Journal of Comparative Physiology A

, Volume 193, Issue 5, pp 495–513 | Cite as

The mapping of visual space by dragonfly lateral ocelli

Original Paper

Abstract

We study the extent to which the lateral ocelli of dragonflies are able to resolve and map spatial information, following the recent finding that the median ocellus is adapted for spatial resolution around the horizon. Physiological optics are investigated by the hanging-drop technique and related to morphology as determined by sectioning and three-dimensional reconstruction. L-neuron morphology and physiology are investigated by intracellular electrophysiology, white noise analysis and iontophoretic dye injection. The lateral ocellar lens consists of a strongly curved outer surface, and two distinct inner surfaces that separate the retina into dorsal and ventral components. The focal plane lies within the dorsal retina but proximal to the ventral retina. Three identified L-neurons innervate the dorsal retina and extend the one-dimensional mapping arrangement of median ocellar L-neurons, with fields of view that are directed at the horizon. One further L-neuron innervates the ventral retina and is adapted for wide-field intensity summation. In both median and lateral ocelli, a distinct subclass of descending L-neuron carries multi-sensory information via graded and regenerative potentials. Dragonfly ocelli are adapted for high sensitivity as well as a modicum of resolution, especially in elevation, suggesting a role for attitude stabilisation by localization of the horizon.

