López-Riquelme GO

Language: Spanish
References: 63
Page: 15-31
PDF size: 1183.97 Kb.

ABSTRACT

In this work, the organization of the antennal lobes (ALs) and its topographic representation in the mushroom bodies (MBs) in soldiers of two species of ants has been compared. Morphologic comparison between these species suggests that ALs of A. mexicana could be more specialized than that of C. ocreatus at the expense of general capabilities. In both species the AL is organized in six groups of glomeruli, each of which innervated by its own tract. Glomeruli clusters are grouped in two regions, anterior and posterior, by the innervation of projection neurons (PNs) that connect AL with MBs via antennoprotocerebral tracts (APT). Calyces of MBs are layered and receive segregated olfactory information: PNs innervating anterior glomeruli clusters send axons through lateral-APT to the lateral horn (LH) and then to inner layer of the calyx, while PNs innervating posterior glomeruli clusters send axons through medial-APT to inner layers of the calyx and then to the LH. These results show that AL organization is topographically represented in the MB forming a coarse odotopic map. The two pathways connecting AL with MB could represent two channels for processing different kinds of odors or different properties of olfactory stimuli. The neuroanatomical results suggest a conserved functional organization in social hymenopterans.

REFERENCES

1. Hölldobler, B. & Wilson, E.O. The ants (Belknap Harvard, Cambridge, 1990).

2. Bullock, T.H. & Horridge, G.A. Structure and function in the nervous system of invertebrates, Vol. I y II. (Freeman, San Francisco, 1965).

3. Leal, W.S. Odorant reception in insects: roles of receptors, binding proteins, and degrading enzymes. Annu. Rev. Entomol. 58, 373-391 (2013).

4. Jaisson, P. Sobre el determinismo del comportamiento en las hormigas del género Atta. Folia Entomólogica Mexicana 23-24, 108-110 (1972).

5. Nakanishi, A., Nishino, H., Watanabe, H., Yokohari, F. & Nishikawa, M. Sex-specific antennal sensory system in the ant Camponotus japonicus: structure and distribution of sensilla on the flagellum. Cell and tissue research 338(1), 79-97 (2009).

6. Hildebrand, J.G. & Shepherd, G.M. Mechanisms of olfactory discrimination: Convergence evidence for a common principles acros phyla. Annu. Rev. Neurosci. 20, 595-631 (1997).

7. Stocker, R.F. Drosophila as a focus in olfactory research: mapping of olfactory sensilla by fine structure, odor specificity, odorant receptor expression, and central connectivity. Microscopy Research and Technique 55, 284-296 (2001).

8. Martin, J.P. et al. The neurobiology of insect olfaction: sensory processing in a comparative context. Progress in neurobiology 95(3), 427-447 (2011).

9. Vosshall, L.B. The molecular logic of olfaction in Drosophila. Chem. Sens. 26, 207-213 (2001).

10. Couto, A., Alenius, M. & Dickson, B.J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biology 15(17), 1535-1547 (2005).

11. Hanson, B.S. & Anton, S. Function and morphology of the antennal lobe: new developments. Annu. Rev. Entomol. 45, 203-231 (2000).

12. Vosshall, L.B., Wong, A.M. & Axel, R. An olfactory sensory map in the fly brain. Cell 102, 147-159 (2000).

13. Homberg, U., Christensen, T.A. & Hildebrand, J.G. Structure and function of the deutocerebrum in insects. Annu. Rev. Entomol. 34, 477-501 (1989).

14. Sachse, S., Rappert, A. & Galizia, C.G. The spatial representation of chemical structures in the antennal lobe of honeybees: steps towards the olfactory code. European Journal of Neuroscience 11, 3970-3982 (1999).

15. Galizia, C.G. & Menzel, R. Odour perception in honeybees: coding information in glomerular patterns. Curr. Opin. Neurobiol. 10, 504-510 (2000).

16. Galizia, C.G. & Menzel, R. The role of glomeruli in the neural representation of odours: results from optical recording stidues. J. Insect Physiol. 47, 115-130 (2001).

17. Fahrbach, S.E. Structure of the mushroom bodies of the insect brain. Annu. Rev. Entomol. 51, 209-232 (2006).

18. Strausfeld, N.J., Buschbeck, E.K. & Gómez, R.S. The arthropod mushroom body: its functional roles, evolutionary enigmas and mistaken identities. In The nervous systems of invertebrates: an evolutionary and comparative approach (ed. Briedbach, O. & Kutsch, W.) 349-381 (Birkhäuser-Verlag, Berlin, 1995).

