Temporal responses of C. elegans chemosensory neurons are preserved in behavioral dynamics.
Animals track fluctuating stimuli over multiple timescales during natural olfactory behaviors. Here, we define mechanisms underlying these computations in Caenorhabditis elegans. By characterizing neuronal calcium responses to rapidly fluctuating odor sequences, we show that sensory neurons reliably track stimulus fluctuations relevant to behavior. AWC olfactory neurons respond to multiple odors with subsecond precision required for chemotaxis, whereas ASH nociceptive neurons integrate noxious cues over several seconds to reach a threshold for avoidance behavior. Each neuron's response to fluctuating stimuli is largely linear and can be described by a biphasic temporal filter and dynamical model. A calcium channel mutation alters temporal filtering and avoidance behaviors initiated by ASH on similar timescales. A sensory G-alpha protein mutation affects temporal filtering in AWC and alters steering behavior in a way that supports an active sensing model for chemotaxis. Thus, temporal features of sensory neurons can be propagated across circuits to specify behavioral dynamics.
Department of Neuroscience and Department of Physiology and Cellular Biophysics, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA.
Saul
S
Kato
Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10065, USA.
Yifan
Y
Xu
Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10065, USA.
Christine E
CE
Cho
Department of Neuroscience and Department of Physiology and Cellular Biophysics, Columbia University College of Physicians and Surgeons, New York, NY 10032, USA. Electronic address: lfa2103@columbia.edu.
L F
LF
Abbott
Howard Hughes Medical Institute, The Rockefeller University, New York, NY 10065, USA. Electronic address: cori@rockefeller.edu.
Cornelia I
CI
Bargmann
D000818:Animals; D030801:Animals, Genetically Modified; D001522:Behavior, Animal / Q000502:physiology*; D017173:Caenorhabditis elegans; D029742:Caenorhabditis elegans Proteins / Q000235:genetics; D002118:Calcium / Q000378:metabolism; D002628:Chemoreceptor Cells / Q000502:physiology*; D005071:Evoked Potentials / Q000235:genetics; D008954:Models, Biological; D009619:Nociceptors / Q000378:metabolism; D017711:Nonlinear Dynamics; D009812:Odorants; D009833:Olfactory Pathways / Q000166:cytology; D012903:Smell / Q000502:physiology*
D029742:Caenorhabditis elegans Proteins; D002118:Calcium