Cell and Tissue Research

, Volume 321, Issue 2, pp 273–284

Photoreceptor projection and termination pattern in the lamina of gonodactyloid stomatopods (mantis shrimp)

Regular Article

Abstract

The apposition compound eyes of gonodactyloid stomatopods are divided into a ventral and a dorsal hemisphere by six equatorial rows of enlarged ommatidia, the mid-band (MB). Whereas the hemispheres are specialized for spatial vision, the MB consists of four dorsal rows of ommatidia specialized for colour vision and two ventral rows specialized for polarization vision. The eight retinula cell axons (RCAs) from each ommatidium project retinotopically onto one corresponding lamina cartridge, so that the three retinal data streams (spatial, colour and polarization) remain anatomically separated. This study investigates whether the retinal specializations are reflected in differences in the RCA arrangement within the corresponding lamina cartridges. We have found that, in all three eye regions, the seven short visual fibres (svfs) formed by retinula cells 1–7 (R1–R7) terminate at two distinct lamina levels, geometrically separating the terminals of photoreceptors sensitive to either orthogonal e-vector directions or different wavelengths of light. This arrangement is required for the establishment of spectral and polarization opponency mechanisms. The long visual fibres (lvfs) of the eighth retinula cells (R8) pass through the lamina and project retinotopically to the distal medulla externa. Differences between the three eye regions exist in the packing of svf terminals and in the branching patterns of the lvfs within the lamina. We hypothesize that the R8 cells of MB rows 1–4 are incorporated into the colour vision system formed by R1–R7, whereas the R8 cells of MB rows 5 and 6 form a separate neural channel from R1 to R7 for polarization processing.

Keywords

Visual system First optic ganglion Long visual fibres Short visual fibres Gonodactyloid stomatopods Shrimp Haptosquilla glyptocercus Gonodactylus chiragra (Crustacea) 

