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Processing of antennal information in extrinsic mushroom body neurons of the bee brain

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Summary

In the bee brain neural activity of interneurons of the inner antenno-cerebral tract (inputs to the mushroom body) and extrinsic neurons of theβ-lobe (output cells) was recorded intracellularly. The cells were stained with Lucifer Yellow. The response characteristics of the neurons to light, various antennal stimuli and mechanical stimuli to thorax and abdomen were studied.

The cells of the inner antenno-cerebral tract (ACT) have uniglomerular dendritic arborizations in the antennal lobe and send projections into the calyces of the ipsilateral mushroom body and the lateral protocerebral lobe. 93% of the neurons are bi- or multimodal. No responses to light stimuli were found. Tactile stimuli to the antennae are only effective when applied ipsilaterally. Only one neuron showed marked differences in the responses to the qualitative testing of three odors: rose, lavender and isoamyl acetate.

The cells can be classified according to their response characteristics; the following response types were found: (1) inhibitory responses to the stimuli, (2) inhibitory responses to olfactory and excitatory responses to mechanical stimuli or vice versa, (3) excitatory responses to mechanical and sugar water stimuli, (4) excitation to olfactory stimuli and to touching the antenna with a drop of water or sugar water, (5) excitation to mechanical stimuli to head, thorax and abdomen and inhibition to sugar water stimuli.

The recorded extrinsicβ-lobe neurons have small dendritic bands perpendicular to the Kenyon cells, their axons project to the contralateral median protocerebrum. These cells have ipsilateral antennal and mostly ipsilateral optic inputs and process information from thoracic and abdominal mechanoreceptors. All responses are excitatory.

The recordings suggest that the mushroom bodies are multimodal integration centers, where antennal information is first combined with visual inputs.

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Abbreviations

ACT :

antenno-cerebral tract

References

  1. Boeckh J (1974) Die Reaktionen olfaktorischer Neurone im Deutocerebrum von Insekten im Vergleich zu den Antwortmustern der Geruchssinneszellen. J Comp Physiol 90:183–205

  2. Boeckh J, Boeckh V (1979) Threshold and odor specificity of pheromone-sensitive neurons in the deutocerebrum ofAntherea pernii andA. polyphemus. J Comp Physiol 132:235–242

  3. Boeckh J, Ernst K-D, Sass H, Waldow U (1976) Zur nervösen Organisation antennaler Sinneseingänge bei Insekten unter besonderer Berücksichtigung der Riechbahn. Verh Dtsch Zool Ges 1976:123–139

  4. Burrows M, Boeckh J, Esslen J (1982) Physiological and morphological properties of interneurons in the deutocerebrum of male cockroaches, which respond to female pheromone. J Comp Physiol 145:447–457

  5. Erber J (1980) Neural correlates of non-associative and associative learning in the honeybee. Verh Dtsch Zool Ges 1980:250–261

  6. Erber J (1981) Neural correlates of learning in the honeybee. TINS 4:270–273

  7. Erber J (1982) Electrophysiological analysis of central neurons in the bee and correlations with behavior. In: Breed MD, Michener CD, Evans HE (eds) The biology of social insects. Westview Press, Boulder, pp 343–346

  8. Erber J, Gronenberg W (1981) Multimodalität und Plastizität visueller Interneurone der Biene. Verh Dtsch Zool Ges 1981:177

  9. Erber J, Masuhr T, Menzel R (1980) Localization of short-term memory in the brain of the beeApis mellifera. Physiol Entomol 5:343–358

  10. Ernst K-D, Boeckh J (1983) A neuroanatomical study on the organisation of the central antennal pathway in insects. III. Neuroanatomical characterization of physiologically defined response types of deutocerebral neurons inPeriplaneta americana. Cell Tissue Res 229:1–22

  11. Esslen J, Kaissling K-E (1976) Zahl und Verteilung antennaler Sensillen bei der Honigbiene (Apis mellifera L.). Zoomorphologie 83:227–251

  12. Glantz RM (1978) Crayfish antennal neuropile I. Reciprocal synaptic interactions and input-output characteristics of first-order interneurons. J Neurophysiol 41:1297–1313

  13. Homberg U (1982) Das mediane Protocerebrum der Honigbiene (Apis mellifica) im Bereich des Zentralkörpers: physiologische und morphologische Charakterisierung. Dissertation Berlin

  14. Homberg U, Erber J (1979) Response characteristics and identification of extrinsic mushroom body neurons of the bee. Z Naturforsch 34:612–615

