A series of neuropsychological and neurophysi-ological observations are relevant to the phe-nomenological issues we have already discussed. They lead to a number of key conclusions. First, conscious experience is associated with the activation and deactivation of distributed populations of neurons. Second, conscious experience requires strong and rapid reentrant interactions among distributed neural populations. Third, conscious experience requires patterns of neural activity that are highly differentiated. We shall briefly review some evidence supporting these conclusions.
Neuroimaging studies demonstrate that changes in specific aspects of conscious experience correlate with changes in activity in specific brain areas, whether the experience is driven by external stimuli, by memory, or by imagery and dreams. Conscious experience as such involves the activation or deactivation of widely distributed brain areas, although what should count as the appropriate baseline related to the absence of consciousness is not clear. In subjects who are comatose or deeply anesthetized, unconsciousness is associated with a profound depression of neural activity in both the cerebral cortex and the thalamus. During slow-wave sleep, in which consciousness is severely reduced or lost, cerebral blood flow is globally reduced, compared with both waking and REM sleep, two brain states associated with vivid conscious reports. Neural activity in slow-wave sleep is reduced in both anterior neocortical regions (most of prefrontal cortex) and posterior cortical regions (especially parietal association areas), in paralimbic structures (anterior cingulate cortex and anterior insula), and in centrencephalic structures (reticular activating system, thalamus, and basal ganglia). In contrast, it is not depressed in unimodal sensory areas (primary visual, auditory, and somatosensory cortex (Braun et al. 1997; Maquet et al. 1996, 1997).
Lesion studies indicate that consciousness is abolished by widely distributed damage and not by localized cortical damage. The only localized brain lesions resulting in loss of consciousness typically affect the reticular core in the upper brain stem and hypothalamus or its rostral extensions in the reticular and intralaminar thalamic nuclei (Plum 1991). While it has been suggested that the reticular core may have a privileged connection to conscious experience, its activity may simply be required to sustain distributed activity patterns in the cortex.
What about the waking state? The transition between conscious, controlled performance and unconscious, automated performance may be accompanied by a change in the degree to which neural signals are distributed in the brain. When tasks are novel, brain activation related to a task is widely distributed; when the task has become automatic, activation is more localized and may shift to a different set of areas (Petersen et al. 1998). In animal studies, neural activity related to sensory stimuli can be recorded in many brain regions before habituation. After habituation sets in (a time when humans report that stimuli tend to fade from consciousness), the same stimuli evoke neural activity exclusively along their specific sensory pathways (Horel et al. 1967). These observations suggest that when tasks are automatized and require less or no conscious control, the spread of signals that influence the performance of a task involves a more restricted and dedicated set of circuits that become "functionally insulated." This produces a gain in speed and precision, but a loss in context-sensitivity, accessibility, and flexibility (Baars 1988).
Activation and deactivation of distributed neural populations in the thalamocortical system are not sufficient bases for conscious experience unless the activity of the neuronal groups involved is integrated rapidly and effectively. We have suggested that such rapid integration is achieved through the process of reentry—the ongoing, recursive, highly parallel signaling within and among brain areas (Edelman 1987, 1989; Tononi et al. 1992). An indication comes from the study of patients with disconnection syndromes, in which one or more brain areas are anatomically or functionally disconnected from the rest of the brain due to some pathological process. In the paradigmatic disconnection syndrome, the split brain, visual or somatosensory stimuli can activate the nondominant hemisphere and lead to behavioral responses, but the dominant, verbal hemisphere is not aware of them (Gazzaniga 1995). Although the two hemispheres can still communicate through indirect, subcortical routes, rapid and effective neural interactions mediated by direct reentrant connections are abolished by the lesion of the corpus callosum.
Modeling studies suggest that a telltale sign of effective reentrant interactions is the occurrence of short-term temporal correlations between the neuronal groups involved (Sporns et al. 1991). Experiments on cats show that short-term temporal correlations between the activity of neuronal groups responding to the same stimulus, but located in different hemispheres, are abolished by callosal transections (Engel et al. 1991). Other studies indicate that various kinds of cognitive tasks are accompanied by the occurrence of short-term temporal correlations among distributed populations of neurons in the thalamo-cortical system (Bressler et al. 1993; Gevins et al. 1996; Joliot et al. 1994; Singer and Gray 1995).
The requirement for fast, strong, and distributed neural interactions may explain why stimuli that are feeble, degraded, or short-lasting often fail to be consciously perceived. Although such stimuli may produce a behavioral response (perception without awareness [Marcel 1983]), they are unlikely to ignite neural activity of sufficient strength or duration to support fast-distributed interactions. Conversely, attention may increase the conscious salience of certain stimuli by boosting the corresponding neural responses as well as the strength of neural interactions (Friston 1998; Maunsell 1995). Neural activity is also more likely to contribute effectively to distributed neural interactions if it is sustained for hundreds of msec. This would lead to the functional closure of longer reentrant loops and thereby support reentrant interactions among more distant regions. Experimental findings are consistent with this idea. High-frequency somatosensory stimuli delivered to the thalamus require about 500 msec for the production of a conscious sensory experience, while less than 150 msec is sufficient for sensory detection without awareness (Libet 1993). The sustained evoked potentials associated with a conscious somato-sensory sensation are apparently generated by the excitation of pyramidal neurons of primary somatosensory cortex through reentrant interactions with higher cortical areas (Cauller 1995).
Evidence for a correlation between conscious experience and sustained neural activity also comes from tasks involving visuospatial working memory, that is, the ability to rehearse or "keep in mind" a spatial location. Working memory is used to bring or keep some item in consciousness or close to conscious access. In working memory tasks, sustained neural activity is invariably found in prefrontal cortex of monkeys, and it is apparently maintained by reentrant interactions between frontal and parietal regions (Fuster et al. 1985; Goldman-Rakic and Chafee 1994). Sustained neural activity may facilitate the integration of the activity of spatially segregated brain regions into a coherent, multimodal neural pro cess that is stable enough to permit decision making and planning.
Although strong and fast reentrant interactions among distributed groups of neurons are necessary for conscious experience, in themselves they are not sufficient. This is strikingly demonstrated by the unconsciousness accompanying generalized seizures and slow-wave sleep. During generalized seizures, the brain not only is extremely active, but most neurons fire in a highly synchronous manner. For example, the electroencephalogram (EEG) during petit mal absences indicates that groups of neurons over the whole brain are either all firing together or all silent together, and these two states alternate every third of a second. Although such hypersyn-chronous firing is indicative of strong and distributed interactions, a subject who experiences such a seizure is unconscious. Similarly, during slow-wave sleep, neurons in the thalamocortical system are both active and remarkably interactive, as shown by their synchronous firing in a stereotyped, burst-pause pattern. During this stage of sleep, however, it is rare to obtain vivid and extensive conscious reports. By contrast, during REM sleep, when neural activity is not globally synchronous but resembles the rapid and complex patterns of waking, subjects typically report vivid dreams if awakened. We suggest that the low-voltage, fast-activity EEG characteristic of waking and REM sleep reflects the availability of a rich and diverse repertoire of neural activity patterns. If the repertoire of differentiated neural states is large, consciousness is possible. Conversely, if this repertoire is reduced, as when most groups of neurons in the cortex discharge synchronously and functional discriminations among them are obliterated, consciousness is curtailed or lost.
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