An open mind, an open question…

An Information Integration Theory of Consciousness

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Abstract Background Consciousness poses two main problems. The first is understanding the conditions that determine to what extent a system has conscious experience. For instance, why is our consciousness generated by certain parts of our brain, such as the thalamocortical system, and not by other parts, such as the cerebellum? And why are we conscious [...]
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Testing the hypothesis

Consciousness, information integration, and the brain

Based on a phenomenological analysis, we have argued that consciousness corresponds to the capacity to integrate information. We have then considered how such capacity can be measured, and we have developed a theoretical framework for consciousness as information integration. We will now consider several neuroanatomical or neurophysiological factors that are known to influence consciousness. After briefly discussing the empirical evidence, we will use simplified computer models to illustrate how these neuroanatomical and neurophysiological factors influence information integration. As we shall see, the information integration theory not only fits empirical observations reasonably well, but offers a principled explanation for them.

Consciousness is generated by a distributed thalamocortical network that is at once specialized and integrated

Ancient Greek philosophers disputed whether the seat of consciousness was in the lungs, in the heart, or in the brain. The brain’s pre-eminence is now undisputed, and scientists are trying to establish which specific parts of the brain are important. For example, it is well established that the spinal cord is not essential for our conscious experience, as paraplegic individuals with high spinal transactions are fully conscious. Conversely, a well-functioning thalamocortical system is essential for consciousness [15]. Opinions differ, however, about the contribution of certain cortical areas [1, 16–21]. Studies of comatose or vegetative patients indicate that a global loss of consciousness is usually caused by lesions that impair multiple sectors of the thalamocortical system, or at least their ability to work together as a system. [22–24]. By contrast, selective lesions of individual thalamocortical areas impair different submodalities of conscious experience, such as the perception of color or of faces [25]. Electrophysiological and imaging studies also indicate that neural activity that correlates with conscious experience is widely distributed over the cortex (e.g [20, 26–29]). It would seem, therefore, that the neural substrate of consciousness is a distributed thalamocortical network, and that there is no single cortical area where it all comes together (see Appendix, ix).

The fact that consciousness as we know it is generated by the thalamocortical system fits well with the information integration theory, since what we know about its organization appears ideally suited to the integration of information. On the information side, the thalamocortical system comprises a large number of elements that are functionally specialized, becoming activated in different circumstances. [12, 30]. Thus, the cerebral cortex is subdivided into systems dealing with different functions, such as vision, audition, motor control, planning, and many others. Each system in turn is subdivided into specialized areas, for example different visual areas are activated by shape, color, and motion. Within an area, different groups of neurons are further specialized, e.g. by responding to different directions of motion. On the integration side, the specialized elements of the thalamocortical system are linked by an extended network of intra- and inter-areal connections that permit rapid and effective interactions within and between areas [31–35]. In this way, thalamocortical neuronal groups are kept ready to respond, at multiple spatial and temporal scales, to activity changes in nearby and distant thalamocortical areas. As suggested by the regular finding of neurons showing multimodal responses that change depending on the context [36, 37], the capacity of the thalamocortical system to integrate information is probably greatly enhanced by nonlinear switching mechanisms, such as gain modulation or synchronization, that can modify mappings between brain areas dynamically [34, 38–40]. In summary, the thalamocortical system is organized in a way that appears to emphasize at once both functional specialization and functional integration.

As shown by computer simulations, systems of neural elements whose connectivity jointly satisfies the requirements for functional specialization and for functional integration are well suited to integrating information. Fig. 3a shows a representative connection matrix obtained by optimizing for Φ starting from random connection weights. A graph-theoretical analysis indicates that connection matrices yielding the highest values of information integration (Φ = 74 bits) share two key characteristics [8]. First, connection patterns are different for different elements, ensuring functional specialization. Second, all elements can be reached from all other elements of the network, ensuring functional integration. Thus, simulated systems having maximum Φ appear to require both functional specialization and functional integration. In fact, if functional specialization is lost by replacing the heterogeneous connectivity with a homogeneous one, or if functional integration is lost by rearranging the connections to form small modules, the value of Φ decreases considerably (Fig 3b,3c). Further simulations show that it is possible to construct a large complex of high Φ by joining smaller complexes through reciprocal connections [8]. In the thalamocortical system, reciprocal connections linking topographically organized areas may be especially effective with respect to information integration. In summary, the coexistence of functional specialization and functional integration, epitomized by the thalamocortical system [30], is associated with high values of Φ.

Figure 3

figure3

Information integration for a thalamocortical-like architecture. a. Optimization of information integration for a system that is both functionally specialized and functionally integrated. Shown is the causal interaction diagram for a network whose connection matrix was obtained by optimization for Φ (Φ = 74 bits). Note the heterogeneous arrangement of the incoming and outgoing connections: each element is connected to a different subset of elements, with different weights. Further analysis indicates that this network jointly maximizes functional specialization and functional integration among its 8 elements, thereby resembling the anatomical organization of the thalamocortical system [8]. b. Reduction of information integration through loss of specialization. The same amount of connectivity, distributed homogeneously to eliminate functional specialization, yields a complex with much lower values of Φ (Φ = 20 bits). c. Reduction of information integration through loss of integration. The same amount of connectivity, distributed in such a way as to form four independent modules to eliminate functional integration, yields four separate complexes with much lower values of Φ (Φ = 20 bits).

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