Abbreviations

epl1

Outer lamina stratum

epl2

inner lamina stratum

lvf

long visual fibre

MB

mid-band

MPA

axial monopolar cell

MPL

lateral monopolar cell

RCA

retinula cell axon

R1–R8

retinula cells 1–8

svf

short visual fibre

References

  1. Armett-Kibel C, Meinertzhagen IA (1977) Cellular and synaptic organisation in the lamina of the dragonfly Sympetrum rubicundulum. Proc R Soc Lond [Biol] 196:385–413Google Scholar
  2. Armett-Kibel C, Meinertzhagen IA (1985) The long visual fibers of the dragonfly optic lobe: their cells of origin and lamina connections. J Comp Neurol 242:459–474PubMedGoogle Scholar
  3. Ball E, Kao L, Stone R, Land M (1986) Eye structure and optics in the pelagic shrimp Acetes sibolgae (Decapoda, Natantia, Sergestidae) in relation to light–dark adaptation and natural history. Philos Trans R Soc Lond Biol 313:251–270Google Scholar
  4. Bernard GD, Wehner R (1977) Functional similarities between polarization vision and color vision. Vis Res 17:1019–1028CrossRefPubMedGoogle Scholar
  5. Boschek CB (1971) On the fine structure of the peripheral retina and lamina ganglionaris of the fly, Musca domestica. Z Zellforsch 118:369–409CrossRefPubMedGoogle Scholar
  6. Caldwell RL, Dingle H (1975) Ecology and evolution of agonistic behavior in stomatopods. Naturwissenschaften 62:214–222CrossRefGoogle Scholar
  7. Caldwell RL, Dingle H (1976) Stomatopods. Sci Am 234:80–89PubMedGoogle Scholar
  8. Chiao C-C, Cronin TW, Marshall NJ (2000) Eye design and color signaling in a stomatopod crustacean Gonodactylus smithii. Brain Behav Evol 56:107–122CrossRefPubMedGoogle Scholar
  9. Cronin TW, Marshall NJ (1989) Multiple spectral classes of photoreceptors in the retinas of gonodactyloid stomatopod crustaceans. J Comp Physiol [A] 166:261–275Google Scholar
  10. Cronin TW, Marshall NJ (2004) The unique visual world of the mantis shrimp. In: Prete FR (ed) Complex worlds from simpler nervous systems. A Bradford book. MIT, Cambridge, pp 239–268Google Scholar
  11. Cronin TW, Marshall NJ, Quinn CA, King CA (1994a) Ultraviolet photoreception in mantis shrimp. Vis Res 34:1443–1449CrossRefPubMedGoogle Scholar
  12. Cronin TW, Marshall NJ, Caldwell RL, Shashar N (1994b) Specialisation of retinal function in the compound eyes of mantis shrimps. Vis Res 34:2639–2656CrossRefPubMedGoogle Scholar
  13. Cummins D, Goldsmith TH (1981) Cellular identification of the violet receptor in the crayfish eye. J Comp Physiol 142:199–202CrossRefGoogle Scholar
  14. Glantz MR (1996) Polarization sensitivity in the crayfish lamina monopolar neurons. J Comp Physiol [A] 178:413–425Google Scholar
  15. Glantz MR (2001) Polarization analysis in the crayfish visual system. J Exp Biol 204:2383–2390Google Scholar
  16. Goldsmith TH, Fernandez HR (1968) Comparative studies of crustacean spectral sensitivity. Z Vgl Physiol 60:156–175CrossRefGoogle Scholar
  17. Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. Springer, Berlin Heidelberg New YorkGoogle Scholar
  18. Hardie RC, Franceschini N, Ribi W, Kirschfeld K (1981) Distribution and properties of sex-specific photoreceptors in the fly Musca domestica. J Comp Physiol 145:139–152CrossRefGoogle Scholar
  19. Horch K, Salmon M, Forward R (2002) Evidence for a two pigment visual system in the fiddler crab, Uca thayeri. J Comp Physiol [A] 188:493–499Google Scholar
  20. Hyatt GW (1975) Physiological and behavioural evidence for colour discrimination by fiddler crabs, Brachyura, Ocypodidae, genus Uca. In: Vernberg FJ (ed) Physiological ecology of estuarine organisms. University of Carolina, Columbia, pp 333–365Google Scholar
  21. Kleinlogel S, Marshall NJ, Horwood JM, Land MF (2003) Neuroarchitecture of the color and polarization vision system of the stomatopod Haptosquilla. J Comp Neurol 467:326–342CrossRefPubMedGoogle Scholar
  22. Kunze P (1968) Die Orientierung der Retinulazellen im Auge von Ocypode. Z Zellforsch 90:454–462CrossRefPubMedGoogle Scholar
  23. Land MF, Marshall NJ, Brownless D, Cronin TW (1990) The eye-movements of the mantis shrimp Odontodactylus scyllarus (Crustacea: Stomatopoda). J Comp Physiol [A] 167:155–166Google Scholar
  24. Marshall NJ (1988) A unique colour and polarization vision system in mantis shrimps. Nature 333:557–560Google Scholar
  25. Marshall NJ, Land MF (1993a) Some optical features of the eyes of stomatopods. I. Eye shape, optical axis and resolution. J Comp Physiol [A] 173:565–582Google Scholar
  26. Marshall NJ, Land MF (1993b) Some optical features of the eyes of stomatopods. II. Ommatidial design, sensitivity and habitat. J Comp Physiol [A] 173:583–594Google Scholar
  27. Marshall NJ, Oberwinkler J (1999) The colourful world of the mantis shrimp. Nature 401:873–874Google Scholar
  28. Marshall NJ, Land MF, Cronin TW (1989) The structure and function of the mid-band in the eyes of stomatopod crustaceans. J Mar Biol Assoc UK 69:735Google Scholar
  29. Marshall NJ, Land MF, King CA, Cronin TW (1991a) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). II. Colour pigments in the eyes of stomatopod crustaceans: polychromatic vision by serial and lateral filtering. Philos Trans R Soc Lond Biol 334:57–84Google Scholar
