Gamma coherence and conscious perception

BackgroundHigh-frequency (e.g., gamma 30 to 50 Hz) coherent neural activity has been postulated to underlie binding of independent neural assemblies and thus integrate processing across distributed neuronal networks to achieve a unified conscious experience. Prior studies suggest that gamma activity may play a role in perceptual mechanisms, but design limitations raise concerns. Thus, controversy exists as to the hypothesis that gamma activity is necessary for perceptual awareness. In addition, controversy exists as to whether the primary sensory cortices are involved directly in the mechanisms of conscious perception or just in processes prior to conscious awareness. Objective To investigate the relation of gamma coherence and perception. MethodsDigital intracranial electrocorticographic recordings from implanted electrodes were obtained in six patients with intractable epilepsy during a simple somatosensory detection task for near-threshold stimuli applied to the contralateral hand. Signal analyses were then conducted using a quantitative approach that employed two-way Hanning digital bandpass filters to compute running correlations across pairs of channels at various time epochs for each patient and each perception state across multiple bandwidths. Results Gamma coherence occurs in the primary somatosensory cortex approximately 150 to 300 milliseconds after contralateral hand stimuli that are perceived, but not for nonperceived stimuli, which did not differ in character/intensity or early somatosensory evoked potentials. Conclusion The results are consistent with the possible direct involvement of primary sensory cortex in elemental awareness and with a role for gamma coherence in conscious perception.

[1]  R. Llinás,et al.  Human oscillatory brain activity near 40 Hz coexists with cognitive temporal binding. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[2]  C. Gray The Temporal Correlation Hypothesis of Visual Feature Integration Still Alive and Well , 1999, Neuron.

[3]  K. D. Singh,et al.  Magnetic field tomography of coherent thalamocortical 40-Hz oscillations in humans. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[4]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. 1. Depth recorded potentials in the human occipital and parietal lobes , 1994, Journal of Physiology-Paris.

[5]  J. Desmedt,et al.  Transient phase-locking of 40 Hz electrical oscillations in prefrontal and parietal human cortex reflects the process of conscious somatic perception , 1994, Neuroscience Letters.

[6]  F. Varela,et al.  Perception's shadow: long-distance synchronization of human brain activity , 1999, Nature.

[7]  C. Koch,et al.  Some reflections on visual awareness. , 1990, Cold Spring Harbor symposia on quantitative biology.

[8]  C. Perez-Borja,et al.  Depth electrographic studies of a focal fast response to sensory stimulation in the human , 1961 .

[9]  W. Singer Synchronization of cortical activity and its putative role in information processing and learning. , 1993, Annual review of physiology.

[10]  W W Alberts,et al.  Responses of human somatosensory cortex to stimuli below threshold for conscious sensation. , 1967, Science.

[11]  R. Lesser,et al.  Functional mapping of human sensorimotor cortex with electrocorticographic spectral analysis. II. Event-related synchronization in the gamma band. , 1998, Brain : a journal of neurology.

[12]  F. Varela,et al.  A quantitative study of gamma‐band activity in human intracranial recordings triggered by visual stimuli , 2000, The European journal of neuroscience.

[13]  J. Haxby,et al.  fMRI study of face perception and memory using random stimulus sequences. , 1998, Journal of neurophysiology.

[14]  E. Renzi,et al.  Prosopagnosia can be associated with damage confined to the right hemisphere—An MRI and PET study and a review of the literature , 1994, Neuropsychologia.

[15]  R Kakigi,et al.  Human face perception traced by magneto- and electro-encephalography. , 1999, Brain research. Cognitive brain research.

[16]  E. Halgren,et al.  Spatio-temporal stages in face and word processing. I. Depth-recorded potentials in the human occipital, temporal and parietal lobes [corrected]. , 1994, Journal of physiology, Paris.

[17]  A. Treisman The binding problem , 1996, Current Opinion in Neurobiology.

[18]  A. Destexhe,et al.  Cortical Feedback Controls the Frequency and Synchrony of Oscillations in the Visual Thalamus , 2000, The Journal of Neuroscience.

[19]  C. Koch,et al.  Are we aware of neural activity in primary visual cortex? , 1995, Nature.

