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Diverse speed response properties of motion sensitive neurons in the fly’s optic lobe

Abstract

Speed and acceleration are fundamental components of visual motion that animals can use to interpret the world. Behavioral studies have established that insects discriminate speed largely independently of contrast and spatial frequency, and physiological recordings suggest that a subset of premotor descending neurons is in this sense speed-selective. Neural substrates and mechanisms of speed selectivity in insects, however, are unknown. Using blow flies Phaenicia sericata, intracellular recordings and dye-fills were obtained from medulla and lobula complex neurons which, though not necessarily speed-selective themselves, are positioned to participate in circuits that produce speed-selectivity in descending neurons. Stimulation with sinusoidally varied grating motion (0–200°/s) provided a range of instantaneous velocities and accelerations. The resulting speed response profiles are indicative of four distinct speed ranges, supporting the hypothesis that the spatiotemporal tuning of mid-level neurons contains sufficient diversity to account for the emergence of speed selectivity at the descending neuron level. This type of mechanism has been proposed to explain speed discrimination in both insects and mammals, but has seemed less likely for insects due to possible constraints on small brains. Two additional recordings are suggestive of acceleration-selectivity, a potentially useful visual capability that is of uncertain functional significance for arthropods.

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Abbreviations

cpd:

Cycles per degree

emd:

Elementary motion detector

STF:

Spatiotemporal frequency

References

  • Borst A, Egelhaaf M (1989) Principles of visual motion detection. Trends Neurosci 12(8):297–306

    PubMed  Article  CAS  Google Scholar 

  • Cao P, Gu Y, Wang SR (2004) Visual neurons in the pigeon brain encode the acceleration of stimulus motion. J Neurosci 24(35):7690–7698

    PubMed  Article  CAS  Google Scholar 

  • Couto A, Alenius M, Dickson BJ (2005) Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr Biol 15:1535–1547

    PubMed  Article  CAS  Google Scholar 

  • David CT (1982) Compensation for height in the control of groundspeed by Drosophila in a new, “Barber’s Pole” wind tunnel. J Comp Physiol 147:485–493

    Article  Google Scholar 

  • Douglass JK, Strausfeld NJ (1996) Visual motion-detection circuits in flies: parallel direction- and non-direction-sensitive pathways between the medulla and lobula plate. J Neurosci 16:4551–4562

    PubMed  CAS  Google Scholar 

  • Douglass JK, Strausfeld NJ (1998) Functionally and anatomically segregated visual pathways in the lobula complex of a calliphorid fly. J Comp Neurol 396:84–104

    PubMed  Article  CAS  Google Scholar 

  • Douglass JK, Strausfeld NJ (2003a) Anatomical organization of retinotopic motion-sensitive pathways in the optic lobes of flies. Microsc Res Techn 62:132–150

    Article  Google Scholar 

  • Douglass JK, Strausfeld NJ (2003b) Retinotopic pathways providing motion-selective information to the lobula from peripheral elementary motion-detecting circuits. J Comp Neurol 457:326–344

    PubMed  Article  Google Scholar 

  • Dror RO, O’Carroll DC, Laughlin SB (2001) Accuracy of velocity estimation by Reichardt correlators. J Opt Soc Am A Opt Image Sci Vis 18:241–252

    PubMed  Article  CAS  Google Scholar 

  • Eckert H (1980) Functional properties of the H1 neuron in the third optic ganglion of the blowfly Phaenicia. J Comp Physiol 135:29–39

    Article  Google Scholar 

  • Egelhaaf M, Borst A (1989) Transient and steady-state response properties of movement detectors. J Opt Soc Am A 6:116–127

    PubMed  CAS  Google Scholar 

  • Egelhaaf M, Reichardt W (1987) Dynamic response properties of movement detectors: theoretical analysis and electrophysiological investigation in the visual system of the fly. Biol Cybern 56:69–87