  15. Huber F (1960) Untersuchungen über die Funktion des Zentralnervensystems und insbesondere des Gehirns bei der Fortbewegung und Lauterzeugung der Grillen. Z Vergl Physiol 44:60–132

  16. Huber F (1967) Central control of movements and behavior in invertebrates. In: Wiersma CAG (ed) Invertebrate nervous system. Univ Chicago Press, Chicago, pp 333–351

  17. Kauer JS (1974) Response patterns of amphibian olfactory bulb neurons to odour stimulation. J Physiol 243:695–715

  18. Kauer JS, Shepherd GM (1977) Analysis of the onset phase of olfactory bulb unit responses to odour pulses in the salamander. J Physiol 272:495–516

  19. Kaulen P, Erber J, Mobbs P (1984) Current source-density analysis in the mushroom bodies of the honey bee (Apis mellifera carnica). J Comp Physiol A 154:569–582

  20. 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

  21. Lacher V (1964) Elektrophysiologische Untersuchungen an einzelnen Rezeptoren für Geruch, CO2 und Temperatur auf den Antennen der Arbeitsbiene und Drohne. Z Vergl Physiol 48:587–623

  22. Masson C (1982) Basic mechanisms of sensory antennal information processing in insects, with special reference to social insects. In: Breed MD, Michener CD, Evans HE (eds) The biology of social insects. Westview Press, Boulder, pp 380–384

  23. Masson C, Strambi C (1977) Sensory antennal organisation in an ant and a wasp. J Neurobiol 8:537–548

  24. Matsumoto SG, Hildebrand JG (1981) Olfactory mechanisms in the mothManduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond B 213:249–277

  25. Menzel R, Erber J, Masuhr T (1974) Learning and memory in the honey bee. In: Barton Browne L (ed) Experimental analysis of insect behavior. Springer, Berlin Heidelberg New York, pp 195–217

  26. Mobbs PG (1982) The brain of the beeApis mellifera. I. The connections and spatial organisation of the mushroom bodies. Phil Trans R Soc Lond B 298:309–354

  27. Mobbs PG (1984) Neural networks in the mushroom bodies of the honeybee. J Insect Physiol 30:43–58

  28. Otto D (1969) Hirnreizinduzierte komplexe Verhaltensfolgen bei Grillen. Zool Anz Suppl Bd 33:472–477

  29. Otto D (1971) Untersuchungen zur zentralnervösen Kontrolle der Lauterzeugung von Grillen. Z Vergl Physiol 74:227–271

  30. Schildberger K (1981) Some physiological features of mushroom body linked fibers in the house cricket brain. Naturwissenschaften 68:623–624

  31. Schildberger K (1982) Untersuchungen zur Struktur und Funktion von Interneuronen im Pilzkörperbereich des Gehirns der HausgrilleAcheta domesticus. Dissertation Göttingen

  32. Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154:71–79

  33. Schürmann FW (1974) Bemerkungen zur Funktion der Corpora pedunculata im Gehirn der Insekten aus morphologischer Sicht. Exp Brain Res 19:406–432

  34. Selzer R (1979) Morphological and physiological identification of food odor specific neurons in the deutocerebrum ofPeriplaneta americana. J Comp Physiol 134:159–163

  35. Selzer R (1981) The processing of a complex food odor by antennal olfactory receptors ofPeriplaneta americana. J Comp Physiol 144:509–519

  36. Stewart WW (1978) Functional connections between cells revealed by dye-coupling with a highly fluorescent naphtalimide tracer. Cell 14:741–759

  37. Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York

  38. Vareschi E (1971) Duftunterscheidung bei der Honigbiene — Einzelzellableitungen und Verhaltensreaktionen. Z Vergl Physiol 75:143–173

  39. Waldow U (1975) Muldimodale Neurone im Deutocerebrum vonPeriplaneta americana. J Comp Physiol 101:329–341

  40. Waldow U (1977) CNS units in cockroach (Periplaneta americana): Specificity of response to pheromenes and other odor stimuli. J Comp Physiol 116:1–17

  41. Weiss MJ (1974) Neuronal connections and the function of the corpora pedunculata in the brain of the American cockroachPeriplaneta americana. J Morphol 142:21–70

  42. Wieczorek H (1980) Sugar reception by an insect water receptor. J Comp Physiol 138:167–172

  43. Yamada M (1971) A search for odor encoding in the olfactory lobe. J Physiol 214:127–143

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Homberg, U. Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J. Comp. Physiol. 154, 825–836 (1984). https://doi.org/10.1007/BF00610683

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Keywords

  • Inhibitory Response
  • Mechanical Stimulus
  • Tactile Stimulus
  • Mushroom Body
  • Antennal Lobe