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Temporal and directional processing by an identified interneuron, ON1, compared in cricket species that sing with different tempos

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Abstract

We compare the temporal and directional processing properties of an identified auditory interneuron, ON1, between species with calling songs containing relatively low and high pulse rates (Teleogryllus oceanicus and Gryllus texensis, respectively). Using information theory, we find that the ON1 of G. texensis encodes higher amplitude-modulation frequencies than that of T. oceanicus. Bilateral differences in ON1 responses are also more pronounced in G. texensis, particularly for rapid, G. texensis-like stimuli. We show that brief silent intervals in a pulse train, such as those that occur in the natural calling song of G. texensis, enhance the representation of the stimulus pulse pattern as well as bilateral differences in activity. Our results suggest that the characteristics of an identified neuron vary, across cricket species, in accordance with the temporal structures of their communication signals.

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References

  • Atkins G, Pollack GS (1986) Age dependent occurrence of an ascending axon on the omega neuron of the cricket, Teleogryllus oceanicus. J Comp Neurol 243:527–534

    Google Scholar 

  • Atkins G, Ligman S, Burghardt F, Stout J (1984) Changes in phonotaxis by the female cricket after killing identified acoustic interenurons. J Comp Physiol A 154:795–804

    Google Scholar 

  • Balakrishnan R, Pollack GS (1996) Recognition of courtship song in the field cricket, Teleogryllus oceanicus. Anim Behav 51:353–366

    Google Scholar 

  • Borst A, Theunissen FE (1999) Information theory and neural coding. Nat Neurosci 2:947–957

    Google Scholar 

  • Brown WD (1999) Mate choice in tree crickets and their kin. Annu Rev Entomol 44:371–396

    Article  CAS  PubMed  Google Scholar 

  • Casaday GB, Hoy RR (1977) Auditory interneurons in the cricket Teleogryllus oceanicus: physiological and anatomical properties. J Comp Physiol 121:1–13

    Google Scholar 

  • Codon CJ, Galazyuk A, Feng AS (1997) Neurons in the auditory cortex of the little brown bat exhibit selectivity for complex-amplitude modulated signals that mimic echoes from fluttering targets insects. Audit Neurosci 3:269–287

    Google Scholar 

  • Coro F, Pérez M, Mora E, Boada D, Conner WE, Sandeford MV, Avila H (1998) Receptor cell habituation in the A1 auditory receptor of four noctuoid moths. J Exp Biol 201:2879–2890

    Google Scholar 

  • Doherty JA (1991) Song recognition and localization in the phonotaxis behavior of the field cricket Gryllus bimaculatus (Orthoptera, Gryllidae). J Comp Physiol A 168:213–222

    Google Scholar 

  • Faulkes Z, Pollack GS (2000) Effects of inhibitory timing on contrast enhancement in auditory circuits in crickets (Teleogryllus oceanicus). J Neurophysiol 84:1247–1255

    Google Scholar 

  • Givois V, Pollack GS (2000) Sensory habituation of auditory receptor neurons: Implications for sound localisation. J Exp Biol 203:2629–2537

    Google Scholar 

  • Grace JA, Amin N, Singh NC, Theunissen FE (2003) Selectivity for conspecific song in the zebra finch auditory forebrain. J Neurophysiol 89:472–487

    PubMed  Google Scholar 

  • Gray DA, Cade WH (1999) Sex, death and genetic variation: natural and sexual selection on cricket song. Proc R Soc Lond B 266:707–709

    Google Scholar 

  • Hedwig B, Poulet JFA (2004) Complex auditory behaviour emerges from simple reactive steering. Nature 430:781–785

    Google Scholar 

  • Helversen D von, Rheinlaender J (1988) Interaural intensity and time discrimination in an unrestrained grasshopper: a tentative behavioural approach. J Comp Physiol A 162:333–340

    Google Scholar 

  • Helversen D von, Helversen O von (1995) Acoustic pattern recognition and orientation in orthopteran insects: Parallel or serial processing? J Comp Physiol A 177:767–774

    Google Scholar 

  • Horseman G, Huber F (1994) Sound localisation in crickets. II. Modeling the role of a simple neural network in the prothoracic ganglion. J Comp Physiol A 175:399–413

    Google Scholar 

  • Krahe R, Larsen ON, Ronacher B (2000) Directional hearing is only weakly dependent on the rise time of acoustic stimuli. J Acoust Soc Am 107:1067–1070

    Google Scholar 

  • Machens CK, Stemmler MB, Prinz P, Krahe R, Ronacher B, Herz AV (2001) Representation of acoustic communication signals by insect auditory receptor neurons. J Neurosci 21:3215–3227

    Google Scholar 

  • Marsat G, Pollack GS (2004) Differential temporal coding of diverse acoustic signals by a single interneuron. J Neurophysiol 92:939–948

    Google Scholar 

  • Martin SD, Gray DA, Cade WH (2000) Fine-scale temperature effects on cricket calling song. Can J Zool 78:706–712

    Google Scholar 

  • Michelsen A (1998) Biophysics of sound localization in insects. In: Hoy R, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, Berlin Heidelberg New York

    Google Scholar 

  • Nabatiyan A, Poulet JFA, de Polavieja GG, Hedwig B (2003) Temporal pattern recognition based on instantaneous spike rate coding in a simple auditory system. J Neurophysiol 90:2484–2493