    Article  Google Scholar 

  • Gilbert C, Strausfeld NJ (1992) Small-field neurons associated with oculomotor and optomotor control in muscoid flies: functional organization. J Comp Neurol 316:72–86

    PubMed  Article  CAS  Google Scholar 

  • Gronenberg W, Milde JJ, Strausfeld NJ (1995) Oculomotor control in calliphorid flies: organization of descending neurons to neck motor neurons responding to visual stimuli. J Comp Neurol 361:267–284

    PubMed  Article  CAS  Google Scholar 

  • Grzywacz NM, Yuille AL (1990) A model for the estimate of local image velocity by cells in the visual cortex. Proc R Soc Lond B 239:120–161

    Google Scholar 

  • Haag J, Borst A (1997) Encoding of visual motion information and reliability in spiking and graded potential neurons. J Neurosci 17:4809–4819

    PubMed  CAS  Google Scholar 

  • Hassenstein B, Reichardt W (1956) Systemtheoretische Analyse der Zeit-, Reihenfolgen- unt Vorzeichenauswertung bei der Bewegungsperzeption des Rüsselkäfers Chlorophanus. Z Naturforsch 11:513–524

    Google Scholar 

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

    PubMed  Article  Google Scholar 

  • Hausen K (1984) The lobula complex of the fly: structure, function and significance in visual behavior. In: Ali MA (ed) Photoreception and vision in invertebrates. Plenum, New York, pp 523–599

    Google Scholar 

  • Higgins CM (2004) Nondirectional motion may underlie insect behavioral dependence on image speed. Biol Cybern 91:326–332

    PubMed  Article  Google Scholar 

  • Higgins CM, Douglass JK, Strausfeld NJ (2004) The computational basis of an identified neuronal circuit for elementary motion detection in dipterous insects. Visual Neurosci 21:567–586

    Article  Google Scholar 

  • Horridge GA, Marcelja L (1992) On the existence of ‘fast’ and ‘slow’ directionally sensitive motion detector neurons in insects. Proc R Soc Lond B 248:47–54

    Article  CAS  Google Scholar 

  • Ibbotson MR (2001) Evidence for velocity-tuned motion-sensitive descending neurons in the honeybee. Proc R Soc Lond B 268:2195–2201

    Article  CAS  Google Scholar 

  • Juusola M, French AS (1997) Visual acuity for moving objects in first- and second-order neurons of the fly compound eye. J Neurophysiol 77:1487–1495

    PubMed  CAS  Google Scholar 

  • Kien J (1975) Neuronal mechanisms subserving directional selectivity in the locust optomotor system. J Comp Physiol 102:337–355

    Article  Google Scholar 

  • Land MF (1999) Motion and vision: why animals move their eyes. J Comp Physiol A 185(4):341–352

    PubMed  Article  CAS  Google Scholar 

  • Landolfa MA, Jacobs GA (1995) Direction sensitivity of the filiform hair population of the cricket cercal system. J Comp Physiol A 177:759–766

    Google Scholar 

  • Maddess T, Laughlin SB (1985) Adaptation of the motion-sensitive neuron H1 is generated locally and governed by contrast frequency. Proc R Soc Lond B 225:251–275

    Article  Google Scholar 

  • Meinertzhagen IA, Hanson TA (1993) The development of the optic lobes. In: Bate M, Arias AM (eds) The development of Drosophila melanogaster. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, pp 1363–1490

    Google Scholar 

  • O’Carroll DC, Bidwell NJ, Laughlin SB, Warrant EJ (1996) Insect motion detectors matched to visual ecology. Nature 382:63–66

    Article  CAS  Google Scholar 

  • O’Carroll DC, Laughlin SB, Bidwell NJ, Harris RA (1997) Spatio-temporal properties of motion detectors matched to low image velocities in hovering insects. Vision Res 37:3427–3439

    PubMed  Article  CAS  Google Scholar 

  • Olberg RM (1981) Object- and self-movement detectors in the ventral nerve cord of the dragonfly. J Comp Physiol 141:327–334