[20]  S. Bressler Large-scale cortical networks and cognition , 1995, Brain Research Reviews.

[21]  Richard S. J. Frackowiak,et al.  Modulation of conscious experience by peripheral sensory stimuli , 1995, Nature.

[22]  W. Freeman,et al.  Spatio-temporal correlations in human gamma band electrocorticograms. , 1996, Electroencephalography and clinical neurophysiology.

[23]  M. Gazzaniga,et al.  Speculations on the neural basis of islands of blindsight. , 2001, Progress in brain research.

[24]  David E. Morledge,et al.  Control of the transition from sensory detection to sensory awareness in man by the duration of a thalamic stimulus. The cerebral 'time-on' factor. , 1991, Brain : a journal of neurology.

[25]  Christoph von der Malsburg,et al.  The Correlation Theory of Brain Function , 1994 .

[26]  C. Herrmann,et al.  Gamma responses and ERPs in a visual classification task , 1999, Clinical Neurophysiology.

[27]  E. Niebur,et al.  Growth patterns in the developing brain detected by using continuum mechanical tensor maps , 2022 .

[28]  K. Meador,et al.  Pathophysiology of altered consciousness during seizures: Subtraction SPECT study , 2002, Neurology.

[29]  B LIBET,et al.  PRODUCTION OF THRESHOLD LEVELS OF CONSCIOUS SENSATION BY ELECTRICAL STIMULATION OF HUMAN SOMATOSENSORY CORTEX. , 1964, Journal of neurophysiology.

[30]  Leslie G. Ungerleider,et al.  The Effect of Face Inversion on Activity in Human Neural Systems for Face and Object Perception , 1999, Neuron.

[31]  J. Newman Thalmic Contributions to Attention and Consciousness , 1995, Consciousness and Cognition.

[32]  M. Hallett,et al.  Corticomuscular coherence: a review. , 1999, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[33]  S. Etlinger,et al.  Self-regulation of the brain and behavior , 1986 .

[34]  Eytan Domany,et al.  Models of Neural Networks I , 1991 .

[35]  E. Halgren,et al.  Face-selective spectral changes in the human fusiform gyrus , 1999, Clinical Neurophysiology.

[36]  D. Barth,et al.  Focal stimulation of the thalamic reticular nucleus induces focal gamma waves in cortex. , 1998, Journal of neurophysiology.

[37]  J R Smith,et al.  Physiology of perception , 1999, Neurology.

[38]  Thomas Elbert,et al.  Self-Regulation of The Brain and Behavior , 1984 .

[39]  F. Pirozzolo,et al.  The Neuropsychology of Learning Disabilities , 1985 .

[40]  D. McCloskey,et al.  Selection of motor responses on the basis of unperceived stimuli , 1996, Experimental Brain Research.

[41]  W. Singer,et al.  Temporal coding in the visual cortex: new vistas on integration in the nervous system , 1992, Trends in Neurosciences.

[42]  J. Wolfe,et al.  The Psychophysical Evidence for a Binding Problem in Human Vision , 1999, Neuron.

[43]  C. Koch,et al.  Towards a neurobiological theory of consciousness , 1990 .

[44]  Michael N. Shadlen,et al.  Synchrony Unbound A Critical Evaluation of the Temporal Binding Hypothesis , 1999, Neuron.

[45]  J. Gotman,et al.  Correlation of high-frequency oscillations with the sleep–wake cycle and cognitive activity in humans , 1999, Neuroscience.

[46]  G. Ojemann,et al.  Increased gamma-range activity in human sensorimotor cortex during performance of visuomotor tasks , 1999, Clinical Neurophysiology.

[47]  E. Halgren,et al.  Early widespread cortical distribution of coherent fusiform face selective activity , 2000, Human brain mapping.

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

[49]  Claude Tomberg,et al.  Human perceptual processing: inhibition of transient prefrontal-parietal 40 Hz binding at P300 onset documented in non-averaged cognitive brain potentials , 1998, Neuroscience Letters.

[50]  A Engelien,et al.  The neural correlates of 'deaf-hearing' in man: conscious sensory awareness enabled by attentional modulation. , 2000, Brain : a journal of neurology.

[51]  P. Milner A model for visual shape recognition. , 1974, Psychological review.