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Brain rhythms and neural syntax: implications for efficient coding of cognitive content and neuropsychiatric disease.

, MD, PhD * , MD, PhD

Dialogues in Clinical Neuroscience

Les Laboratoires Servier

brain, oscillation, neuron, coding, action potential, assembly, psychiatry

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      Abstract

      The perpetual activity of the cerebral cortex is largely supported by the variety of oscillations the brain generates, spanning a number of frequencies and anatomical locations, as well as behavioral correlates. First, we review findings from animal studies showing that most forms of brain rhythms are inhibition-based, producing rhythmic volleys of inhibitory inputs to principal cell populations, thereby providing alternating temporal windows of relatively reduced and enhanced excitability in neuronal networks. These inhibition-based mechanisms offer natural temporal frames to group or “chunk” neuronal activity into cell assemblies and sequences of assemblies, with more complex multi-oscillation interactions creating syntactical rules for the effective exchange of information among cortical networks. We then review recent studies in human psychiatric patients demonstrating a variety alterations in neural oscillations across all major psychiatric diseases, and suggest possible future research directions and treatment approaches based on the fundamental properties of brain rhythms.

      Translated abstract

      La perpetua actividad de la corteza cerebral está sustentada en gran medida por la variedad de oscilaciones que genera el cerebro, las que abarcan un número de frecuencias y sitios anatómicos, así como correlatos conductuales. En primer lugar se revisan los hallazgos de estudios animales que muestran que la mayoría de las formas de los ritmos cerebrales se basan en la inhibición, produciendo descargas rítmicas de estímulos inhibitorios a las principales poblaciones celulares, proporcionando por lo tanto ventanas temporales que alternan una excitabilidad relativamente reducida o aumentada en los circuitos neuronales. Estos mecanismos basados en la inhibición ofrecen marcos temporales naturales para agrupar o “fragmentar” la actividad neuronal en conjuntos celulares y secuencias de conjuntos, con interacciones más complejas de multi-oscilación creando reglas sintácticas para el cambio efectivo de información entre los circuitos corticales. Luego se revisan los estudios en pacientes psiquiátricos que demuestran una variedad de alteraciones en las oscilaciones neurales en las principales enfermedades psiquiátricas, y sugieren posibles orientaciones en las investigaciones a futuro y aproximaciones terapéuticas basadas en las propiedades fundamentals de los ritmos cerebrales

      Translated abstract

      L'activité permanente du cortex cérébral est largement basée sur la grande variété d'oscillations que le cerveau génère incluant un grand nombre de fréquences et de localisations anatomiques, ainsi que leurs corrélats comportementaux. Nous présentons tout d'abord les recherches sur les études animales montrant que la plupart des formes des rythmes cérébraux sont basées sur l'inhibition, produisant des volées rythmiques de signaux inhibiteurs vers les populations cellulaires principales, fournissant alors des fenêtres temporales alternatives d'excitabilité relativement réduites et plus importantes dans les réseaux neuronaux. Ces mécanismes inhibiteurs offrent des cadres temporaux naturels à une grosse activité neuronale ou activité groupée dans des ensembles de cellules et des séquences d'ensembles de cellules, avec des interactions multi-oscillatoires plus complexes créant des règles syntaxiques pour l'échange efficace d'information parmi les réseaux corticaux. Nous analysons ensuite des études récentes de patients psychiatriques qui montrent des altérations variées des oscillations neurales dans toutes les principales maladies psychiatriques. De possibles directions de recherche future ainsi que des approches de traitement fondées sur les propriétés fondamentales des rythmes cérébraux sont proposées.

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        Clocks tick, bridges and skyscrapers vibrate, neuronal networks oscillate. Are neuronal oscillations an inevitable by-product, similar to bridge vibrations, or an essential part of the brain's design? Mammalian cortical neurons form behavior-dependent oscillating networks of various sizes, which span five orders of magnitude in frequency. These oscillations are phylogenetically preserved, suggesting that they are functionally relevant. Recent findings indicate that network oscillations bias input selection, temporally link neurons into assemblies, and facilitate synaptic plasticity, mechanisms that cooperatively support temporal representation and long-term consolidation of information.
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          A mechanism for cognitive dynamics: neuronal communication through neuronal coherence.

           Pascal Fries (2005)
          At any one moment, many neuronal groups in our brain are active. Microelectrode recordings have characterized the activation of single neurons and fMRI has unveiled brain-wide activation patterns. Now it is time to understand how the many active neuronal groups interact with each other and how their communication is flexibly modulated to bring about our cognitive dynamics. I hypothesize that neuronal communication is mechanistically subserved by neuronal coherence. Activated neuronal groups oscillate and thereby undergo rhythmic excitability fluctuations that produce temporal windows for communication. Only coherently oscillating neuronal groups can interact effectively, because their communication windows for input and for output are open at the same times. Thus, a flexible pattern of coherence defines a flexible communication structure, which subserves our cognitive flexibility.
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            Author and article information

            Affiliations
            NYU Neuroscience Institute, School of Medicine, New York University, New York, NY, USA
            Department of Psychiatry, Weill-Cornell Medical College, New York, NY, USA
            Author notes
            Contributors
            NYU Neuroscience Institute, School of Medicine, New York University, New York, NY, USA
            Department of Psychiatry, Weill-Cornell Medical College, New York, NY, USA
            Journal
            Dialogues Clin Neurosci
            Dialogues Clin Neurosci
            Dialogues Clin Neurosci
            Dialogues in Clinical Neuroscience
            Les Laboratoires Servier (France )
            1294-8322
            1958-5969
            December 2012
            December 2012
            : 14
            : 4
            : 345-367
            23393413
            3553572
            Copyright: © 2012 LLS

            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.

            Categories
            State of the Art

            Neurosciences

            psychiatry, assembly, action potential, coding, neuron, oscillation, brain

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