The neural network for chemotaxis to tastants in Caenorhabditis elegans is specialized for temporal differentiation

Thiele TR, Faumont S, Lockery SR

J. Neurosci. 2009 Sep;29(38):11904-11

PMID: 19776276


Chemotaxis in Caenorhabditis elegans depends critically on the rate of change of attractant concentration computed as the worm moves through its environment. This computation depends, in turn, on the neuron class ASE, a left-right pair of pair of chemosensory neurons that is functionally asymmetric such that the left neuron is an on-cell, whereas the right neuron is an off-cell. To determine whether this coding strategy is a general feature of chemosensation in C. elegans, we imaged calcium responses in all chemosensory neurons known or in a position to contribute to chemotaxis to tastants in this organism. This survey revealed one new class of on-cells (ADF) and one new class of off-cells (ASH). Thus, the ASE class is unique in having both an on-cell and an off-cell. We also found that the newly characterized on-cells and off-cells promote runs and turns, respectively, mirroring the pattern reported previously for ASEL and ASER. Our results suggest that the C. elegans chemotaxis network is specialized for the temporal differentiation of chemosensory inputs, as required for chemotaxis.

Optogenetic analysis of synaptic transmission in the central nervous system of the nematode Caenorhabditis elegans

Lindsay TH, Thiele TR, Lockery SR

Nat Commun 2011;2:306

PMID: 21556060


A reliable method for recording evoked synaptic events in identified neurons in Caenorhabditis elegans would greatly accelerate our understanding of its nervous system at the molecular, cellular and network levels. Here we describe a method for recording synaptic currents and potentials from identified neurons in nearly intact worms. Dissection and exposure of postsynaptic neurons is facilitated by microfabricated agar substrates, and ChannelRhodopsin-2 is used to stimulate presynaptic neurons. We used the method to analyse functional connectivity between a polymodal nociceptor and a command neuron that initiates a stochastic escape behaviour. We find that escape probability mirrors the time course of synaptic current in the command neuron. Moreover, synaptic input increases smoothly as stimulus strength is increased, suggesting that the overall input-output function of the connection is graded. We propose a model in which the energetic cost of escape behaviours in C. elegans is tuned to the intensity of the threat.

An image-free opto-mechanical system for creating virtual environments and imaging neuronal activity in freely moving Caenorhabditis elegans

Faumont S, Rondeau G, Thiele TR, Lawton KJ, McCormick KE, Sottile M, Griesbeck O, Heckscher ES, Roberts WM, Doe CQ, Lockery SR

PLoS ONE 2011;6(9):e24666

PMID: 21969859


Non-invasive recording in untethered animals is arguably the ultimate step in the analysis of neuronal function, but such recordings remain elusive. To address this problem, we devised a system that tracks neuron-sized fluorescent targets in real time. The system can be used to create virtual environments by optogenetic activation of sensory neurons, or to image activity in identified neurons at high magnification. By recording activity in neurons of freely moving C. elegans, we tested the long-standing hypothesis that forward and reverse locomotion are generated by distinct neuronal circuits. Surprisingly, we found motor neurons that are active during both types of locomotion, suggesting a new model of locomotion control in C. elegans. These results emphasize the importance of recording neuronal activity in freely moving animals and significantly expand the potential of imaging techniques by providing a mean to stabilize fluorescent targets.