Cellular mechanisms for integral feedback in visually guided behavior.
Sensory feedback is a ubiquitous feature of guidance systems in both animals and engineered vehicles. For example, a common strategy for moving along a straight path is to turn such that the measured rate of rotation is zero. This task can be accomplished by using a feedback signal that is proportional to the instantaneous value of the measured sensory signal. In such a system, the addition of an integral term depending on past values of the sensory input is needed to eliminate steady-state error [proportional-integral (PI) control]. However, the means by which nervous systems implement such a computation are poorly understood. Here, we show that the optomotor responses of flying Drosophila follow a time course consistent with temporal integration of horizontal motion input. To investigate the cellular basis of this effect, we performed whole-cell patch-clamp recordings from the set of identified visual interneurons [horizontal system (HS) cells] thought to control this reflex during tethered flight. At high stimulus speeds, HS cells exhibit steady-state responses during flight that are absent during quiescence, a state-dependent difference in physiology that is explained by changes in their presynaptic inputs. However, even during flight, the membrane potential of the large-field interneurons exhibits no evidence for integration that could explain the behavioral responses. However, using a genetically encoded indicator, we found that calcium accumulates in the terminals of the interneurons along a time course consistent with the behavior and propose that this accumulation provides a mechanism for temporal integration of sensory feedback consistent with PI control.
Departments of Biology and Physiology and Biophysics, University of Washington, Seattle, WA 98195.
Bettina
B
Schnell
Peter T
PT
Weir
Eatai
E
Roth
Adrienne L
AL
Fairhall
Michael H
MH
Dickinson
D000818:Animals; D001522:Behavior, Animal / Q000502:physiology*; D002118:Calcium / Q000378:metabolism; D004330:Drosophila / Q000502:physiology*; D005246:Feedback; D005426:Flight, Animal / Q000502:physiology*; D007395:Interneurons / Q000502:physiology*; D008959:Models, Neurological; D009434:Neural Pathways / Q000502:physiology; D018408:Patch-Clamp Techniques; D010775:Photic Stimulation; D017729:Presynaptic Terminals / Q000378:metabolism; D013997:Time Factors; D014785:Vision, Ocular / Q000502:physiology*
D002118:Calcium
feedback control; fruit fly; insect vision; lobula plate tangential cells