Limits...
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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Reverberant Activity in the Global Workspace Model Imposes a Nonlinear Threshold on Incoming StimuliEach 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.
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pbio-0030141-g005: Reverberant Activity in the Global Workspace Model Imposes a Nonlinear Threshold on Incoming StimuliEach 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.

Mentions: In the previous section we saw how, in a single thalamocortical column, the neuronal activity caused by thalamic stimulation does not last much beyond the duration of stimulation. With the present parameters, the local circuitry of a column, although it includes excitatory loops, does not have sufficient strength to maintain activation over a durable interval. In the entire global workspace model, the effect of an identical stimulation is quite different. As show in Figure 4, stimuli of very brief duration elicit only a correspondingly brief pulse of activity, traveling in a feedforward manner through each of the thalamocortical columns. Crucially, however, there exists a critical stimulus duration beyond which activation begins to reverberate for a considerably longer duration (Figure 5A–5C). The existence of such a threshold is a characteristic of the dynamical system created by the recurrent bottom-up and top-down connectivity of the workspace. If the input is sufficiently long and strong, it is able to generate sufficient activation in the higher areas (i.e., areas labeled B, C, and D in Figure 1C), and those areas, in turn, send descending activation to lower areas, thus supporting the very activity that activated them in the first place. The result is the “ignition” of a coherent reverberating neuronal ensemble spanning across all areas (areas A–D in Figure 1C) and lasting 200–300 ms, as previously described [22]. The two successive processes of bottom-up propagation (proportional to stimulus duration) followed by top-down amplification and recurrent firing (incommensurate to stimulus duration) can be clearly seen as two successive firing peaks in the spike train of pyramidal neurons (Figure 5C, right-hand inserts).


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

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

Reverberant Activity in the Global Workspace Model Imposes a Nonlinear Threshold on Incoming StimuliEach 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.
© Copyright Policy
Related In: Results  -  Collection

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

pbio-0030141-g005: Reverberant Activity in the Global Workspace Model Imposes a Nonlinear Threshold on Incoming StimuliEach 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.
Mentions: In the previous section we saw how, in a single thalamocortical column, the neuronal activity caused by thalamic stimulation does not last much beyond the duration of stimulation. With the present parameters, the local circuitry of a column, although it includes excitatory loops, does not have sufficient strength to maintain activation over a durable interval. In the entire global workspace model, the effect of an identical stimulation is quite different. As show in Figure 4, stimuli of very brief duration elicit only a correspondingly brief pulse of activity, traveling in a feedforward manner through each of the thalamocortical columns. Crucially, however, there exists a critical stimulus duration beyond which activation begins to reverberate for a considerably longer duration (Figure 5A–5C). The existence of such a threshold is a characteristic of the dynamical system created by the recurrent bottom-up and top-down connectivity of the workspace. If the input is sufficiently long and strong, it is able to generate sufficient activation in the higher areas (i.e., areas labeled B, C, and D in Figure 1C), and those areas, in turn, send descending activation to lower areas, thus supporting the very activity that activated them in the first place. The result is the “ignition” of a coherent reverberating neuronal ensemble spanning across all areas (areas A–D in Figure 1C) and lasting 200–300 ms, as previously described [22]. The two successive processes of bottom-up propagation (proportional to stimulus duration) followed by top-down amplification and recurrent firing (incommensurate to stimulus duration) can be clearly seen as two successive firing peaks in the spike train of pyramidal neurons (Figure 5C, right-hand inserts).

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