Skip to main content
SpringerLink
Log in

Characterisation of a blowfly male-specific neuron using behaviourally generated visual stimuli

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

The pursuit system controlling chasing behaviour in male blowflies has to cope with extremely fast and dynamically changing visual input. An identified male-specific visual neuron called Male Lobula Giant 1 (MLG1) is presumably one major element of this pursuit system. Previous behavioural and modelling analyses have indicated that angular target size, retinal target position and target velocity are relevant input variables of the pursuit system. To investigate whether MLG1 specifically represents any of these visual parameters we obtained in vivo intracellular recordings while replaying optical stimuli that simulate the visual signals received by a male fly during chasing manoeuvres. On the basis of these naturalistic stimuli we find that MLG1 shows distinct direction sensitivity and is depolarised if the target motion contains an upward component. The responses of MLG1 are jointly determined by the retinal position, the speed and direction, and the duration of target motimotion. Coherence analysis reveals that although retinal target size and position are in some way inherent in the responses of MLG1, we find no confirmation of the hypothesis that MLG1 encodes any of these parameters exclusively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

HS:

Horizontal system

MLG1:

Male lobula giant (neuron) 1

MLGs:

Male lobula giant (neurons)

SNR:

Signal-to-noise ratio

STMD:

Small target motion detector

VS:

Vertical system

References

  • Beersma DGM, Stavenga DG, Kuiper JW (1977) Retinal lattice, visual field and binocularities in flies. J Comp Physiol A 119:207–220

    Article  Google Scholar 

  • Boeddeker N, Egelhaaf M (2003) Steering a virtual blowfly: simulation of visual pursuit. Proc R Soc Lond B 270:1971–1978

    Article  Google Scholar 

  • Boeddeker N, Kern R, Egelhaaf M (2003) Chasing a dummy target: Smooth pursuit and velocity control in male blowflies. Proc R Soc Lond B 270:393–399

    Article  Google Scholar 

  • Boeddeker N, Egelhaaf M (2005) A single control system for smooth and saccade-like pursuit in blowflies. J Exp Biol 208:1563–1572

    Article  PubMed  Google Scholar 

  • Borst A, Haag J (2002) Neural networks in the cockpit of the fly. J Comp Physiol A 188:419–437

    Article  CAS  Google Scholar 

  • Burton BG, Laughlin SB (2003) Neural images of pursuit targets in the photoreceptor arrays of male and female houseflies Musca domestica. J Exp Biol 206:3963–3977

    Article  PubMed  Google Scholar 

  • Collett TS, Land MF (1975) Visual control of flight behaviour in the hoverfly Syritta pipiens L. J Comp Physiol A 99:1–66

    Article  Google Scholar 

  • Collett TS (1980) Angular tracking and the optomotor response. An analysis of visual reflex interaction in a hoverfly. J Comp Physiol A 140:145–158

    Article  Google Scholar 

  • Egelhaaf M, Borst A (1993) A look into the cockpit of the fly: visual orientation, algorithms, and identified neurons. J Neurosci 13(11):4563–4574

    PubMed  CAS  Google Scholar 

  • Egelhaaf M, Kern R, Krapp HG, Kretzberg J, Kurtz R, Warzecha AK (2002) Neural encoding of behaviourally relevant visual-motion information in the fly. J Neurosci 25:96–102

    CAS  Google Scholar 

  • Egelhaaf M, Grewe J, Karmeier K, Kern R, Kurtz R, Warzecha AK (2005) Novel approaches to visual information processing in insects: case studies on neuronal computations in the blowfly. In: Christensen TA (ed) Methods in insect sensory neuroscience. CRC Press, Boca Raton, pp 185–212

    Google Scholar 

  • Franceschini N, Kirschfeld K (1971) Pseudopupil phenomena in the Drosophila compound eye. Kybernetik 9:159–182

    Article  PubMed  CAS  Google Scholar 

  • Franceschini N, Hardie R, Ribi W, Kirschfeld K (1981) Sexual dimorphism in a photoreceptor. Nature 291:241–244

    Article  Google Scholar 

  • Frost BJ, Wylie DR, Wang YC (1990) The processing of object and self-motion in the tectofugal and accessory optic pathways of birds. Vis Res 30:1677–1688

    Article  PubMed  CAS  Google Scholar 

  • Gilbert C, Strausfeld NJ (1991) The functional organisation of male-specific visual neurons in flies. J Comp Physiol A 169:395–411

    Article  PubMed  CAS  Google Scholar 

  • Gronenberg W, Strausfeld NJ (1991) Descending pathways connecting the male-specific visual system of flies to the neck and flight motor. J Comp Physiol A 169:413–426

