Segregation of visual inputs from different regions of the compound eye in two parallel pathways through the anterior optic tubercle of the bumblebee (Bombus ignitus)

Journal of Comparative Neurology

Volumn 520, Issue 2, 2012, Pages 212-229

  Pfeiffer, Keram ^a,b   Kinoshita, Michiyo ^a  

^a GRADUATE UNIVERSITY FOR ADVANCED STUDIES   (Japan)

^b DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Dorsal rim area; Hymenoptera; Insect brain; Parallel processing; Visual system

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ANTERIOR OPTIC TUBERCLE; ARTICLE; BRAIN REGION; BUMBLEBEE; COMPARATIVE ANATOMY; COMPOUND EYE; CONTROLLED STUDY; DORSAL RIM AREA; HONEYBEE; INFORMATION PROCESSING; INTERTUBERCLE TRACT; LOCUST; NERVE CELL; NERVE TRACT; NEUROPIL; NONHUMAN; OPTIC LOBE; OPTIC TRACT; POLARIZATION; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; TUBERCLE ACCESSORY LOBE TRACT; VISUAL DISCRIMINATION; VISUAL INFORMATION;

ANIMALS; BEES; MUSHROOM BODIES; NEURONS; NEUROPIL; OPTIC LOBE, NONMAMMALIAN; ORIENTATION; PHOTORECEPTOR CELLS, INVERTEBRATE; STAINING AND LABELING; VISUAL PATHWAYS;

EID: 82355194983     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.22776     Document Type: Article

References (55)

