Neural correlates of odor learning in the honeybee antennal lobe

European Journal of Neuroscience

Volumn 31, Issue 1, 2010, Pages 119-133

  Denker, Michael ^a   Finke, Robert ^b   Schaupp, Frank ^b   Grün, Sonja ^a,c   Menzel, Randolf ^b,c  

^a RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

^c BERNSTEIN CENTER FOR COMPUTATIONAL NEUROSCIENCE   (Germany)

Author keywords

Ensemble coding; Local field potentials; Memory; Odor coding

Indexed keywords

ANIMAL EXPERIMENT; ANTENNA; ARTICLE; BRAIN; CONDITIONING; CONTROLLED STUDY; ELECTRIC POTENTIAL; EVOKED RESPONSE; HONEYBEE; NERVE CELL PLASTICITY; NERVE CELL STIMULATION; NONHUMAN; ODOR; OSCILLATION; PRIORITY JOURNAL; SPIKE WAVE; STATE DEPENDENT LEARNING;

ACTION POTENTIALS; ANIMALS; ASSOCIATION LEARNING; BEES; BRAIN; CLUSTER ANALYSIS; CONDITIONING, CLASSICAL; EVOKED POTENTIALS; MICROELECTRODES; NEURONAL PLASTICITY; NEURONS; NEUROPSYCHOLOGICAL TESTS; ODORS; OLFACTORY PERCEPTION; PERIODICITY; PHYSICAL STIMULATION; PRINCIPAL COMPONENT ANALYSIS; TIME FACTORS;

EID: 72949103916     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2009.07046.x     Document Type: Article

References (59)

