Summary
Information processing in the mushroom bodies which are an important part of most invertebrate central nervous systems was analysed by extracellular electrophysiological techniques. The mushroom bodies consist of layers of parallel intrinsic neurons which make synaptic contact with extrinsic input and output neurons. The intrinsic neurons (approximately 170,000/mushroom body) have very small axon diameters (0.1–1 μm) which makes it difficult to record their activity intracellularly. In order to analyse the functional properties of this neuropil field potentials were measured extracellularly.
Series of averaged evoked potentials (AEPs) were recorded along electrode tracks at consecutive depth intervals in different parts of the mushroom bodies of the bee. These potentials were elicited by olfactory, mechanical and visual stimuli.
In order to locate the synaptic areas generating these potentials, current source-densities (CSD) were calculated using the consecutively measured evoked potentials. The conductivities of the extracellular space along the electrode tracks in the pedunculus and calyx and in part of the alpha-lobe of the mushroom bodies were found to be constant.
The CSD analysis reveals a complex pattern of source-sink distributions in the mushroom bodies. There is a high degree of correlation between current sinks and sources detected by CSD analysis and the morphological distribution of neurons.
The CSD analysis shows that the inputs and outputs of the mushroom bodies involve multimodal synaptic interactions, whereas information processing in the intrinsic Kenyon-cells is limited to sensory inputs from the antenna.
Comparison of the electrophysiological with the histological results shows that the intrinsic cells of the mushroom bodies are physiologically not a homogeneous group as is often proposed. Among the intrinsic neurons clearly defined areas of current sources and sinks can be identified and attributed to Kenyon-cells in different layers.
Similar content being viewed by others
Abbreviations
- AEP :
-
averaged evoked potentials
- AGT :
-
antennoglomerular tract
- CSD :
-
current source-density
- PCT :
-
antennoglomerular tract
References
Bacon JP, Altman JS (1977) A silver intensification method for cobalt-filled neurones in wholemount preparations. Brain Res 138:359–363
Breckow J, Kalmring K, Eckhorn R (1982) Multichannel-recordings and real-time current source density (CSD) analysis in the central-nervous system of insects. Problems and methods of application. Biol Cybern 45:115–121
Dujardin F (1850) Memoire sur le système nerveux des insects. Ann Sci Natl Zool 14:195–206
Erber J (1978) Response characteristics and after effects of multimodal neurons in the mushroom body area of the honey bee. Physiol Entomol 3:77–89
Erber J, Masuhr T, Menzel R (1980) Localization of short term memory in the brain of the bee (Apis mellifera). Physiol Entomol 5:343–358
Freeman JA, Nicholson C (1975) Experimental optimization of current source-density technique for anuran cerebellum. J Neurophysiol 38:369–382
Goll W (1967) Strukturuntersuchungen am Gehirn vonFormica. Z Morphol Ökol Tiere 59:143–210
Gregory GE (1980a) Alcoholic Bouin fixation of insect nervous systems for Bodian silver staining. II. Modified solutions. Stain Technol 55:151–160
Gregory GE (1980b) Alcoholic Bouin fixation of insect nervous systems for Bodian silver staining. III. A shortened single impregnation method. Stain Technol 55:161–166
Gregory GE, Greenway AR, Lord KA (1980) Alcoholic Bouin fixation of insect nervous systems for Bodian silver staining. I. Composition of ‘aged’ fixative. Stain Technol 55:143–150
Homberg U (1982) Das mediane Protocerebrum der Honigbiene (Apis mellifica) im Bereich des Zentralkörpers: Physiologische und morphologische Charakterisierung. Dissertation, FB Biologie, FU Berlin
Homberg U, Erber J (1979) Response characteristics and identification of extrinsic mushroom body neurons of the bee. Z Naturforsch 34c:612–615
Huber F (1955) Über die Funktion der Pilzkörper (Corpora pedunculata) beim Gesang der KeulenheuschreckeGomphocerus rufus L. (Acrididae). Naturwissenschaften 42:566–567
Huber F (1956) Auslösung von Bewegungsmustern durch elektrische Reizung des Oberschlundganglions bei Orthopteren (Saltatoria: Gryllidae, Acrididae). Zool Anz [Suppl] 23:248–269
Kenyon FC (1896a) The meaning and structure of the so called ‘mushroom bodies’ of the hexapod brain. Am Nat 30:643–650
Kenyon FC (1896b) The brain of the bee. A preliminary contribution to the morphology of the nervous system of the arthropoda. J Comp Neurol 6:133–210
Leydig F (1864) Vom Bau des thierischen Körpers. Handbuch für vergleichende Anatomie 1. Tübingen
Maynard DM (1956) Electric activity in the cockroach cerebrum. Nature 177:529–530
Maynard DM (1967) Organization of central ganglia. In: Wiersma CAG (ed) Invertebrate nervous system. Chicago University Press, Chicago, pp 231–255
Mobbs P (1982) The brain of the beeApis mellifera. I. The connections and spatial organisation of the mushroom bodies. Phil Trans R Soc London Ser B 298:309–354
Nicholson C, Freeman J (1975) Theory of current source-density analysis and determination of conductivity tensor for anuran cerebellum. J Neurophysiol 38:356–368
Nicholson C, Llinás R (1975) Real time current source-density analysis using multielectrode array in cat cerebellum. Brain Res 100:418–424
Nunez PL (1981) Electric fields of the brain. Oxford University Press, New York Oxford
Otto D (1971) Untersuchungen zur zentralnervösen Kontrolle der Lauterzeugung von Grillen. Z Vergl Physiol 74:227–271
Pearson L (1971) The corpora pedunculata ofSphinx ligustri L. and other Lepidoptera: An anatomical study. Phil Trans R Soc London Ser B 259:477–516
Schildberger K (1981) Some physiological features of mushroom-body linked fibers in the house cricket brain. Naturwissenschaften 68:623–624
Schürmann FW (1970) Über die Struktur der Pilzkörper des Insektengehirns. I. Synapsen im Pedunculus. Z Zellforsch 103:365–381
Schürmann FW (1972) Über die Struktur der Pilzkörper des Insektengehirns. II. Synaptische Schaltungen im Alpha-Lobus des HeimchensAcheta domesticus L. Z Zellforsch 127:240–257
Schürmann FW (1973) Über die Struktur der Pilzkörper des Insektengehirns. III. Die Anatomie der Nervenfasern in den Corpora pedunculata beiAcheta domesticus L. (Orthopthera). Eine Golgi-Studie. Z Zellforsch 145:247–285
Schürmann FW (1974) Bemerkungen zur Funktion der Corpora pedunculata im Gehirn der Insekten aus morphologischer Sicht. Exp Brain Res 19:406–432
Strausfeld N (1976) Atlas of an insect brain. Springer, Berlin Heidelberg New York
Wadepuhl M, Huber F (1979) Elicitation of singing and courtship movements by electrical stimulation of the brain of the grasshopper. Naturwissenschaften 66:320
Weiss MJ (1974) Neural connections and the function of the corpora pedunculata in the brain of the American cockroach,Periplaneta americana. J Morphol 142:21–69
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kaulen, P., Erber, J. & Mobbs, P. Current source-density analysis in the mushroom bodies of the honeybee (Apis mellifera carnica). J. Comp. Physiol. 154, 569–582 (1984). https://doi.org/10.1007/BF00610170
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00610170