Cell and Tissue Research

, Volume 273, Issue 3, pp 533–545 | Cite as

Histamine immunoreactivity in the central nervous system of the spider Cupiennius salei

  • Axel Schmid
  • Matthis Duncker
Article
Received:
Accepted:

Abstract

In this study, immunohistochemistry on Vibracut sections is used to demonstrate anti-histamine immunoreactivity in the brain of the spider, Cupiennius salei (Keys.) (Ctenidae). We describe a system of histamine-immunoreactive neurons within the central nervous system that consists of six omnisegmental neurons. These histamine-immunoreactive neurons form two subgroups: a dorsal system with two cells per hemisphere and a ventral system with only one cell per hemisphere. The cells have extended arborizations in the motor and sensory areas of all neuromeres in the suboesophageal ganglionic mass. We have also found histamine immunoreactivity in the photoreceptors of C. salei and suggest that histamine is a neurotransmitter of photoreceptors in all arthropods, since it is also known to occur in the photoreceptors of the other main arthropod taxa (Merostomata, Crustacea, and Insecta).

Key words

Immunohistochemistry Neurotransmitters Neuromodulators Histamine Visual system Nervous system, central Cupiennius salei (Arachnida) 
This is a preview of subscription content, log in to check access.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ache BW, McClintock T (1990) The lobster olfactory receptor cell as a neurobiological model: the action of histamine. In: Wiese K, Krenz WD, Tautz J, Reichert H, Malloney B (eds) Frontiers in crustacean neurobiology. Birkhäuser, Basel, pp 33–90Google Scholar
  2. Anton S, Barth FG (1993) Central nervous projection patterns of the trichobothria and other cuticular sensilla in the wandering spider Cupiennius salei (Arachnida, Araneae). Zoomorphology 113:21Google Scholar
  3. Babu KS, Barth FG (1984) Neuroanatomy of the central nervous system of the wandering spider, Cupiennius salei (Arachnida, Araneida). Zoomorphology 104:344–359Google Scholar
  4. Babu KS, Barth FG (1989) Central nervous projections of mechanoreceptors in the spider Cupiennius salei Keys. Cell Tissue Res 258:69–82Google Scholar
  5. Babu KS, Barth FG, Strausfeld NJ (1985) Intersegmental sensory tracts and contralateral motor neurons in the leg ganglia of the spider Cupiennius salei Keys. Cell Tissue Res 241:53–57Google Scholar
  6. Battelle BA, Calman BG, Andrews AW, Grieco FD, Mleziva MB, Callaway JC, Stuart AE (1991) Histamine: a putative afferent neurotransmitter in Limulus eyes. J Comp Neurol 305:527–542Google Scholar
  7. Baux G, Fossier P, Tauc L (1990) Histamine and FLRFamide regulate acetylcholine release at an identified synapse in Aplysia in opposite ways. J Physiol (Lond) 429:247–255Google Scholar
  8. Bayer TA, McClintock T, Grünert U, Ache BW (1989) Histamine induced modulation of olfactory receptor neurons in two species of lobsters, Panulirus argus and Homarus americanus. J Exp Biol 145:133–146Google Scholar
  9. Callaway JC, Stuart AE (1989) Biochemical and physiological evidence that histamine is the transmitter of barnacle photoreceptors. Vis Neurosci 3:311–325Google Scholar
  10. Claiborne BJ, Selverston AI (1984) Histamine as a transmitter in the stomatogastric nervous system of the spiny lobster. J Neurosci 4:708–721Google Scholar
  11. Duelli P (1980) The neuronal organization of the posterior lateral eyes of jumping spiders (Salticidae). Zool Jb Anat 103:17–40Google Scholar
  12. Eckweiler W, Seyfarth EA (1988) Tactile hairs and the adjustment of body height in wandering spiders: behavior, leg reflexes, and afferent projections in the leg ganglia. J Comp Physiol [A] 162:611–621Google Scholar
