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

Date Published: May 12, 2005

Publisher: Public Library of Science

Author(s): Stanislas Dehaene, Jean-Pierre Changeux, Larry Abbott

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.

Partial Text: Ongoing spontaneous activity is present throughout the nervous system [1], but its function remains enigmatic. In the embryo, 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 also present in the adult brain, where it is responsible for the highly variable patterns of the electroencephalogram (EEG). Thalamocortical networks generate a variety of oscillations whose rhythms change across the sleep-wake cycle [7,8,9]. Optical imaging methods in anesthetized animals also reveal fast spontaneous states of neuronal activity that, far from being random, exhibit patterns that resemble those evoked by external stimuli [10,11]. In parallel, 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, although variable, state of activity [12,13,14,15,16]. At present, the functional roles of this spontaneous activity in the adult brain at rest remains to be elucidated.

We used computer simulations to characterize spontaneous and evoked activity in a complex nested architecture comprising multiple neurons, columns, and areas (Figure 1). To facilitate comprehension, we organize the results section as a progression from local to more global states of activity. We start by describing the spontaneous and evoked activity in the building blocks of the model, namely the single neuron and an isolated thalamocortical column. We then consider the extent to which those properties are affected when multiple thalamocortical columns are interconnected by long-distance, bottom-up and top-down connections.