Ongoing Spontaneous Activity Controls Access to Consciousness: A Neuronal Model for Inattentional Blindness

Stanislas Dehaene,Jean-Pierre Changeux,Larry Abbott

doi:10.1371/journal.pbio.0030141

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.

Highlights

Ongoing spontaneous activity is present throughout the nervous system [1], but its function remains enigmatic
The transition to this state of high correlated activity is fast and characterized by an amplification of local neural activation and the subsequent ignition of multiple distant areas. This state of activity competes with, rather than facilitates, sensory processing, and leads to an extinction of sensory processing. We propose that this blocking may account for the ‘‘inattentional blindness’’ phenomenon, in which normal subjects intensely engaged in mental activity fail to notice salient but taskirrelevant sensory stimuli [26,27,28]
We show the evolution of the power of the local field potential, frequency, and mean firing rate of pyramidal neurons as a function of the injected neuromodulatory current Ineuromodul

Summary

Introduction

Ongoing spontaneous activity is present throughout the nervous system [1], but its function remains enigmatic. Spontaneous movements [2] and waves of endogenous retinal activity [3,4] are thought to play an important role in the epigenesis of neural networks through selective synapse stabilization [5,6]. Ongoing spontaneous activity is present in the adult brain, where it is responsible for the highly variable patterns of the electroencephalogram (EEG). Functional neuroimaging studies in humans have shown a globally elevated brain metabolism at rest, with localized patterns suggesting that particular cortical regions are maintained in a high, variable, state of activity [12,13,14,15,16]. The functional roles of this spontaneous activity in the adult brain at rest remains to be elucidated

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