GABAergic synapses in the antennal lobe and mushroom body of the locust olfactory system

Journal of Comparative Neurology

Volumn 372, Issue 4, 1996, Pages 487-514

  Leitch, Beulah ^a,b   Laurent, Gilles ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b DURHAM UNIVERSITY   (United Kingdom)

Author keywords

immunogold; inhibition; insect; olfaction; oscillations

Indexed keywords

ANIMAL TISSUE; ANTENNA; ARTICLE; CELL DENSITY; GABAERGIC TRANSMISSION; GENE EXPRESSION REGULATION; IMMUNOGOLD STAINING; IMMUNOREACTIVITY; LOCUST; MUSHROOM; NEGATIVE FEEDBACK; NONHUMAN; OLFACTORY SYSTEM; POSTSYNAPTIC INHIBITION; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

ANIMALS; BIOLOGICAL CLOCKS; GAMMA-AMINOBUTYRIC ACID; GRASSHOPPERS; NERVE ENDINGS; OLFACTORY PATHWAYS; SENSE ORGANS; SYNAPSES;

EID: 0029832486     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1096-9861(19960902)372:4<487::AID-CNE1>3.0.CO;2-0     Document Type: Article

References (70)

1. Bendayan, M., and M. Zollinger (1983) Ultrastructural localisation of antigenic sites on osmium-fixed tissues applying the protein-A-gold technique. J. Histochem. Cytochem. 31:101-109.
2. Bicker, G., and R. Menzel (1989) Chemical codes for the control of behaviour in arthropods. Nature 337:33-39.
3. Bicker, G., S. Schafer, and T.G. Kingan (1985) Mushroom body feedback interneurones in the honey bee show GABA-like immunoreactivity. Brain Res. 360:394-397.
4. Bicker, G., S. Schafer, O.P. Ottersen, and J. Storm-Mathisen (1988) Glutamate-like immunoreactivity in identified neuronal populations of insect nervous system. J. Neurosci. 8:2108-2122.
5. Boeckh, J., and L.P. Tolbert (1993) Synaptic organisation and development of the antennal lobe in insects. Microsc. Res. Tech. 24:260-280.
6. Boeckh, J., K.D. Ernst, and P. Selsam (1989) Double labelling reveals monosynaptic connection between antennal receptor cells and identified local interneurons of the deutocerebrum in the American cockroach. Zool. J. Anat. 119:303-312.
7. Christensen, T.A., B.R. Waldrop, I.D. Harrow, and J.G. Hildebrand (1993) Local interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J. Comp. Physiol. 173:385-399.
8. Davis, R.L. (1993) Mushroom bodies and Drosophila learning. Neuron 11:1-14.
9. Distler, P. (1989) Histochemical demonstration of GABA-like immunoreactivity in cobalt labeled neuron individuals in the insect olfactory pathway. Histochemistry 91:245-249.
10. Distler, P. (1990a) GABA-immunohistochemistry as a label for identifying local interneurons and their synaptic contacts in the antennal lobes of the American cockroach. Histochemistry 93:617-626.
11. Distler, P. (1990b) Synaptic connections of dopamine-immunoreactive neurons in the antennal lobes of Periplaneta. Colocalization with GABA-like immunoreactivity. Histochemistry 93:401-408.
12. Erber, J., P. Kloppenburg, and A. Scheidler (1993) Neuromodulation by serotonin and octopamine in the honeybee: behaviour, neuroanatomy and electrophysiology. Experientia 49:1073-1083.
13. Gelperin, A., and D.W. Tank (1990) Odour-modulated collective network oscillations of olfactory interneurons in a terrestrial mollusc. Nature 345:437-440.
14. Gray, C.M. (1994) Synchronous oscillations in neuronal systems: mechanisms and function. J. Comput. Neurosci. 1:11-38.
15. Gronenberg, W. (1987) Anatomical and physiological properties of feedback neurons of the mushroom bodies in the bee brain. Exp. Biol. 46:115-125.
16. Hammer, M. (1993) An identified neuron mediates the unconditioned stimulus in associative olfactory learning in honeybees. Nature 366:59-63.
17. Hammer, M., and R. Menzel (1995) Learning and memory in the honey bee. J. Neurosci. 15:1617-1630.
18. Heisenberg, M., A. Borst, S. Wagner, and D. Byers (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2:1-30.
19. 125I-labelled α-bungarotoxin in normal and deafferented antennal lobes of Manduca sexta. Proc. Natl. Acad. Sci. U.S.A. 76:499-503.
20. Homberg, U. (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J. Comp. Physiol. 154:825-836.
21. Homberg, U., and J.G. Hildebrand (1994) Postembryonic development of γ-aminobutyric acid-like immunoreactivity in the brain of the sphinx moth Manduca sexta. J. Comp. Neurol. 339:132-149.
