How do genes and the environment interact to generate behaviors? How are innate genetic templates for behavior modified by context and experience? To answer these questions we need to understand the relationships among genes, neurons, and circuits that generate behaviors. The nematode worm Caenorhabditis elegans provides an opportunity to understand behaviors at levels of resolution ranging from the molecule to the organism. Furthermore, an anatomical wiring diagram of C. elegans has been known for over twenty years. Still, we cannot predict the animal’s behavior from its connectivity, with the exception of deterministic escape behaviors. To gain a deeper insight into the key functions of the neurons and circuits, we are mapping a probabilistic goal-directed behavior, chemotaxis to attractive odors. Our approaches include genetic manipulation of neurons and circuits, high-resolution behavioral analysis, and quantitative analysis of neuronal responses. The transformation of olfactory information into goal-directed behavior begins with the activation of odorant receptors by their ligands. The neuronal responses to these inputs are shaped on at least two different timescales by intrinsic neuronal dynamics: a fast linear response permits rapid odor tracking, and a slower nonlinear response follows mean odor levels. In some respects these two computations resemble the fast detection and slow adaptation in bacterial chemotaxis that were defined by Howard Berg and his colleagues. Interestingly, different sensory neurons operate in distinct temporal regimes that are suited to their behavioral functions. These sensory signals are interpreted by interneurons with different dynamic properties. By exposing animals to defined temporal and spatial odor patterns and measuring specific parameters of the resulting behaviors, we can preferentially reveal turning dynamics in a biased random walk, directed orientation into an odor stripe, and speed regulation by odor. In addition, we have uncovered information that shapes the connectivity map and resulting behaviors: neuromodulators that are not apparent in the anatomical circuits, flexible information flow through alternative synaptic pathways, and neuronal dynamics that shape responses over time.
Physiology 2012 (Edinburgh) (2012) Proc Physiol Soc 27, PL4
Plenary Lectures: Decoding the olfactory world in time and space
D. Albrecht1, C. Cho1, S. Kato1, J. Larsch1, Y. Xu1, C. Bargmann1
1. The Rockefeller University, New York, New York, United States.
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Where applicable, experiments conform with Society ethical requirements.