Contrast enhancement of stimulus intermittency in a primary olfactory network and its behavioral significance

Background An animal navigating to an unseen odor source must accurately resolve the spatiotemporal distribution of that stimulus in order to express appropriate upwind flight behavior. Intermittency of natural odor plumes, caused by air turbulence, is critically important for many insects, including the hawkmoth, Manduca sexta, for odor-modulated search behavior to an odor source. When a moth's antennae receive intermittent odor stimulation, the projection neurons (PNs) in the primary olfactory centers (the antennal lobes), which are analogous to the olfactory bulbs of vertebrates, generate discrete bursts of action potentials separated by periods of inhibition, suggesting that the PNs may use the binary burst/non-burst neural patterns to resolve and enhance the intermittency of the stimulus encountered in the odor plume. Results We tested this hypothesis first by establishing that bicuculline methiodide reliably and reversibly disrupted the ability of PNs to produce bursting response patterns. Behavioral studies, in turn, demonstrated that after injecting this drug into the antennal lobe at the effective concentration used in the physiological experiments animals could no longer efficiently locate the odor source, even though they had detected the odor signal. Conclusions Our results establish a direct link between the bursting response pattern of PNs and the odor-tracking behavior of the moth, demonstrating the behavioral significance of resolving the dynamics of a natural odor stimulus in antennal lobe circuits.

[1]  M. Dickinson,et al.  Free-flight responses of Drosophila melanogaster to attractive odors , 2006, Journal of Experimental Biology.

[2]  J. Hildebrand,et al.  Functionally distinct subdivisions of the macroglomerular complex in the antennal lobe of the male sphinx moth Manduca sexta , 1991, The Journal of comparative neurology.

[3]  R. Cardé,et al.  Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths , 1994, Nature.

[4]  K. Daly,et al.  Disruption of GABAA in the insect antennal lobe generally increases odor detection and discrimination thresholds. , 2008, Chemical senses.

[5]  M. Lehrer Orientation and Communication in Arthropods , 1997, EXS.

[6]  WHEN DOES MOTION RELATIVE TO NEIGHBORING SURFACES ALTER THE FLOW THROUGH ARRAYS OF HAIRS? , 1994, The Journal of experimental biology.

[7]  L. Tolbert,et al.  Glial cells stabilize axonal protoglomeruli in the developing olfactory lobe of the moth Manduca sexta , 1996, The Journal of comparative neurology.

[8]  B. Hansson,et al.  Central processing of pulsed pheromone signals by antennal lobe neurons in the male moth Agrotis segetum. , 1999, Journal of neurophysiology.

[9]  P. Moore,et al.  Boundary-layer effect on chemical signal movement near the antennae of the sphinx moth, Manduca sexta : temporal filters for olfaction , 1998, Journal of Comparative Physiology A.

[10]  J. Hildebrand,et al.  Multitasking in the Olfactory System: Context-Dependent Responses to Odors Reveal Dual GABA-Regulated Coding Mechanisms in Single Olfactory Projection Neurons , 1998, The Journal of Neuroscience.

[11]  J. Tumlinson,et al.  Field tests of syntheticManduca sexta sex pheromone , 1994, Journal of Chemical Ecology.

[12]  M. Koehl,et al.  Sniffing by a silkworm moth: wing fanning enhances air penetration through and pheromone interception by antennae. , 2000, The Journal of experimental biology.

[13]  M. Koehl,et al.  The fluid mechanics of arthropod sniffing in turbulent odor plumes. , 2006, Chemical senses.

[14]  T. Baker,et al.  Reiterative responses to single strands of odor promote sustained upwind flight and odor source location by moths. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[15]  R. T. Cardé,et al.  Dissection of the pheromone-modulated flight of moths using single-pulse response as a template , 1996, Experientia.

[16]  K. Kaissling,et al.  Pheromone-controlled anemotaxis in moths , 1997 .

[17]  J. Hildebrand,et al.  Pheromone receptor cells in the male moth Manduca sexta , 1989 .

