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Graded potentials and action potentials in the large ocellar interneurons of the bee

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Summary

The response characteristics to light stimuli of first order ocellar interneurons in the bee (Apis mellifera carnica) were analysed with intracellular recordings. The neurons were identified using intracellular dye injection (Lucifer yellow).

The responses of L-(large) neurons can vary. They range from transient graded hyperpolarizations in response to light-On and -Off, (sometimes accompanied by tonic hyperpolarization during the light stimulus), to spontaneous tonic action potentials which are inhibited by light. Some neurons show both hyperpolarizations and action potentials.

The varying responses to light stimuli are dependent only on the state of the L-neuron and are not correlated systematically with particular types of L-neurons.

The experiments demonstrate that the action potentials are generated within the L-neurons and are not conducted antidromically from other neurons. The amplitude and frequency of the action potentials depend on the membrane potential of the L-neuron.

With light stimulation, or application of hyperpolarizing current, spikes can be generated within some of the L-neurons. Presumably non-spiking L-neurons are refractory due to maintained depolarization. They have membrane potentials of about −40 mV.

Action potentials in L-neurons were recorded only with high resistance microelectrodes. The vitality of the animal can not be correlated with the occurrence of spikes.

Functional significance of spontaneous tonic spike discharges in L-neurons is discussed in the context of behavioural experiments in the bee.

It is possible, that a given L-neuron uses either spiking or non-spiking signal transmission depending on the behavioural situation.

Although very fine microcapillary electrodes were used, no successful recordings or stainings of S-(small) neurons in the ocellar nerve were achieved. Therefore, results of non-identified ocellar interneurons which have been attributed to S-neurons should be critically reviewed.

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References

  • Autrum H, Metschl N (1963) Die Arbeitsweise der Ocellen der Insekten. Z Vergl Physiol 47:256–273

    Google Scholar 

  • Autrum H, Zettler F, Järvilehto M (1970) Postsynaptic potentials from a single monopolar neuron of the ganglion opticum I of the blowflyCalliphora. Z Vergl Physiol 70:414–424

    Google Scholar 

  • Burrows M, Siegler MVS (1976) Transmission without spikes between locust interneurons and motoneurones. Nature 262:222–224

    Google Scholar 

  • Cajal SR (1918) Observaciones sobre la estructura de los ocelos y vias nerviosas ocelares de algunos insectos. Trab Lab Invest Biol Univ (Madrid) 16:109–131

    Google Scholar 

  • Chappell RL, Dowling JE (1972) Neural organization of the median ocellus of the dragonfly. I. Intracellular electrical activity. J Gen Physiol 60:121–147

    Google Scholar 

  • Chappell RL, Goodman LJ, Kirkham JB (1978) Lateral ocellar nerve projections in the dragonfly brain. Cell Tissue Res 190:99–114

    Google Scholar 

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

    Google Scholar 

  • Erber J, Menzel R (1977) Visual interneurons in the median protocerebrum of the bee. J Comp Physiol 121:65–77

    Google Scholar 

  • Erber J, Sandeman DC (1976) The detection of real and apparent motion by the crabLeptograpsus variegatus. II. Electrophysiology. J Comp Physiol 112:189–197

    Google Scholar 

  • Goodman CS (1976) Anatomy of the ocellar interneurons of acridid grasshoppers. I. The large interneurons. Cell Tissue Res 175:184–203

    Google Scholar 

  • Goodman CS, Williams JLD (1976) Anatomy of locust ocellar interneurons. II. The small interneurons. Cell Tissue Res 175:203–225

    Google Scholar 

  • Goodman LJ (1970) The structure and function of the insect dorsal ocellus. Adv Insect Physiol 7:97–195

    Google Scholar 

  • Goodman LJ (1975) The neural organization and physiology of the insect dorsal ocellus. InHorridge GA (ed) The compound eye and vision of insects. Oxford University Press, Oxford

    Google Scholar 

  • Goodman LJ, Patterson JA, Mobbs PG (1975) The projection of ocellar neurons within the brain of the locust,Schistocerca gregaria. Cell Tissue Res 157:467–492

    Google Scholar 

  • Gould JL (1975) Honey bee recruitment: The dance-language controversy. Science 189:685–693

    Google Scholar 

  • Guy RG, Goodman LJ, Mobbs PG (1977) Ocellar connections with the ventral nerve cord in the locust,Schistocerca gregaria— Electrical and anatomical characteristics. J Comp Physiol 115:337–350

    Google Scholar 

  • Guy RG, Goodman LJ, Mobbs PG (1979) Visual interneurons in the bee brain: Synaptic organization and transmission by graded potentials. J Comp Physiol 134:253–264

    Google Scholar 

  • Heinzeller T (1976) Second-order ocellar neurons in the brain of the honeybee (Apis mellifera). Cell Tissue Res 171:91–99

    Google Scholar 

  • Hengstenberg R (1977) Spike responses of “non-spiking” visual interneurone. Nature 270:338–340

