Tonic signaling from O2 sensors sets neural circuit activity and behavioral state

K.E. Busch, P. Laurent, Z. Soltesz, R.J. Murphy, O. Faivre, B. Hedwig, M. Thomas, H.L. Smith, M. de Bono, Nature Neuroscience 15 (2012) 581–591.


Journal Article | Published | English
Author
; ; ; ; ; ; ; ;
Abstract
Tonic receptors convey stimulus duration and intensity and are implicated in homeostatic control. However, how tonic homeostatic signals are generated and how they reconfigure neural circuits and modify animal behavior is poorly understood. Here we show that Caenorhabditis elegans O2-sensing neurons are tonic receptors that continuously signal ambient [O2] to set the animal's behavioral state. Sustained signaling relied on a Ca2+ relay involving L-type voltage-gated Ca2+ channels, the ryanodine and the inositol-1,4,5-trisphosphate receptors. Tonic activity evoked continuous neuropeptide release, which helps elicit the enduring behavioral state associated with high [O2]. Sustained O2 receptor signaling was propagated to downstream neural circuits, including the hub interneuron RMG. O2 receptors evoked similar locomotory states at particular O2 concentrations, regardless of previous d[O2]/dt. However, a phasic component of the URX receptors' response to high d[O2]/dt, as well as tonic-to-phasic transformations in downstream interneurons, enabled transient reorientation movements shaped by d[O2]/dt. Our results highlight how tonic homeostatic signals can generate both transient and enduring behavioral change.
Publishing Year
Date Published
2012-03-04
Journal Title
Nature Neuroscience
Volume
15
Issue
4
Page
581-591
IST-REx-ID

Cite this

Busch KE, Laurent P, Soltesz Z, et al. Tonic signaling from O2 sensors sets neural circuit activity and behavioral state. Nature Neuroscience. 2012;15(4):581-591. doi:10.1038/nn.3061
Busch, K. E., Laurent, P., Soltesz, Z., Murphy, R. J., Faivre, O., Hedwig, B., … de Bono, M. (2012). Tonic signaling from O2 sensors sets neural circuit activity and behavioral state. Nature Neuroscience, 15(4), 581–591. https://doi.org/10.1038/nn.3061
Busch, Karl Emanuel, Patrick Laurent, Zoltan Soltesz, Robin Joseph Murphy, Olivier Faivre, Berthold Hedwig, Martin Thomas, Heather L Smith, and Mario de Bono. “Tonic Signaling from O2 Sensors Sets Neural Circuit Activity and Behavioral State.” Nature Neuroscience 15, no. 4 (2012): 581–91. https://doi.org/10.1038/nn.3061.
K. E. Busch et al., “Tonic signaling from O2 sensors sets neural circuit activity and behavioral state,” Nature Neuroscience, vol. 15, no. 4, pp. 581–591, 2012.
Busch KE, Laurent P, Soltesz Z, Murphy RJ, Faivre O, Hedwig B, Thomas M, Smith HL, de Bono M. 2012. Tonic signaling from O2 sensors sets neural circuit activity and behavioral state. Nature Neuroscience. 15(4), 581–591.
Busch, Karl Emanuel, et al. “Tonic Signaling from O2 Sensors Sets Neural Circuit Activity and Behavioral State.” Nature Neuroscience, vol. 15, no. 4, Springer Nature, 2012, pp. 581–91, doi:10.1038/nn.3061.

Link(s) to Main File(s)
Access Level
OA Open Access

Export

Marked Publications

Open Data IST Research Explorer

Sources

PMID: 22388961
PubMed | Europe PMC

Search this title in

Google Scholar