Encoding of Both Analog- and Digital-like Behavioral Outputs by One C. elegans Interneuron

Abstract

Summary Model organisms usually possess a small nervous system, but nevertheless execute a large array of complex behaviors, suggesting that some neurons are likely multifunctional and may encode multiple behavioral outputs. Here, we show that the C. elegans interneuron AIY regulates two distinct behavioral outputs: locomotion speed and direction-switch by recruiting two different circuits. The “speed” circuit is excitatory with a wide dynamic range, which is well suited to encode speed, an analog-like output. The “direction-switch” circuit is inhibitory with a narrow dynamic range, which is ideal for encoding direction-switch, a digital-like output. Both circuits employ the neurotransmitter ACh, but utilize distinct postsynaptic ACh receptors, whose distinct biophysical properties contribute to the distinct dynamic ranges of the two circuits. This mechanism enables graded worm synapses to encode both analog- and digital-like outputs. Our studies illustrate how an interneuron in a simple organism encodes multiple behavioral outputs at the circuit, synaptic, and molecular levels.

A Gustatory Neural Circuit ofCaenorhabditis elegansGenerates Memory-Dependent Behaviors in Na+Chemotaxis

“…Extending the stimulation time caused no change in worms' behavioral patterns (Fig. 1g), which was also the case in earlier reports on photoactivation of AIY (Li et al, 2014) and AWA (Larsch et al, 2015). After cultivation at 50 or 100 mM Na ϩ , worms showed larger forward locomotion responses upon ASEL photoactivation on test plates with 100 mM Na ϩ compared with those with 50 or 0 mM Na ϩ (Fig.…”

“…All C. elegans strains were derived from the wild-type strain Bristol N2. All strains used for optogenetics carried the lite-1(ce314 ) mutation to diminish the innate avoidance of blue light (Edwards et al, 2008;Ward et al, 2008;Liu et al, 2010;Li et al, 2014). Fast-growing E. coli NA22 was used as food source in behavioral assays and chemotaxis assays to avoid starvation (Tomioka et al, 2006;Adachi et al, 2010;Kunitomo et al, 2013).…”

“…In contrast, AIY was reported to show increased calcium level upon odor addition and decreased calcium level upon odor removal (Chalasani et al, 2007) and AIY activation promoted forward locomotion and inhibited turning ( Fig. 1a; Li et al, 2014). For stimulation of AIY, we used two strains that express ChR2 in AIY (strain #1 and #2; see Materials and Methods).…”

Whole-brain calcium imaging with cellular resolution in freely behaving Caenorhabditis elegans

“…Because C. elegans nuclei are thought to be porous to calcium and because the nuclei take up a large portion of the cell body, nuclear recordings used here likely capture calcium transients observed in the cell body. There are, however, known neurons where calcium signals in the processes are different from those in the cell body and, by extension, the nuclei (24,(35)(36)(37). It remains to be seen whether independent calcium dynamics in the processes are unique to these few specific neurons or are a more general phenomenon.…”

The C. elegans Taste Receptor Homolog LITE-1 Is a Photoreceptor

“…Calcium imaging to quantify LITE-1 function-Calcium imaging of muscle cells was performed on an inverted microscope (Olympus IX73) under a 60× lens as previously described (Li et al, 2014;Xiao et al, 2013). RCaMP was expressed as a transgene in muscle cells using the myo-3 promoter.…”