Spatio‐temporal Ca2+ dynamics of moth olfactory projection neurones

We studied the Ca2+ dynamics of odour‐evoked glomerular patterns in the antennal lobe of the moth Spodoptera littoralis using optical imaging. Here we selectively stained a large population of antennal lobe output neurones, projection neurones, by retrograde filling with FURA‐dextran from the inner antennocerebral tract in the protocerebrum. Different plant‐associated odorants evoked distributed patterns of activated glomeruli that were odour dependent and repeatable. These patterns were, however, dynamic during the period of odour exposure. Temporal responses differed across glomeruli and were stimulus dependent. Next we examined how the correlations between patterns evoked by different odorants changed with time. Initially, responses to structurally similar compounds were highly correlated, whereas responses to structurally different compounds differed. Within the period of odour exposure (1 s) we found a significant reduction in similarity of responses evoked by different odours, irrespective of initial similarity, whereas trial‐to‐trial correlations remained high. Our results suggested an ability for coarse classification at the initial encounter with an odour source. With time, however, the discrimination ability increases and structurally similar odours can be distinguished.

[1]  B. Hansson,et al.  Oviposition deterring components in larval frass of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae): a behavioural and electrophysiological evaluation , 1993 .

[2]  C. Hinks,et al.  BIOSYSTEMATICS OF THE GENUS EUXOA (LEPIDOPTERA: NOCTUIDAE): V. REARING PROCEDURES, AND LIFE CYCLES OF 36 SPECIES , 1976, The Canadian Entomologist.

[3]  B. Hansson,et al.  Plant‐odour‐specific receptor neurones on the antennae of female and male Spodoptera littoralis , 1995 .

[4]  J. Hildebrand,et al.  Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta , 1993, Journal of Comparative Physiology A.

[5]  M. Carlsson,et al.  Spatial representation of odorant structure in the moth antennal lobe: A study of structure–response relationships at low doses , 2003, The Journal of comparative neurology.

[6]  M. M. Sadek,et al.  Glomerular representation of plant volatiles and sex pheromone components in the antennal lobe of the female Spodoptera littoralis. , 2002, The Journal of experimental biology.

[7]  John G. Hildebrand,et al.  Frequency coding by central olfactory neurons in the sphinx moth Manduca sexta , 1988 .

[8]  A. Chess,et al.  Convergent projections of Drosophila olfactory neurons to specific glomeruli in the antennal lobe , 2000, Nature Neuroscience.

[9]  V. Jayaraman,et al.  Intensity versus Identity Coding in an Olfactory System , 2003, Neuron.

[10]  Uwe Homberg,et al.  Antennal Lobe Structure , 1999 .

[11]  A. Grinvald,et al.  Spatio-Temporal Dynamics of Odor Representations in the Mammalian Olfactory Bulb , 2002, Neuron.

[12]  G. Laurent,et al.  Odor encoding as an active, dynamical process: experiments, computation, and theory. , 2001, Annual review of neuroscience.

[13]  Richard Axel,et al.  An Olfactory Sensory Map in the Fly Brain , 2000, Cell.

[14]  G. Laurent,et al.  Impaired odour discrimination on desynchronization of odour-encoding neural assemblies , 1997, Nature.

[15]  Paul F. M. J. Verschure,et al.  Decoding a Temporal Population Code , 2004, Neural Computation.

[16]  W. Cain,et al.  Latency and accuracy of discriminations of odor quality between binary mixtures and their components. , 2000, Chemical senses.

[17]  G. Laurent,et al.  Who reads temporal information contained across synchronized and oscillatory spike trains? , 1998, Nature.

[18]  J. Hildebrand,et al.  Organization and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze-fracture , 1981, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[19]  C. Galizia,et al.  Odor similarity does not influence the time needed for odor processing. , 2003, Chemical senses.

[20]  G. Laurent,et al.  Odour encoding by temporal sequences of firing in oscillating neural assemblies , 1996, Nature.

