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Ongoing spontaneous activity controls access to consciousness: a neuronal model for inattentional blindness.

Dehaene S, Changeux JP - PLoS Biol. (2005)

Bottom Line: During such an ignited state, spontaneous activity can block external sensory processing.We relate those properties to experimental observations on the neural bases of endogenous states of consciousness, and particularly the blocking of access to consciousness that occurs in the psychophysical phenomenon of "inattentional blindness," in which normal subjects intensely engaged in mental activity fail to notice salient but irrelevant sensory stimuli.Although highly simplified, the generic properties of a minimal network may help clarify some of the basic cerebral phenomena underlying the autonomy of consciousness.

View Article: PubMed Central - PubMed

Affiliation: INSERM-CEA Unit 562, Cognitive Neuroimaging, Service Hospitalier Frédéric Joliot, Orsay, France. dehaene@shfj.cea.fr <dehaene@shfj.cea.fr>

ABSTRACT
Even in the absence of sensory inputs, cortical and thalamic neurons can show structured patterns of ongoing spontaneous activity, whose origins and functional significance are not well understood. We use computer simulations to explore the conditions under which spontaneous activity emerges from a simplified model of multiple interconnected thalamocortical columns linked by long-range, top-down excitatory axons, and to examine its interactions with stimulus-induced activation. Simulations help characterize two main states of activity. First, spontaneous gamma-band oscillations emerge at a precise threshold controlled by ascending neuromodulator systems. Second, within a spontaneously active network, we observe the sudden "ignition" of one out of many possible coherent states of high-level activity amidst cortical neurons with long-distance projections. During such an ignited state, spontaneous activity can block external sensory processing. We relate those properties to experimental observations on the neural bases of endogenous states of consciousness, and particularly the blocking of access to consciousness that occurs in the psychophysical phenomenon of "inattentional blindness," in which normal subjects intensely engaged in mental activity fail to notice salient but irrelevant sensory stimuli. Although highly simplified, the generic properties of a minimal network may help clarify some of the basic cerebral phenomena underlying the autonomy of consciousness.

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All-or-None Stochastic Fluctuations in the Processing of a Fixed Stimulus(A) Variability in sample spike trains evoked in area A1 by the same 15-ms stimulus, whose duration was close to ignition threshold (with Ineuromodul = −0.9 μA/cm2). Each of the twenty lines represents one trial. Note that the first peak is present on a majority of trials, while most of the variability affects the second peak.(B) Distribution of the mean firing rate in area A1 during the second peak (75–225 ms poststimulus), showing a bimodal distribution.(C) Mean local field potential in area A1, computed separately for trials that lead to ignition (firing peak > 40 spikes/s in the above time window) and for trials that did not (firing peak < 15 spikes/s). Note (1) the essentially identical stimulus-induced waves up to the sharp divergence about 110 ms poststimulus; and (2) the presence of a small but significant difference prior to the stimulus, which indicates that ignition is more likely to occur when stimulus presentation coincides with the depolarized phase of spontaneous ongoing oscillations.
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pbio-0030141-g006: All-or-None Stochastic Fluctuations in the Processing of a Fixed Stimulus(A) Variability in sample spike trains evoked in area A1 by the same 15-ms stimulus, whose duration was close to ignition threshold (with Ineuromodul = −0.9 μA/cm2). Each of the twenty lines represents one trial. Note that the first peak is present on a majority of trials, while most of the variability affects the second peak.(B) Distribution of the mean firing rate in area A1 during the second peak (75–225 ms poststimulus), showing a bimodal distribution.(C) Mean local field potential in area A1, computed separately for trials that lead to ignition (firing peak > 40 spikes/s in the above time window) and for trials that did not (firing peak < 15 spikes/s). Note (1) the essentially identical stimulus-induced waves up to the sharp divergence about 110 ms poststimulus; and (2) the presence of a small but significant difference prior to the stimulus, which indicates that ignition is more likely to occur when stimulus presentation coincides with the depolarized phase of spontaneous ongoing oscillations.

Mentions: Each panel shows the firing rate of pyramidal neurons in the lowest area A1 (coded by gray level) as a function of time (x-axis), in response to stimuli of variable duration (y-axis). Ignition is present when the duration of firing extends much beyond the duration of the stimulus, i.e., when a long tail of firing is present. In (A–C), the vigilance level—set by the ascending neuromodulation parameter Ineuromodul—is progressively increased. This increase leads to a systematic change in the minimum duration necessary for ignition. Note that the figure is an average over 20 trials at each duration. Thus, the small trailing activation that can be seen in (A) and (B) even at durations below the threshold is due to a very small proportion of trials in which ignition did occur, due to stochastic variability, as further explained in Figure 6. The insets in (C) show the peristimulus-time histograms for stimulus of 10- or 100-ms duration, showing clearly the two firing peaks successively evoked by bottom-up activation and by top-down amplification. In a simulation in which top-down connections are disabled (D), the first peak is preserved, but the second peak is abolished.


