|Movie tracking centers of masses of worms navigating a thermal gradient ranging from 23.5-28.5°C (left-right). Animals were raised at 20°C and move towards the colder side (negative thermotaxis); animals at the edges are no longer tracked.|
Animals have evolved complex mechanisms to respond and adapt to changes in critical external cues such as temperature. Many of these adaptations are homeostatic, allowing animals to maintain a relatively constant internal state in order to optimize functions. Ectotherms such as C. elegans primarily use behavioral strategies such as directed movement towards or away from temperature sources to mediate thermoregulation, although this is a strategy that is also employed by endotherms. The overall goal of this project is to identify the molecular and neuronal principles by which temperature is detected, transduced, and processed into specific behavioral outputs in an experience- and context-dependent manner. Given the strong conservation of neuron, synaptic and circuit mechanisms across species, we expect that information from this work will inform our general understanding of sensory processing and behavioral plasticity in higher animals, as well as expand our relatively poor knowledge of thermosensory signal transduction.
C. elegans exhibits particularly complex, experience-dependent thermosensory behaviors, providing an excellent system in which to explore the mechanisms that generate precise, yet flexible behaviors. Worms form a 'memory' of the temperature at which they are cultivated (Tc) and exhibit defined behaviors in temperature ranges relative to Tc. Thus, at temperatures higher than Tc worms move towards colder temperatures, whereas at temperatures lower than Tc they move towards warmer temperatures. At temperatures around Tc worms track isotherms. Remarkably, Tc memory is plastic and can be reset on short and long timescales of minutes to hours. Work from our lab and that of many others has identified several molecules and neurons required for the ability of C. elegans to respond to temperature changes of as little as 0.01ºC.
Members of the Axis of (Thermo)Taxis employ a multifaceted strategy combining genetic and molecular tools, quantitative behavioral assays, and in vivo calcium imaging to address the following questions:
- What are the thermosensors and signal transduction molecules required for detecting small changes in temperature?
- What are the molecular and neuronal mechanisms underlying short- and long-term adaptation to Tc?
- How do different thermosensory neurons communicate and coordinate their responses?
- How is temperature information integrated with stimuli such as food to alter behavior?
- Is there natural variation in the developmental responses of wild C. elegans strains to temperature?
- Asuka Takeishi, Yanxun V. Yu, Vera M. Hapiak, Harold W. Bell, Timothy O'Leary, Piali Sengupta Receptor-type Guanylyl Cyclases Confer Thermosensory Responses in C. elegans Neuron. S0896-6273(16)00181-1. [PubMed]
- Schild LC, Zbinden L, Bell HW, Sengupta P, Goodman MB, Glauser DA.(2014) The balance between cytoplasmic and nuclear CaM kinase-1 signaling controls the operating range of noxious heat avoidance. Neuron. 84(5):983-96. [PubMed]
- Yu YV, Bell HW, Glauser DA, Van hooser SD, Goodman MB, Sengupta P. (2014) CaMKI-dependent regulation of sensory gene expression mediates experience-dependent plasticity in the operating range of a thermosensory neuron. Neuron. 84(5):919-26. [PubMed]
- Beverly M, Anbil S, Sengupta P. (2011) Degeneracy and neuromodulation among thermosensory neurons contribute to robust thermosensory behaviors in Caenorhabditis elegans. J Neurosci. 31, 11718-27. [PubMed]
- Wasserman SM, Beverly M, Bell HW, Sengupta P. (2011) Regulation of Response Properties and Operating Range of the AFD Thermosensory Neurons by cGMP Signaling. Curr Biol. 21, 353-62. [PubMed]
- van der Linden AM*, Beverly M, Kadener S, Rodriguez J, Wasserman S, Rosbash M, Sengupta P* (2010) Genome-wide analysis of light and temperature-entrained circadian transcripts in C. elegans. PloS Biology. 8, e1000503 (*co-corresponding authors.) [PubMed]
- Biron, D.*, Wasserman, S.*, Thomas, J.H., Samuel, A.D., and Sengupta, P. (2008). An olfactory neuron responds stochastically to temperature and modulates Caenorhabditis elegans thermotactic behavior. Proc Natl Acad Sci USA 105, 11002-11007. [PubMed] (*equal contributors)