High-Frequency Oscillations in Schizophrenia

Neural oscillations and their synchronization may represent a versatile signal to realize flexible communication within and between cortical areas. There is extensive evidence that cognitive functions depending on coordination of distributed neural responses are associated with synchronized oscillatory activity, suggesting a functional mechanism of neural oscillations in cortical networks. In addition to their role in normal brain functioning, there is increasing evidence that altered oscillatory activity may be associated with certain neuropsychiatric disorders, such as schizophrenia, that involve dysfunctional cognition and behavior. In the present paper, the focus is on the role of high-frequency oscillations for cortical computations through establishing correlations between the modulation of oscillations in the β/γ frequency range and specific cognitive processes during normal brain functioning and in schizophrenia. Specifically, it is suggested that in addition to oscillations in the low (30–60 Hz) γ-band range, γ-band oscillations > 60 Hz may have a crucial role for the understanding of cognitive dysfunctions in schizophrenia. Perspectives for future research will be discussed in relationship to methodological issues, the utility of neural oscillations as a biomarker and the neurodevelopmental hypothesis of schizophrenia.

[1]  T. Tsumoto,et al.  Change of conduction velocity by regional myelination yields constant latency irrespective of distance between thalamus and cortex , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[2]  M. Hasselmo,et al.  Gamma frequency-range abnormalities to auditory stimulation in schizophrenia. , 1999, Archives of general psychiatry.

[3]  J. Martinerie,et al.  The brainweb: Phase synchronization and large-scale integration , 2001, Nature Reviews Neuroscience.

[4]  W. Singer,et al.  HIGH-FREQUENCY GAMMA-BAND OSCILLATIONS DURING PERCEPTUAL ORGANISATION IN CHRONIC AND FIRST-EPISODE SCHIZOPHRENIA PATIENTS , 2010, Schizophrenia Research.

[5]  W. Singer,et al.  Rapid feature selective neuronal synchronization through correlated latency shifting , 2001, Nature Neuroscience.

[6]  W. Singer,et al.  Progress in Biophysics and Molecular Biology , 1965 .

[7]  W. Singer,et al.  Short- and Long-Term Effects of Cholinergic Modulation on Gamma Oscillations and Response Synchronization in the Visual Cortex , 2004, The Journal of Neuroscience.

[8]  W. Singer,et al.  Interhemispheric synchronization of oscillatory neuronal responses in cat visual cortex , 1991, Science.

[9]  D. Johnston,et al.  Regulation of Synaptic Efficacy by Coincidence of Postsynaptic APs and EPSPs , 1997 .

[10]  Fiona E. N. LeBeau,et al.  Region-Specific Reduction in Entorhinal Gamma Oscillations and Parvalbumin-Immunoreactive Neurons in Animal Models of Psychiatric Illness , 2006, The Journal of Neuroscience.

[11]  W. Singer,et al.  Phase Sensitivity of Synaptic Modifications in Oscillating Cells of Rat Visual Cortex , 2004, The Journal of Neuroscience.

[12]  Eugenio Rodriguez,et al.  The development of neural synchrony reflects late maturation and restructuring of functional networks in humans , 2009, Proceedings of the National Academy of Sciences.

[13]  B. O’Donnell,et al.  Perceptual anomalies in schizophrenia co-occur with selective impairments in the gamma frequency component of midlatency auditory ERPs. , 2008, Journal of abnormal psychology.

[14]  A. von Stein,et al.  Different frequencies for different scales of cortical integration: from local gamma to long range alpha/theta synchronization. , 2000, International journal of psychophysiology : official journal of the International Organization of Psychophysiology.

[15]  W. Singer,et al.  Cortical Oscillatory Activity Is Critical for Working Memory as Revealed by Deficits in Early-Onset Schizophrenia , 2009, The Journal of Neuroscience.

[16]  W. Singer,et al.  Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties , 1989, Nature.

[17]  Karl J. Friston The disconnection hypothesis , 1998, Schizophrenia Research.

[18]  Wolf Singer,et al.  Neuronal Synchrony: A Versatile Code for the Definition of Relations? , 1999, Neuron.