22. Homberg, U., T.G. Kingan, and J.G. Hildebrand (1987) Immunocytochemistry of GABA in the brain and suboesophageal ganglion of Manduca sexta. Cell Tissue Res. 248:1-24.
23. Homberg, U., R.A. Montague, and J.G. Hildebrand (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res. 254:225-281.
24. Homberg, U., S.G. Hoskins, and J.G. Hildebrand (1995) Distribution of acetylcholinesterase activity in the deutocerebrum of the sphinx moth Manduca sexta. Cell Tissue Res. 279:249-259.
25. Hoskins, S.G., U. Homberg, T.G. Kingan, T.A. Christensen, and J.G. Hildebrand (1986) Immunocytochemistry of GABA in the antennal lobes of the sphinx moth Manduca sexta. Cell Tissue Res. 244:243-252.
26. Kanzaki, R., E.A. Arbas, N.J. Strausfeld, and J.G. Hildebrand (1987) Physiology and morphology of projection neurons in the antennal lobes of the male Manduca sexta. J. Comp. Physiol. [A] 165:427-453.
27. Kent, K.S., I.D. Harrow, P. Quartararo, and J.G. Hildebrand (1986) An accessory olfactory pathway in Lepidoptera: the labial pit organ and its central projections in Manduca sexta and certain other sphinx moths and silk moths. Cell Tissue Res. 245:237-245.
28. Kreissl, S., and G. Bicker (1989) Histochemistry of acetylcholinesterase and immunocytochemistry of an acetylcholine receptor-like antigen in the brain of the honeybee. J. Comp. Neurol. 286:71-84.
29. Laurent, G. (1993) Adaptive gain control by nonlinear properties of local circuit neuron dendrites. J. Physiol. (Lond.) 470:45-54.
30. Laurent, G., and M. Burrows (1989) Intersegmental interneurons can control the gain of local reflexes in adjacent segments by their action on nonspiking local interneurons. J. Neurosci. 9:3030-3039.
31. Laurent, G., and H. Davidowitz (1994) Encoding of olfactory information with oscillating neural assemblies. Science 265:1872-1875.
32. Laurent, G., and M. Naraghi (1994) Odorant-induced oscillations in the mushroom bodies of the locust. J. Neurosci. 14:2993-3004.
33. Laurent, G., M. Wehr, and H. Davidowitz (1996) Temporal representations of odors in an olfactory network. J. Neurosci. 16:3837-3847.
34. Leitch, B., and G. Laurent (1993) Distribution of GABAergic synaptic terminals on the dendrites of locust spiking local interneurones. J. Comp. Neurol. 337:461-470.
35. Lutz, E.M., and N.M. Tyrer (1987) Immunohistochemical localisation of choline acetyl transferase in the central nervous system of the locust. Brain Res. 407:173-179.
36. Malun, D. (1991a) Inventory and distribution of synapses of identified uniglomerular projection neurons in the antennal lobe of Periplaneta americana. J. Comp. Neurol. 305:348-360.
37. Malun, D. (1991b) Synaptic relationship between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana: a double labeling electron microscopic study. Histochemistry 98:197-207.
38. Malun, D., U. Waldow, D. Kraus, and J. Boeckh (1993) Connections between the deutocerebrum and the protocerebrum, and neuroanatomy of several classes of deutocerebral projection neurons in the brain of male Periplaneta americana. J. Comp. Neurol. 329:143-162.
39. Masson, C., and H. Mustaparta (1990) Chemical information processing in the olfactory system of insects. Part I: Periphery. Physiol. Rev. 70:199-245.
40. Maxwell, G.D., J.F. Tait, and J.G. Hildebrand (1978) Regional synthesis of neurotransmitter candidates in the CNS of the moth Manduca sexta. Comp. Biochem. Physiol. [C] 61:109-119.
41. Menzel, A.R. (1987) Memory traces in honeybees. In R. Menzel and A. Mercer (eds): Neurobiology and Behaviour of Honeybees. pp. 310-325. Berlin Springer.
42. Mercer, A.R., and J. Erber (1983) The effects of amines on the provoked potentials recorded in the mushroom bodies of the bee brain. J. Comp. Physiol. [A] 151:469-476.
43. Mercer, A.R., and R. Menzel (1982) The effects of biogenic amines on conditioned and unconditioned responses to olfactory stimuli in the honeybee Apis mellifera. J. Comp. Physiol. [A] 145:363-368.
44. Mercer, A.R., P.G. Mobbs, A.P. Davenport, and P.D. Evans (1983) Biogenic amines in the brain of the honeybee, Apis mellifera. Cell Tissue Res. 234:655-677.
45. Mobbs, P.G. (1982) The brain of the honeybee Apis mellifera. I. The connections and spatial organisation of the mushroom bodies. Phil. Trans. R. Soc. Lond. [Biol] 298:309-354.
46. Mobbs, P.G. (1984) Neural networks in the mushroom bodies of the honeybee. J. Insect Physiol. 30:43-58.
