TY - JOUR
T1 - The synaptic organization in the Caenorhabditis elegans neural network suggests significant local compartmentalized computations
AU - Ruach, Rotem
AU - Ratner, Nir
AU - Emmons, Scott W.
AU - Zaslaver, Alon
N1 - Publisher Copyright:
Copyright © 2023 the Author(s). Published by PNAS.
PY - 2023/1/17
Y1 - 2023/1/17
N2 - Neurons are characterized by elaborate tree-like dendritic structures that support local computations by integrating multiple inputs from upstream presynaptic neurons. It is less clear whether simple neurons, consisting of a few or even a single neurite, may perform local computations as well. To address this question, we focused on the compact neural network of Caenorhabditis elegans animals for which the full wiring diagram is available, including the coordinates of individual synapses. We find that the positions of the chemical synapses along the neurites are not randomly distributed nor can they be explained by anatomical constraints. Instead, synapses tend to form clusters, an organization that supports local compartmentalized computations. In mutually synapsing neurons, connections of opposite polarity cluster separately, suggesting that positive and negative feedback dynamics may be implemented in discrete compartmentalized regions along neurites. In triple-neuron circuits, the nonrandom synaptic organization may facilitate local functional roles, such as signal integration and coordinated activation of functionally related downstream neurons. These clustered synaptic topologies emerge as a guiding principle in the network, presumably to facilitate distinct parallel functions along a single neurite, which effectively increase the computational capacity of the neural network.
AB - Neurons are characterized by elaborate tree-like dendritic structures that support local computations by integrating multiple inputs from upstream presynaptic neurons. It is less clear whether simple neurons, consisting of a few or even a single neurite, may perform local computations as well. To address this question, we focused on the compact neural network of Caenorhabditis elegans animals for which the full wiring diagram is available, including the coordinates of individual synapses. We find that the positions of the chemical synapses along the neurites are not randomly distributed nor can they be explained by anatomical constraints. Instead, synapses tend to form clusters, an organization that supports local compartmentalized computations. In mutually synapsing neurons, connections of opposite polarity cluster separately, suggesting that positive and negative feedback dynamics may be implemented in discrete compartmentalized regions along neurites. In triple-neuron circuits, the nonrandom synaptic organization may facilitate local functional roles, such as signal integration and coordinated activation of functionally related downstream neurons. These clustered synaptic topologies emerge as a guiding principle in the network, presumably to facilitate distinct parallel functions along a single neurite, which effectively increase the computational capacity of the neural network.
KW - C. elegans
KW - neurite computation
KW - synapses
UR - http://www.scopus.com/inward/record.url?scp=85146193343&partnerID=8YFLogxK
U2 - 10.1073/pnas.2201699120
DO - 10.1073/pnas.2201699120
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C2 - 36630454
AN - SCOPUS:85146193343
SN - 0027-8424
VL - 120
JO - Proceedings of the National Academy of Sciences of the United States of America
JF - Proceedings of the National Academy of Sciences of the United States of America
IS - 3
M1 - e2201699120
ER -