Ensemble Response in Mushroom Body Output Neurons of the Honey Bee Outpaces Spatiotemporal Odor Processing Two Synapses Earlier in the Antennal Lobe

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Strube Bloss, Martin F ^a,c   Herrera Valdez, Marco A ^b   Smith, Brian H ^c  

^a MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^b UNIVERSITY OF PUERTO RICO AT CAYEY   (Puerto Rico)

^c ARIZONA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CONTROLLED STUDY; DENDRITE; ELECTROPHYSIOLOGY; FEEDBACK SYSTEM; GENETIC VARIABILITY; HONEYBEE; LATENT PERIOD; MOLECULAR DYNAMICS; MUSHROOM BODY; NERVE PROJECTION; NEUROPIL; NONHUMAN; ODOR; OLFACTORY DISCRIMINATION; OLFACTORY SYSTEM; PRINCIPAL COMPONENT ANALYSIS; SIGNAL TRANSDUCTION; SYNAPSE;

ANIMALS; ARTHROPOD ANTENNAE; BEES; BRAIN; BRAIN MAPPING; ELECTRODES; ELECTROPHYSIOLOGY; FLUORESCENT DYES; HONEY; MUSHROOM BODIES; NEURONS; ODORS; OLFACTORY PATHWAYS; OLFACTORY RECEPTOR NEURONS; PRINCIPAL COMPONENT ANALYSIS; SMELL; SYNAPSES; TIME FACTORS;

ANIMALIA; APIS MELLIFERA; BASIDIOMYCOTA; HEXAPODA; MAMMALIA;

EID: 84870604648     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050322     Document Type: Article

References (59)