  30. Marshall NJ, Land MF, King CA, Cronin TW (1991b) The compound eyes of mantis shrimps (Crustacea, Hoplocarida, Stomatopoda). I. Compound eye structure: the detection of polarised light. Philos Trans R Soc Lond Biol 334:33–56Google Scholar
  31. Marshall NJ, Jones JP, Cronin TW (1996) Behavioural evidence for colour vision in stomatopod crustaceans. J Comp Physiol [A] 179:473–481Google Scholar
  32. Marshall NJ, Oberwinkler J, Cronin TW, Land MF (1998) The 16 sensitivities of the stomatopod eye—what are they for? 26th Neurobiology Conference, GöttingenGoogle Scholar
  33. Menzel R, Blakers M (1975) Colour receptors in the bee eye—morphology and spectral sensitivity. J Comp Physiol 108:11–33CrossRefGoogle Scholar
  34. Meyer EP (1979) Golgi–EM-study of first and second order neurons in the visual system of Cataglyphis bicolor Fabricius (Hymenoptera, Formicidae). Zoomorphology 92:115–139CrossRefGoogle Scholar
  35. Nässel DR (1975) The organization of the lamina ganglionaris of the prawn, Pandalus borealis (Kroyer). Cell Tissue Res 163:445–464PubMedGoogle Scholar
  36. Nässel DR (1977) Types and arrangements of neurons in the crayfish optic lamina. Cell Tissue Res 179:45–75PubMedGoogle Scholar
  37. Nässel DR, Waterman TH (1977) Golgi EM evidence for visual information channelling in the crayfish lamina ganglionaris. Brain Res 130:556–563CrossRefPubMedGoogle Scholar
  38. Nässel DR, Elofsson R, Odselius R (1978) Neuronal connectivity patterns in the compound eyes of Artemia salina and Daphina magna. Cell Tissue Res 190:435–457PubMedGoogle Scholar
  39. Nilsson DE, Osorio D (1997) Homology and parallelism in arthropod sensory processing. Chapman and Hall, LondonGoogle Scholar
  40. Osorio D, Marshall NJ, Cronin TW (1997) Stomatopod photoreceptor spectral tuning as an adaptation for colour constancy in water. Vis Res 37:3299–3309CrossRefPubMedGoogle Scholar
  41. Reynolds ES (1963) The use of lead citrate at high pH as an electron–opaque stain in electron microscopy. J Cell Biol 17:208–212CrossRefPubMedGoogle Scholar
  42. Ribi WA (1975) The neurons of the first optic ganglion of the bee (Apis melifera). Adv Anat Embryol Cell Biol 50:1–42PubMedGoogle Scholar
  43. Ribi WA (1981) The first optic ganglion of the bee. VI. Synaptic fine structure and connectivity patterns of receptor cell axons and first order interneurons. Cell Tissue Res 215:443–464CrossRefPubMedGoogle Scholar
  44. Rossel S (1989) Polarization sensitivity in compound eyes. In: Stavenga DG, Hardie RC (eds) Facets of vision. Springer, Berlin Heidelberg New York, pp 298–316Google Scholar
  45. Sabra R, Glantz RM (1985) Polarisation sensitivity of crayfish photoreceptors is correlated with their termination sites in the lamina ganglionaris. J Comp Physiol 156:315–318CrossRefGoogle Scholar
  46. Schiff H (1987) Optical and neural pooling in visual processing in crustacea. Comp Biochem Physiol 88A:1–13CrossRefGoogle Scholar
  47. Schiff H, Abbott BC, Manning RB (1986) Optics, range-finding and neuroanatomy of the eye of a mantis shrimp, Squilla mantis (Linnaeus) (Crustacea; Stomatopoda; Squillidae). Smithsonian Contrib Zool 440:1–32Google Scholar
  48. Souza JD, Hertel H, Ventura DF, Menzel R (1992) Response properties of stained monopolar cells in the honeybee lamina. J Comp Physiol [A] 170:267–274Google Scholar
  49. Stavenga DG (1979) Pseudopupils of compound eyes. In: Autrum H (ed) Handbook of sensory physiology. Springer, Berlin Heidelberg New York, pp 225–313Google Scholar
  50. Stowe S, Ribi WA, Sandeman DC (1977) The organisation of the lamina ganglionaris of the crabs Scylla serrata and Leptograpsus variegatus. Cell Tissue Res 178:517–532CrossRefPubMedGoogle Scholar
  51. Strausfeld NJ, Blest AD (1970) Golgi studies on insects. I. The optic lobes of Lepidoptera. Philos Trans R Soc Lond 258:81–134Google Scholar
  52. Strausfeld NJ, Nässel DR (1981) Neuroarchitecture of brain regions that subserve the compound eyes of crustacea and insects. In: Autrum H (ed) Handbook of sensory physiology. Springer, Berlin Heidelberg New York, pp 344–357Google Scholar
  53. Warrant EJ, McIntyre PD (1990) Limitations to resolution in superposition eyes. J Comp Physiol [A] 167:785–803Google Scholar
  54. Waterman TH (1981) Polarisation sensitivity. In: Autrum H (ed) Handbook of sensory physiology. Springer, Berlin Heidelberg New York, pp 283–469Google Scholar
  55. Waterman TH, Fernandez HR (1970) E-vector and wavelength discrimination by retinular cells of the crayfish Procambarus. Z Vgl Physiol 68:154–174CrossRefGoogle Scholar
  56. Wehner R (2001) Polarization vision—a uniform sensory capacity? Exp Biol 204:2589–2596Google Scholar
  57. Zeil J (1983) Sexual dimorphism in the visual system of flies: the free flight behaviour of male Bibionidae (Diptera). J Comp Physiol 150:395–412CrossRefGoogle Scholar
  58. Zufall F, Schmitt M, Menzel R (1989) Spectral and polarized light sensitivity of photoreceptors in the compound eye of the cricket (Gryllus bimaculatus). J Comp Physiol [A] 164:597–608CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  1. 1.Vision, Touch and Hearing Research Centre, School of Biomedical SciencesUniversity of QueenslandBrisbaneAustralia

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