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The operation of connexions between photoreceptors and large second-order neurones in dragonfly ocelli

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Summary

Photoreceptors and large second-order neurones (L-neurones) of dragonfly ocelli have been penetrated simultaneously with microelectrodes to study the operation of the synapse between them. The responses of L-neurones to changes in illumination are of opposite polarity and are more phasic than those of photoreceptors.

  1. 1.

    When pulses of light are superimposed on a constant background illumination, the phasic nature of L-neurone responses is often enhanced. Sometimes, during a light stimulus, an L-neurone is depolarised relative to its resting potential. With rapidly repeated short pulses of light, responses of L-neurones decrement markedly, although the full response of photoreceptors is maintained.

  2. 2.

    Passive membrane properties of L-neurones cannot contribute significantly to the cutback in the hyperpolarising response of these neurones to light on.

  3. 3.

    When depolarising or hyperpolarising currents are injected into a photoreceptor, responses in an L-neurone it synapses with are of opposite polarity and markedly phasic. The voltage gain of the connexion between one photoreceptor and an L-neurone can be as great as nine.

  4. 4.

    No evidence for feedback connexions from L-neurones to photoreceptors has been found.

  5. 5.

    Conductance measurements on some L-neurones indicate that synaptically-induced currents may make a small contribution to the cutback in the hyperpolarising response to light on.

  6. 6.

    Some L-neurones make rapidly decrementing inhibitory connexions with other L-neurones.

  7. 7.

    A variety of neurones which respond to changes in illumination by alterations in spike rate have been found. Some of these connect with L-neurones.

  8. 8.

    Possible mechanisms for the cutback in the hyperpolarising response of an L-neurone at light on include intrinsic properties of the pre- or postsynaptic terminals, and excitatory synapses made by small second-order neurones on L-neurones.

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References

  • Blight AR, Llinás R (1980) The non-impulsive stretch receptor complex of the crab: a study of depolarisation-release coupling at a tonic sensorimotor synapse. Philos Trans R Soc Lond [Biol] 290:219–276

    Google Scholar 

  • Cajal SR (1918) Observaciones sobre la estructura de los ocelos y vias nerviosos de algunos insectos. Trab Lab Invest Biol Univ Madrid 16:109–137

    Google Scholar 

  • Chappell RL, Dowling JE (1972) Neural organisation of the median ocellus of the dragonfly. 1. 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 

  • Dowling JE, Chappell RL (1972) Neural organisation of the median ocellus of the dragonfly. 2. Synaptic structure. J Gen Physiol 60:148–165

    Google Scholar 

  • Dubs A, Laughlin SB, Srinivasan MV (1981) Single photon signals in fly photoreceptors and first order interneurones at visual threshold. J Physiol (Lond) 317:317–334

    Google Scholar 

  • Eibl E (1978) Morphology of the sense organs in the proximal parts of the tibiae ofGryllus campestris andGryllus bimaculatus de Geer (Insecta, Ensifera). Zoomorphologie 89:185–205

    Google Scholar 

  • Goodman LJ (1981) Organisation and physiology of the insect dorsal ocellar system. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates. Springer, Berlin Heidelberg New York (Handbook of sensory physiology, vol VII/6C, pp 201–286

    Google Scholar 

  • Katz B, Miledi R (1967) A study of synaptic transmission in the absence of nerve impulses. J Physiol (Lond) 192:409–426

    Google Scholar 

  • Katz B, Miledi R (1971) The effect of prolonged depolarisation on synaptic transfer in the stellate ganglion of the squid. J Physiol (Lond) 216:503–512

    Google Scholar 

  • Klingman A, Chappell RL (1978) Feedback synaptic interaction in the dragonfly ocellar retina. J Gen Physiol 71:157–175

    Google Scholar 

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

    Google Scholar 

  • Kusano K, Landau EM (1975) Depression and recovery of transmission at the squid giant synapse. J Physiol (Lond) 245:13–32

    Google Scholar 

  • Laughlin SB (1981) Neural principles in the visual system. In: Autrum H (ed) Comparative physiology and evolution of vision in invertebrates. Springer, Berlin Heidelberg New York (Handbook of sensory physiology, vol VII/6 B, pp 135–280)

    Google Scholar 

  • Mobbs PG, Guy RG, Goodman LJ, Chappell RL (1981) Relative spectral sensitivity and reverse Purkinje shift in identified L-neurones of the ocellar retina. J Comp Physiol 144:91–97

    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 of the ocelli of the locustSchistocerca gregaria. J Comp Physiol 95:237–250

    Google Scholar 

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

    Google Scholar 

  • Ruck P, Edwards GA (1964) The structure of the insect dorsal ocellus. 1. General organisation of the ocellus in dragonflies. J Morphol 115:1–26

    Google Scholar 

  • Shaw SR (1969) Interreceptor coupling in ommatidia of drone honeybee and locust compound eyes. Vision Res 9:999–1029

    Google Scholar 

  • Shaw SR (1975) Retinal resistance barriers and electrical lateral inhibition. Nature (Lond) 255:480–483

    Google Scholar 

  • Simmons PJ (1981) Synaptic transmission between second- and third-order neurones of a locust ocellus. J Comp Physiol 145:265–276

    Google Scholar 

  • Simmons PJ (1982) Transmission mediated with and without spikes at connexions between large second-order neurones of locust ocelli. J Comp Physiol 147:401–414

    Google Scholar 

  • Stange G (1981) The ocellar component of flight equilibrium control in dragonflies. J Comp Physiol 141:335–347

    Google Scholar 

  • Stone SL, Chappell RL (1981) Synaptic feedback onto photoreceptors in the ocellar retina. Brain Res 221:374–481

    Google Scholar 

  • Wilson M (1978a) The functional organisation 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 hyperpolarising potentials in the second-order cells of the locust ocellus. J Comp Physiol 128:347–358

    Google Scholar 

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Simmons, P.J. The operation of connexions between photoreceptors and large second-order neurones in dragonfly ocelli. J. Comp. Physiol. 149, 389–398 (1982). https://doi.org/10.1007/BF00619154

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