1. Abercrombie M. 1946. Estimation of nuclear population from microtome sections. Anat Rec 94: 239-247.
2. Aepli F, Labhart T, Meyer EP. 1985. Structural specializations of the cornea and retina at the dorsal rim of the compound eye in hymenopteran insects. Cell Tissue Res 239: 19-24.
3. DeVoe RD, Kaiser W, Ohm J, Stone LS. 1982. Horizontal movement detectors of honeybees: directionally-selective visual neurons in the lobula and brain. J Comp Physiol A 147: 155-170.
4. Dyer AG, Paulk AC, Reser DH. 2011. Colour processing in complex environments: insights from the visual system of bees. Proc R Soc B 278: 952-959.
5. El Jundi B, Hütteroth W, Kurylas AE, Schachtner J. 2009. Anisometric brain dimorphism revisited: implementation of a volumetric 3D standard brain in Manduca sexta. J Comp Neurol 517: 210-225.
6. Giurfa M. 2007. Behavioral and neural analysis of associative learning in the honeybee: a taste from the magic well. J Comp Physiol A 193: 801-824.
7. Heinze S, Reppert SM. 2011. Sun compass integration of skylight cues in migratory monarch butterflies. Neuron 69: 345-358.
8. Hertel H. 1980. Chromatic properties of identified interneurons in the optic lobes of the bee. J Comp Physiol A 137: 215-231.
9. Hertel H, Maronde U. 1987. The physiology and morphology of centrally projecting visual interneurones in the honeybee brain. J Exp Biol 133: 301-315.
10. Hertel H, Schäfer S, Maronde U. 1987. The physiology and morphology of visual commissures in the honeybee brain. J Exp Biol 133: 283-300.
11. Homberg U. 1994. Flight-correlated activity changes in neurons of the lateral accessory lobes in the brain of the locust Schistocerca gregaria. J Comp Physiol A 175: 597-610.
12. Homberg U. 2004. In search of the sky compass in the insect brain. Naturwissenschaften 91: 199-208.
13. Homberg U, Paech A. 2002. Ultrastructure and orientation of ommatidia in the dorsal rim area of the locust compound eye. Arthropod Struct Dev 30: 271-280.
14. Homberg U, Kingan TG, Hildebrand JG. 1990. Distribution of FMRFamide-like immunoreactivity in the brain and suboesophageal ganglion of the sphinx moth Manduca sexta and colocalization with SCPB-, BPP-, and GABA-like immunoreactivity. Cell Tissue Res 259: 401-419.
15. Homberg U, Hofer S, Pfeiffer K, Gebhardt S. 2003. Organization and neural connections of the anterior optic tubercle in the brain of the locust, Schistocerca gregaria. J Comp Neurol 462: 415-430.
16. Homberg U, Heinze S, Pfeiffer K, Kinoshita M, el Jundi B. 2011. Central neural coding of sky polarization in insects. Philos Trans R Soc Lond B 366: 680-687.
17. Jawlowski H. 1963. On the origin of corpora pedunculata and the structure of the tuberculum opticum (Insecta). Acta Anat (Basel) 53: 346-359.
18. Kenyon FC. 1896. The brain of the bee. A preliminary contribution to the morphology of the nervous system of the Arthropoda. J Comp Neurol 6: 133-210.
19. Kien J, Menzel R. 1977a. Chromatic properties of interneurons in the optic lobes of the bee. I. Broad band neurons. J Comp Physiol A 113: 17-34.
20. Kien J, Menzel R. 1977b. Chromatic properties of interneurons in the optic lobes of the bee. II. Narrow band and colour opponent neurons. J Comp Physiol A 113: 35-53.
21. Kinoshita M, Pfeiffer K, Homberg U. 2007. Spectral properties of identified polarized-light sensitive interneurons in the brain of the desert locust Schistocerca gregaria. J Exp Biol 210: 1350-1361.
22. Klinke I, Menzel R. 2011. Neural correlates of combined olfactory and visual learning in mushroom body extrinsic neurons of the honeybee (Apis mellifera). Ninth Göttingen Meeting of the German Neuroscience Society. T25-13B.
23. Kraft P, Evangelista C, Dacke M, Labhart T, Srinivasan MV. 2011. Honeybee navigation: following routes using polarized-light cues. Philos Trans R Soc Lond B 366: 703-708.
24. Kreissl S, Bicker G. 1989. Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J Comp Neurol 286: 71-84.
25. Labhart T, Meyer EP. 1999. Detectors for polarized skylight in insects: a survey of ommatidial specializations in the dorsal rim area of the compound eye. Microsc Res Tech 47: 368-379.
26. Labhart T, Meyer EP, Schenker L. 1992. Specialized ommatidia for polarization vision in the compound eye of cockchafers, Melolontha melolontha (Coleoptera, Scarabaeidae). Cell Tissue Res 268: 419-429.
27. Lehrer M. 1998. Looking all around: honeybees use different cues in different eye regions. J Exp Biol 201: 3275-3292.
28. Maimon G. 2011. Modulation of visual physiology by behavioral state in monkeys, mice, and flies. Curr Opin Neurobiol 21: 1-6.