    Article  PubMed  CAS  Google Scholar 

  • Haag J, Borst A (1998) Active membrane properties and signal encoding in graded potential neurons. J Neurosci 18(19):7972–7986

    PubMed  CAS  Google Scholar 

  • Hardie RC, Franceschini N, Ribi W, Kirschfeld K (1981) Distribution and properties of sex-specific photoreceptors in the fly Musca domestica. J Comp Physiol A 145:139–152

    Article  Google Scholar 

  • Hausen K (1982a) Motion sensitive interneurons in the optomotor system of the fly. I The horizontal cells: structure and signals. Biol Cybern 45:143–156

    Article  Google Scholar 

  • Hausen K (1982b) Motion sensitive interneurons in the optomotor system of the fly. II The horizontal cells: receptive field organization and response characteristics. Biol Cybern 46:67–79

    Article  Google Scholar 

  • Hausen K, Strausfeld NJ (1980) Sexually dimorphic interneuron arrangements in the fly visual system. Proc R Soc Lond B 208:57–71

    Article  Google Scholar 

  • Hausen K, Egelhaaf M (1989) Neural mechanisms of visual course control in insects. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Heidelberg, pp 391–424

    Google Scholar 

  • Hengstenberg R (1982) Common visual response properties of giant vertical cells in the lobula plate of the blowfly Calliphora. J Comp Physiol A 149:179–193

    Article  Google Scholar 

  • Hengstenberg R (1993) Multisensory control in insect oculomotor systems. In: Miles FA, Wallmann J (eds) Visual motion and its role in the stabilisation of gaze. Elsevier, Amsterdam, pp 285–298

    Google Scholar 

  • Hengstenberg R, Hausen K, Hengstenberg B (1982) The number and structure of giant vertical cells (VS) in the lobula plate of the blowfly Calliphora erythrocephala. J Comp Physiol A 149:163–177

    Article  Google Scholar 

  • Hornstein EP, O’Carrol DC, Anderson JC, Laughlin SB (2000) Sexual dimorphism matches photoreceptor performance to behavioural requirements. Proc R Soc Lond B 267:2111–2117

    Article  CAS  Google Scholar 

  • Hüls T (2005) Instability helps virtual flies to mate. Biol Cybern 93:222–229

    Article  PubMed  Google Scholar 

  • Kayser C, Körding KP, König P (2004) Processing of complex stimuli and natural scenes in the visual cortex. Curr Opin Neurobiol 14:468–473

    Article  PubMed  CAS  Google Scholar 

  • Kern R, van Hateren JH, Michaelis C, Lindemann JP, Egelhaaf M (2005) Function of a fly motion-sensitive neuron matches eye movements during free flight. PloS Biol 3(6):e171

    Article  PubMed  CAS  Google Scholar 

  • Krapp HG, Hengstenberg B, Hengstenberg R (1998) Dendritic structure and receptive-field organization of optic flow processing interneurons in the fly. J Neurophysiol 79:1902–1917

    PubMed  CAS  Google Scholar 

  • Kurtz R, Warzecha AK, Egelhaaf M (2001) Transfer of visual motion information via graded synapses operates linearly in the natural activity range. J Neurosci 21(17):6957–6966

    PubMed  CAS  Google Scholar 

  • Land MF (1973) Head movement of flies during visually guided flight. Nature 243:299–300

    Article  Google Scholar 

  • Land MF (1992) Visual tracking and pursuit: Humans and arthropods compared. J Insect Physiol 38:939–951

    Article  Google Scholar 

  • Land MF (1993a) The visual control of courtship behaviour in the fly Poecilobothrus nobilitatus. J Comp Physiol A 173:595–603

    Google Scholar 

  • Land MF (1993b) Chasing and pursuit in the dolichopodid fly Poecilobothrus nobilitatus. J Comp Physiol A 173:605–613

    Google Scholar 

  • Land MF (1997) Visual acuity in insects. Annu Rev Entomol 42:147–177

    Article  PubMed  CAS  Google Scholar 

  • Land MF, Collett TS (1974) Chasing behaviour of house flies (Fannia canicularis). J Comp Physiol A 89:331–357

    Article  Google Scholar 

  • Land MF, Eckert H (1985) Maps of the acute zones of fly eyes. J Comp Physiol A 156:525–538

    Article  Google Scholar 

  • Lindemann JP, Kern R, Michaelis C, Meyer P, van Hateren JP, Egelhaaf M (2003) FliMax, a novel stimulus device for panoramic and highspeed presentation of behaviourally generated optic flow. Vis Res 43:779–791

    Article  PubMed  CAS  Google Scholar 

  • Nordström K, Barnett PD, O’Carroll DC (2006) Insect detection of small targets moving in visual clutter. PLoS Biol 4(3):e54

