Raising the Connectome: The Emergence of Neuronal Activity and Behavior in Caenorhabditis elegans.

Bradly Alicea

doi:10.3389/fncel.2020.524791

Abstract

The differentiation of neurons and formation of connections between cells is the basis of both the adult phenotype and behaviors tied to cognition, perception, reproduction, and survival. Such behaviors are associated with local (circuits) and global (connectome) brain networks. A solid understanding of how these networks emerge is critical. This opinion piece features a guided tour of early developmental events in the emerging connectome, which is crucial to a new view on the connectogenetic process. Connectogenesis includes associating cell identities with broader functional and developmental relationships. During this process, the transition from developmental cells to terminally differentiated cells is defined by an accumulation of traits that ultimately results in neuronal-driven behavior. The well-characterized developmental and cell biology of Caenorhabditis elegans will be used to build a synthesis of developmental events that result in a functioning connectome. Specifically, our view of connectogenesis enables a first-mover model of synaptic connectivity to be demonstrated using data representing larval synaptogenesis. In a first-mover model of Stackelberg competition, potential pre- and postsynaptic relationships are shown to yield various strategies for establishing various types of synaptic connections. By comparing these results to what is known regarding principles for establishing complex network connectivity, these strategies are generalizable to other species and developmental systems. In conclusion, we will discuss the broader implications of this approach, as what is presented here informs an understanding of behavioral emergence and the ability to simulate related biological phenomena.

Highlights

The field of connectomics provides opportunities to view the structure and function of nervous systems in a new light
Our inquiry begins before the differentiation of neuronal cells, and the proto-connectome as it exists at five points during embryogenesis (265, 280, 290, 300, and 400 min postfertilization)
The neuronal symmetry (NSY)-5 network demonstrates how developmental asymmetry begins to emerge in connectogenesis

Summary

INTRODUCTION

The field of connectomics provides opportunities to view the structure and function of nervous systems in a new light. Our contribution to this understanding is to flesh out the structure of this timing relative to differentiation events This includes making connections between the terminal differentiation of specific neurons in development, their eventual functional identity, and the systemslevel significance of this temporal process. These relationships help us understand the tempo and scope of connectogenesis relative to the adult phenotype. This analysis yields information regarding ion channel types present at a specific time point in embryogenesis In terms of the latter, the data set featured in Packer et al (2019) is used in conjunction with annotation metadata and embryonic gene expression information to draw conclusions regarding the phylogenetic and developmental origins of the connectome. The final component relies upon how stereotypical C. elegans behaviors are heavily influenced by genetics to establish a link between the presence of certain neurons and the potential for early forms of chemosensation, thermosensation, and even learning and memory (Walker et al, 2018)

MATERIALS AND METHODS

RESULTS

DISCUSSION