    Google Scholar 

  • Hertel H (1980) Chromatic properties of identified interneurons in the optic lobes of the bee. J Comp Physiol 137:215–231

    Google Scholar 

  • Hoyle G (1955) Functioning of the insect ocellar nerve. J Exp Biol 32:397–407

    Google Scholar 

  • Kondo H (1978) Efferent system of the lateral ocellus in the dragonfly: Its relationship with the ocellar afferent units, the compound eyes, and the wing sensory system. J Comp Physiol 125:341–349

    Google Scholar 

  • Labhart T (1978) Electrophysiological investigations on the ocelli of the honeybee. Experientia 34:900

    Google Scholar 

  • Laughlin SB (1973) Neural integration in the first optic neuropile of dragonflies. I. Signal amplification in dark adapted second order neurons. J Comp Physiol 84:335–355

    Google Scholar 

  • Laughlin SB (1981) Neural principles in the peripheral visual system of invertebrates. In: Autrum H (ed) Handbook of sensory physiology, vol VII/6B. Springer, Berlin Heidelberg New York, pp 133–280

    Google Scholar 

  • Menzel R (1974) Spectral sensitivity of monopolar cells in the bee lamina. J Comp Physiol 93:337–346

    Google Scholar 

  • Metschl N (1963) Elektrophysiologische Untersuchungen an den Ocellen vonCalliphora. Z Vergl Physiol 47:230–255

    Google Scholar 

  • Oertel D, Stuart AE (1981) Transformation of signals by interneurons in the barnackl's visual pathways. J Physiol 311:127–146

    Google Scholar 

  • Pan KC, Goodman LJ (1977) Ocellar projections within the central nervous system of the worker honeybee (Apis mellifera). Cell Tissue Res 176:505–527

    Google Scholar 

  • Patterson JA, Chappell RL (1980) Intracellular responses of procion filled cells and whole nerve cobalt impregnation in the dragonfly median ocellus. J Comp Physiol 139:25–39

    Google Scholar 

  • Patterson JA, Goodman LJ (1974) Intracellular responses of receptor cells and second order cells in the ocelli of the desert locustSchistocerca gregaria. J Comp Physiol 95:237–250

    Google Scholar 

  • Pearson KG (1976) Nerve cells without action potentials. In: Fentress JC (ed) Simpler network and behavior. Sinauer, Sunderland, MA, pp 99–110

    Google Scholar 

  • Pearson KG, Fourtner CR (1975) Non-spiking interneurons in walking system of the cockroach. J Neurophysiol 38:33–52

    Google Scholar 

  • Rosser BL (1974) A study of the afferent pathways of the dragonfly lateral ocellus from extracellularly recorded spike discharges. J Exp Biol 60:135–160

    Google Scholar 

  • Ruck P (1961a) Electrophysiology of the insect dorsal ocellus. I. Origin of the components of the electroretinogram. J Gen Physiol 44:605–627

    Google Scholar 

  • Ruck P (1961b) Electrophysiology of the insect dorsal ocellus. II. Mechanisms of generation and inhibition of impulses in the ocellar nerve of dragonflies. J Gen Physiol 44:629–639

    Google Scholar 

  • Schricker B (1965) Die Orientierung der Honigbiene in der Dämmerung. Zugleich ein Beitrag zur Frage der Ocellenfunktion bei Bienen. Z Vergl Physiol 49:420–458

    Google Scholar 

  • Shaw SR (1968) Organization of the locust retina. Symp Zool Soc(Lond)23:135–163

    Google Scholar 

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

    Google Scholar 

  • Stuart AE, Oertel D (1978) Neuronal properties underlying processing of visual information in the barnacle. Nature 275:287–290

    Google Scholar 

  • Taylor CP (submitted) Contribution of compound eyes and ocelli to steering of locust in flight. I. Behavioral analysis. J Exp Biol

  • Wilson M (1978a) The functional organization of locust ocelli. J Comp Physiol 124:297–316

    Google Scholar 

  • Wilson M (1978b) Generation of graded potential signals in the second order cells of locust ocellus. J Comp Physiol 124:317–331

    Google Scholar 

  • Wilson M (1978c) The origin and properties of discrete hyperpolarizing potentials in the second order cells of locust ocellus. J Comp Physiol 128:347–358

    Google Scholar 

  • Zettler F, Järvilehto M (1973) Active and passive axonal propagation of non-spike signals in the retina ofCalliphora. J Comp Physiol 85:89–104

    Google Scholar 

Download references

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I am gtreatful to Benjamina Cwienczek, Alison Mercer, Joachim Erber and Randolf Menzel for their help with the manuscript. This work was supported by DFG grant Me 365/7

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Milde, J. Graded potentials and action potentials in the large ocellar interneurons of the bee. J. Comp. Physiol. 143, 427–434 (1981). https://doi.org/10.1007/BF00609909

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