19. Strausfeld, N.J., Hansen, L., Li, Y., Gómez, R.S. & Ito, K. Evolution, discovery, and interpretation of arthropod mushroom bodies. Learning and Memory 5, 11-37 (1998).

20. Heisenberg, M. Mushroom bodies memoir: from maps to models. Nature Reviews Neuroscience 4, 266-275 (2003).

21. Strausfeld, N.J., Sinakevitch, I., Brown, S.M. & Farris, S.M. Ground plan of the insect mushroom body: functional and evolutionary implications. J. Comp. Neurol. 513, 265-291 (2009).

22. Gronenberg, W. & López-Riquelme, G.O. Multisensory convergence in the mushroom bodies of ants and bees. Acta Biol. Hung. 55(1-4), 31-37 (2004).

23. Homberg, U. Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J. Comp. Physiol. A 154, 825-836 (1984).

24. Mobbs, P.G. The brain of the noneybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Phil. Trans. R. Soc. Lond. B 298, 309-354 (1982).

25. Gronenberg, W. Physiological and anatomical properties of optical input-fibres to the mushroom body in the bee brain. J. Insect Physiol. 32, 695-704 (1986).

26. Gronenberg, W. Modality-specific segregation of input to ant mushroom bodies. Brain Behav. Evol. 54, 85-95 (1999).

27. Ehmer, B. & Gronenberg, W. Segregation of visual input to the mushroom bodies in the honey bee (Apis mellifera). J. Comp. Neurol. 451, 362-373 (2002).

28. Gronenberg, W. Subdivisions of hymenopteran mushroom body calyces by their afferent supply. J. Comp. Neurol. 436, 474- 489 (2001).

29. Arnold, G., Masson, C. & Budharugsa, S. Comparative study of the antennal lobes and their afferent pathway in the worker bee and the drone. Cell Tissue Res. 242, 593-605 (1985).

30. Abel, R., Rybak, J. & Menzel, R. Structure and response patterns of olfactory interneurons in the honeybee, Apis mellifera. J. Comp. Neurol. 437, 363-383 (2001).

31. López-Riquelme, G.O., Gronenberg, W. & Fanjul-Moles, M.L. Organization of the antennal lobes and their efferent connections to the mushroom bodies of the ants Camponotus ocreatus and Atta mexicana. Program no. 414.18. Abstract. Viewer/Itinerary Planner. Society for Neuroscience, Washington, District of Columbia (2004).

32. López-Riquelme, G.O. Hormigas como sistemas modelo para el comportamiento complejo. Bases neurobiológicas de la comunicación química y la división del trabajo en las hormigas. Tesis de Doctorado (Facultad de Ciencias, UNAM, México, D.F., 2008). 232 págs.

33. Kirschner, S. et al. Dual olfactory pathway in the honeybee, Apis mellifera. J. Comp. Neurol. 499, 933–952 (2006).

34. Zube, C., Kleineidam, C.J., Kirschner, S., Neef, J. & Rössler, W. Organization of the olfactory pathway and odor processing in the antennal lobe of the ant Camponotus floridanus. J. Comp. Neurol. 506, 425-441 (2008).

35. Galizia, C.G. & Rössler, W. Parallel olfactory systems in insects: anatomy and function. Annu. Rev. Entomol. 55, 399-420 (2010).

36. Ache, B.W. & Young, J.M. Olfaction: diverse species, conserved principles. Neuron 48(3), 417-430 (2005).

37. Wilson, R.I. & Mainen, Z.F. Early events in olfactory processing. Annu. Rev. Neurosci. 29, 163-201 (2006).

38. Arnold, G., Budharugsa, S. & Masson, C. Organization of the antennal lobe in the queen honey bee, Apis mellifera L. (Hymenoptera:Apidae). J. Morphol. Embriol. 17(3), 185- 195 (1988).

39. Galizia, C.G., McIlwarht, S.L. & Menzel, R. A digital threedimensional atlas of the honeybee antennal lobe based on optical sections acquired by confocal microscopy. Cell Tissue Res. 295, 383-394 (1999).

40. Mysore, K. et al. Caste and sex specific olfactory glomerular organization and brain architecture in two sympatric ant species Camponotus sericeus and Camponotus compressus (Fabricius, 1798). Arthropod structure & development 38(6), 485-497 (2009).

41. Nakanishi, A., Nishino, H., Watanabe, H., Yokohari, F. & Nishikawa, M. Sex-specific antennal sensory system in the ant Camponotus japonicus: glomerular organizations of antennal lobes. Journal of Comparative Neurology 518(12), 2186-2201 (2010).

