Skip to main content
Log in

Patterns and projections of crustacean cardioactive-peptide-immunoreactice neurones of the terminal ganglion of crayfish

  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

Three distinct clusters of crustacean cardioactive-peptide-immunoreactive neurones occur in the terminal abdominal ganglion of the crayfish species Orconectes limosus, Astacus leptodactylus, Astacus astacus and Procambarus clarkii, as revealed by immunocytochemistry of whole-mount preparations and sections. They exhibit similar topology and projection patterns in all four studied species. An anterior ventral lateral and a posterior lateral cluster contain one small, strongly stained perikaryon and two large, less intensely stained perikarya, each showing contralateral projections. A posterior medial lateral cluster of up to six cells also contains these two types of perikarya. Whereas the small type perikarya belong to putative interneurones, the large type perikarya give rise to extensive neurohaemal plexuses in perineural sheaths of the third roots of the fifth abdominal ganglia, the connectives, the dorsal telson nerves, the ganglion itself, its roots and arteriolar supply. Thin fibres from these plexuses reach newly discovered putative neurohaemal areas around the hindgut and anus via the intestinal and the anal nerves, and directly innervate the phasic telson musculature. A comparison with earlier investigations of motoneurones and segmentation indicates that these three cell groups containing putative neurosecretory neurones may be members of at least three neuromeres in this ganglion. Crustacean cardioactive peptide released from these neurones may participate in the neurohumoral and modulatory control of different neuronal and muscle targets, thereby exceeding its previously established hindgut and heart excitatory effects.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Abbreviations

AG :

abdominal ganglion

adpl :

arteria dorsalis pleica

Ala :

arreria lateralis abdominalis

Asub :

arteria subneuralis

CCAP :

crustacean cardioactive peptide

CNS :

central nervous system

IR :

immunoreactive

LG :

lateral giant axon

LTr :

lateral tract

MDT :

medial dorsal tract

MG :

medial giant axon

M Tr :

medial tract

mcan :

musculus compressor ani

mfltp :

museulus flexor telsonos posterior

nan :

nervus ani (AG6 N5)

nant :

nervus anterior (AG6 N1, N2)

nia :

nervus intestinal anterior

nin :

nervus intestinalis (AG6 N7)

nip :

nervus intestinalis posterior

nteld :

nervus telsonos dorsalis (AG6 N6)

nielv :

nervus telsonos ventralis (AG6 N4)

nur :

nervus uropedalis (AG6 N3)

nven :

nervus ventralis (AG5 N3)

PIR :

peri-intestinal ring

PTF :

posterior telson flexor

VLT :

ventral lateral tract

VMT :

ventral medial tract

VNC :

ventral nerve cord

VIF :

ventral telson flexor

AVLC, PLC, PMLC :

anterior ventral lateral, posterior lateral, posterior medial lateral CCAP-immunoreactive cell cluster

A6AVC, A7AVC :

anterior ventral commissures

A7DCI :

dorsal commissure I

A7PVC :

posterior ventral commissure

A7SCII :

sensory commissure II

A7VCII, A7VCIII :

ventral commissures II and III of the sixth (A6) and seventh (A7) abdominal neuromer

References

  • Alexandrowicz JS (1909) Zur Kenntnis des sympatischen Nerven-systems bei Crustaceen. Jena Z Naturwiss 45:395–444

    Google Scholar 

  • Altman JS, Tyrer NM (1980) Filling selected neurons with cobalt through cut axons. In: Strausfeld NJ, Miller TA (eds) Neuroanatomical techniques. Insect nervous system. Springer, New York Heidelberg Berlin, pp 373–402

    Google Scholar 

  • Audehm U, Dircksen H, Keller R (1991) Projections of crustacean cardioactive peptide (CCAP)-immunoreactive neurons of the sixth abdominal ganglion of crayfishes. Gen Comp Endocrinol 82:284

    Google Scholar 

  • Baumann H (1918) Das Gefäßsystem von Astacus fluviatilis (Potamobius astacus L.). Z Wiss Zool 118:246–312

    Google Scholar 

  • Bishop CA, Wine JJ, O'Shea M (1984) Neuropeptide proctolin in postural motoneurones of the crayfish. J Neurosci 4:2001–2009

    Google Scholar 

  • Bishop CA, Wine JJ, Nagy F, O'Shea M (1987) Physiological consequences of a peptide cotransmitter in a crayfish nerve-muscle preparation. J Neurosci 7:1769–1779

    Google Scholar 

  • Boer HH, Schot LPC, Roubos EW, Maat A ter, Lodder JC, Reichelt D, Swaab DF (1979) ACTH-like immunoreactivity in two electronically coupled giant neurons in the pond snail Lymnea stagnalis. Cell Tissue Res 202:231–240

