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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: According to the model, the thalamocortical network is under a permanent state of spontaneous activity. Therefore, the processing of an identical external input may change with the local context of ongoing activation. For stimuli close to threshold, this “resonance” of external inputs with internal spontaneous activity plays a determinant role in allowing or blocking ignition. To demonstrate this point, we analyzed the impact of stimuli presented close to the ignition threshold by simulating 100 trials with an identical stimulus (15 ms duration) and a fixed, intermediate intensity of neuromodulation (Ineuromodul = −0.9 μA/cm2). We observed a considerable variability in neuronal responses, even in the first area, A1 (Figure 6). The first peak of bottom-up activation was present in a majority of trials, even in area D, although with some small variance in its exact onset and intensity (Figure 6A). However, the bulk of the variability occurred in the second peak, which could be completely absent or very intense and prolonged. In fact, the distribution of firing rates during this second peak was bimodal (Figure 6B). Thus, the variability actually betrayed an all-or-none stochastic process, with fluctuations in ongoing activity modifying, on a trial-by-trial basis, the probability of crossing the dynamic threshold for ignition.


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

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: According to the model, the thalamocortical network is under a permanent state of spontaneous activity. Therefore, the processing of an identical external input may change with the local context of ongoing activation. For stimuli close to threshold, this “resonance” of external inputs with internal spontaneous activity plays a determinant role in allowing or blocking ignition. To demonstrate this point, we analyzed the impact of stimuli presented close to the ignition threshold by simulating 100 trials with an identical stimulus (15 ms duration) and a fixed, intermediate intensity of neuromodulation (Ineuromodul = −0.9 μA/cm2). We observed a considerable variability in neuronal responses, even in the first area, A1 (Figure 6). The first peak of bottom-up activation was present in a majority of trials, even in area D, although with some small variance in its exact onset and intensity (Figure 6A). However, the bulk of the variability occurred in the second peak, which could be completely absent or very intense and prolonged. In fact, the distribution of firing rates during this second peak was bimodal (Figure 6B). Thus, the variability actually betrayed an all-or-none stochastic process, with fluctuations in ongoing activity modifying, on a trial-by-trial basis, the probability of crossing the dynamic threshold for ignition.

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