1. Abel, R., Rybak, J. Menzel, R. (2001) Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J. Comp. Neurol., 437, 363 383.
2. Batschelet, E. (1981) Circular Statistics in Biology. Academic Press, New York.
3. Bitterman, M.E., Menzel, R., Fietz, A. Schäfer, S. (1983) Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psych., 97, 107 119.
4. Braun, G. Bicker, G. (1992) Habituation of an appetitive reflex in the honeybee. J. Neurophysiol., 67, 588 598.
5. Buzsáki, G. Draguhn, A. (2004) Neuronal oscillations in cortical networks. Science, 304, 1926 1929.
6. Chandra, S.B., Hosler, J.S. Smith, B.H. (2000) Heritable variation for latent inhibition and its correlation with reversal learning in honeybees (Apis mellifera). J. Comp. Psychol., 114, 86 97.
7. Christensen, T.A., Pawlowski, V.M., Lei, H. Hildebrand, J.G. (2000) Multi-unit recordings reveal context-dependent modulation of synchrony in odor-specific neural ensembles. Nat. Neurosci., 3, 927 931.
8. Christensen, T.A., Lei, H. Hildebrand, J.G. (2003) Coordination of central odor representations through transient, non-oscillatory synchronization of glomerular output neurons. Proc. Natl Acad. Sci. USA, 100, 11076 11081.
9. Daly, K.C., Christensen, T.A., Lei, H., Smith, B.H. Hildebrand, J.G. (2004) Learning modulates the ensemble representations for odors in primary olfactory networks. Proc. Natl Acad. Sci. USA, 101, 10476 10481.
10. Denker, M., Roux, S., Timme, M., Riehle, A. Grün, S. (2007) Phase synchronization between LFP and spiking activity in motor cortex during movement preparation. Neurocomputing, 70, 2096 2101.
11. Faber, T., Joerges, J. Menzel, R. (1999) Associative learning modifies neural representations of odors in the insect brain. Nat. Neurosci., 2, 74 78.
12. Finelli, L.A., Haney, S., Bazhenov, M., Stopfer, M. Sejnowski, T.J. (2008) Synaptic learning rules and sparse coding in a model sensory system. PLoS Comput. Biol., 4, e1000062.
13. Froemke, R.C., Merzenich, M.M. Schreiner, C.E. (2007) A synaptic memory trace for cortical receptive field plasticity. Nature, 450, 425 429.
14. Galizia, C.G. Menzel, R. (2000) Odour perception in honeybees: coding information in glomerular patterns. Curr. Opin. Neurobiol., 10, 504 510.
15. Galizia, C.G., Joerges, J., Küttner, A., Faber, T. Menzel, R. (1997) A semi-in-vivo preparation for optical recording of the insect brain. J. Neurosci. Methods, 76, 61 69.
16. Gelperin, A. (1990) A taste for learning. Am. Zool., 30, 549 558.
17. Georgopoulos, A.P., Schwartz, A.B. Kettner, R.E. (1986) Neuronal population coding of movement direction. Science, 233, 1416 1419.
18. Goldman-Rakic, P.S. (1995) Cellular basis of working memory. Neuron, 14, 477 485.
19. Hallem, E.H. Carlson, J.R. (2006) Coding of odors by a receptor repertoire. Cell, 125, 143 160.
20. Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature, 366, 59 63.
21. Hammer, M. Menzel, R. (1998) Multiple sites of associative odor learning as revealed by local brain microinjections of octopamine in honeybees. Learn. Mem., 5, 146 156.
22. Harris, K.D., Henze, D.A., Hirase, H., Leinekugel, X., Dragoi, G., Czurko, A. Buzsáki, G. (2002) Spike train dynamics predicts theta-related phase precession in hippocampal pyramidal cells. Nature, 417, 738 741.
23. Hellstern, F., Malaka, R. Hammer, M. (1998) Backward inhibitory learning in honeybees: a behavioral analysis of reinforcement processing. Learn. Mem., 4, 429 444.
24. Hurtado, J.M., Rubchinsky, L.L. Sigvardt, K.A. (2004) Statistical method for detection of phase-locking episodes in neural oscillations. J. Neurophysiol., 91, 1883 1998.
25. Joerges, J., Küttner, A., Galizia, C.G. Menzel, R. (1997) Representation of odours and odour mixtures visualized in the honeybee brain. Nature, 387, 285 288.
26. Keverne, E.B. (1995) Olfactory learning. Curr. Opin. Neurobiol., 5, 482 488.
27. Krofczik, S., Menzel, R. Nawrot, M.P. (2009) Rapid odor processing in the honeybee antennal lobe network. Front. Comput. Neurosci., 2, 1 9.
28. Laurent, G.J. (1996) Dynamical representation of odors by oscillating and evolving neural assemblies. Trends Neurosci., 19, 489 496.
29. Laurent, G.J. (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat. Rev. Neurosci., 3, 884 895.
30. Laurent, G.J., Stopfer, M., Friedrich, R.W., Rabinovich, M.I., Volkovskii, A. Abarbanel, H.D.I. (2001) Odor encoding as an active, dynamical process: experiments, computation, and theory. Annu. Rev. Neurosci., 24, 263 297.
31. Le Van Quyen, M., Foucher, J., Lachaux, J., Rodriguez, E., Lutz, A., Martinerie, J. Varela, F.J. (2001) Comparison of Hilbert transform and wavelet methods for the analysis of neuronal synchrony. J. Neurosci. Methods, 111, 83 98.