47. Nighorn, A., M.J. Healey, and R.L. Davis (1991) The cyclic AMP phosphodiesterase encoded by Drosophila dunce gene is concentrated in the mushroom body neuropil. Neuron 6:445-467.
48. Pasantes-Morales, H., and C. Cruz (1985) Taurine and hypotaurine inhibit light-induced lipid peroxidation and protect rod outer segment structure. Brain Res. 330:154-157.
49. Pasantes-Morales, H., and J. Moran (1981) Taurine as a neuromodulator: its action on calcium fluxes and neurotransmitter release. In R. Tapia and C.W. Cotman (eds): Regulatory Mechanisms of Synaptic Transmission. Oxford: Plenum Press, pp. 141-154.
50. Pearson, L. (1971) The corpora pedunculata of Sphinx ligustri L. and other Lepidoptera: an anatomical study. Phil. Trans. R. Soc. Lond. [Biol] 259:477-516.
51. Rybak, J., and R. Menzel (1993) Anatomy of the mushroom bodies in the honeybee brain: the neuronal connections of the alpha-lobe. J. Comp. Neurol. 334:444-465.
52. Salecker, I., and P. Distler (1990) Serotonin-immunoreactive neurons in the antennal lobes of the American cockroach Periplaneta americana: light- and electron-microscopic observations. Histochemistry 94:463-473.
53. Sanes, J.R., and J.G. Hildebrand (1976) Acetylcholine and its metabolic enzymes in developing antenna of the moth, Manduca sexta. Dev. Biol. 52:105-120.
54. Sanes, J.R., D.J. Prescott, and J.G. Hildebrand (1977) Cholinergic neuroγ chemical development of normal and deafferented antennal lobes in the brain of the moth, Manduca sexta. Brain Res. 119:389-402.
55. Schafer, S., G. Bicker, O.P. Ottersen, and J. Storm-Mathisen (1988) Taurine-like immunoreactivity in the brain of the honeybee. J. Comp. Neurol. 268:60-70.
56. Schildberger, K. (1983) Local interneurons associated with the mushroom bodies and the central body in the brain of Acheta domesticus. Cell Tissue Res. 230:573-586.
57. Schildberger, K. (1984) Local interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J. Comp. Physiol. [A] 154: 71-79.
58. Schürmann, F.W. (1974) Bemerkungen zur Funktion der Corpora pedunculata in Gehirn der Insekten aus morphologischer Sicht. Exp. Brain Res. 19:406-432.
59. Schümann, F.W. (1987) The architecture of the mushroom bodies and related neuropils in the insect brain. In Gupta A.P. (ed): Arthropod Brain. Its Evolution, Development, Structure and Functions. New York: Wiley, pp. 231-264.
60. Seguela, P., M. Geffard, R. Buijs, and M. Le Moal (1984) Antibodies against gamma aminobutyric acid; specificity studies and immunocytochemical results. Proc. Natl. Acad. Sci. U.S.A. 81:3888-3892.
61. Shepherd, G.M. (1988) Neurobiology. Oxford University Press.
62. Sun, X.J., L.P. Tolbert, and J.G. Hildebrand (1993) Ramification pattern and ultrastructural characteristics of the serotonin-immunoreactive neuron in the antennal lobe of the moth Manduca sexta. J. Comp. Neurol. 338:5-16.
63. Tolbert, L.P. (1989) Afferent axons from the antenna influence the number and placement of intrinsic synapses in the antennal lobes of Manduca sexta. Synapse 3:83-95.
64. Tolbert, L.P., and J.G. Hildebrand (1981) Organisation and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze-fracture. Proc. Roy. Soc. Lond. [Biol.] 213:279-301.
65. Waldrop, B., T.A. Christensen, and J.G. Hildebrand (1987) GABA-mediated synaptic inhibition of projection neurons in the antennal lobes of the sphinx moth Manduca sexta. J. Comp. Physiol. [A] 161:23-32.
66. Wang, X.J., and J. Rinzel (1994) Spindle rhythimicity in the reticularis-thalaminucleus: synchronisation among mutually inhibitory neurons. Neuroscience 53:899-904.
67. Watson, A.D.H., and M. Burrows (1981) Input and output synapses on identified motor neurones of a locust revealed by the intracellular injection of horseradish peroxidase. Cell Tissue Res. 215:325-332.
68. Wendt, B., and U. Homberg (1992) Immunocytochemistry of dopamine in the brain of the locust Schistocerca gregaria. J. Comp. Neurol. 321:387-403.
69. Withers, G.S., S.E. Fahrbach, and G.E. Robinson (1993) Selective neuroanatomical plasticity and division of labour in the honeybee. Nature 364:238-240.
70. Yang, M.Y., J.D. Armstrong, I. Vilinsky, N.J. Strausfeld, and K. Kaiser (1995) Subdivision of Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15:45-54.