    Google Scholar 

  • Breidbach O, Dircksen H (1991) Crustacean cardioactive peptide-immunoreactive neurons in the ventral nerve cord and the brain of the meal beetle Tenebrio molitor during postembryonic development. Cell Tissue Res 265:129–144

    Google Scholar 

  • Breidbach O, Kutsch W (1990) Structural homology of identified motoneurones in larval and adult stages of hemi-and holometabolous insects. J Comp Neurol 297:392–409

    Google Scholar 

  • Brown SK, Sherwood DN (1981) Vascularization of the crayfish abdominal cord. J Comp Physiol 143:93–101

    Google Scholar 

  • Dircksen H, Breidbach O (1991a) Crustacean cardioactive peptide (CCAP)-immunoreactive neurons in the central and peripheral nervous system of the locust Locusta migratoria and the metamorphosing meal beetle Tenebrio molitor. Gen Comp Endocrinol 82:286

    Google Scholar 

  • Dircksen H, Breidbach O (1991b) Peripheral projection sites of crustacean cardioactive peptide (CCAP)-immunoreactive neurons of the central nervous system of the locust Locusta migratoria and the metamorphosing meal beetle Tenebrio molitor. In: Elsner N, Penzlin H (eds) Synapse-transmission-modulation. Thieme, Stuttgart New York, p 14

    Google Scholar 

  • Dircksen H, Keller R (1988) Immunocytochemical localisation of CCAP, a novel crustacean cardioactive peptide, in the nervous system of the shore crab, Carcinus meanas L. Cell Tissue Res 254:347–360

    Google Scholar 

  • Dircksen H, Müller A, Keller R (1991) Crustacean cardioactive peptide in the nervous system of the locust, Locusta migratoria: an immunocytochemical study on the ventral nerve cord and peripheral innervation. Cell Tissue Res 263:439–457

    Google Scholar 

  • Dumont JPC, Wine JJ (1987) The telson flexor neuromuscular system of the crayfish. I. Homology with the fast flexor system. J Exp Biol 127:249–277

    Google Scholar 

  • Elekes F, Florey E, Cahill MA (1988) Morphology and central synaptic connections of the efferent neurons innervating the crayfish hindgut. Cell Tissue Res 254:369–379

    Google Scholar 

  • Hagiwara G, Wheat G (1983) Cited in Reichert et al. (1983), below

  • Homberg U (1991) Neuroarchitecture of the central complex in the brain of the locust Schistocerca gregaria and S. americana as revealed by serotonin immunocytochemistry. J Comp Neurol 303:245–254

    Google Scholar 

  • Keim W (1915) Das Nervensystem von Astacus fluviatilis (Potamobius astacus L.). Z Wiss Zool 113:485–545

    Google Scholar 

  • Kobierski LA, Beltz BS, Trimmer BA, Kravitz EA (1987) FMRFamide-like peptides of Homarus americanus: distribution, immunocytochemical mapping and ultrastructural localisation in terminal varicosities. J Comp Neurol 266:1–15

    Google Scholar 

  • Kondoh Y, Hisada M (1986) Neuroanatomy of the terminal (sixth abdominal) ganglion of the crayfish, Procambarus clarkii (Girard). Cell Tissue Res 243:273–288

    Google Scholar 

  • Kondoh Y, Hisada M (1987) The topological organization of primary efferents in the terminal ganglion of crayfish, Procambarus clarkii. Cell Tissue Res 247:17–24

    Google Scholar 

  • Kornberg T (1981) engrailed: A gene controlling compartment and segment formation in Drosophila. Proc Natl Acad Sci USA 78:1095–1099

    Google Scholar 

  • Larimer JL, Kennedy D (1969) Innervation patterns of fast and slow muscle in the uropods of crayfish. J Exp Biol 51:119–133

    Google Scholar 

  • Leise E, Mulloney B (1986) The osmium-ethyl gallate procedure is superior to silver impregnations for mapping neuronal pathways. Brain Res 367:265–272

    Google Scholar 

  • Mittenthal JE, Wine JJ (1978) Segmental homology and variation in flexor motoneurons of the crayfish abdomen. J Comp Neurol 117:311–334

    Google Scholar 

  • Muramoto A (1971) The afferent nerve response of the movement receptor around the anal region of the crayfish. J Fac Sci Hokkaido Univ Ser VI Zool 17:545–563

    Google Scholar 

  • Muramoto A (1977) Neural control of rhythmic anal contraction in the crayfish. Comp Biochem Physiol [A] 56:551–557

    Google Scholar 

  • Orlov J (1926) Die Innervation des Darmes des Flusskrebses. Z Mikrosk Anat Forsch 4:101–149