1. Wilson RI, Mainen ZF, (2006) Early events in olfactory processing. Annual review of neuroscience 29: 163-201.
2. Martin JP, Beyerlein A, Dacks AM, Reisenman CE, Riffell JA, et al. (2011) Progress in Neurobiology The neurobiology of insect olfaction: Sensory processing in a comparative context. Progress in Neurobiology 95: 427-447.
3. Perez-Orive J, Mazor O, Turner GC, Cassenaer S, Wilson RI, et al. (2002) Oscillations and sparsening of odor representations in the mushroom body. Science (New York, NY) 297: 359-365.
4. Krofczik S, Menzel R, Nawrot MP, (2008) Rapid odor processing in the honeybee antennal lobe network. Frontiers in computational neuroscience 2: 9.
5. Nawrot MP, Krofczik S, Farkhooi F, Menzel R (2009) Fast dynamics of odor rate coding in the insect antennal lobe. Neuroscience: 1-17.
6. Seki Y, Rybak J, Wicher D, Sachse S, Hansson BS, (2010) Physiological and morphological characterization of local interneurons in the Drosophila antennal lobe. Journal of neurophysiology 104: 1007-1019.
7. Fernandez PC, Locatelli FF, Person-Rennell N, Deleo G, Smith BH, (2009) Associative conditioning tunes transient dynamics of early olfactory processing. The Journal of neuroscience 29: 10191-10202.
8. Rössler W, Zube C, (2011) Dual olfactory pathway in Hymenoptera: evolutionary insights from comparative studies. Arthropod structure & development 40: 349-357.
9. Jortner RA, Farivar SS, Laurent G, (2007) A Simple Connectivity Scheme for Sparse Coding in an Olfactory System. Physiology 27: 1659-1669.
10. Turner GC, Bazhenov M, Laurent G, Honegger KS, Campbell RAA, et al. (2007) Olfactory Representations by Drosophila Mushroom Body Neurons. Journal of Neurophysiology: 734-746.
11. Laurent G, (2002) Olfactory network dynamics and the coding of multidimensional signals. Nature Rev Neurosci 3: 884-895.
12. Demmer H, Kloppenburg P, Ong RC, Stopfer M, (2009) Intrinsic Membrane Properties and Inhibitory Synaptic Input of Kenyon Cells as Mechanisms for Sparse Coding? Journal of Neurophysiology 102: 1538-1550.
13. Gupta N, Stopfer M, (2011) Olfactory Coding: Giant Inhibitory Neuron Governs Sparse Odor Codes. Current Biology 21: R504-R506.
14. Mobbs P, (1982) The Brain of the Honeybee Apis Mellifera. I. The Connections and Spatial Organization of the Mushroom Bodies. Phil Trans R Soc Lond 298: 309-354.
15. Bicker G, Kreissl S, Hofbauer A, (1993) Monoclonal antibody labels olfactory and visual pathways in Drosophila and Apis brains. Journal of Comparative Neurology 335: 413-424.
16. Kirschner S, Kleineidam CJ, Zube C, Rybak J, Grünewald B, et al. (2006) Dual olfactory pathway in the honeybee, Apis mellifera. Journal of comparative neurology 499: 933-952.
17. Rybak J, Menzel R, (1993) Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. Journal of Comparative Neurology 334: 444-465.
18. Iwama A, Shibuya T, (1998) Physiology and morphology of olfactory neurons associating with the protocerebral lobe of the honeybee brain. Journal of insect physiology 44: 1191-1204.
19. Hansson BS, Anton S, (2000) Function and morphology of the antennal lobe: new developments. Annual review of entomology 45: 203-231.
20. Gebhardt S, Homberg U, (2004) Immunocytochemistry of histamine in the brain of the locust Schistocerca gregaria. Cell and tissue research 317: 195-205.
21. Ignell R, Hansson BS, (2005) Projection patterns of gustatory neurons in the suboesophageal ganglion and tritocerebrum of mosquitoes. Journal of comparative neurology 492: 214-233.
22. Strube-Bloss MF, Nawrot MP, Menzel R, (2011) Mushroom body output neurons encode odor-reward associations. The Journal of Neuroscience 31: 3129-3140.
23. Hoel P, Port S, Stone C (1971) Introduction to statistical theory. Boston, USA: Houghton Mifflin. p. 237.
24. Mood A, Graybill F, Boes D (1974) Introduction to the Theory of Statistics. New York, USA: McGraw-Hill. p. 577.
25. Mazor O, Laurent G, (2005) Transient dynamics versus fixed points in odor representations by locust antennal lobe projection neurons. Neuron 48: 661-673.
26. MacLeod K, Laurent G, (1996) Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274/5289: 976-979.
27. Menzel R, Manz G, (2005) Neural plasticity of mushroom body-extrinsic neurons in the honeybee brain. The Journal of experimental biology 208: 4317-4332.
28. Okada R, Rybak J, Manz G, Menzel R, (2007) Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. The Journal of neuroscience 27: 11736-11747.
29. Grünewald B, (1999) Physiological properties and response modulations of mushroom body feedback neurons during olfactory learning in the honeybee, Apis mellifera. J. Comp. Physiol. A 185: 565-576.
30. Mauelshagen J, (1993) Neural correlates of olfactory learning paradigms in an identified neuron in the honeybee brain. Journal of neurophysiology 69: 609-625.
