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The effects of temperature on signalling in ocellar neurons of the desert locust, Schistocerca gregaria

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Abstract

In Schistocerca gregaria ocellar pathways, large second-order L-neurons use graded potentials to communicate signals from the ocellar retina to third-order neurons in the protocerebrum. A third-order neuron, DNI, converts graded potentials into axonal spikes that have been shown in experiments at room temperature to be sparse and precisely timed. I investigated effects of temperature changes that a locust normally experiences on these signals. With increased temperature, response latency decreases and frequency responses of the neurons increase. Both the graded potential responses in the two types of neuron and the spikes in DNI report greater detail about a fluctuating light stimulus. Over a rise from 22 to 35°C the power spectrum of the L-neuron response encompasses higher frequencies and its information capacity increases from about 600 to 1,700 bits/s. DNI generates spikes more often during a repeated stimulus but at all temperatures it reports rapid decreases in light rather than providing a continual measure of light intensity. Information rate carried by spike trains increases from about 50 to 185 bits/s. At warmer temperatures, increased performance by ocellar interneurons may contribute to improved aerobatic performance by delivering spikes earlier and in response to smaller, faster light stimuli.

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References

  • Abrams TW, Pearson KG (1982) Effects of temperature on identified central neurons that control jumping in grasshoppers. J Neurosci 11:1538–1553

    Google Scholar 

  • Ammermüller J, Zettler F (1986) Time-dependent and voltage-dependent currents in locust ocellar L-neurons. J Comp Physiol A 159:363–376

    Article  Google Scholar 

  • Bacon J, Möhl B (1983a) The tritocerebral commissure giant (TCG) wind-sensitive interneurone in the locust. I. Its activity in straight flight. J Comp Physiol A 150:439–452

    Article  Google Scholar 

  • Bacon J, Möhl B (1983b) The tritocerebral commissure giant (TCG) wind-sensitive interneurone in the locust. 2. Directional sensitivity and role in flight stabilisation. J Comp Physiol 150:453–465

    Article  Google Scholar 

  • Brenner N, Bialek W, de Ruyter van Steveninck RR (2000) Adaptive rescaling maximizes information transmission. Neuron 26:695–702

    Article  PubMed  CAS  Google Scholar 

  • Burrows M (1975) Monosynaptic connexions between wing stretch receptors and flight motoneurones of the locust. J Exp Biol 62:189–219

    PubMed  CAS  Google Scholar 

  • Burrows M (1989) Effects of temperature on a central synapse between identified motor neurons in the locust. J Comp Physiol A 165:687–695

    Article  PubMed  CAS  Google Scholar 

  • Büschges A, Ramirez JM, Driesang R, Pearson KG (1992) Connections of the forewing tegulae in the locust flight system and their modification following partial deafferentation. J Neurobiol 23:44–60

    Article  PubMed  Google Scholar 

  • Chapman KM, Pankhurst JH (1967) Conduction velocities and their temperature coefficients in sensory nerve fibres of cockroach legs. J Exp Biol 46:63–84

    Google Scholar 

  • Chapman RF (1965) The behaviour of nymphs of Schistocerca gregaria (Forskål) (orthoptera, acrididae) in a temperature gradient with special reference to temperature preference. Behaviour 24:283–317

    Article  Google Scholar 

  • Coro F, Perez M, Machado A (1994) Effects of temperature on a moth auditory receptor. J Comp Physiol A 174:517–525

    Article  Google Scholar 

  • de Ruyter van Steveninck R, Laughlin SB (1996) The rate of information transfer at graded-potential synapses. Nature 379:642–645

    Article  CAS  Google Scholar 

  • Faivre O, Juusola M (2008) Visual coding in locust photoreceptors. PLoS ONE 3:e2173

    Article  PubMed  Google Scholar 

  • Fischer H, Ebert E (1999) Tegula function during free locust flight in relation to motor pattern, flight speed and aerodynamic output. J Exp Biol 202:711–721

    PubMed  Google Scholar 

  • Foster JA, Robertson RM (1992) Temperature dependency of wing-beat frequency in intact and deafferented locusts. J Exp Biol 162:295–312

    Article  Google Scholar 

  • Franz A, Ronacher B (2002) Temperature dependence of temporal resolution in an insect nervous system. J Comp Physiol A 188:261–271

    Article  CAS  Google Scholar 

  • French AS (1985) The effects of temperature on action potential encoding in the cockroach tactile spine. J Comp Physiol A 156:817–821