    Article  Google Scholar 

  • Osorio D, Vorobyev M (2005) Photoreceptor spectral sensitivities in terrestrial animals; adaptations for luminance and colour vision. Proc Biol Sci 272:1745–1752

    PubMed  Article  CAS  Google Scholar 

  • Perrone JA, Thiele A (2001) Speed skills: measuring the visual speed analyzing properties of primate MT neurons. Nat Neurosci 4:526–532

    PubMed  CAS  Google Scholar 

  • Priebe NJ, Lisberger SG, Movshon JA (2006) Tuning for spatiotemporal frequency and speed in directionally selective neurons of macaque striate cortex. J Neurosci 26:2941–2950

    PubMed  Article  CAS  Google Scholar 

  • Shoemaker PA, O’Carroll DC and Straw AD (2005) Velocity constancy and models for wide-field visual motion detection in insects. Biol Cybern 93:275–287

    PubMed  Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1981) Biometry, 2nd edn. W.H. Freeman & Co., New York, p 859

  • Srinivasan MV, Bernard G (1975) The effect of motion on visual acuity of the compound eye: a theoretical analysis. Vision Res 15:515–525

    PubMed  Article  CAS  Google Scholar 

  • Srinivasan MV, Lehrer M, Kirchner WH, Zhang SW (1991) Range perception through apparent image speed in freely flying honeybees. Vis Neurosci 6:519–535

    PubMed  CAS  Google Scholar 

  • Srinivasan M, Zhang S, Lehrer M, Collett T (1996) Honeybee navigation en route to the goal: visual flight control and odometry. J Exp Biol 199:237–244

    PubMed  Google Scholar 

  • Srinivasan MV, Zhang SW, Chahl JS, Barth E, Venkatesh S (2000) How honeybees make grazing landings on flat surfaces. Biol Cybern 83:171–183

    PubMed  Article  CAS  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Strausfeld NJ (2005) The evolution of crustacean and insect optic lobes and the origins of chiasmata. Arthropod Struct Dev 34:235–256

    Article  Google Scholar 

  • Strausfeld NJ, Gilbert C (1992) Small-field neurons associated with oculomotor and optomotor control in muscoid flies: cellular organization in the lobula plate. J Comp Neurol 316:56–71

    PubMed  Article  CAS  Google Scholar 

  • Strausfeld NJ, Gronenberg W (1990) Descending neurons supplying the neck and flight motor of Diptera: organization and neuroanatomical relationships with visual pathways. J Comp Neurol 302:954–972

    PubMed  Article  CAS  Google Scholar 

  • Strausfeld NJ, Lee J-K (1991) Neuronal basis for parallel visual processing in the fly. Visual Neurosci 7:13–33

    CAS  Article  Google Scholar 

  • Streidter GF (2005) Principles of brain evolution. Sinauer Associates, Sunderland

    Google Scholar 

  • Walpole RE (1974) Introduction to statistics. The Macmillan Co., New York, 340 pp

  • Zanker JM, Srinivasan MV, Egelhaaf M (1999) Speed tuning in elementary motion detectors of the correlation type. Biol Cybern 80:109–116

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank Drs. Wulfila Gronenberg, Charles M. Higgins and two anonymous reviewers for helpful discussions and critical comments on the manuscript. This work was supported by NIH 5 R01 RR008688-17. The experiments complied with the current laws of the United States and with “Principles of animal care”, publication No. 86-23, revised 1985 of the National Institutes of Health.

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Correspondence to John K. Douglass.

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Douglass, J.K., Strausfeld, N.J. Diverse speed response properties of motion sensitive neurons in the fly’s optic lobe. J Comp Physiol A 193, 233–247 (2007). https://doi.org/10.1007/s00359-006-0185-7

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  • DOI: https://doi.org/10.1007/s00359-006-0185-7

Keywords

  • Vision
  • Motion processing
  • Speed discrimination
  • Acceleration
  • Insecta