31. Yamagata N, Schmuker M, Szyszka P, Mizunami M, Menzel R, (2009) Differential odor processing in two olfactory pathways in the honeybee. Frontiers in systems neuroscience 3: 16.
32. Gronenberg W. 2001. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J Comp Neurol. 435: 474-489.
33. Strausfeld NJ, (2002) Organization of the honey bee mushroom body: Representation of the calyx within the vertical and gamma lobes. J. Comp. Neuro. 450: 4-33.
34. Nowotny T, Huerta R, Abarbanel HDI, Rabinovich MI, (2005) Self-organization in the olfactory system: one shot odor recognition in insects. Biological Cybernetics 93: 436-446.
35. Huerta R, Nowotny T, Garcia-Sanchez M, Abarbanel HDI, Rabinovich MI, (2004) Learning Classification in the Olfactory System of Insects. Neural Computation 16: 1601-1640.
36. Abel R, Rybak J, Menzel R, (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. The Journal of comparative neurology 437: 363-383.
37. Müller D, Abel R, Brandt R, Zöckler M, Menzel R, (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. Journal Of Comparative Physiology A. 188: 359-370.
38. Galizia C, Kimmerle B, (2004) Physiological and morphological characterization of honeybee olfactory neurons combining electrophysiology, calcium imaging and confocal microscopy. Journal Of Comparative Physiology A 190: 21-38.
39. Bhandawat V, Olsen SR, Gouwens NW, Schlief ML, Wilson RI, (2007) Sensory processing in the Drosophila antennal lobe increases reliability and separability of ensemble odor representations. Nature neuroscience 10: 1474-1482.
40. Wilson RI, Turner GC, Laurent G, (2004) Transformation of Olfactory Representation in the Drosophila Antennal Lobe. Science 303: 366-370.
41. Olsen SR, Bhandawat V, Wilson RI, (2007) Excitatory Interactions between Olfactory Processing Channels in the Drosophila Antennal Lobe. Neuron 54: 89-103.
42. Namiki S, Kanzaki R, (2008) Reconstructing the population activity of olfactory output neurons that innervate identifi able processing units. Frontiers in neural circuits 2: 1-11.
43. Stopfer M, Jayaraman V, Laurent G, (2003) Intensity versus Identity Coding in an Olfactory System. Neuron 39: 991-1004.
44. Tabor R, Yaksi E, Weislogel J-M, Friedrich RW, (2004) Processing of odor mixtures in the zebrafish olfactory bulb. The Journal of neuroscience 24: 6611-6620.
45. Friedrich RW, Laurent G, (2004) Dynamics of olfactory bulb input and output activity during odor stimulation in zebrafish. Journal of neurophysiology 91: 2658-2669.
46. Ito I, Ong RC-Y, Raman B, Stopfer M, (2008) Sparse odor representation and olfactory learning. Nature neuroscience 11: 1177-1184.
47. Szyszka P, Ditzen M, Galkin A, Galizia CG, Menzel R, (2005) Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. J Neurophysiol 94: 3303-3313.
48. Szyszka P, Galkin A, Menzel R, (2008) Associative and non-associative plasticity in Kenyon cells of the honeybee mushroom body. Frontiers in systems neuroscience 2: 1-10 doi:10.3389/neuro.06.003.2008.
49. Nawrot MP (2012) Dynamics of sensory processing in the dual olfactory pathway of the honeybee. Apidologie. Available:http://www.springerlink.com/index/10.1007/s13592-012-0131-3. Accessed 28 March 2012.
50. Staudacher EM, Huetteroth W, Schachtner M, Daly KC, (2009) A 4-dimensional representation of antennal lobe output based on an ensemble of characterized projection neurons Journal of Neuroscience Methods. 180: 208-223.
51. Wright G, Carlton M, Smith BH, (2009) A honeybee's ability to learn, recognize, and discriminate odors depends upon odor sampling time and concentration. Behavioral neuroscience 123: 36-43.
52. Smith BH, Menzel R, (1989) An analysis of variability in the feeding motor program of the honey bee; the role of learning in releasing a modal action pattern. Ethology 82: 68-81.
53. Hammer M, (1997) The neural basis of associative reward learning in honeybees. Trends Neurosci. 20: 245-252.
54. Hammer M, Menzel R, (1998) Multiple Sites of Associative Odor Learning as Revealed by Local Brain Microinjections of Octopamine in Honeybees. Learning & Memory 5: 146-156.
55. Rath L, Galizia CG, Szyszka P, (2011) Multiple memory traces after associative learning in the honey bee antennal lobe. Eur J Neurosci. 34: 352-60.
56. Galizia CG, Rössler W, (2010) Parallel Olfactory Systems in Insects: Anatomy and Function. Annual Review of Entomology 55: 399-420.
57. Kent K, Hoskins S, Hildebrand J, (1987) A novel serotonin-immunoreactive neuron in the antennal lobe of the sphinx moth Manduca sexta persists throughout postembryonic life. Journal of Neurobiology 18: 451-465.
58. Salecker I, Distler P, (1990) Serotonin-immunoreactive neurons in the antennal lobes of the American cockroach Periplaneta americana: light- and electron-microscopic observations. Histochemistry 95: 463-473.
59. Hu A, Zhang W, Wang Z, (2010) Functional feedback from mushroom bodies to antennal lobes in the Drosophila olfactory pathway. Proc Natl Acad Sci U S A 107: 10262-7.