Life and Understanding: The Origins of "Understanding" in Self-Organizing Nervous Systems

This article is motivated by a formulation of biotic self-organization in Friston (2013), where the emergence of "life" in coupled material entities (e.g., macromolecules) was predicated on bounded subsets that maintain a degree of statistical independence from the rest of the network. Boundary elements in such systems constitute a Markov blanket; separating the internal states of a system from its surrounding states. In this article, we ask whether Markov blankets operate in the nervous system and underlie the development of intelligence, enabling a progression from the ability to sense the environment to the ability to understand it. Markov blankets have been previously hypothesized to form in neuronal networks as a result of phase transitions that cause network subsets to fold into bounded assemblies, or packets (Yufik and Sheridan, 1997; Yufik, 1998a). The ensuing neuronal packets hypothesis builds on the notion of neuronal assemblies (Hebb, 1949, 1980), treating such assemblies as flexible but stable biophysical structures capable of withstanding entropic erosion. In other words, structures that maintain their integrity under changing conditions. In this treatment, neuronal packets give rise to perception of "objects"; i.e., quasi-stable (stimulus bound) feature groupings that are conserved over multiple presentations (e.g., the experience of perceiving "apple" can be interrupted and resumed many times). Monitoring the variations in such groups enables the apprehension of behavior; i.e., attributing to objects the ability to undergo changes without loss of self-identity. Ultimately, "understanding" involves self-directed composition and manipulation of the ensuing "mental models" that are constituted by neuronal packets, whose dynamics capture relationships among objects: that is, dependencies in the behavior of objects under varying conditions. For example, movement is known to involve rotation of population vectors in the motor cortex (Georgopoulos et al., 1988, 1993). The neuronal packet hypothesis associates "understanding" with the ability to detect and generate coordinated rotation of population vectors-in neuronal packets-in associative cortex and other regions in the brain. The ability to coordinate vector representations in this way is assumed to have developed in conjunction with the ability to postpone overt motor expression of implicit movement, thus creating a mechanism for prediction and behavioral optimization via mental modeling that is unique to higher species. This article advances the notion that Markov blankets-necessary for the emergence of life-have been subsequently exploited by evolution and thus ground the ways that living organisms adapt to their environment, culminating in their ability to understand it.