  13. Eckweiler W, Hammer K, Seyfarth EA (1989) Long, smooth hair sensilla on the spider leg coxa: sensory physiology, central projection pattern, and proprioceptive function (Arachnida, Araneida). Zoomorphology 109:97–102Google Scholar
  14. Elias MS, Evans PD (1983) Histamine in the insect nervous system: distribution, synthesis and metabolism. J Neurochem 41:562–568Google Scholar
  15. Elias MS, Evans PD (1984) Autoradiographic localization of 3H-histamine accumulation in the visual system of the locust. Cell Tissue Res 238:105–112Google Scholar
  16. Elste A, Koester J, Shapiro E, Panula P, Schwartz JH (1990) Identification of histaminergic neurons in Aplysia. J Neurophysiol 64:736–744Google Scholar
  17. Gronenberg W (1989) Anatomical and physiological observations on the organization of mechanoreceptors and local interneurons in the central nervous system of the wandering spider Cupiennius salei. Cell Tissue Res 258:163–175Google Scholar
  18. Gronenberg W (1990) The organization of plurisegmental mechanosensitive interneurons in the central nervous system of the wandering spider Cupiennius salei. Cell Tissue Res 260:49–61Google Scholar
  19. Gupta AP (1987) Evolutionary trends in the central and mushroom bodies of the arthropod brain. A dilemma. In: AP Gupta (ed) Arthropod brain. Wiley, New York Singapore, pp 27–42Google Scholar
  20. Hanström B (1928) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere unter Berücksichtigung seiner Funktion. Springer, BerlinGoogle Scholar
  21. Hardie RC (1987) Is histamine a neurotransmitter in insect photoreceptors? J Comp Physiol [A] 161:201–213Google Scholar
  22. Hardie RC (1989) A histamine-activated chloride channel involved in neurotransmission at a photoreceptor synapse. Nature 339:704–706Google Scholar
  23. Holmgren N (1916) Zur vergleichenden Anatomie des Gehirns von Polychaeten, Onychophoren, Xiphosuren, Arachniden, Crustaceen, Myriapoden und Insekten. Kungl Svenska Vetenskapskad Handlingar 56:1–290Google Scholar
  24. Homberg U, Hildebrand JG (1991) Histamine-immunoreactive neurons in the midbrain and suboesophageal ganglion of the sphinx moth Manduca sexta. J Comp Neurol 307:647–657Google Scholar
  25. Hough LB (1988) Cellular localization and possible functions for brain histamine: recent progress. Prog Neurobiol 30:469–505Google Scholar
  26. Itowi N, Yamatodani A, Kiyono S, Hiraiwa ML, Wada H (1991) Effect of histamine depletion on the circadian amplitude of the sleep-wakefulness cycle. Physiol Behav 49:643–641Google Scholar
  27. Kravitz EA (1988) Hormonal control of behavior: amines and the biasing of behavioral output in lobster. Science 241:1775–1781Google Scholar
  28. Lin JT, Toh Y, Mizunami M, Tateda H (1990) Putative neurotransmitter in the ocellar neuropil of American cockroaches. Zool Sci 7:593–603Google Scholar
  29. McCaman RE, Weinreich D (1985) Histaminergic synaptic transmission in the cerebral ganglion of Aplysia. Neurophysiology 53:1016–1037Google Scholar
  30. McClintock T, Ache BW (1989) Histamine directly gates a chloride channel in lobster olfactory receptor neurons. Proc Natl Acad Sci USA 86:8137–8141Google Scholar
  31. Melamed J, Trujillo-Cenoz O (1966) The fine structure of the visual system of Lycosa (Araneae: Lycosidae). Part I. Retina and optic nerve. Z Zellforsch 74:12–31Google Scholar
  32. Milde JJ, Seyfarth EA (1988) Tactile hairs and leg reflexes in wandering spiders: physiological and anatomical correlates of reflex activity in the leg ganglia. J Comp Physiol [A] 162:623–631Google Scholar
  33. Mulloney B, Hall WM (1991) Neurons with histamine-like immunoreactivity in the segmental and stomatogastric nervous system of the crayfish Pacifastacus leniusculus and the lobster Homarus americanus. Cell Tissue Res 266:197–207Google Scholar
