Journal of Comparative Physiology A

, Volume 200, Issue 7, pp 627–639 | Cite as

Response differences of intersegmental auditory neurons recorded close to or far away from the presumed spike-generating zone

Original Paper

Abstract

Intracellular recordings may give valuable information about processing of a neuron and possibly its input from the network. Impalement with an electrode causes injury to the cell and depolarization from intrusion of extracellular fluid. Thus, penetration artefacts may contaminate recordings and conceal or even alter relevant information. These penetration artefacts may have the strongest impact close to the spike-generating zone near the dendrites. Recordings in axonal portions might therefore be less vulnerable while providing insufficient information about the synaptic input. In this study, we present data of five previously identified intersegmental auditory neurons of a bushcricket independently recorded in their dendrites (prothorax) and axon (brain). Generally, responses to acoustic pulses of the same parameter combination were similar within a neuronal class at the two recording sites. However, all neuronal classes showed significantly higher response variability and a tendency for higher spike activity when recorded in the dendrites. Unexpectedly, the combined activity of two neurons (Ascending Neurons 1 and 2) recorded in the brain provides a better fit to song recognition than when recorded in the thorax. Axonal recordings of T-shaped Neuron 1 revealed graded potentials originating in the brain and modulating its output in a potentially behaviourally relevant manner.

