Color processing in the medulla of the bumblebee (Apidae: Bombus impatiens)

Journal of Comparative Neurology

Volumn 513, Issue 5, 2009, Pages 441-456

  Paulk, Angelique C ^a   Dacks, Andrew M ^b   Gronenberg, Wulfila ^b  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

Adaptation; Insect brain; Temporal response properties

Indexed keywords

ANATOMICAL VARIATION; ANIMAL EXPERIMENT; ARTICLE; BUMBLEBEE; CELL COUNT; CELL SIZE; CELL STRUCTURE; COLOR DISCRIMINATION; COMPARATIVE ANATOMY; HISTOCHEMISTRY; HONEYBEE; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; NERVE CELL; NERVE FIBER; NEURITE; NEUROTRANSMISSION; NONHUMAN; PHOTORECEPTOR; PRIORITY JOURNAL; RETINA AMACRINE CELL; RETINA RECEPTIVE FIELD; STIMULUS RESPONSE; VISUAL ADAPTATION; VISUAL STIMULATION; ANIMAL; BEE; CELL MEMBRANE POTENTIAL; COLOR VISION; CYTOLOGY; ELECTROPHYSIOLOGY; HISTOLOGY; METABOLISM; METHODOLOGY; OPTIC LOBE; PHOTOSTIMULATION; PHYSIOLOGY; VISION; VISUAL SYSTEM;

4 AMINOBUTYRIC ACID; HISTAMINE; SEROTONIN;

ANIMALS; BEES; COLOR PERCEPTION; ELECTROPHYSIOLOGY; GAMMA-AMINOBUTYRIC ACID; HISTAMINE; IMMUNOHISTOCHEMISTRY; MEDULLA OBLONGATA; MEMBRANE POTENTIALS; NEURONS; OPTIC LOBE, NONMAMMALIAN; PHOTIC STIMULATION; SEROTONIN; VISUAL PATHWAYS; VISUAL PERCEPTION;

EID: 64549134189     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21993     Document Type: Article

References (60)