    Google Scholar 

  • Patel NH, Marin-Blanco E, Coleman KG, Poole SJ, Ellis MC, Kornberg TB, Goodman CG (1989a) Expression of engrailed proteins in arthropods, annelids, and chordates. Cell 58:955–968

    Google Scholar 

  • Patel NH, Kornberg TB, Goodman CS (1989b) Expression of engrailed during segmentation in grasshopper and crayfish. Development 107:201–212

    Google Scholar 

  • Paul DH (1989) A neurophylogenist's view of decapod Crustacea. Bull Mar Sci 45:487–504

    Google Scholar 

  • Paul DH, Then AM, Magnuson DS (1985) Evolution of the telson neuromusculature in decapod Crustacea. Biol Bull 168:106–124

    Google Scholar 

  • Reichert H, Plummer MR, Wine JJ (1983) Lateral inhibition mediated by a non-spiking interneuron: circuit properties and consequences for behavior. J Physiol (Paris) 78:786–792

    Google Scholar 

  • Sandeman DC (1982) Organization of the central nervous system. In: Bliss DE (ed) The biology of Crustacea. Academic Press, New York, pp 1–61

    Google Scholar 

  • Schmidt W (1915) Die Muskulatur von Astacus fluviatilis (Potamobius astacus L.). Z Wiss Zool 113:166–251

    Google Scholar 

  • Selverston AJ, Remler MP (1972) Neural geometry and activation of crayfish fast flexor motoneurons. J Neurophysiol 35:797–814

    Google Scholar 

  • Stangier J (1991) Biological effects of crustacean cardioactive peptide (CCAP), a putative neurohormone/neurotransmitter from crustacean pericardial organs. In: Stefano GB, Florey E (eds) Comparative aspects of neuropeptide function. Manchester University Press, Manchester New York, pp 201–210

    Google Scholar 

  • Stangier J, Keller R (1990) Occurrence of the crustacean cardioactive peptide (CCAP) in the nervous system of the crayfish Orconectes limosus. In: Wiese K, Krenz WD, Tautz J, Reichert H, Molloney B (eds) Frontiers in crustacean neurobiology. Birkhäuser, Basel, pp 394–400

    Google Scholar 

  • Stangier J, Hilbich C, Beyreuther K, Keller R (1987) Unusual cardioactive peptide (CCAP) from pericardial organs of the shore crab Carcinus maenas. Proc Natl Acad Sci USA 84:575–579

    Google Scholar 

  • Stangier J, Hilbich C, Keller R (1989) Occurrence of crustacean cardioactive peptide (CCAP) in the nervous system of an insect, Locusta migratoria. J Comp Physiol [B] 159:5–11

    Google Scholar 

  • Stefanini M, De Martino C, Zamboni L (1967) Fixation of ejaculated spermatozoa for electron microscopy. Nature 216:173–174

    Google Scholar 

  • Stoll E (1925) Über den Bau des Zentralnervensystems von Astacus fluviatilis (Potamobius astacus L.). Z Wiss Zool 126:145–179

    Google Scholar 

  • Trube A, Dircksen H, Keller R (1991a) CCAP-(crustacean cardioactive peptide-) immunoreactive structures in the central nervous system of crayfishes. Gen Comp Endocrinol 82:284

    Google Scholar 

  • Trube A, Audehm U, Dircksen H (1991b) Crustacean cardioactive peptide-immunoreactive structures in the nervous system of crayfish. In: Elsner N, Penzlin H (eds) Synapse-transmission-modulation. Thieme, Stuttgart New York, p 408

    Google Scholar 

  • Van Harreveld A (1936) A physiological solution for freshwater crustaceans. Proc Soc Exp Biol Med 34:428–432

    Google Scholar 

  • Wine JJ, Mittenthal JE, Kennedy D (1974) The structure of tonic flexor motoneurons in the crayfish abdominal ganglia. J Comp Physiol 93:313–335

    Google Scholar 

  • Winlow W, Laverack MS (1972a) The control of hindgut motility in the lobster, Homarus gammarus (L.). I. Analysis of hindgut movements and receptor activity. Mar Behav Physiol 1:1–27

    Google Scholar 

  • Winlow W, Laverack MS (1972b) The control of hindgut motility in the lobster, Homarus gammarus (L.). III. Structure of the sixth abdominal ganglion (6 A.G.) and associated ablation and microelectrode studies. Mar Behav Physiol 1:93–121

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Audebm, U., Trube, A. & Dircksen, H. Patterns and projections of crustacean cardioactive-peptide-immunoreactice neurones of the terminal ganglion of crayfish. Cell Tissue Res 272, 473–485 (1993). https://doi.org/10.1007/BF00318553

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00318553

Key words

Navigation