Keywords

Bushcricket Acoustic Intracellular Impalement Interneurons 

References

  1. Alle H, Geiger JR (2006) Combined analog and action potential coding in hippocampal mossy fibers. Science 311:1290–1293CrossRefPubMedGoogle Scholar
  2. Anton S, Dufour MC, Gadenne C (2007) Plasticity of olfactory guided behaviour and its neurobiological basis: lessons from moths and locusts. Entomol Exp Appl 123:1–11CrossRefGoogle Scholar
  3. Baden T, Hedwig B (2010) Primary afferent depolarization and frequency processing in auditory afferents. J Neurosci 30:14862–14869CrossRefPubMedGoogle Scholar
  4. Burrows M, Laurent G (1993) Synaptic potentials in the central terminals of locust proprioceptive afferents generated by other afferents from the same organ. J Neurosci 13(2):808–819PubMedGoogle Scholar
  5. Cattaert D, El Manira A (1999) Shunting versus inactivation: analysis of presynaptic inhibitory mechanisms in primary afferents of the crayfish. J Neurosci 19:6079–6089PubMedGoogle Scholar
  6. Cattaert D, El Manira A, Clarac F (1994) Chloride conductance process both presynaptic inhibition and antidromic spikes in primary afferent. Brain Res 666:109–112CrossRefPubMedGoogle Scholar
  7. Clarac F, Cattaert D, Le Ray D (2000) Central control components of a ‘simple’ stretch reflex. Trends Neurosci 23:199–208CrossRefPubMedGoogle Scholar
  8. Comer CM, Robertson RM (2001) Identified nerve cells and insect behavior. Prog Neurobiol 63:409–439CrossRefPubMedGoogle Scholar
  9. Dobler S, Heller KG, von Helversen O (1994a) Song pattern recognition and an auditory time window in the female bushcricket Ancistrura nigrovittata. J Comp Physiol A 175:67–74Google Scholar
  10. Dobler S, Stumpner A, Heller KG (1994b) Sex-specific spectral tuning for the partner’s song in the duetting bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Comp Physiol A 175:303–310Google Scholar
  11. Edwards DH (1990) Mechanisms of depolarizing inhibition at the crayfish giant motor synapse I. Electrophysiology. J Neurophysiol 64:532–540PubMedGoogle Scholar
  12. Faure PA, Hoy RR (2000) Neuroethology of the katydid T-cell. I. Tuning and responses to pure tones. J Exp Biol 203:3225–3242PubMedGoogle Scholar
  13. Fielden A (1960) Transmission through the last abdominal ganglion of the dragonfly nymph, Anax imperator. J Exp Biol 37:832–844Google Scholar
  14. Furshpan EJ, Furukawa T (1962) Intracellular and extracellular responses of the several regions of the Mauthner cell of the goldfish. J Neurophysiol 25:732–771PubMedGoogle Scholar
  15. Fuster JM, Creutzfeldt OD, Straschill M (1965) Intracellular recording of neuronal activity in the visual system. Z Vergl Physiol 49:605–622CrossRefGoogle Scholar
  16. Hardt M (1988) Zur Phonotaxis von Laubheuschrecken: Eine vergleichend verhaltensphysiologisch/neuroanatomische Untersuchung. Dissertation, Universität BochumGoogle Scholar
  17. Heinrich R (2002) Impact of descending brain neurons on the control of stridulation, walking, and flight in Orthoptera. Microsc Res Tech 56(4):292–301CrossRefPubMedGoogle Scholar
  18. Heller KG, von Helversen D (1986) Acoustic communication in phaneropterid bushcrickets: species-specific delay of female stridulatory response. Behav Ecol Sociobiol 18:189–198CrossRefGoogle Scholar
  19. Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Göpfert MC, Ito K (2009) The neural basis of drosophila gravity-sensing and hearing. Nature 458:165–171CrossRefPubMedGoogle Scholar
  20. Kennedy D, McVitte J, Calabrese R, Fricke RA, Craelius W, Chiapella P (1980) Inhibition of mechanosensory interneurons in the crayfish. I. Presynaptic inhibition from giant fibers. J Neurophysiol 43:1495–1509PubMedGoogle Scholar
  21. Lang F, Brandt G, Glahe M (1993) A versatile multichannel acoustic stimulator controlled by a personal computer. In: Elsner N, Heisenberg M (eds) Gene-brain-behaviour. Thieme, Stuttgart, p A892Google Scholar
  22. Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884–895CrossRefPubMedGoogle Scholar
  23. McIlwain JT, Creutzfeld OD (1967) Microelectrode study of synaptic excitation and inhibition in the lateral geniculate nucleus of the rat. J Neurophysiol 30:1–21Google Scholar
  24. Nicholls J, Wallace BG (1978) Modulation of transmission at an inhibitory synapse in the central nervous system of the leech. J Physiol 281:157–170PubMedCentralPubMedGoogle Scholar
  25. Ostrowski TD (2009) Filtering of species specific song parameters via interneurons in a bush cricket’s brain. Dissertation, Universität GöttingenGoogle Scholar
  26. Ostrowski TD, Stumpner A (2010) Frequency processing at consecutive levels in the auditory system of bush crickets (Tettigoniidae). J Comp Neurol 518:3101–3116CrossRefPubMedGoogle Scholar
