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.
© 2014 National Academy of Sciences. Freely available online through the PNAS open access option. Edited by Terrence J. Sejnowski, Salk Institute for Biological Studies, La Jolla, CA, and approved March 7, 2014 (received for review January 14, 2014) We thank Anne Sustar for the confocal image of the R27B03-Gal4 line. This work was supported by the Raymond and Beverly Sackler Foundation (B.S.), the Paul G. Allen Family Foundation (M.H.D.), and Air Force Office of Scientific Research Grant FA9550-10-1-0368 (M.H.D). Author contributions: B.S., P.T.W., A.L.F., and M.H.D. designed research; B.S., P.T.W., and E.R. performed research; B.S., P.T.W., and E.R. analyzed data; and B.S., P.T.W., A.L.F., and M.H.D. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1400698111/-/DCSupplemental.
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