[19]  R. Desimone,et al.  Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention , 2001, Science.

[20]  Thomas E. Smith,et al.  Reduced top-down influences in contour detection in schizophrenia , 2006, Cognitive neuropsychiatry.

[21]  R. McCarley,et al.  γ-Band Auditory Steady-State Responses Are Impaired in First Episode Psychosis , 2008, Biological Psychiatry.

[22]  W. Singer,et al.  Selection of intrinsic horizontal connections in the visual cortex by correlated neuronal activity. , 1992, Science.

[23]  Catherine Tallon-Baudry,et al.  The many faces of the gamma band response to complex visual stimuli , 2005, NeuroImage.

[24]  J. Lisman,et al.  Heightened synaptic plasticity of hippocampal CA1 neurons during a Cholinergically induced rhythmic state , 1993, Nature.

[25]  W. Singer,et al.  Role of Reticular Activation in the Modulation of Intracortical Synchronization , 1996, Science.

[26]  Robert W. McCarley,et al.  γ-Band Auditory Steady-State Responses Are Impaired in First Episode Psychosis , 2008, Biological Psychiatry.

[27]  A. Meyer-Lindenberg,et al.  Intermediate phenotypes and genetic mechanisms of psychiatric disorders , 2006, Nature Reviews Neuroscience.

[28]  P. Jonas,et al.  Synaptic mechanisms of synchronized gamma oscillations in inhibitory interneuron networks , 2007, Nature Reviews Neuroscience.

[29]  W. Singer,et al.  Abnormal neural oscillations and synchrony in schizophrenia , 2010, Nature Reviews Neuroscience.

[30]  D. Lewis,et al.  Cortical inhibitory neurons and schizophrenia , 2005, Nature Reviews Neuroscience.

[31]  W. Singer,et al.  Dysfunctional Long-Range Coordination of Neural Activity during Gestalt Perception in Schizophrenia , 2006, The Journal of Neuroscience.

[32]  J. Pernier,et al.  Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans , 1997, The Journal of Neuroscience.

[33]  K. Deisseroth,et al.  Parvalbumin neurons and gamma rhythms enhance cortical circuit performance , 2009, Nature.

[34]  Eugenio Rodriguez,et al.  Neural synchrony and the development of cortical networks , 2010, Trends in Cognitive Sciences.

[35]  J. Pernier,et al.  Oscillatory gamma-band (30-70 Hz) activity induced by a visual search task in humans. , 1997, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  W. A. Phillips,et al.  Theory of mind and perceptual context‐processing in schizophrenia , 2006, Cognitive neuropsychiatry.

[37]  R. McCarley,et al.  Abnormal Neural Synchrony in Schizophrenia , 2003, The Journal of Neuroscience.

[38]  P. Somogyi,et al.  Cell Type- and Input-Specific Differences in the Number and Subtypes of Synaptic GABAA Receptors in the Hippocampus , 2002, The Journal of Neuroscience.

[39]  Karl J. Friston,et al.  Dysconnection in Schizophrenia: From Abnormal Synaptic Plasticity to Failures of Self-monitoring , 2009, Schizophrenia bulletin.

[40]  Takanori Hashimoto,et al.  Protracted Developmental Trajectories of GABA A Receptor α1 and α2 Subunit Expression in Primate Prefrontal Cortex , 2009, Biological Psychiatry.

[41]  T. Hashimoto,et al.  Developmental trajectories of GABAA receptor α subunit expression in primate prefrontal cortex , 2009, Neuroscience Research.

[42]  W. Singer,et al.  Neuroelectromagnetic Correlates of Perceptual Closure Processes , 2010, The Journal of Neuroscience.

[43]  Miles A Whittington,et al.  Cellular mechanisms of neuronal population oscillations in the hippocampus in vitro. , 2004, Annual review of neuroscience.

[44]  Alan C. Evans,et al.  Structural maturation of neural pathways in children and adolescents: in vivo study. , 1999, Science.

[45]  W. Iacono,et al.  The status of spectral EEG abnormality as a diagnostic test for schizophrenia , 2008, Schizophrenia Research.