The hourglass organization of the Caenorhabditis elegans connectome

PLoS Comput Biol. 2020 Feb 6;16(2):e1007526. doi: 10.1371/journal.pcbi.1007526. eCollection 2020 Feb.

Abstract

We approach the C. elegans connectome as an information processing network that receives input from about 90 sensory neurons, processes that information through a highly recurrent network of about 80 interneurons, and it produces a coordinated output from about 120 motor neurons that control the nematode's muscles. We focus on the feedforward flow of information from sensory neurons to motor neurons, and apply a recently developed network analysis framework referred to as the "hourglass effect". The analysis reveals that this feedforward flow traverses a small core ("hourglass waist") that consists of 10-15 interneurons. These are mostly the same interneurons that were previously shown (using a different analytical approach) to constitute the "rich-club" of the C. elegans connectome. This result is robust to the methodology that separates the feedforward from the feedback flow of information. The set of core interneurons remains mostly the same when we consider only chemical synapses or the combination of chemical synapses and gap junctions. The hourglass organization of the connectome suggests that C. elegans has some similarities with encoder-decoder artificial neural networks in which the input is first compressed and integrated in a low-dimensional latent space that encodes the given data in a more efficient manner, followed by a decoding network through which intermediate-level sub-functions are combined in different ways to compute the correlated outputs of the network. The core neurons at the hourglass waist represent the information bottleneck of the system, balancing the representation accuracy and compactness (complexity) of the given sensory information.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Caenorhabditis elegans / physiology*
  • Computational Biology
  • Connectome*
  • Gap Junctions / physiology
  • Interneurons / physiology
  • Motor Neurons / physiology
  • Sensory Receptor Cells / physiology
  • Synapses / physiology

Grants and funding

Since the submission of the original manuscript, the contact author CD has received funding by DARPA to complete this work, https://www.darpa.mil/program/lifelong-learning-machines (Grant number: Lifelong Learning Machines (L2M) program of DARPA/MTO: Cooperative Agreement HR0011-18-2-0019). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.