The evolution of distributed association networks in the human brain

Randy L. Buckner, Fenna M. Krienen
2013 Trends in Cognitive Sciences  
The human cerebral cortex is vastly expanded relative to other primates and disproportionately occupied by distributed association regions. Here we offer a hypothesis about how association networks evolved their prominence and came to possess circuit properties vital to human cognition. The rapid expansion of the cortical mantle may have untethered large portions of the cortex from strong constraints of molecular gradients and early activity cascades that lead to sensory hierarchies. What fill
more » ... he gaps between these hierarchies are densely interconnected networks that widely span the cortex and mature late into development. Limitations of the tethering hypothesis are discussed as well as its broad implications for understanding critical features of the human brain as a byproduct of size scaling. A speculative hypothesis Our ancestors advanced tool use, evolved language, and achieved complex social order during the past 3 million years. From one perspective, that is a lot of time for drift and selection to mold a new species. Changes in gene frequencies and adaptive mutations can arise rapidly in isolated populations. From another perspective, it is unexpected given the trajectories of closely related primate species. To anchor this point, consider the divergent evolution of the common chimpanzee and the bonobo over the past 1-2 million years. These two great apes became genetically isolated from one another when the Congo River formed allowing distinct phenotypes to evolve over a short time period [1]. Bonobos display a matriarchal social order that differs from the aggressive alpha maledominated society of the chimpanzee [2,3]. Chimpanzees use primitive tools to extract food in the wild, whereas Review Glossary Allometric evolution (within the context of brain evolution): evolutionary changes in one brain component that are predicted by changes in whole-brain size or by changes in another brain component. The relationship can deviate from isometric scaling, meaning that one component differs to a greater degree than the other, but the two components must show a predictable relationship. Association cortex: portions of the cerebral cortex that do not fall within primary sensory or motor projection areas. The term was popularized by Flechsig (1896) to identify regions of cortex that function as integration or association centers for more complex or elaborated mental processes. Australopiths: an early, extinct hominin genus discovered in Africa that walked upright but possessed brains only slightly larger than those of apes. Canonical circuit (canonical macrocircuit): a network of brain areas characterized by dense local connectivity between areas and a serial, hierarchical flow of information across areas. Such networks link incoming sensory information to the development of a motor response or action. Default network: a set of brain regions more active when people rest passively compared with when they focus on features of the external environment. The network is also active when people remember, think about the future, or engage in other forms of internal mentation, leading to the hypothesis that the network is important to advanced forms of cognition including the ability to mentally imagine oneself in alternative scenarios. Encephalization: brain size that exceeds the size predicted by body mass. Across species, most variation in brain size is predicted by body mass. The ratio of actual brain size versus the predicted brain size from body mass is known as the encephalization quotient. Humans have the highest encephalization quotient among mammals. Hierarchical organization: organization by which connections between areas facilitate ascending (forward) information flow and are often paired with reciprocal (descending) feedback connections. Information is successively transformed and elaborated at each step in the hierarchical sequence. Note that the term hierarchical as used here to describe anatomical connection patterns differs from other (but related) forms of hierarchical control that refer to how certain networks control other networks (e.g., [59] ). Hominin: humans and extinct human ancestors that are more closely associated with the human line of evolution than with chimpanzees and other apes. Hominids: humans, the great apes (chimpanzees, gorillas, orangutans), and their extinct ancestors. Mosaic evolution (within the context of brain evolution): evolutionary changes in one brain component without simultaneous changes in another brain component. Also called modular evolution. Noncanonical circuit: network organization in which widely distributed regions possess connections that do not conform to a sequential sequence of feedforward and feedback relationships; rather, they tend to be reciprocally connected with multiple violations for simple feedforward/feedback connectivity and share common targets and inputs that are distributed across the brain. Spandrel (in evolutionary biology): a characteristic or feature that was not the product of direct adaptive selection, but rather emerged as a side effect of direct pressure on some other feature. 1364-6613/$ -see front matter ß
doi:10.1016/j.tics.2013.09.017 pmid:24210963 fatcat:qhorja6njveodcfz4pfvfayliq