  27. Otto C, Kalmring K, Lorenzen S, Sippel M (1983) Problems of recordings of nervous activity with glass microelectrodes in the CNS of insects. Biol Cybern 49:63–67CrossRefPubMedGoogle Scholar
  28. Palmer LM, Stuart GJ (2006) Site of action potential initiation in layer 5 pyramidal neurons. J Neurosci 26:1854–1863CrossRefPubMedGoogle Scholar
  29. Peña JL, Konishi M (2001) Auditory spatial receptive fields created by multiplication. Science 292:249–252CrossRefPubMedGoogle Scholar
  30. Poulet JF (2005) Corollary discharge inhibition and audition in the stridulating cricket. J Comp Physiol A 191:979–986CrossRefGoogle Scholar
  31. Purves D, Sakmann B (1974) The effect of contractile activity on fibrillation and extrajunctional acetylcholine-sensitivity in rat muscle maintained in organ culture. J Physiol (Lond) 237:157–182Google Scholar
  32. Rheinlaender J (1975) Transmission of acoustic information at three neuronal levels in the auditory system of Decticus verrucivorus (Tettigoniidae, Orthoptera). J Comp Physiol A 97:1–53CrossRefGoogle Scholar
  33. Römer H, Rheinlaender J, Dronse R (1981) Intracellular studies on auditory processing in the metathoracic ganglion of the locust. J Comp Physiol 144:305–312CrossRefGoogle Scholar
  34. Römer H, Marquart V, Hardt M (1988) Organization of a sensory neuropile in the auditory pathway of two groups of Orthoptera. J Comp Neurol 275:201–215CrossRefPubMedGoogle Scholar
  35. Schmitt A (2010) Erkennung der Weibchenantwort bei den Männchen der Laubheuschrecke Ancistrura nigrovittata. Bachelor-thesis, University GöttingenGoogle Scholar
  36. Schul J, Sheridan RA (2006) Auditory stream segregation in an insect. Neuroscience 138:1–4CrossRefPubMedGoogle Scholar
  37. Shen JX (1993) Morphology and physiology of auditory interneurons of the bushcricket Gampsocleis gratiosa. Jpn J Physiol 43:S239–S246CrossRefPubMedGoogle Scholar
  38. Shu Y, Hasenstaub A, Duque A, Yu Y, McCormick DA (2006) Modulation of intracortical synaptic potentials by presynaptic somatic membrane potential. Nature 441:761–765CrossRefPubMedGoogle Scholar
  39. Siegelbaum SA, Koester J (2000) Ion channels. In: Kandel E, Schwartz J, Jessell T (eds) Principles of neural science, 4th edn. McGraw-Hill, New York, pp 105–124Google Scholar
  40. Silver S, Kalmring K, Kühne R (1980) The responses of central acoustic and vibratory interneurones in bushcrickets and locusts to ultrasonic stimulation. Physiol Entomol 5:427–435CrossRefGoogle Scholar
  41. Stumpner A (1997) An auditory interneurone tuned to the male song frequency in the duetting bushcricket Ancistrura nigrovittata (Orthoptera, Phaneropteridae). J Exp Biol 200:1089–1101PubMedGoogle Scholar
  42. Stumpner A (1998) Picrotoxin eliminates frequency selectivity of an auditory interneuron in a bushcricket. J Neurophysiol 79:2408–2415PubMedGoogle Scholar
  43. Stumpner A (1999a) Comparison of morphology and physiology of two plurisegmental sound-activated interneurones in a bushcricket. J Comp Physiol A 185:199–205CrossRefGoogle Scholar
  44. Stumpner A (1999b) An interneurone of unusual morphology is tuned to the female song in the bushcricket Ancistrura nigrovittata (Orthoptera: Phaneropteridae). J Exp Biol 202:2071–2081PubMedGoogle Scholar
  45. Stumpner A (2001) Sound activated neurones and their potential function in a bushcricket—a synopsis. In: Elsner N, Kreutzberg GW (eds) Göttingen Neurobiology report 2001. Thieme, Stuttgart, p A370Google Scholar
  46. Stumpner A, Molina J (2006) Diversity of intersegmental auditory neurons in a bush cricket. J Comp Physiol A 192:1359–1376CrossRefGoogle Scholar
  47. Tal D, Schwartz EL (1997) Computing with the leaky integrate-and-fire neuron: logarithmic computation and multiplication. Neural Comp 9:305–318CrossRefGoogle Scholar
  48. Tauc L (1962) Identification of active membrane areas in the giant neuron of Aplysia. J Gen Physiol 45:1099–1115PubMedCentralCrossRefPubMedGoogle Scholar
  49. Wohlers DW, Huber F (1978) Intracellular recording and staining of cricket auditory interneurons (Gryllus campestris L., Gryllus bimaculatus De Geer). J Comp Physiol A 127:11–28CrossRefGoogle Scholar
  50. Wollner DA, Catterall WA (1986) Localization of sodium channels in axon hillocks and initial segments of retinal ganglion cells. Proc Natl Acad Sci USA 83:8424–8428PubMedCentralCrossRefPubMedGoogle Scholar
  51. Zhantiev RD, Korsunovskaya OS, Chukanov VS (2004) Effect of sound signals on spontaneous activity in grasshopper interneurons (Orthoptera, Tettigoniidae). J Evol Biochem Physiol 40:653–661CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  1. 1.Dalton Cardiovascular Research CenterUniversity of MissouriColumbiaUSA
  2. 2.Department of Cellular NeurobiologyGeorg-August-University of GöttingenGöttingenGermany

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