    Article  Google Scholar 

  • French AS, Järvilehto M (1978) The dynamic behaviour of photoreceptor cells in the fly in response to random (white noise) stimulation at a range of temperatures. J Physiol 274:311–322

    PubMed  CAS  Google Scholar 

  • Griss C, Rowell CHF (1986) Three descending interneurons reporting deviation from course in the locust. I. Anatomy. J Comp Physiol A 158:765–774

    Article  PubMed  CAS  Google Scholar 

  • Heinrich B (1971a) Temperature regulation in the sphinx moth, Manduca sexta. I. Flight energetics and body temperature during free and tethered flight. J Exp Biol 54:141–151

    PubMed  CAS  Google Scholar 

  • Heinrich B (1971b) Temperature regulation in the sphinx moth, Manduca sexta. II. Regulation of heat loss by control of blood circulation. J Exp Biol 54:153–166

    PubMed  CAS  Google Scholar 

  • Heinrich B, Casey TM (1978) Heat transfer in dragonflies, ‘fliers’ and ‘perchers’. J Exp Biol 74:17–36

    Google Scholar 

  • Heitler WJ, Goodman CS, Rowell CHF (1977) The effects of temperature on the threshold of identified neurons in the locust. J Comp Physiol 117:163–182

    Article  Google Scholar 

  • Horsmann U, Heinzel HG, Wendler G (1983) The phasic influence of self-generated air current modulations on the locust flight motor. J Comp Physiol A 150:427–438

    Article  Google Scholar 

  • Juusola M, Hardie RC (2001a) Light adaptation in Drosophila photoreceptors: I. Response dynamics and signaling efficiency at 25°C. J Gen Physiol 117:3–25

    Article  PubMed  CAS  Google Scholar 

  • Juusola M, Hardie RC (2001b) Light adaptation in Drosophila photoreceptors: II. Rising temperature increases the bandwidth of reliable signaling. J Gen Physiol 117:27–41

    Article  PubMed  CAS  Google Scholar 

  • May ML (1976) Thermoregulation and adaptation to temperature in dragonflies (Odonata: Anisoptera). Ecol Monogr 46:1–32

    Article  Google Scholar 

  • May ML (1995a) Dependence of flight behavior and heat production on air temperature in the green darner dragonfly Anax junius (Odonata: Aeshnidae). J Exp Biol 198:2385–2392

    PubMed  Google Scholar 

  • May ML (1995b) Simultaneous control of head and thoracic temperatures by the green darner dragonfly Anax junius (Odonata: Aeshnidae). J Exp Biol 198:2373–2384

    PubMed  Google Scholar 

  • Miles CI (1985) The effects of behaviourally relevant temperatures on mechanosensory neurones of the grasshopper, Schistocerca americana. J Exp Biol 116:121–139

    PubMed  CAS  Google Scholar 

  • Miles CI (1992) Temperature compensation in the nervous system of the grasshopper. Physiol Entomol 17:169–175

    Google Scholar 

  • Mizisin AP, Josephson RK (1987) Mechanical power output of locust flight muscle. J Comp Physiol A 160:413–419

    Article  Google Scholar 

  • Money TGA, Anstey ML, Robertson RM (2005) Heat stress-mediated plasticity in a locust looming-sensitive visual interneuron. J Neurophysiol 93:1908–1919

    Article  PubMed  Google Scholar 

  • Neville AC, Weis-Fogh T (1963) The effect of temperature on locust flight muscle. J Exp Biol 40:111–121

    Google Scholar 

  • Pfau HK, Koch UT, Möhl B (1989) Temperature dependence and response characteristics of the isolated wing hinge stretch receptor in the locust. J Comp Physiol 165:247–252

    Article  Google Scholar 

  • Prinz P, Ronacher B (2002) Temporal modulation transfer functions in auditory receptor fibres of the locust (Locusta migratoria L.). J Comp Physiol A 188:577–587

    Article  CAS  Google Scholar 

  • Reichert H, Rowell CHF (1985) Integration of nonphaselocked exteroceptive information in the control of rhythmic flight in the locust. J. Neurophysiol. 53:1201–1218

    PubMed  CAS  Google Scholar 

  • Roebroek JGH, van Tjonger M, Stavenga DG (1990) Temperature dependence of receptor potential and noise in fly (Calliphora erythrocephala) photoreceptor cells. J Insect Physiol 36:499–505

