Depending on certain neurophysiological parameters, the same thalamocortical network can generate much or little conscious experience
Another example of the importance of neurophysiological parameters is provided by sleep – the most familiar of the alterations of consciousness, and yet one of the most striking. Upon awakening from dreamless sleep, we have the peculiar impression that for a while we were not there at all nor, as far as we are concerned, was the rest of the world. This everyday observation tells us vividly that consciousness can come and go, grow and shrink. Indeed, if we did not sleep, it might be hard to imagine that consciousness is not a given, but depends somehow on the way our brain is functioning. The loss of consciousness between falling asleep and waking up is relative, rather than absolute. . Thus, careful studies of mental activity reported immediately after awakening have shown that some degree of consciousness is maintained during much of sleep. Many awakenings, especially from rapid eye movement (REM) sleep, yield dream reports, and dreams can be at times as vivid and intensely conscious as waking experiences. Dream-like consciousness also occurs during various phases of slow wave sleep, especially at sleep onset and during the last part of the night. Nevertheless, a certain proportion of awakenings do not yield any dream report, suggesting a marked reduction of consciousness. Such “empty” awakenings typically occur during the deepest stages of slow wave sleep (stages 3 and 4), especially during the first half of the night.
Which neurophysiological parameters are responsible for the remarkable changes in the quantity and quality of conscious experience that occur during sleep? We know for certain that the brain does not simply shut off during sleep. During REM sleep, for example, neural activity is as high, if not higher, than during wakefulness, and EEG recordings show low-voltage fast-activity. This EEG pattern is known as “activated” because cortical neurons, being steadily depolarized and close to their firing threshold, are ready to respond to incoming inputs. Given these similarities, it is perhaps not surprising that consciousness should be present during both states. Changes in the quality of consciousness, however, do occur, and they correspond closely to relative changes in the activation of different brain areas. .
During slow wave sleep, average firing rates of cortical neurons are also similar to those observed during quiet wakefulness. However, due to changes in the level of certain neuromodulators, virtually all cortical neurons engage in slow oscillations at around 1 Hz, which are reflected in slow waves in the EEG . Slow oscillations consist of a depolarized phase, during which the membrane potential of cortical neurons is close to firing threshold and spontaneous firing rates are similar to quiet wakefulness, and of a hyperpolarized phase, during which neurons become silent and are further away from firing threshold. From the perspective of information integration, a reduction in the readiness to respond to stimuli during the hyperpolarization phase of the slow oscillation would imply a reduction of consciousness. It would be as if we were watching very short fragments of a movie interspersed with repeated unconscious “blanks” in which we cannot see, think, or remember anything, and therefore have little to report. A similar kind of unreadiness to respond, associated with profound hyperpolarization, is found in deep anesthesia, another condition where consciousness is impaired. Studies using transcranial magnetic stimulation in conjunction with high-density EEG are currently testing how response readiness changes during the sleep waking cycle.
From the perspective of information integration, a reduction of consciousness during certain phases of sleep would occur even if the brain remained capable of responding to perturbations, provided its response were to lack differentiation. This prediction is borne out by detailed computer models of a portion of the visual thalamocortical system (Hill and Tononi, in preparation). According to these simulations, in the waking mode different perturbations of the thalamocortical network yield specific responses. In the sleep mode, instead, the network becomes bistable: specific effects of different perturbations are quickly washed out and their propagation impeded: the whole network transitions into the depolarized or into the hyperpolarized phase of the slow oscillation – a stereotypic response that is observed irrespective of the particular perturbation (see Appendix, xiii). And of course, this bistability is also evident in the spontaneous behavior of the network: during each slow oscillation, cortical neurons are either all firing or all silent, with little freedom in between. In summary, these simulations indicate that, even if the anatomical connectivity of a complex stays the same, a change in key parameters governing the readiness of neurons to respond and the differentiation of their responses may alter radically the Φ value of the complex, with corresponding consequences on consciousness.
Conscious experience and time requirements
Consciousness not only requires a neural substrate with appropriate anatomical structure and appropriate physiological parameters: it also needs time. As was mentioned earlier, studies of how a percept is progressively specified and stabilized indicate that it takes up to 100–200 milliseconds to develop a fully formed sensory experience, and that the surfacing of a conscious thought may take even longer. Experiments in which the somatosensory areas of the cerebral cortex were stimulated directly indicate that low intensity stimuli must be sustained for up to 500 milliseconds to produce a conscious sensation . Multi-unit recordings in the primary visual cortex of monkeys show that, after a stimulus is presented, the firing rate of many neurons increases irrespective of whether the animal reports seeing a figure or not. After 80–100 milliseconds, however, their discharge accurately predicts the conscious detection of the figure. Thus, the firing of the same cortical neurons may correlate with consciousness at certain times, but not at other times . What determines when the firing of the same cortical neurons contributes to conscious experience and when it does not? And why may it take up to hundreds of milliseconds before a conscious experience is generated?
The theory predicts that the time requirements for the generation of conscious experience in the brain emerge directly from the time requirements for the build-up of effective interactions among the elements of the main complex. As was mentioned above, if one were to perturb half of the elements of the main complex for less than a millisecond, no perturbations would produce any effect on the other half within this time window, and Φ would be equal to zero. After say 100 milliseconds, however, there is enough time for differential effects to be manifested, and Φ should grow. This prediction is confirmed by results obtained using large-scale computer simulations of the thalamocortical system, where the time course of causal interactions and functional integration can be studied in detail [38, 58, 59], Hill and Tononi, unpublished results). For example, in a model including nine functionally segregated visual areas, the time it takes for functionally specialized neurons located in several different areas to interact constructively and produce a specific, correlated firing pattern is at least 80 milliseconds . These correlated firing patterns last for several hundred milliseconds. After one or more seconds, however, the network settles into spontaneous activity states that are largely independent of previous perturbations. Thus, the characteristic time scale for maximally differentiated responses in thalamocortical networks appears to be comprised between a few tens of milliseconds and a few seconds at the most.
In summary, the time scale of neurophysiological interactions needed to integrate information among distant cortical regions appears to be consistent with that required by psychophysical observations (microgenesis), by stimulation experiments, and by recording experiments.