Three systems of circuit formation: assembly, updating and tuning

Abstract

Understanding the relationship between genotype and neuronal circuit phenotype necessitates an integrated view of genetics, development, plasticity and learning. Challenging the prevailing notion that emphasizes learning and plasticity as primary drivers of circuit assembly, in this Perspective, we delineate a tripartite framework to clarify the respective roles that learning and plasticity might have in this process. In the first part of the framework, which we term System One, neural circuits are established purely through genetically driven algorithms, in which spike timing-dependent plasticity serves no instructive role. We propose that these circuits equip the animal with sufficient skill and knowledge to successfully engage the world. Next, System Two is governed by rare but critical ‘single-shot learning’ events, which occur in response to survival situations and prompt rapid synaptic reconfiguration. Such events serve as crucial updates to the existing hardwired knowledge base of an organism. Finally, System Three is characterized by a perpetual state of synaptic recalibration, involving continual plasticity for circuit stabilization and fine-tuning. By outlining the definitions and roles of these three core systems, our framework aims to resolve existing ambiguities related to and enrich our understanding of neural circuit formation. In this Perspective, Barabási, Ferreira Castro and Engert challenge the notion that learning and plasticity primarily drive the assembly of neural circuits. They present a tripartite framework for how neural circuits form, outlining the relative contributions of developmental, associative learning and tuning-based factors to this process and knowledge acquisition.