Perception's shadow: long-distance synchronization of human brain activity

Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Resu...

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Published inNature (London) Vol. 397; no. 6718; pp. 430 - 433
Main Authors Varela, Francisco J, Rodriguez, Eugenio, George, Nathalie, Lachaux, Jean-Philippe, Martinerie, Jacques, Renault, Bernard
Format Journal Article
LanguageEnglish
Published London Nature Publishing 04.02.1999
Nature Publishing Group
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Abstract Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea (see, for example, refs 4,5,6,7,8,9,10). In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography and magnetoencephalography) and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.
AbstractList Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act.
Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integratire mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea. In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography, and magnetoencephalography), and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.
Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea. In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography and magnetoencephalography) and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.
Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea (see, for example, refs 4,5,6,7,8,9,10). In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography and magnetoencephalography) and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.
Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an integrative mechanism that may bring a widely distributed set of neurons together into a coherent ensemble that underlies a cognitive act. Results of several experiments in animals provide support for this idea (see, for example, refs 4,5,6,7,8,9,10). In humans, gamma oscillations have been described both on the scalp (measured by electroencephalography and magnetoencephalography) and in intracortical recordings, but no direct participation of synchrony in a cognitive task has been demonstrated so far. Here we record electrical brain activity from subjects who are viewing ambiguous visual stimuli (perceived either as faces or as meaningless shapes). We show for the first time, to our knowledge, that only face perception induces a long-distance pattern of synchronization, corresponding to the moment of perception itself and to the ensuing motor response. A period of strong desynchronization marks the transition between the moment of perception and the motor response. We suggest that this desynchronization reflects a process of active uncoupling of the underlying neural ensembles that is necessary to proceed from one cognitive state to another.
Author Martinerie, Jacques
George, Nathalie
Rodriguez, Eugenio
Varela, Francisco J
Lachaux, Jean-Philippe
Renault, Bernard
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  organization: Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA)
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  fullname: Renault, Bernard
  organization: Laboratoire de Neurosciences Cognitives et Imagerie Cérbréale (LENA)
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https://www.ncbi.nlm.nih.gov/pubmed/9989408$$D View this record in MEDLINE/PubMed
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IsPeerReviewed true
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Issue 6718
Keywords Human
Visual stimulus
Stimulus ambiguity
Vision
Central nervous system
Discharge pattern
Electrophysiology
Perception
Cognition
Synchronization
Brain (vertebrata)
Language English
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M Joliot (BF17120_CR14) 1994; 91
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AR Damasio (BF17120_CR2) 1990; 2
SR Friedman-Hill (BF17120_CR26) 1995; 269
WFG Mecklenbräuker (BF17120_CR20) 1993
T Shallice (BF17120_CR27) 1994; 368
CM Mooney (BF17120_CR18) 1957; 11
DA Jeffreys (BF17120_CR21) 1996; 3
S Neuenschwander (BF17120_CR9) 1996; 13
WJ Freeman (BF17120_CR1) 1975
W Singer (BF17120_CR4) 1995; 18
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CM Gray (BF17120_CR6) 1989; 338
V Menon (BF17120_CR23) 1996; 98
N George (BF17120_CR19) 1997; 8
E Vaadia (BF17120_CR7) 1995; 373
J Yordanova (BF17120_CR24) 1997; 8
R Llinas (BF17120_CR11) 1993; 90
C Tallon-Baudry (BF17120_CR16) 1997; 17
AK Kreiter (BF17120_CR10) 1996; 16
C Pantev (BF17120_CR15) 1995; 7
SL Bressler (BF17120_CR5) 1993; 366
JE Desmedt (BF17120_CR13) 1994; 168
RJ Dolan (BF17120_CR25) 1997; 389
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Snippet Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an...
Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80 Hz (gamma oscillations) have been proposed to act as an...
Transient periods of synchronization of oscillating neuronal discharges in the frequency range 30-80Hz (gamma oscillations) have been proposed to act as an...
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SubjectTerms Adult
Behavioral psychophysiology
Biological and medical sciences
Brain
Cognition - physiology
Cortical Synchronization
Electroencephalography
Electrophysiology
Face
Female
Fundamental and applied biological sciences. Psychology
Humans
Male
Perception
Psychology. Psychoanalysis. Psychiatry
Psychology. Psychophysiology
Reaction Time
Sensory perception
Space life sciences
Visual Perception - physiology
Title Perception's shadow: long-distance synchronization of human brain activity
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