1. Baumann F, Hadjilazaro B. 1972. A depolarizing aftereffect of intense light in the drone visual system. Vis Res 12:17-31.
2. Bornhauser BC, Meyer EP. 1997. Histamine-like immunoreactivity in the visual system and brain of an orthopteran and a hymenopteran insect. Cell Tissue Res 287:211-221.
3. Callaway EM. 2005. Structure and function of parallel processing pathways in the primate early visual system. J Physiol 566:13-19.
4. Campos-Ortega JA, Strausfeld NJ. 1972. The columnar organization of the second synaptic region of the visual system of Musca domestica L. I. Receptor terminals in the medulla. Z Zellforsch 124:561-582.
5. Dacks AM, Christensen TA, Hildebrand JG. 2006. Phylogeny of a serotonin-immunoreactive neuron in the primary olfactory center of the insect brain. J Comp Neurol 498:727-746.
6. De Souza J, Hertel H, Ventura DF, Menzel R. 1992. Response properties of stained monopolar cells in honeybee lamina. J Comp Physiol A 170: 267-274.
7. 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 147:155-170.
8. Douglass JK, Strausfeld NJ. 1996. Visual motion-detection circuits in flies: parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate. J Neurosci 16:4551-4562.
9. Douglass JK, Strausfeld NJ. 1998. Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly. J Comp Neurol 396:84-104.
10. Douglass JK, Strausfeld NJ. 2003. Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion-detecting circuits. J Comp Neurol 457:326-344.
11. Douglass JK, Strausfeld NJ. 2005. Sign-conserving amacrine neurons in the fly's external plexiform layer. Vis Neurosci 22:345-358.
12. Douglass JK, Strausfeld NJ. 2007. Diverse speed response properties of motion sensitive neurons in the fly's optic lobe. J Comp Physiol A 193:233-247.
13. Ehmer B, Gronenberg W. 2002. Segregation of visual input to the mushroom bodies in the honeybee (Apis mellifera). J Comp Neurol 451:362-373.
14. Erber J, Kloppenburg P. 1995. The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.) I. Behavioral analysis of the motion-sensitive antennal reflex. J Comp Physiol A 176:111-118.
15. Fischbach KF, Dittrich APM. 1989. The optic lobe of Drosophila melanogaster. I. A Golgi analysis of wild-type structure. Cell Tissue Res 258:441-475.
16. Gilbert C, Penisten DK, DeVoe RD. 1991. Discrimination of visual motion from flicker by identified neurons in the medulla of the fleshfly Sarcophaga bullata. J Comp Physiol A 168:653-673.
17. 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.
18. Gregory CE. 1980. The Bodian Protargol Technique. In: Strausfeld NJ, Miller TA, editors. Neuroanatomical techniques. New York: Springer. p 75-95.
19. Gribakin FG. 1969. Cellular basis of colour vision in the honey bee. Nature (Lond) 223:639-641.
20. Gribakin FG. 1972. The distribution of the long wave photoreceptors in the compound eye of the honey bee as revealed by selective osmic staining. Vision Res 12:1225-1230.
21. Gronenberg W. 1986. Physiological and anatomical properties of optical input-fibres to the mushroom bodies in the bee brain. J Insect Physiol 32:695-704.
22. Hardie RC. 1987. Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol 161:301-213.
23. Heisenberg M. 1998. What do the mushroom bodies do for the insect brain? Learn Mem 5:1-10.
24. Heisenberg M. 2003. Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266-275.
25. Hertel H. 1980. Chromatic properties of identified interneurons in the optic lobes of the bee. J Comp Physiol A 137:215-231.
26. Hertel H, Maronde U. 1987. The physiology and morphology of centrally projecting visual interneurons in the honeybee brain. J Exp Biol 133: 301-315.
27. Hertel H, Schäfer S, Maronde U. 1987. The physiology and morphology of visual commissures in the honeybee brain. J Exp Biol 133:283-300.
28. Homberg U, Hildebrand JG. 1991. Histamine-immunoreactive neurons in the midbrain and suboesophageal ganglion of sphinx moth Manduca sexta. J Comp Neurol 307:647-657.
29. Homberg U, Würden S. 1997. Movement-sensitive, polarization-sensitive, and light-sensitive neurons of the medulla and accessory medulla of the locust, Schistocerca gregaria. 386:329-346.
30. Hubel DH, Livingstone MS. 1987. Segregation of form, color, and stereopsis in primate area 18. J Neurosci 7:3378-3415.
31. Ibbotson MR. 2001. Evidence for velocity-tuned motion-sensitive descending neurons in the honeybee. Proc Biol Sci 268:2195-2201.
32. Kien J, Menzel R. 1977a. Chromatic properties of interneurons in the optic lobes of the bee. I. Broad-band neurons. J Comp Physiol 113:17-34.
33. Kien J, Menzel R. 1977b. Chromatic properties of interneurons in the optic lobes of the bee. II. Narrow band and color opponent neurons. J Comp Physiol 113:35-53.
34. Kloppenburg P, Erber J. 1995. The modulatory effects of serotonin and octopamine in the visual system of the honey bee (Apis mellifera L.) II. Electrophysiological analysis of motion-sensitive neurons in the lobula. J Comp Physiol A 176:119-129.
35. Melzig J, Buchner S, Wiebel F, Wolf R, Burg M, Pak WL, Buchner E. 1996. Genetic depletion of histamine from the nervous system of Drosophila eliminates specific visual and mechanosensory behavior. J Comp Physiol A 179:763-773.
36. Menzel R. 1974. Spectral sensitivity of monopolar cells in the bee lamina. J Comp Physiol 93:337-346.
37. Menzel R, Giurfa M. 2006. Dimensions of cognition in an insect, the honeybee. Behav Cogn Neurosci Rev 5:24-40.
38. Milde J. 1981. Graded potentials and action potentials in the large ocellar interneurons of the bee. J Comp Physiol 143:427-434.
39. Morante J, Desplan C. 2008. The color-vision circuit in the medulla of Drosophila. Curr Biol 18:553-565
40. Ney-Nifle M, Keasar T, Shmida A. 2001. Location and color learning in bumblebees in a two-phase conditioning experiment. J Insect Behav 14:697-711.
41. O'Carroll DC, Osorio D, James AC, Bush T. 1992. Local feedback mediated via amacrine cells in the insect optic lobe. J Comp Physiol A 171:447-455.
42. Osorio D. 1986. Directionally selective cells in the locust medulla. J Comp Physiol A 159:841-847.
43. Pan KC, Goodman LJ. 1977. Ocellar projections within the central nervous system of the worker honeybee (Apis mellifera). Cell Tissue Res 176: 505-527.
44. Paulk AC, Gronenberg W. 2008. Higher order visual input to the mushroom bodies in the bee, Bombus impatiens. Arthropod Struct Dev 37:443-458.
45. Paulk AC, Phillips-Portillo J, Dacks AM, Fellous JM, Gronenberg W. 2008. The processing of color, motion, and stimulus timing are anatomically segregated in the bumblebee brain. J Neurosci 28:6319-6332.
46. Peitsch D, Feitz A, Hertel H, de Souza J, Ventura DF, Menzel R. 1992. The spectral input systems of hymenopteran insects and their receptor-based colour vision. J Comp Physiol A 170:23-40.
47. Ribi WA. 1975a. 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.
48. Ribi WA. 1975b. The neurons in the first optic ganglion of the bee ( Apis mellifera). Advan Anat Embryol Cell Biol 50:1-43.
49. 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.
50. Roig-Alsina A, Michener CD. 1993. Studies of the phylogeny and classification of long-tongued bees (Hymenoptera: Apidae). Univ Kansas Sci Bull 55:124-162.
51. Schultz TR, Engel MS, Ascher JS. 2001. Evidence for the origin of eusociality in the corbiculate bees (Hymenoptera: Apidae). J Kansas Entomol Soc 74:10-16.
52. Souza JM, Hertel H, Menzel R, Ventura DF. 1987. Marking and recording of monopolar cells in the bee lamina. Braz J Med Biol Res. 20:851-855
53. Srinivasan MV. 1993. Pattern recognition in the honeybee: recent progress. J Insect Physiol 40:183-194.
54. Srinivasan MV, Zhang SW. 1998. Probing perception in a miniature brain: pattern recognition and maze navigation in honeybees. Zoology 101: 246-259.
55. Strausfeld NJ. 1976. Atlas of an insect brain. Berlin: Springer.
56. Strausfeld NJ. 1989. Beneath the compound eye: neuroanatomical analysis and physiological correlates in the study of insect vision. In: Stavenga DG, Hardie RC, editors. Facets of vision. Heidelberg, New York: Springer. p 318-359.
57. Straw AD. 2008. Vision egg: an open-source library for realtime visual stimulus generation. Front Neuroinform 2:4.
58. Straw AD, Warrant EJ, O'Carroll DC. 2006. A 'bright zone' in male hoverfly (Eristalis tenax) eyes and associated faster motion detection and increased contrast sensitivity. J Exp Biol 209:4339-4354.
59. Van Kleef J, Berry R, Stange G. 2008. Directional selectivity in the simple eye of an insect. J Neurosci 28:2845-2855.
60. Witthöft W. 1967. Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morph Tiere 61:160-184.