[18]  J. Hildebrand,et al.  Coincident stimulation with pheromone components improves temporal pattern resolution in central olfactory neurons. , 1997, Journal of neurophysiology.

[19]  R. Kanzaki,et al.  Morphological and physiological properties of pheromone-triggered flipflopping descending interneurons of the male silkworm moth, Bombyx mori , 1994, Journal of Comparative Physiology A.

[20]  B. Hansson,et al.  Dose-dependent response characteristics of antennal lobe neurons in the male moth Agrotis segetum (Lepidoptera: Noctuidae) , 1997, Journal of Comparative Physiology A.

[21]  T. Baker,et al.  A pulsed cloud of sex pheromone elicits upwind flight in male moths , 1985 .

[22]  J. Hildebrand,et al.  Temporal tuning of odor responses in pheromone‐responsive projection neurons in the brain of the sphinx moth Manduca sexta , 1999, The Journal of comparative neurology.

[23]  N. Vickers Mechanisms of animal navigation in odor plumes. , 2000, The Biological bulletin.

[24]  Mark A. Willis,et al.  Effects of intermittent and continuous pheromone stimulation on the flight behaviour of the oriental fruit moth, Grapholita molesta , 1984 .

[25]  M. Brazier The Electrical Activity of the Nervous System , 1961, Science.

[26]  John G Hildebrand,et al.  Spatial and Temporal Organization of Ensemble Representations for Different Odor Classes in the Moth Antennal Lobe , 2004, The Journal of Neuroscience.

[27]  T. Baker,et al.  Odour-plume dynamics influence the brain's olfactory code , 2001, Nature.

[28]  Hong Lei,et al.  Local inhibition modulates odor-evoked synchronization of glomerulus-specific output neurons , 2002, Nature Neuroscience.

[29]  A. Ludlow,et al.  Guidance of flying male moths by wind‐borne sex pheromone , 1981 .

[30]  Ring T. Cardé,et al.  Antennal resolution of pulsed pheromone plumes in three moth species. , 2002, Journal of insect physiology.

[31]  D. Pinault,et al.  A novel single-cell staining procedure performed in vivo under electrophysiological control: morpho-functional features of juxtacellularly labeled thalamic cells and other central neurons with biocytin or Neurobiotin , 1996, Journal of Neuroscience Methods.

[32]  J. Hildebrand,et al.  Representation of binary pheromone blends by glomerulus-specific olfactory projection neurons , 2004, Journal of Comparative Physiology A.

[33]  M. Sanders Handbook of Sensory Physiology , 1975 .

[34]  John G. Hildebrand,et al.  Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the mothManduca sexta , 1987, Journal of Comparative Physiology A.

[35]  J. Tumlinson,et al.  Identification of a pheromone blend attractive to Manduca sexta (L.) males in a wind tunnel , 1989 .

[36]  J. Thorson,et al.  Insect Olfactory Sensilla: Structural, Chemical and Electrical Aspects of the Functional Organisation , 1980 .

[37]  Jeffrey A. Riffell,et al.  Behavioral consequences of innate preferences and olfactory learning in hawkmoth–flower interactions , 2008, Proceedings of the National Academy of Sciences.

[38]  J. Murlis,et al.  Fine‐scale structure of odour plumes in relation to insect orientation to distant pheromone and other attractant sources , 1981 .

[39]  Steven Schofield,et al.  Flight behaviour of Cadra cautella males in rapidly pulsed pheromone plumes , 2002 .

[40]  J. Hildebrand,et al.  Olfactory interneurons in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[41]  M. Carlsson,et al.  Olfactory activation patterns in the antennal lobe of the sphinx moth, Manduca sexta , 2003, Journal of Comparative Physiology A.

[42]  J. Hildebrand,et al.  Insect Olfaction , 1999, Springer Berlin Heidelberg.

[43]  M. Willis,et al.  Effects of altering flow and odor information on plume tracking behavior in walking cockroaches, Periplaneta americana (L.) , 2008, Journal of Experimental Biology.

[44]  T. L. Payne,et al.  Mechanisms in Insect Olfaction , 1986 .