Ongoing spontaneous activity controls access to consciousness: a neuronal model for inattentional blindness.

Dehaene S, Changeux JP - PLoS Biol. (2005)

All-or-None Stochastic Fluctuations in the Processing of a Fixed Stimulus(A) Variability in sample spike trains evoked in area A1 by the same 15-ms stimulus, whose duration was close to ignition threshold (with Ineuromodul = −0.9 μA/cm2). Each of the twenty lines represents one trial. Note that the first peak is present on a majority of trials, while most of the variability affects the second peak.(B) Distribution of the mean firing rate in area A1 during the second peak (75–225 ms poststimulus), showing a bimodal distribution.(C) Mean local field potential in area A1, computed separately for trials that lead to ignition (firing peak > 40 spikes/s in the above time window) and for trials that did not (firing peak < 15 spikes/s). Note (1) the essentially identical stimulus-induced waves up to the sharp divergence about 110 ms poststimulus; and (2) the presence of a small but significant difference prior to the stimulus, which indicates that ignition is more likely to occur when stimulus presentation coincides with the depolarized phase of spontaneous ongoing oscillations.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC1074751&req=5

pbio-0030141-g006: All-or-None Stochastic Fluctuations in the Processing of a Fixed Stimulus(A) Variability in sample spike trains evoked in area A1 by the same 15-ms stimulus, whose duration was close to ignition threshold (with Ineuromodul = −0.9 μA/cm2). Each of the twenty lines represents one trial. Note that the first peak is present on a majority of trials, while most of the variability affects the second peak.(B) Distribution of the mean firing rate in area A1 during the second peak (75–225 ms poststimulus), showing a bimodal distribution.(C) Mean local field potential in area A1, computed separately for trials that lead to ignition (firing peak > 40 spikes/s in the above time window) and for trials that did not (firing peak < 15 spikes/s). Note (1) the essentially identical stimulus-induced waves up to the sharp divergence about 110 ms poststimulus; and (2) the presence of a small but significant difference prior to the stimulus, which indicates that ignition is more likely to occur when stimulus presentation coincides with the depolarized phase of spontaneous ongoing oscillations.
Mentions: Each panel shows the firing rate of pyramidal neurons in the lowest area A1 (coded by gray level) as a function of time (x-axis), in response to stimuli of variable duration (y-axis). Ignition is present when the duration of firing extends much beyond the duration of the stimulus, i.e., when a long tail of firing is present. In (A–C), the vigilance level—set by the ascending neuromodulation parameter Ineuromodul—is progressively increased. This increase leads to a systematic change in the minimum duration necessary for ignition. Note that the figure is an average over 20 trials at each duration. Thus, the small trailing activation that can be seen in (A) and (B) even at durations below the threshold is due to a very small proportion of trials in which ignition did occur, due to stochastic variability, as further explained in Figure 6. The insets in (C) show the peristimulus-time histograms for stimulus of 10- or 100-ms duration, showing clearly the two firing peaks successively evoked by bottom-up activation and by top-down amplification. In a simulation in which top-down connections are disabled (D), the first peak is preserved, but the second peak is abolished.

Bottom Line: During such an ignited state, spontaneous activity can block external sensory processing.We relate those properties to experimental observations on the neural bases of endogenous states of consciousness, and particularly the blocking of access to consciousness that occurs in the psychophysical phenomenon of "inattentional blindness," in which normal subjects intensely engaged in mental activity fail to notice salient but irrelevant sensory stimuli.Although highly simplified, the generic properties of a minimal network may help clarify some of the basic cerebral phenomena underlying the autonomy of consciousness.

View Article: PubMed Central - PubMed

Affiliation: INSERM-CEA Unit 562, Cognitive Neuroimaging, Service Hospitalier Frédéric Joliot, Orsay, France. dehaene@shfj.cea.fr <dehaene@shfj.cea.fr>

ABSTRACT
Even in the absence of sensory inputs, cortical and thalamic neurons can show structured patterns of ongoing spontaneous activity, whose origins and functional significance are not well understood. We use computer simulations to explore the conditions under which spontaneous activity emerges from a simplified model of multiple interconnected thalamocortical columns linked by long-range, top-down excitatory axons, and to examine its interactions with stimulus-induced activation. Simulations help characterize two main states of activity. First, spontaneous gamma-band oscillations emerge at a precise threshold controlled by ascending neuromodulator systems. Second, within a spontaneously active network, we observe the sudden "ignition" of one out of many possible coherent states of high-level activity amidst cortical neurons with long-distance projections. During such an ignited state, spontaneous activity can block external sensory processing. We relate those properties to experimental observations on the neural bases of endogenous states of consciousness, and particularly the blocking of access to consciousness that occurs in the psychophysical phenomenon of "inattentional blindness," in which normal subjects intensely engaged in mental activity fail to notice salient but irrelevant sensory stimuli. Although highly simplified, the generic properties of a minimal network may help clarify some of the basic cerebral phenomena underlying the autonomy of consciousness.

Show MeSH
Related in: MedlinePlus