    Article  Google Scholar 

  • Rowell CHF, Reichert H (1986) Three descending interneurons reporting deviation from course in the locust. II. Physiology. J Comp Physiol A 158:775–794

    Article  PubMed  CAS  Google Scholar 

  • Schmeling F, Stange G, Homberg U (2010) Synchronization of wing beat cycle of the desert locust, Schistocerca gregaria, by periodic light flashes. J Comp Physiol A 196:199–211

    Article  Google Scholar 

  • Shannon CE, Weaver W (1949) The mathematical theory of information. University of Illinois Press, Urbana

    Google Scholar 

  • Simmons P (1980) A locust wind and ocellar brain neurone. J Exp Biol 85:281–294

    Google Scholar 

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

    Article  Google Scholar 

  • Simmons PJ (1986) Interactions made by large second-order neurones of the median ocellus of the locust. J Comp Physiol A 159:97–105

    Article  Google Scholar 

  • Simmons PJ (1990) The effects of temperature on locust ocellar L-neurones and their interconnections. J Comp Physiol A 166:575–583

    Google Scholar 

  • Simmons PJ (1993) Adaptation and responses to changes in illumination by second- and third-order neurones of locust ocelli. J Comp Physiol A 173:635–648

    Google Scholar 

  • Simmons PJ, de Ruyter van Steveninck R (2005) Reliability of signal transfer at a tonically transmitting, graded potential synapse of the locust ocellar pathway. J Neurosci 25:7529–7537

    Article  PubMed  CAS  Google Scholar 

  • Simmons PJ, de Ruyter van Steveninck RR (2010) Sparse but specific temporal coding by spikes in an insect sensory-motor ocellar pathway. J Exp Biol 213:2629–2639

    Article  PubMed  Google Scholar 

  • Stavenga DG, Schwering PBW, Tinbergen J (1993) A three-compartment model describing temperature changes in tethered flying blowflies. J Exp Biol 185:326–333

    Google Scholar 

  • Strong SP, Koberle R, de Ruyter van Steveninck RR, Bialek W (1998) Entropy and information in neural spike trains. Phys Rev Lett 80:197–200

    Article  CAS  Google Scholar 

  • Tatler B, O’Carroll DC, Laughlin SB (2000) Temperature and the temporal resolving power of fly photoreceptors. J Comp Physiol A 186:399–407

    Article  PubMed  CAS  Google Scholar 

  • Waldron I (1968) The mechanism of coupling of the locust flight oscillator to oscillatory inputs. Z Vergl Physiol 57:331–347

    Article  Google Scholar 

  • Waloff Z (1963) Field studies on solitary and transient desert locusts in the Red Sea area. Anti Locust Bull 40:1–93

    Google Scholar 

  • Warzecha AK, Egelhaaf M (2000) Response latency of a motion-sensitive neuron in the fly visual system: Dependence on stimulus parameters and physiological conditions. Vision Res 40:2973–2983

    Article  PubMed  CAS  Google Scholar 

  • Warzecha AK, Horstmann W, Egelhaaf M (1999) Temperature-dependence of neuronal performance in the motion pathway of the blowfly Calliphora erythrocephala. J Exp Biol 202:3161–3170

    PubMed  Google Scholar 

  • Weis-Fogh T (1956) Biology and physics of locust flight. II. Flight performance of the desert locust (Schistocerca gregaria). Phil Trans R Soc B 239:459–510

    Article  Google Scholar 

  • Weis-Fogh T (1964) Biology and physics of locust flight. VIII. Lift and metabolic rate of flying locusts. J Exp Biol 41:257–271

    PubMed  CAS  Google Scholar 

  • Wilson DM, Weis-Fogh T (1962) Patterned activity of co-ordinated motor units, studied in flying locusts. J Exp Biol 39:643–667

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Xu H, Robertson RM (1996) Neural parameters contributing to temperature compensation in the flight CPG of the locust, Locusta migratoria. Brain Res 734:213–222

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

I thank Rob de Ruyter van Steveninck for advice on data analysis, and Julieta Sztarker for comments on the manuscript.

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Correspondence to Peter J. Simmons.

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Simmons, P.J. The effects of temperature on signalling in ocellar neurons of the desert locust, Schistocerca gregaria . J Comp Physiol A 197, 1083–1096 (2011). https://doi.org/10.1007/s00359-011-0669-y

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