    Google Scholar 

  • Nagarajan SS, Cheung SW, Bedenbaugh P, Beitel RE, Scheiner CE, Merzenich MM (2002) Representation of spectral and temporal envelope of twitter vocalization in common marmoset primary auditory cortex. J Neurophysiol 87:1723–11737

    Google Scholar 

  • Pollack GS (1986) Discrimination of calling song models by the cricket, Teleogryllus oceanicus: the influence of sound direction on neural encoding of the stimulus temporal pattern and on phonotactic behavior. J Comp Physiol A 158:549–561

    Google Scholar 

  • Pollack GS (1998) Neural processing of acoustic signals. In: Hoy R, Popper AN, Fay RR (eds) Comparative hearing: insects. Springer, Berlin Heidelberg New York, pp 139–196

    Google Scholar 

  • Pollack GS (2003) Sensory cues for sound localization in the cricket Teleogryllus oceanicus: interaural difference in response strength versus interaural latency difference. J Comp Physiol A 189:143–151

    Google Scholar 

  • Pollack GS, El-Feghaly E (1993) Calling song recognition in the cricket Teleogryllus oceanicus: comparison of the effects of stimulus intensity and sound spectrum on selectivity for temporal pattern. J Comp Physiol A 171:759–766

    Google Scholar 

  • Rice WR (1988) Analyzing tables of statistical tests. Evolution 43:223–225

    Google Scholar 

  • Rieke F, Bodnar DA, Bialek W (1995) Naturalistic stimuli increase the rate and efficiency of information transmission by primary auditory afferents. Proc R Soc Lond B 262:259–265

    CAS  PubMed  Google Scholar 

  • Roddey JC, Girish B, Miller JP (2000) Assessing the performance of neural encoding models in the presence of noise. J Comput Neurosci 8:95–112

    Google Scholar 

  • Rose GJ, Capranica RR (1984) Processing amplitude-modulated sounds by the auditory midbrain of two species of toads—matched temporal filters. J Comp Physiol A 154:211–219

    Google Scholar 

  • Rose GJ, Brenowitz EA, Capranica RR (1985) Species specificity and temperature dependency of temporal processing by the auditory midbrain of 2 species of treefrogs. J Comp Physiol A 157:763–769

    Google Scholar 

  • Samson A-H, Pollack GS (2002) Encoding of sound localisation cues by an identified auditory interneuron: effects of stimulus temporal pattern. J Neurophysiol 88:2322–2328

    Google Scholar 

  • Schildberger K, Hörner M (1988) The function of auditory neurons in cricket phonotaxis. I. Influence of hyperpolarization of identified neurons on sound localization. J Comp Physiol A 163:621–631

    Google Scholar 

  • Selverston AI, Kleindienst HU, Huber F (1985) Synaptic connectivity between cricket auditory interneurons as studied by photoinactivation. J Neurosci 5:1283–1292

    Google Scholar 

  • Sippel M, Breckow J (1984) Non-monotonic response-intensity characteristics of auditory receptor cells in Locusta migratoria. J Comp Physiol A 155:633–638

    Google Scholar 

  • Smith SW (1997) The scientist and engineer’s guide to digital signal processing. California Technical Publishing, San Diego

    Google Scholar 

  • Souroukis K, Cade WH, Rowell G (1992). Factors that possibly influence variation in the calling song of field cricket: temperature, time, and male size, age, and wing morphology. Can J Zool 70:950–955

    Google Scholar 

  • Stabel J, Wendler G, Scharstein H (1989) Cricket phonotaxis: localization depends on recognition of the calling song pattern. J Comp Physiol A 165:167–177

    Google Scholar 

  • Strausfeld NJ, Seyan HS, Wohlers D, Bacon JP (1983). Lucifer Yellow histology. In: Strausfeld NJ (ed) Functional neuroanatomy. Springer, Berlin Heidelberg New York, pp 132–155

    Google Scholar 

  • Wagner WE Jr, Murray A-M, Cade WH (1995) Phenotypic variation in the mating preferences of female field crickets, Gryllus integer. Anim Behav 49:1269–1281

    Google Scholar 

  • Walker TJ (2000) Pulse rates in the songs of trilling field crickets (Orthoptera: Gryllidae: Gryllus). Ann Entomol Soc Am 93:565–572

    Google Scholar 

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Acknowledgements

We thank David Gray and Gary Marsat for generously providing song recordings, and the two anonymous referees for their helpful comments. This work was supported by the Natural Sciences and Engineering Research Council of Canada. The experiments comply with the “Principles of animal care”, publication No. 86-23, revised 1985, of the National Institute of Health, and also with the current laws of Canada.

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  1. Department of Biology, McGill University, 1205 Avenue Docteur Penfield, Montreal, QC, Canada, H3A 1B1

    D. Nicole Tunstall & Gerald S. Pollack

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  1. D. Nicole Tunstall
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  2. Gerald S. Pollack
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Correspondence to Gerald S. Pollack.

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Tunstall, D.N., Pollack, G.S. Temporal and directional processing by an identified interneuron, ON1, compared in cricket species that sing with different tempos. J Comp Physiol A 191, 363–372 (2005). https://doi.org/10.1007/s00359-004-0591-7

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  • DOI: https://doi.org/10.1007/s00359-004-0591-7

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