42. Rospars, J.P. Structure and development of the insect antennodeutocerebral system. Int. J. Insect Morphol. & Embriol. 17(3), 243-294 (1988).

43. Gronenberg, W. & Hölldobler, B. Morphologic representation of visual and antennal information in the ant brain. J. Comp. Neurol. 412, 229-240 (1999).

44. Laissue, P.P. et al. Three-dimensional reconstruction of the antennal lobe in Drosophila melanogaster. J. Comp. Neurol. 405, 543-552 (1999).

45. Kleineidam, C.J., Obermayer, M., Halbich, W. & W. Rössler. A macroglomerulus in the antennal lobe of leaf-cutting ant workers and its possible functional significance. Chem. Sens. 30, 1-10 (2005).

46. López-Riquelme, G.O., Malo, E.A., Cruz-López, L. & Fanjul- Moles, M.L. Antennal olfactory sensitivity in response to task-related odours of three castes of the ant Atta mexicana (Hymenoptera: Formicidae). Physiol. Entomol. 31, 353-360 (2006).

47. Gronenberg, W., Heeren, S. & Hölldobler, B. Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J. Exp. Biol. 199, 2011-2019 (1996).

48. Kübler, L.S., Kelber, C. & Kleineidam, C.J. Distinct antennal lobe phenotypes in the leaf-cutting ant (Atta vollenweideri). J. Comp. Neurol. 518(3), 352-365 (2010).

49. Yamagata, N., Nishino, H. & Mizunami, M. Pheromone-sensitive glomeruli in the primary olfactory centre of ants. Proc. R. Soc. B, 273, 2219-2225 (2006).

50. Jaffe, K. & Pérez, E. Comparative study of brain morphology in ants. Brain Behav. Evol. 33, 25-33 (1989).

51. Anderson, C. & McShea, D.W. Individual versus social complexity, with particular reference to ant colonies. Biological Reviews 76(2), 211-237 (2001).

52. Lin, H.H., Lai, J.S. Y., Chin, A.L., Chen, Y.C. & Chiang, A.S. A map of olfactory representation in the Drosophila mushroom body. Cell 128(6), 1205-1217 (2007).

53. Marin, E.C., Jefferis, G.S., Komiyama, T., Zhu, H. & Luo, L. Representation of the glomerular olfactory map in the Drosophila brain. Cell 109(2), 243-255 (2002).

54. Wong, A.M., Wang, J.W. & Axel, R. Spatial representation of the glomerular map in the Drosophila protocerebrum. Cell 109(2), 229-241 (2002).

55. Nishikawa, M., Watanabe, H. & Yokohari, F. Higher brain centers for social tasks in worker ants, Camponotus japonicus. Journal of Comparative Neurology 520(7), 1584-1598 (2012).

56. Lihoreau, M., Latty, T. & Chittka, L. An exploration of the social brain hypothesis in insects. Frontiers in Physiology 3 (2012).

57. Farris, S.M. Evolution of insect mushroom bodies: old clues, new insights. Arthropod Structure & Development 34(3), 211-234 (2005).

58. Tanaka, N. K., Tanimoto, H. & Ito, K. Neuronal assemblies of the Drosophila mushroom body. Journal of Comparative Neurology 508(5), 711-755 (2008).

59. Wang, Y. et al. Stereotyped odor-evoked activity in the mushroom body of Drosophila revealed by green fluorescent proteinbased Ca2+ imaging. The Journal of Neuroscience 24(29), 6507-6514 (2004).

60. Turner, G.C., Bazhenov, M. & Laurent, G. Olfactory representations by Drosophila mushroom body neurons. Journal of Neurophysiology 99(2), 734-746 (2008).

61. Szyszka, P., Ditzen, M., Galkin, A., Galizia, C.G. & Menzel, R. Sparsening and temporal sharpening of olfactory representations in the honeybee mushroom bodies. Journal of Neurophysiology 94(5), 3303-3313 (2005).

62. Seid, M.A., Harris, K.M. & Traniello, J.F.A. Age-related changes in the number and structure of synapses in the lip region of the mushroom bodies in the ant Pheidole dentata. J. Comp. Neurol. 488(3), 269-277 (2005).

63. Farris, S.M. & Schulmeister, S. Parasitoidism, not sociality, is associated with the evolution of elaborate mushroom bodies in the brains of hymenopteran insects. Proceedings of the Royal Society B: Biological Sciences 278(1707), 940-951 (2011).