29. Menzel R, Blakers M. 1976. Colour receptors in the bee eye-morphology and spectral sensitivity. J Comp Physiol A 108: 11-13.
30. Meyer EP, Labhart T. 1981. Pore canals in the cornea of a functionally specialized area of the honey bee's compound eye. Cell Tissue Res 216: 491-501.
31. Meyer EP, Labhart T. 1993. Morphological specializations of dorsal rim ommatidia in the compound eye of dragonflies and damselfies (Odonata). Cell Tissue Res 272: 17-22.
32. Mobbs PG. 1982. The brain of the honeybee Apis mellifera. I. The connections and spatial organization of the mushroom bodies. Philos Trans R Soc Lond B 298: 309-354.
33. Mobbs P. 1985. Brain structure. In: Kerkut GA, Gilbert LI, editors. Comprehensive insect physiology biochemistry and pharmacology. Oxford, UK: Pergamon Press. p 299-370.
34. Paulk AC, Gronenberg W. 2008. Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. Arthropod Struct Dev 37: 443-458.
35. Paulk AC, Phillips-Portillo J, Dacks AM, Fellous J, Gronenberg W. 2008. The processing of color, motion, and stimulus timing are anatomically segregated in the bumblebee brain. J Neurosci 28: 6319-6332.
36. Paulk AC, Dacks AM, Gronenberg W. 2009a. Color processing in the medulla of the bumblebee (Apidae: Bombus impatiens). J Comp Neurol 513: 441-456.
37. Paulk AC, Dacks AM, Phillips-Portillo J, Fellous J, Gronenberg W. 2009b. Visual processing in the central bee brain. J Neurosci 29: 9987-9999.
38. Pfeiffer K, Homberg U. 2007. Coding of azimuthal directions via time-compensated combination of celestial compass cues. Curr Biol 17: 960-965.
39. Pfeiffer K, Kinoshita M, Homberg U. 2005. Polarization-sensitive and light-sensitive neurons in two parallel pathways passing through the anterior optic tubercle in the locust brain. J Neurophysiol 94: 3903-3915.
40. Pfeiffer K, Negrello M, Homberg U. 2011. Conditional perception under stimulus ambiguity: polarization- and azimuth-sensitive neurons in the locust brain are inhibited by low degrees of polarization. J Neurophysiol 105: 28-35.
41. Reischig T, Stengl M. 2002. Optic lobe commissures in a three-dimensional brain model of the cockroach Leucophaea maderae: a search for the circadian coupling pathways. J Comp Neurol 443: 388-400.
42. Ribi WA. 1975. The first optic ganglion of the bee. I. Correlation between visual cell types and their terminals in the lamina and medulla. Cell Tissue Res 165: 103-111.
43. Ribi WA, Scheel M. 1981. The second and third optic ganglia of the worker bee: Golgi studies of the neuronal elements in the medulla and lobula. Cell Tissue Res 221: 17-43.
44. Rybak J, Menzel R. 1993. Anatomy of the mushroom bodies in the honey bee brain: the neuronal connections of the alpha-lobe. J Comp Neurol 334: 444-465.
45. Skorupski P, Chittka L. 2010. Differences in photoreceptor processing speed for chromatic and achromatic vision in the bumblebee, Bombus terrestris. J Neurosci 30: 3896-3903.
46. Skorupski P, Döring TF, Chittka L. 2007. Photoreceptor spectral sensitivity in island and mainland populations of the bumblebee, Bombus terrestris. J Comp Physiol A 193: 485-494.
47. Srinivasan MV. 2011. Honeybees as a model for the study of visually guided flight, navigation, and biologically inspired robotics. Physiol Rev 91: 413-460.
48. Strausfeld N. 1976. Atlas of an insect brain. New York: Springer.
49. Strausfeld NJ, Blest AD. 1970. Golgi studies on insects part I. The optic lobes of Lepidoptera. Philos Trans R Soc Lond B 258: 81-134.
50. Strausfeld NJ, Okamura J. 2007. Visual system of calliphorid flies: organization of optic glomeruli and their lobula complex efferents. J Comp Neurol 500: 166-188.
51. Träger U, Wagner R, Bausenwein B, Homberg U. 2008. A novel type of microglomerular synaptic complex in the polarization vision pathway of the locust brain. J Comp Neurol 506: 288-300.
52. Viallanes H. 1887a. Études histologiques et organologiques sur les centres nerveux et les organes des sens des animaux articulés. Quatrième mémoire. Le cerveau de la guêpe (Vespa crabro et V. vulgaris). Ann Sci Nat Zool 7: 5-100.
53. Viallanes H. 1887b. Études histologiques et organologiques sur les centres nerveux et les organes des sens des animaux articulés. Cinquième mémoire. I. Le cerveau du criquet (Oedipoda coerulescens et Caloptenus italicus). Ann Sci Nat Zool 7: 1-98.
54. von Frisch K. 1949. Die Polarisation des Himmelslichtes als orientierender Faktor bei den Tänzen der Bienen. Experientia 5: 142-148.
55. Wehner R, Strasser S. 1985. The POL area of the honey bee's eye: behavioural evidence. Physiol Entomol 10: 337-349.