Keywords

Dragonfly Ocelli Optics L-neuron Receptive field 

Abbreviations

BFD

Back focal distance

LCD

Liquid crystal display

L-neuron

Large second-order ocellar neuron

LED

Light emitting diode

PSL

Posterior slope

S-neuron

Small second-order ocellar neuron

UV

Ultraviolet

References

  1. Berry R, Stange G, Olberg R, van Kleef J (2006) The mapping of visual space by identified large second-order neurons in the dragonfly median ocellus. J Comp Physiol A 192:1105–1123CrossRefGoogle Scholar
  2. Berry RP, Stange G, Warrant EJ (2007a) Form vision in the insect dorsal ocelli: an anatomical and optical analysis of the dragonfly median ocellus. Vis Res (in press)Google Scholar
  3. Berry RP, Warrant EJ, Stange G (2007b) Form vision in the insect dorsal ocelli: an anatomical and optical analysis of the locust ocelli. Vis Res (in press)Google Scholar
  4. Campbell FW, Green DG (1965) Optical and retinal factors affecting visual resolution. J Physiol 181:576–593PubMedGoogle Scholar
  5. Campbell FW, Gubisch RW (1966) Optical quality of the human eye. J Physiol 186:558–578PubMedGoogle Scholar
  6. Chahl J, Thakoor S, Le Bouffant N, Stange G, Srinivasan MV, Hine B, Zornetzer S (2003) Bioinspired engineering of exploration systems: a horizon sensor/attitude reference system based on the dragonfly ocelli for Mars exploration applications. J Robotic Syst 20(1):35–42CrossRefGoogle Scholar
  7. Chappell RL, Dowling JE (1972) Neural organization of the median ocellus of the dragonfly. I. Intracellular electrical activity. J Gen Physiol 60:121–147PubMedCrossRefGoogle Scholar
  8. Chappell RL, Goodman LJ, Kirkham JB (1978) Lateral ocellar nerve projections in the dragonfly brain. Cell Tissue Res 190:99–114PubMedCrossRefGoogle Scholar
  9. Cornwell PB (1955) The functions of the ocelli of Calliphora (Diptera) and Locusta (Orthoptera). J Exp Biol 32:217–237Google Scholar
  10. Goodman LJ (1981) Organisation and physiology of the insect dorsal ocellar system. In: Autrum H (eds) Handbook of sensory physiology, Vol VII 6C. Springer, Berlin, pp 201–286Google Scholar
  11. Homann H (1924) Zum Problem der Ocellenfunktion bei den Insekten. Z Vergl Physiol 1:541–578CrossRefGoogle Scholar
  12. Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34:477–501PubMedCrossRefGoogle Scholar
  13. James AC, Ruseckaite R, Maddess T (2005) Effect of temporal sparseness and dichoptic presentation on multifocal visual evoked potentials. Vis Neur 22:45–54CrossRefGoogle Scholar
  14. Kondo H (1978) Efferent system of the lateral ocellus in the dragonfly: Its relationships with the ocellar afferent units, the compound eyes, and the wing sensory system. J Comp Physiol A 125:341–349CrossRefGoogle Scholar
  15. Labhart T, Nilsson D-E (1995) The dorsal eye of the dragonfly Sympetrum: specializations for prey detection against the blue sky. J Comp Physiol A 176:437–453CrossRefGoogle Scholar
  16. Land MF (1981) Optics and vision in invertebrates. In:Autrum H (ed) Handbook of sensory physiology, Vol VII 6B. Springer, Berlin, pp 471–592Google Scholar
  17. Milde J, Homberg U (1984) Ocellar interneurons in the honeybee: characteristics of spiking L-neurons. J Comp Physiol A155:151–160CrossRefGoogle Scholar
  18. Mizunami M (1994). Functional diversity of neural organization in insect ocellar systems. Vision Res 35:443–452CrossRefGoogle Scholar
  19. Mobbs PG, Guy RG, Goodman LJ, Chappell RL (1981) Relative spectral sensitivity and reverse Purkinje shift in identified L-neurons of the ocellar retina. J Comp Physiol A 144:91–97CrossRefGoogle Scholar
  20. Neumann TR, Bülthoff HH (2002) Behaviour-oriented vision for biomimetic flight control. In: Proceedings of the EPSRC/BBSRS international workshop on biologically inspired robotics 14–16, pp 196–203Google Scholar
  21. Parry DA (1947) The function of the insect ocellus. J Exp Biol 24:211–219Google Scholar
  22. Parsons MM, Krapp HG, Laughlin SB (2006) A motion-sensitive neurone responds to signals from the two visual systems of the blowfly, the compound eyes and ocelli. J Exp Biol 209:4464–4474PubMedCrossRefGoogle Scholar
  23. Patterson JA, Chappell RL (1980) Intracellular responses of procion filled cells and whole nerve cobalt impregnation in the dragonfly median ocellus. J Comp Physiol A 139:25–39CrossRefGoogle Scholar
  24. Rosser BL (1974) A study of the afferent pathways of the dragonfly lateral ocellus from extracellularly recorded spike discharges. J Exp Biol 60:135–160Google Scholar
  25. Ruck P (1958) A comparison of the electrical responses of compound eyes and dorsal ocelli in four insect species. J Insect Physiol 2:261–274CrossRefGoogle Scholar
  26. Ruck P (1961a) Electrophysiology of the insect dorsal ocellus. I. Origin of the components of the electroretinogram. J Gen Physiol 44:605–627CrossRefGoogle Scholar
  27. Ruck P (1961b) Electrophysiology of the insect dorsal ocellus. II. Mechanism of generation and inhibition of impulses in the ocellar nerve of dragonflies. J Gen Physiol 44:629–639CrossRefGoogle Scholar
  28. Ruck P, Edwards GA (1964) The structure of the insect dorsal ocellus. I. General organization of the ocellus in dragonflies. J Morphol 115:1–26CrossRefGoogle Scholar
  29. Schachtner J, Schmidt M, Homberg U (2005) Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea + Hexapoda). Arthropod Struct Dev 34:257–299CrossRefGoogle Scholar
  30. Schuppe H, Hengstenberg R (1993) Optical properties of the ocelli of Calliphora erythrocephala and their role in the dorsal light response. J Comp Physiol A 173:143–149CrossRefGoogle Scholar
  31. Simmons PJ (1982a) The operation of connexions between photoreceptors and large second-order neurons in dragonfly ocelli. J Comp Physiol 149:389–398CrossRefGoogle Scholar
  32. Simmons PJ (1982b) Transmission mediated with and without spikes at connexions between large second-order neurones of locust ocelli. J Comp Physiol A 147:401–414CrossRefGoogle Scholar
  33. Stange G, Howard J (1979) An ocellar dorsal light response in a dragonfly. J Exp Biol 83:351–355Google Scholar
  34. Stange G (1981) The ocellar component of flight equilibrium control in dragonflies. J Comp Physiol A 141:335–347CrossRefGoogle Scholar
  35. Stange G, Stowe S, Chahl JS, Massaro A (2002) Anisotropic imaging in the dragonfly median ocellus: a matched filter for horizon detection. J Comp Physiol A 188:455–467CrossRefGoogle Scholar
  36. Taylor CP (1981) Contribution of compound eyes and ocelli to steering of locusts in flight. I. Behavioural analysis. J Exp Biol 93:1–18Google Scholar
  37. van Kleef J, James AC, Stange G (2005) A spatiotemporal white noise analysis of photoreceptor responses to UV and green light in the dragonfly median ocellus. J Gen Physiol 126:481–497PubMedCrossRefGoogle Scholar
  38. Warrant EJ, Kelber A, Wallén R, Wcislo WT (2006) Ocellar optics in nocturnal and diurnal bees and wasps. Arthropod Struct Dev (in press)Google Scholar
  39. Warrant EJ, McIntyre PD (1993) Arthropod eye design and the physical limits to spatial resolving power. Prog Neurobiol 40:413–461PubMedCrossRefGoogle Scholar
  40. Warrant EJ, Nilsson D-E (1998) Absorption of white light in photoreceptors. Vision Res 38(2):195–207PubMedCrossRefGoogle Scholar
  41. Weber G, Renner M (1976) The ocellus of the cockroach Periplanta americana (Blattariae). Receptor area. Cell Tissue Res 168:209–222PubMedCrossRefGoogle Scholar
  42. Wehner R (1981) Spatial vision in arthropods. In: Autrum H (ed) Handbook of sensory physiology, Vol VII 6C. Springer, Berlin, pp 287–616Google Scholar
  43. Wilson M (1978) The functional organisation of locust ocelli. J Comp Physiol A 124:297–316CrossRefGoogle Scholar
  44. Zenkin GM, Pigarev IN (1971) Optically determined activity in the cervical nerve chain of the dragonfly. Biofizika 16:299–306PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Richard Berry
    • 1
    • 2
  • Joshua van Kleef
    • 1
  • Gert Stange
    • 1
  1. 1.Centre for Visual Sciences, Research School of Biological SciencesAustralian National UniversityCanberraAustralia
  2. 2.Research School of Biological SciencesAustralian National UniversityCanberraAustralia

Personalised recommendations