Motor output reflects the linear superposition of visual and olfactory inputs in Drosophila

SUMMARY Animals actively seeking food and oviposition sites must integrate feedback from multiple sensory modalities. Here, we examine visual and olfactory sensorimotor interactions in Drosophila. In a tethered-flight simulator, flies modulate wingbeat frequency and amplitude in response to visual and olfactory stimuli. Responses to both cues presented simultaneously are nearly identical to the sum of responses to stimuli presented in isolation for the onset and duration of odor delivery, suggesting independent sensorimotor pathways. Visual feedback does, however, alter the time course of the odor-off response. Based on the physiology of the flight motor system and recent free-flight analyses, we present a hypothetical model to account for the summation or superposition of sensorimotor responses during flight.

[1]  L. Vosshall.  Olfaction in Drosophila , 2000, Current Opinion in Neurobiology.

[2]  M. Dickinson,et al.  The changes in power requirements and muscle efficiency during elevated force production in the fruit fly Drosophila melanogaster. , 1997, The Journal of experimental biology.

[3]  Bill S Hansson,et al.  Novel natural ligands for Drosophila olfactory receptor neurones , 2003, Journal of Experimental Biology.

[4]  K. Götz,et al.  Optomotor control of course and altitude in Drosophila melanogaster is correlated with distinct activities of at least three pairs of flight steering muscles. , 1996, The Journal of experimental biology.

[5]  Roger C. Hardie,et al.  Light Adaptation in Drosophila Photoreceptors: II. Rising Temperature Increases the Bandwidth of Reliable Signaling , 2001 .

[6]  Roger C. Hardie,et al.  Light Adaptation in Drosophila Photoreceptors: I. Response Dynamics and Signaling Efficiency at 25°C , 2001 .

[7]  J. Truman,et al.  Soluble Guanylate Cyclase Is Required during Development for Visual System Function in Drosophila , 2001, The Journal of Neuroscience.

[8]  A Guo,et al.  Association of visual objects and olfactory cues in Drosophila. , 1997, Learning & memory.

[9]  N. Strausfeld,et al.  The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. , 1998, Learning & memory.

[10]  Tim Tully,et al.  Associative Learning Disrupted by Impaired Gs Signaling in Drosophila Mushroom Bodies , 1996, Science.

[11]  Michael H Dickinson,et al.  Collision-avoidance and landing responses are mediated by separate pathways in the fruit fly, Drosophila melanogaster. , 2002, The Journal of experimental biology.

[12]  N. Perrimon,et al.  Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. , 1993, Development.

[13]  T. Préat,et al.  Localization of Long-Term Memory Within the Drosophila Mushroom Body , 2001, Science.

[14]  J. Trimarchi,et al.  Different neural pathways coordinate Drosophila flight initiations evoked by visual and olfactory stimuli. , 1995, The Journal of experimental biology.

[15]  T. Kitamoto.  Conditional modification of behavior in Drosophila by targeted expression of a temperature-sensitive shibire allele in defined neurons. , 2001, Journal of neurobiology.

[16]  Michael H Dickinson,et al.  Spatial organization of visuomotor reflexes in Drosophila , 2004, Journal of Experimental Biology.

[17]  Mark A. Willis,et al.  Pheromone-modulated optomotor response in male gypsy moths, Lymantria dispar L.: Directionally selective visual interneurons in the ventral nerve cord , 1990, Journal of Comparative Physiology A.

[18]  W. Gronenberg,et al.  Descending neurons supplying the neck and flight motor of diptera: Physiological and anatomical characteristics , 1990, The Journal of comparative neurology.

[19]  M Heisenberg,et al.  Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. , 1994, Science.

[20]  Michael H Dickinson,et al.  Fly Flight A Model for the Neural Control of Complex Behavior , 2001, Neuron.

[21]  C. H. F. Rowell,et al.  Three descending interneurons reporting deviation from course in the locust , 1986, Journal of Comparative Physiology A.

[22]  Michael H Dickinson,et al.  Odor localization requires visual feedback during free flight in Drosophila melanogaster , 2003, Journal of Experimental Biology.

[23]  I A Meinertzhagen,et al.  Experience-Dependent Developmental Plasticity in the Optic Lobe of Drosophila melanogaster , 1997, The Journal of Neuroscience.

[24]  C. Rowell,et al.  The perception of the visual flow field by flying locusts : a behavioural and neuronal analysis , 1992 .

[25]  K. Götz,et al.  Activation phase ensures kinematic efficacy in flight-steering muscles of Drosophila melanogaster , 1996, Journal of Comparative Physiology A.

[26]  C. H. F. Rowell,et al.  Three descending interneurons reporting deviation from course in the locust , 1986, Journal of Comparative Physiology A.

[27]  M. Dickinson,et al.  The Control of Mechanical Power in Insect Flight , 1998 .

[28]  M. Dickinson,et al.  The production of elevated flight force compromises manoeuvrability in the fruit fly Drosophila melanogaster. , 2001, The Journal of experimental biology.

[29]  R. Wolf,et al.  Visual control of straight flight in Drosophila melanogaster , 1990, Journal of Comparative Physiology A.

[30]  S. N. Fry,et al.  The Aerodynamics of Free-Flight Maneuvers in Drosophila , 2003, Science.

[31]  R. Strauss.  The central complex and the genetic dissection of locomotor behaviour , 2002, Current Opinion in Neurobiology.

[32]  M. S. Tu,et al.  The Function of Dipteran Flight Muscle , 1997 .

[33]  Robert M. Olberg,et al.  Parallel encoding of direction of wind, head, abdomen, and visual pattern movement by single interneurons in the dragonfly , 1981, Journal of comparative physiology.

[34]  W. Gronenberg,et al.  Premotor descending neurons responding selectively to local visual stimuli in flies , 1992, The Journal of comparative neurology.

[35]  R. Wyman,et al.  Motor outputs of giant nerve fiber in Drosophila. , 1980, Journal of neurophysiology.

[36]  W. Gronenberg,et al.  Oculomotor control in calliphorid flies: Organization of descending neurons to neck motor neurons responding to visual stimuli , 1995, The Journal of comparative neurology.

[37]  M. Dickinson,et al.  A comparison of visual and haltere-mediated equilibrium reflexes in the fruit fly Drosophila melanogaster , 2003, Journal of Experimental Biology.

[38]  Michael H Dickinson,et al.  The influence of visual landscape on the free flight behavior of the fruit fly Drosophila melanogaster. , 2002, The Journal of experimental biology.