrony of oscillatory activity, in particular, at high (beta/gamma) frequencies. These abnormalities are observed during task-related and spontaneous neuronal activity which may be important for understanding the pathophysiology of the syndrome. In this paper, we shall review the current evidence for impaired beta/gamma-band oscillations and their involvement in cognitive functions and certain symptoms of the disorder. In the first part, we will provide an update on neural oscillations during normal brain functions and discuss underlying mechanisms. This will be followed by a review of studies that have examined high-frequency oscillatory activity in schizophrenia and discuss evidence that relates abnormalities of oscillatory activity to disturbed excitatory/inhibitory (E/I) balance. Finally, we shall identify critical issues for future research in this area.

          Translated abstract

          Las oscilaciones neurales en los rangos de baja y alta frecuencia constituyen una característica fundamental de las redes a gran escala. La evidencía reciente ha indicado que la esquizofrenia está asociada con la amplitud anormal y la sincronía de la actividad oscilatoria, en particular, a altas frecuencias (beta/gama). Estas alteraciones se observan tanto durante la actividad neuronal espontánea como en la relacionada con tareas, to que puede ser importante para la comprensión de la fisiopatología del síndrome. En este artículo, se revisa la evidencia actual del deterioro de las oscilaciones de las bandas beta/gama y su participatión en las funciones cognitivas y algunos síntomas de este trastorno. En la primera parte, se entrega una actualización sobre las oscilaciones neuronales durante las funciones normales del cerebro y se discuten los mecanismos subyacentes. A continuación se revisan los estudios que han examinado la actividad oscilatoria de alta frecuencia en la esquizofrenia y se discute la evidencia que relaciona las alieraciones de la actividad oscilatoria con el deterioro del balance excitatorio/inhibitorio (E/I). Finalmente se identifican los temas críticos para el futuro de la investigación en esta área.

          Translated abstract

          Les oscillations neuronales de basse et de haute fréquences sont une caractéristique fondamentale des réseaux de grande échelle. D'après des données récentes, l'amplitude et la synchronisation de l'activité oscillatoire sont anormales dans la schizophrénie, en particulier aux hautes fréquences (bêta/gamma). Ces anomalies sont observées lors de l'activité neuronale de repos et de travail, ce qui peut être important pour comprendre la physiopathologie de ce syndrome. Nous analysons dans cet article les preuves actuelles de l'altération des oscillations gamma/bêta et de leur rôle dans les fonctions cognitives et certains symptômes de la maladie. Dans la première partie, nous proposons une mise a jour sur les oscillations neuronales lors de l'activité normale du cerveau et nous en étudions les mécanismes. Puis nous examinons les études qui ont analysé l'activité oscillatoire à haute fréquence dans la schizophrénie et nous discutons les preuves reliant les anomalies de l'activité oscillatoire à la perturbation de l'équilibre excitation/inhibition (E/I). Enfin, nous identifions les points cruciaux de la recherche à venir dans ce domaine.

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          Most cited references78

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          Mechanisms of gamma oscillations.

          Gamma rhythms are commonly observed in many brain regions during both waking and sleep states, yet their functions and mechanisms remain a matter of debate. Here we review the cellular and synaptic mechanisms underlying gamma oscillations and outline empirical questions and controversial conceptual issues. Our main points are as follows: First, gamma-band rhythmogenesis is inextricably tied to perisomatic inhibition. Second, gamma oscillations are short-lived and typically emerge from the coordinated interaction of excitation and inhibition, which can be detected as local field potentials. Third, gamma rhythm typically concurs with irregular firing of single neurons, and the network frequency of gamma oscillations varies extensively depending on the underlying mechanism. To document gamma oscillations, efforts should be made to distinguish them from mere increases of gamma-band power and/or increased spiking activity. Fourth, the magnitude of gamma oscillation is modulated by slower rhythms. Such cross-frequency coupling may serve to couple active patches of cortical circuits. Because of their ubiquitous nature and strong correlation with the "operational modes" of local circuits, gamma oscillations continue to provide important clues about neuronal population dynamics in health and disease.
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            Abnormal neural oscillations and synchrony in schizophrenia.

            Converging evidence from electrophysiological, physiological and anatomical studies suggests that abnormalities in the synchronized oscillatory activity of neurons may have a central role in the pathophysiology of schizophrenia. Neural oscillations are a fundamental mechanism for the establishment of precise temporal relationships between neuronal responses that are in turn relevant for memory, perception and consciousness. In patients with schizophrenia, the synchronization of beta- and gamma-band activity is abnormal, suggesting a crucial role for dysfunctional oscillations in the generation of the cognitive deficits and other symptoms of the disorder. Dysfunctional oscillations may arise owing to anomalies in the brain's rhythm-generating networks of GABA (gamma-aminobutyric acid) interneurons and in cortico-cortical connections.
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              Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks.

              Gamma frequency oscillations are thought to provide a temporal structure for information processing in the brain. They contribute to cognitive functions, such as memory formation and sensory processing, and are disturbed in some psychiatric disorders. Fast-spiking, parvalbumin-expressing, soma-inhibiting interneurons have a key role in the generation of these oscillations. Experimental analysis in the hippocampus and the neocortex reveals that synapses among these interneurons are highly specialized. Computational analysis further suggests that synaptic specialization turns interneuron networks into robust gamma frequency oscillators.
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                Author and article information

                Contributors
                Department of Neurophysiology, Max Planck Institute for Brain Research, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Ernst Strüngmann Institute (ESI) for Neuroscience, in Cooperation with Max Planck Society, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Institute of Neuroscience and Psychology, University of Glasgow, 58 Hillheacl Street, Glasgow G12 8QB, UK
                Department of Neurophysiology, Max Planck Institute for Brain Research, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Ernst Strüngmann Institute (ESI) for Neuroscience, in Cooperation with Max Planck Society, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Frankfurt Institute for Advanced Studies, Johann Wolfgang Goethe University, Ruth-Moufang-Str. 1, Frankfurt am Main, 60438, Germany
                Journal
                Dialogues Clin Neurosci
                Dialogues Clin Neurosci
                Dialogues Clin Neurosci
                Dialogues in Clinical Neuroscience
                Les Laboratoires Servier (France )
                1294-8322
                1958-5969
                September 2013
                September 2013
                : 15
                : 3
                : 301-313
                Affiliations
                Department of Neurophysiology, Max Planck Institute for Brain Research, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Ernst Strüngmann Institute (ESI) for Neuroscience, in Cooperation with Max Planck Society, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Institute of Neuroscience and Psychology, University of Glasgow, 58 Hillheacl Street, Glasgow G12 8QB, UK
                Department of Neurophysiology, Max Planck Institute for Brain Research, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Ernst Strüngmann Institute (ESI) for Neuroscience, in Cooperation with Max Planck Society, Deutschorclenstr. 46, Frankfurt am Main, 60528, Germany; Frankfurt Institute for Advanced Studies, Johann Wolfgang Goethe University, Ruth-Moufang-Str. 1, Frankfurt am Main, 60438, Germany
                Author notes
                Article
                10.31887/DCNS.2013.15.3/puhlhaas
                3811102
                24174902
                97a7e0d3-bf78-4a3f-9d33-35b98a2e1ac4
                Copyright: © 2013 Institut la Conférence Hippocrate - Servier Research Group

                This is an open-access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by-nc-nd/3.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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                Categories
                Translational Research

                Neurosciences
                oscillations,gamma,synchrony,cognition,schizophrenia,neurobiology
                Neurosciences
                oscillations, gamma, synchrony, cognition, schizophrenia, neurobiology

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