JTW's Evolutionary Origins - Author: Edelman, Gerald M.
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Gerald Edelman's Dynamic Core Hypothesis

A final issue we should consider is whether the neural process underlying conscious experience extends to most of the brain, as was concluded by William James, or is restricted to varying subsets of neuronal groups. Several observations support the latter possibility.

  • Classical lesion and stimulation studies suggest that many brain structures outside the thalamocortical system have no direct influence on conscious experience. Even within the thalamocortical system, many regions can be lesioned or stimulated without producing direct effects on conscious experience (41).
  • Neurophysiological studies indicate a possible dissociation between conscious experience and ongoing neural activity within portions of the thalamocortical system. During binocular rivalry in monkeys, a large proportion of neurons in early visual areas, such as V1, V4, and MT, continued to fire to their preferred stimulus even when it was not consciously perceived (42). The activity of only a subset of the neurons recorded in these areas was correlated with the percept, although in higher areas such as IT and STS, the percentage reached 95%. In our magnetoencephalographic study of binocular rivalry in humans (Fig. 1) (15), we found that the responses of only a subset of occipital, temporal, and frontal areas was correlated with the conscious perception of a stimulus, although several other regions showed widespread responses to stimuli that were not consciously perceived.
  • The firing of neurons dealing with rapidly varying local details of a sensory input or a motor output does not seem to map to conscious experience. The latter deals with invariant properties of objects that are highly informative as well as more stable and easily manipulated. For example, patterns of neural activity in the retina and other early visual structures correspond faithfully to spatial and temporal details of the visual input and are in constant flux. During each visual fixation, however, humans extract the meaning of a scene and are not conscious of considerable changes in its local details (43). Groups of neurons responding in a stable way to invariant properties of objects are therefore more likely to contribute to conscious experience.
  • Many neural processes devoted to carrying out highly automated routines that make it possible to talk, listen, read, write, and so forth, in a fast and effortless way do not appear to contribute directly to conscious experience, although they are essential in determining its content (44). As mentioned above, neural circuits carrying out such highly practiced neural routines may become functionally insulated except at the input or output stages. There is also some evidence that cortical regions that are part of a fast system for controlling action, such as the dorsal visual stream, may not contribute significantly to conscious experience (45).
  • Although the sheer anatomical connectivity of the brain may hint that, over a sufficiently long time scale, everything can interact with everything else, modeling studies indicate that only certain interactions within the thalamocortical system are fast and strong enough to lead to the formation of a large functional cluster within a few hundred milliseconds (46).

These observations suggest that changes in the firing of only certain distributed subsets of the neuronal groups that are activated or deactivated in response to a given task are associated with conscious experience. What is special about these subsets of neuronal groups, and how can they be identified? We suggest the following:

  • A group of neurons can contribute directly to conscious experience only if it is part of a distributed functional cluster that achieves high integration in hundreds of milliseconds.
  • To sustain conscious experience, it is essential that this functional cluster be highly differentiated, as indicated by high values of complexity.

We propose that a large cluster of neuronal groups that together constitute, on a time scale of hundreds of milliseconds, a unified neural process of high complexity be termed the "dynamic core," in order to emphasize both its integration and its constantly changing activity patterns. The dynamic core is a functional cluster: its participating neuronal groups are much more strongly interactive among themselves than with the rest of the brain. The dynamic core must also have high complexity: its global activity patterns must be selected within less than a second out of a very large repertoire.

The dynamic core would typically include posterior corticothalamic regions involved in perceptual categorization interacting reentrantly with anterior regions involved in concept formation, value-related memory, and planning (4), although it would not necessarily be restricted to the thalamocortical system. The term "dynamic core" deliberately does not refer to a unique, invariant set of brain areas (be they prefrontal, extrastriate, or striate cortex), and the core may change in composition over time (47). Because our hypothesis highlights the role of the functional interactions among distributed groups of neurons rather than their local properties (2), the same group of neurons may at times be part of the dynamic core and underlie conscious experience, while at other times it may not be part of it and thus be involved in unconscious processes. Furthermore, since participation in the dynamic core depends on the rapidly shifting functional connectivity among groups of neurons rather than on anatomical proximity, the composition of the core can transcend traditional anatomical boundaries (48). Finally, as suggested by imaging studies (15), the exact composition of the core related to particular conscious states is expected to vary significantly across individuals.

The dynamic core hypothesis avoids the category error of assuming that certain local, intrinsic properties of neurons have, in some mysterious way, a privileged correlation with consciousness. Instead, this hypothesis accounts for fundamental properties of conscious experience by linking them to global properties of particular neural processes. We have seen that conscious experience is a process that is unified and private, that is extremely differentiated, and that evolves on a time scale of hundreds of milliseconds. The dynamic core is a process, since it is characterized in terms of time-varying neural interactions, not as a thing or a location. It is unified and private, because its integration must be high at the same time as its mutual information with what surrounds is low, thus creating a functional boundary between what is part of it and what is not. The requirement for high complexity means that the dynamic core must be highly differentiated--it must be able to select, based on its intrinsic interactions, among a large repertoire of different activity patterns. Finally, the selection among integrated states must be achieved within hundreds of milliseconds, thus reflecting the time course of conscious experience (49).

A number of experimental questions and associated predictions are generated by this hypothesis. A central prediction is that, during cognitive activities involving consciousness, there should be evidence for a large but distinct set of distributed neuronal groups that interact over fractions of a second much more strongly among themselves than with the rest of the brain. This prediction could, in principle, be tested by recording, in parallel, multiple neurons whose activity is correlated with conscious experience. Multielectrode recordings have already indicated that rapid changes in the functional connectivity among distributed populations of neurons can occur independently of firing rate (50). Recent studies in monkey frontal cortex also show abrupt and simultaneous shifts among stationary activity states involving several, but not all recorded neurons (51). A convincing demonstration of rapid functional clustering among distributed neuronal groups requires, however, that these studies be extended to larger populations of neurons in several brain areas. Another possibility would be to examine whether the effects of direct cortical microstimulation spread more widely in the brain if they are associated with conscious experience than if they are not. In humans, the extent and boundaries of neural populations exchanging coherent signals can be evaluated through methods of frequency tagging (15). Techniques offering both wide spatial coverage and high temporal resolution could also help establish how large a dynamic core normally is, how its composition changes, and whether certain brain regions are always included or always excluded. It is also significant to ask whether the dynamic core can split, and thus whether multiple dynamic cores can coexist in a normal subject.

A reasonable prediction would be that certain disorders of consciousness, notably dissociative disorders and schizophrenia, should be reflected in abnormalities of the dynamic core and possibly result in the formation of multiple cores. A strong prediction based on our hypothesis is that the complexity of the dynamic core should correlate with the conscious state of the subject. For example, we predict that neural complexity should be much higher during waking and REM sleep than during the deep stages of slow-wave sleep, and that it should be extremely low during epileptic seizures despite the overall increase in brain activity. We also predict that neural processes underlying automatic behaviors, no matter how sophisticated, should have lower complexity than neural processes underlying consciously controlled behaviors.

Finally, a systematic increase in the complexity of coherent neural processes is expected to accompany cognitive development. The outcome of such tests should indicate whether conscious phenomenology can indeed be related, as we suggest, to a distributed neural process that is both highly integrated and highly differentiated. The evidence available so far supports the belief that a scientific explanation of consciousness is becoming increasingly feasible (52).

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