32. Manley, B.F.J. (2007) Randomization, Bootstrap and Monte Carlo Methods in Biology. Chapman & Hall/CRC, Boca Raton, FL.
33. Mardia, K.V. Jupp, P.E. (2000) Directional Statistics. Wiley, New York.
34. Martin, C., Gervais, R., Messaoudi, B. Ravel, N. (2006) Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur. J. Neurosci., 23, 1801 1810.
35. Mauelshagen, J. (1993) Neural correlates of olfactory learning in an identified neuron in the honey bee brain. J. Neurophysiol., 69, 609 625.
36. Menzel, R. (1990) Learning, memory, and "cognition" in honey bees. In Kesner, R.P. Olton, D.S. (Eds Neurobiology of Comparative Cognition. Erlbaum Inc, Hillsdale, N.J, pp. 237 292.
37. Menzel, R. Müller, U. (1996) Learning and memory in honeybees: from behavior to neural substrates. Annu. Rev. Neurosci., 19, 379 404.
38. Müller, U. (2000) Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron, 27, 159 168.
39. Müller, D., Abel, R., Brandt, R., Zöckler, M. Menzel, R. (2002) Differential parallel processing of olfactory information in the honeybee, Apis mellifera L. J. Comp. Physiol. [A], 188, 359 370.
40. Okada, R., Rybak, J., Manz, G. Menzel, R. (2007) Learning-related plasticity in PE1 and other mushroom body-extrinsic neurons in the honeybee brain. J. Neurosci., 27, 11736 11747.
41. Peele, P., Ditzen, M., Menzel, R. Galizia, C.G. (2006) Appetitive odor learning does not change olfactory coding in a subpopulation of honeybee antennal lobe neurons. J. Comp. Physiol. [A], 192, 1083 1103.
42. Pelz, C., Gerber, B. Menzel, R. (1997) Odorant intensity as a determinant for olfactory conditioning in honeybees: roles in discrimination, overshadowing and memory consolidation. J. Exp. Biol., 200, 837 847.
43. Ravel, N., Chabaud, P., Martin, C., Gaveau, V., Hugues, E., Tallon-Baudry, C., Bertrand, O. Gervais, R. (2003) Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60-90 Hz) and beta (15-40 Hz) bands in the rat olfactory bulb. Eur. J. Neurosci., 17, 350 358.
44. Rolls, E.T., Critchley, H.D., Mason, R. Wakeman, E.A. (1996) Orbitofrontal cortex neurons: role in olfactory and visual association learning. J. Neurophysiol., 75, 1970 1981.
45. Rosenblum, M.G., Pikovsky, A.S. Kurths, J. (1996) Phase synchronization of chaotic oscillators. Phys. Rev. Lett., 76, 1804 1807.
46. Sachse, S. Galizia, C.G. (2002) The role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J. Neurophysiol., 87, 1106 1117.
47. Sandoz, J.C., Galizia, C.G. Menzel, R. (2003) Side-specific olfactory conditioning leads to more specific odor representation between sides but not within sides in the honeybee antennal lobes. Neuroscience, 120, 1137 1148.
48. Schultz, W. (1998) Predictive reward signal of dopamine neurons. J. Neurophysiol., 80, 1 27.
49. Sharott, A., Moll, C.K.E., Engler, G., Denker, M., Grün, S. Engel, A.K. (2009) Different subtypes of striatal neurons are selectively modulated by cortical oscillations. J. Neurosci., 29, 4571 4585.
50. Stopfer, M., Bhagavan, S., Smith, B.H. Laurent, G.J. (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature, 390, 70 74.
51. Sun, X.-J., Fonta, C. Masson, C. (1993) Odour quality processing by bee antennal lobe interneurones. Chem. Senses, 18, 355 377.
52. Sutherland, G.R. McNaughton, B. (2000) Memory trace reactivation in hippocampal and neocortical neuronal ensembles. Curr. Opin. Neurobiol., 10, 180 186.
53. Tank, D.W., Gelperin, A. Kleinfeld, D. (1994) Odors, oscillations, and waves: does it all compute? Science, 265, 1819 1820.
54. Varela, F., Lachaux, J.P., Rodriguez, E. Martinerie, J. (2001) The brainweb: phase synchronization and large-scale integration. Nat. Rev. Neurosci., 2, 229 239.
55. Wang, Z., Wong, A.M., Flores, J., Vosshall, L.B. Axel, R. (2003) Two-photon calcium imaging reveals an odor-evoked map of activity in the fly brain. Cell, 112, 271 282.
56. Weidert, M., Galizia, C.G. Menzel, R. (2004) Learning induced changes of neuronal representation of odors in the antennal lobe of honeybee. Proceedings of the Berlin Neuroscience Forum, April 22-24, 2004, Liebenwalde, Germany, 75.
57. Wilson, D.A., Sullivan, R.M. Leon, M. (1987) Single-unit analysis of postnatal olfactory learning: modified olfactory bulb output response patterns to learned attractive odors. J. Neurosci., 7, 3154 3162.
58. Yu, D., Ponomarev, A. Davis, R.L. (2004) Altered representation of the spatial code for odors after olfactory classical conditioning; memory trace formation by synaptic recruitment. Neuron, 42, 437 449.
59. Zar, J.H. (1999) Biostatistical Analysis. Prentice Hall, Upper Saddle River, NJ.