[21]  M. Carlsson,et al.  Dose-response characteristics of glomerular activity in the moth antennal lobe. , 2003, Chemical senses.

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

[23]  G. Laurent,et al.  Dynamic optimization of odor representations by slow temporal patterning of mitral cell activity. , 2001, Science.

[24]  Gilles Laurent,et al.  Olfactory network dynamics and the coding of multidimensional signals , 2002, Nature Reviews Neuroscience.

[25]  T. Baker,et al.  Manoeuvres used by flying male oriental fruit moths to relocate a sex pheromone plume in an experimentally shifted wind‐field , 1987 .

[26]  G. Laurent,et al.  Intrinsic and Circuit Properties Favor Coincidence Detection for Decoding Oscillatory Input , 2004, The Journal of Neuroscience.

[27]  B. Hansson,et al.  Central processing of sex pheromone, host odour, and oviposition deterrent information by interneurons in the antennal lobe of female Spodoptera littoralis (Lepidoptera: Noctuidae) , 1994, The Journal of comparative neurology.

[28]  J. Hildebrand,et al.  GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth,Manduca sexta , 2004, Journal of Comparative Physiology A.

[29]  P. Distler,et al.  Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: II. local multiglomerular interneurons , 1997, The Journal of comparative neurology.

[30]  S. Sachse,et al.  Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. , 2002, Journal of neurophysiology.

[31]  C. Galizia,et al.  Spatial representation of odours in the antennal lobe of the moth Spodoptera littoralis (Lepidoptera: Noctuidae). , 2002, Chemical senses.

[32]  Andreas T. Schaefer,et al.  Maintaining Accuracy at the Expense of Speed Stimulus Similarity Defines Odor Discrimination Time in Mice , 2004, Neuron.

[33]  G. Laurent,et al.  Distinct Mechanisms for Synchronization and Temporal Patterning of Odor-Encoding Neural Assemblies , 1996, Science.

[34]  Menzel,et al.  Odour representation in honeybee olfactory glomeruli shows slow temporal dynamics: an optical recording study using a voltage-sensitive dye. , 2000, Journal of insect physiology.

[35]  B. Hansson Antennal Lobe Projection Patterns of Pheromone-Specific Olfactory Receptor Neurons in Moths , 1997 .

[36]  J. Hildebrand,et al.  Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles , 2000, Nature Neuroscience.

[37]  J S Kauer,et al.  Imaging and coding in the olfactory system. , 2001, Annual review of neuroscience.

[38]  Z. Mainen,et al.  Speed and accuracy of olfactory discrimination in the rat , 2003, Nature Neuroscience.

[39]  R. Menzel,et al.  The glomerular code for odor representation is species specific in the honeybee Apis mellifera , 1999, Nature Neuroscience.

[40]  P. Anderson,et al.  Electrophysiological response to herbivore‐induced host plant volatiles in the moth Spodoptera littoralis , 1999 .

[41]  B. Smith,et al.  Molecular features of odorants systematically influence slow temporal responses across clusters of coordinated antennal lobe units in the moth Manduca sexta. , 2004, Journal of neurophysiology.

[42]  J. Hildebrand,et al.  GABAergic Mechanisms That Shape the Temporal Response to Odors in Moth Olfactory Projection Neurons a , 1998, Annals of the New York Academy of Sciences.

[43]  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.

[44]  G. Laurent,et al.  Temporal Representations of Odors in an Olfactory Network , 1996, The Journal of Neuroscience.

[45]  R. Menzel,et al.  Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. , 2002, Journal of Comparative Physiology A.

[46]  B. Hansson,et al.  Sex pheromone and plant-associated odour processing in antennal lobe interneurons of male Spodoptera littoralis (Lepidoptera: Noctuidae) , 1995, Journal of Comparative Physiology A.

[47]  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.

[48]  R. Menzel,et al.  Olfactory discrimination ability and odor structure-activity relationships in honeybees. , 1999, Chemical senses.

[49]  Gilles Laurent,et al.  Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. , 2004, Journal of neurophysiology.