    Article  PubMed  CAS  Google Scholar 

  • Orfanidis SJ (1996) Introduction to signal processing. Prentice-Hall, Englewood Cliffs

  • Reinagel P (2001) The many faces of adaptation. Nature 412:776–777

    Article  PubMed  CAS  Google Scholar 

  • Schilstra C, van Hateren JH (1998) Using miniature sensor coils for simultaneous measurement of orientation and position of small, fast-moving animals. J Neurosci Methods 83:125–131

    Article  PubMed  CAS  Google Scholar 

  • Simoncelli EP (2003) Vision and the statistics of the visual environment. Curr Opin Neurobiol 13:144–149

    Article  PubMed  CAS  Google Scholar 

  • Simoncelli EP, Olshausen BA (2001) Natural image statistics and neural representation. Annu Rev Neurosci 24:1193–1216

    Article  PubMed  CAS  Google Scholar 

  • Strausfeld NJ (1991) Structural organisation of male-specific visual neurons in calliphorid optic lobes. J Comp Physiol A 169:379–393

    Article  PubMed  CAS  Google Scholar 

  • van Hateren JH (1997) Processing of natural time series of intensities by the visual system of the blowfly. Vis Res 37:3407–3416

    Article  PubMed  Google Scholar 

  • van Hateren JH, Schilstra C (1999) Blowfly flight and optic flow. II. Head movements during flight. J Exp Biol 202:1491–1500

    PubMed  Google Scholar 

  • van Hateren JH, Snippe HP (2001) Information theoretical evaluation of parametric models of gain control in blowfly photoreceptor cells. Vision Research 41:1851–1865

    Article  PubMed  Google Scholar 

  • van Hateren JH, Kern R, Schwerdtfeger G, Egelhaaf M (2005) Function and coding in the blowfly H1 neuron during naturalistic optic flow. J Neurosci 25:4343–4352

    Article  PubMed  CAS  Google Scholar 

  • Wachenfeld A (1994) Elektrophysiologische Untersuchungen und funktionelle Charakterisierung männchenspezifischer visueller Interneurone in der Schmeißfliege Calliphora erythrocephala (Meig.). Doctoral dissertation, Universität Köln

  • Wagner H (1986a) Flight performance and visual control of flight of the free-flying housefly (Musca domestica L.) I. Organisation of the flight motor. Philos Trans R Soc Lond B 312:527–551

    Google Scholar 

  • Wagner H (1986b) Flight performance and visual control of flight of the free-flying housefly (Musca domestica L.) II. Pursuit of targets. Philos Trans R Soc Lond B 312:553–579

    Google Scholar 

  • Wagner H (1986c) Flight performance and visual control of flight of the free-flying housefly (Musca domestica L.) III. Interactions between angular movement induced by wide- and smallfield stimuli. Philos Trans R Soc Lond B 312:581–595

    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. Vis Res 40:2973–2983

    Article  PubMed  CAS  Google Scholar 

  • Wehrhahn C (1979) Sex-specific differences in the chasing behaviour of houseflies (Musca). Biol Cybern 32:239–241

    Article  Google Scholar 

  • Wehrhahn C, Poggio T, Buelthoff H (1982) Tracking and chasing in houseflies (Musca) An analysis of 3-D flight trajectories. Biol Cybern 45:123–130

    Article  Google Scholar 

  • Zeil J (1983) Sexual dimorphism in the visual system of flies: the free flight behaviour of male Bibionidae (Diptera). J Comp Physiol A 150:395–412

    Article  Google Scholar 

Download references

Acknowledgments

We are grateful to Roland Kern and Rafael Kurtz for discussion and critical reading, whose comments helped to improve the manuscript, and we thank Amin Hleihil and Roland Kern for programming assistance. This research was supported by the Deutsche Forschungsgemeinschaft (DFG; Graduate Programme 518 ‘Strategies and Optimisation of Behaviour’). The experiments complied with the current German law and with the ‘Principles of animal care’, publication No. 86-23, revised 1985 of the National Institute of Health.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Bielefeld University, Post Box 100131, 33501, Bielefeld, Germany

    Christine Trischler & Martin Egelhaaf

  2. Centre for Visual Sciences, RSBS, Australian National University, Canberra, ACT, 2601, Australia

    Norbert Boeddeker

Authors
  1. Christine Trischler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Norbert Boeddeker
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Egelhaaf
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Christine Trischler.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Trischler, C., Boeddeker, N. & Egelhaaf, M. Characterisation of a blowfly male-specific neuron using behaviourally generated visual stimuli. J Comp Physiol A 193, 559–572 (2007). https://doi.org/10.1007/s00359-007-0212-3

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00359-007-0212-3

Keywords

Search

Navigation