  34. Nässel DR, Holmquist MH, Hardie RC, Håkanson R, Sundler F (1988) Histamine like immunoreactivity in photoreceptors of the compound eyes and ocelli of the flies Calliphora erythrocephala and Musca domestica. Cell Tissue Res 253:639–646Google Scholar
  35. Nässel DR, Pirvola U, Panula P (1990) Histamine-like immunoreactive neurons innervating putative neurohaemal areas and central neuropil in the thoraco-abdominal ganglia of the flies Drosophila and Calliphora. J Comp Neurol 297:525–536Google Scholar
  36. Oberdorfer MD (1977) The neural organization of the first optic ganglion of the principal eyes of jumping spiders (Salticidae). J Comp Neurol 174:95–118Google Scholar
  37. Orona E, Battelle BA, Ache BW (1990) Immunohistochemical and biochemical evidence for the putative inhibitory neurotransmitters histamine and GABA in lobster olfactory lobes. J Comp Neurol 294:633–646Google Scholar
  38. Panula P, Häppölä O, Airaksinen MS, Auvinen MS, Virkamäki A (1988) Carbodiimide as a tissue fixative in histamine immunohistochemistry and its application to developmental biology. J Histochem Cytochem 36:259–269Google Scholar
  39. Pasztor VM, Bush BMH (1987) Peripheral modulation of mechanosensitivity in primary afferent neurons. Nature 326:793–795Google Scholar
  40. Pirvola U, Tuomisto L, Yamatodani A, Panula P (1988) Distribution of histamine in the cockroach brain and visual system: an immunocytochemical and biochemical study. J Comp Neurol 276:514–526Google Scholar
  41. Pollack I, Hofbauer A (1991) Histamine-like immunoreactivity in the visual system and brain of Drosophila melanogaster. Cell Tissue Res 266:391–396Google Scholar
  42. Schlemermeyer E, Schütte M, Ammermüller J (1989) Immunohistochemical and electrophysiological evidence that locust ocellar photoreceptors contain and release histamine. Neurosci Lett 99:73–78Google Scholar
  43. Schmid A, Sperk G, Reiter H (1992) Quantitative determination of neuroactive substances in the CNS of the spider Cupiennius salei Keys. Comp Biochem Physiol (C) 102:447–450Google Scholar
  44. Simmons PJ, Hardie RC (1988) Evidence that histamine is a neurotransmitter of photo-receptors in the locust ocellus. J Exp Biol 138:205–219Google Scholar
  45. Skiebe P, Corrette BJ, Wiese K (1990) Evidence that histamine is the inhibitory transmitter of the auditory interneuron ON1 of crickets. Neurosci Lett 116:361–366Google Scholar
  46. Strausfeld NJ, Barth FG (1993) Two visual systems in one brain: neuropils serving the secondary eyes of the spider Cupiennius salei. J Comp Neurol 328:43–62Google Scholar
  47. Strausfeld NJ, Weltzien P, Barth FG (1993) Two visual systems in one brain: neuropils serving the principal eyes of the spider Cupiennius salei. J Comp Neurol 328:63–75Google Scholar
  48. Trujillo-Cenoz O, Melamed J (1967) The fine structure of the visual system of Lycosa (Araneae: Lycosidae) Part II. Primary visual centers. Z Zellforsch 76:377–388Google Scholar
  49. Wada H, Inagaki N, Yamatodani A, Watanabe T (1991) Is the histaminergic neuron system a regulatory center for whole-brain activity? Trends Neurosci 14:415–418Google Scholar
  50. Weinreich D (1977) Synaptic responses mediated by identified histamine-containing neurons. Nature 267:854–856Google Scholar
  51. Weinreich D, Weiner C, McCaman R (1975) Endogenous levels of histamine in single neurons isolated from CNS of Aplysia californica. Brain Res 84:341–345Google Scholar
  52. Wikgren M, Reuter M, Gustafsson MKS, Lindroos P (1990) Immunocytochemical localization of histamine in flatworms. Cell Tissue Res 260:479–484Google Scholar
  53. Yamashita S, Tateda H (1981) Efferent neural control in the eyes of orb weaving spiders. J Comp Physiol [A] 143:477–483Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • Axel Schmid
    • 1
  • Matthis Duncker
    • 1
  1. 1.Institut für ZoologieUniversität WienWienAustria

Personalised recommendations