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Journal of Comparative Physiology A

, Volume 178, Issue 5, pp 579–604 | Cite as

Processing of antennular input in the brain of the spiny lobster, Panulirus argus

I. Non-olfactory chemosensory and mechanosensory pathway of the lateral and median antennular neuropils
  • M. Schmidt
  • B. W. Ache
Original Paper

Abstract

Neurons in the brain of the spiny lobster that respond to chemical and mechanical stimulation of the antennule (antenna I) were recorded and stained intracellularly. Described here are neurons that do not arborize in the olfactory and accessory lobes of the deutocerebrum, but rather primarily target the lateral and/or the median antennular neuropils of the deutocerebrum. Some of the neurons also extend into the antennal and tegumentary neuropils of the tritocerebrum and the neuropils of the median protocerebrum. Included are antennular sensory afferents, antennular motoneurons, projection neurons descending from the central brain, projection neurons ascending from the central brain and projection neurons descending from the eyestalk ganglia. Collectively, these neurons consitutute a novel antennular sensory pathway that is parallel to and independent of the antennular olfactory pathway. The novel pathway integrates mechanosensory and non-olfactory chemosensory information in the lateral and/or the median antennular neuropils, which also serve as lower motor centers of the antennule. Division of the arthropod deutocerebrum into two, functionally distinct chemosensory pathways may reflect differences in how chemosensory information is processed that is fundamental to understanding the origin of the sense of smell.

Key words

Crustacean Chemoreception Mechanoreception Deutocerebrum Motoneurons Projection neurons 

Abbreviations

AC

anterior cluster (cluster 6, 7)

AL

ccessory lobe

aMC

anterior subcluster of medial cluster (cluster 9)

AnN

antenna II (antennal) neuropil

AINv

main antenna I (antennular) nerve

AINM

antenna I (antennular) motor nerve

AIINv

main antenna II (antennal) nerve

AIINM

antenna II (antennal) motor nerve

DCN

deutocerbral commissure neuropil

dDLC

dorsal subcluster of dorsal lateral cluster (cluster 15)

dDUMC

dorsal subcluster of dorsal unpaired median cluster (cluster 17)

DUGC

dorsal unpaired globuli cell cluster

LAN

lateral antenna I (antennular) neuropil

IDUMC

lateral subcluster of dorsal unpaired median cluster (cluster 16)

LF

lateral flagellum of antenna I (antennule)

MAN

median antenna I (antennular) neuropil

mDUMC

median subcluster of dorsal unpaired median cluster (cluster 17)

MF

medial flagellum of antenna I (antennule)

MPN

anterior and posterior median protocerebral neuropils

OC

oesophageal connective

OCM

oculomotor nerve

OL

olfactory lobe

PT

protocerebral tract

TN

tegumentary neuropil

TNv

tegumentary nerve

vDLC

ventral subcluster of dorsal lateral cluster (cluster 14)

VPALC

ventral paired anterolateral cluster (cluster 8)

VUMC

ventral unpaired median cluster (cluster 13)

AMP

adenosine monophosphate

ASC

L-ascorbic acid

ASW

artificial sea water

BET

betaine HCl

M1

mixture 1 (TAU, BET, ASC, NH4)

M2

mixture 2 (SUC, NIC, AMP, TMA)

M3

mixture 3 (M1, M2, PRO)

NH4

NH4Cl

NIC

nicotinic acid

PRO

L-proline

SUC

sucrose

TAU

taurine

TM

TetraMarin extract

TMA

trimethylamine HCl

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References

  1. Ache BW, Fuzessery ZM (1979) Chemosensory integration in the spiny lobster: Ascending activity in the olfactory-globular tract. J Comp Physiol 130: 63–69Google Scholar
  2. Arbas EA, Humphreys CJ, Ache BW (1988) Morphology and physiological properties of interneurons in the olfactory midbrain of the crayfish. J Comp Physiol A 164: 231–241Google Scholar
  3. Blaustein DN, Derby CD, Simmons RB, Beall AC (1988) Structure of the brain and medulla terminalis of the spiny lobster Panulirus argus and the crayfish Procambarus clarkii, with an emphasis on olfactory centers. J Crust Biol 8: 493–519Google Scholar
  4. Derby CD, Ache BW (1984) Quality coding of a complex odorant in an invertebrate. J Neurophysiol 51(5): 906–924Google Scholar
  5. Derby CD, Blaustein DN (1988) Morphological and physiological characterization of individual olfactory interneurons connecting the brain and eyestalk ganglia of the crayfish. J Comp Physiol A 163: 777–794Google Scholar
  6. Derby CD, Hamilton KA, Ache BW (1984) Processing of olfactory information at three neuronal levels in the spiny lobster. Brain Res 300: 311–319Google Scholar
  7. Derby CD, Ache BW, Kennel EW (1985) Mixture suppression in olfaction: electrophysiological evaluation of the contribution of peripheral and central neural components. Chem Senses 10: 301–316Google Scholar
  8. Fraser PJ (1974) Interneurones in crab connectives (Carcinus maenas (L.)): directional statocyst fibres. J Exp Biol 61: 615–628Google Scholar
  9. Fraser PJ, Sandeman DC (1975) Effects of angular and linear accelerations on semicircular canal interneurons of the crab Scylla serrata. J Comp Physiol 96: 205–221Google Scholar
  10. Fuzessery ZM (1978) Quantitative stimulation of antennular chemoreceptors of the spiny lobster, Panulirus argus. Comp Biochem Physiol 60: 303–308Google Scholar
  11. Glantz RM, Kirk M, Viancour T (1981) Interneurons in the crayfish brain: The relationship between dendrite location and afferent input. J Neurobiol 12: 311–328PubMedGoogle Scholar
  12. Gleeson RA (1982) Morphological and behavioral identification of the sensory structures mediating pheromone reception in the blue crab, Callinectes sapidus. Biol Bull 163: 162–171Google Scholar
  13. Grünert U, Ache BW (1988) Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus. Cell Tissue Res 251: 95–103Google Scholar
  14. Hamilton KA, Ache BW (1983) Olfactory excitation of interneurons in the brain of the spiny lobster. J Comp Physiol 150: 129–140Google Scholar
  15. Helm F (1928) Vergleichend-anatomische Untersuchungen über das Gehirn, insbesondere das “Antennalganglion” der Dekapoden. Z Morph Ökol Tiere 12: 70–134Google Scholar
  16. Horikawa K, Armstrong WE (1988) A versatile means of intracellular labeling: injection of biocytin and its detection with avidin conjugates. J Neurosci Methods 25: 1–11Google Scholar
  17. Kouyama N, Shimozawa T (1982) The structure of a hair mechanoreceptor in the antennule of crayfish (Crustacea). Cell Tissue Res 226: 565–578Google Scholar
  18. Laverack MS (1964) The antennular sense organs of Panulirus argus. Comp Biochem Physiol 13: 301–321Google Scholar
  19. Masson C, Mustaparta H (1990) Chemical information processing in the olfactory system of insects. Physiol Rev 70: 199–245Google Scholar
  20. Maynard DM (1965) Integration in crustacean ganglia. Symp Soc Exp Biol 20: 111–149Google Scholar
  21. Maynard DM, Dingle H (1963) An effect of eyestalk ablation on the antennular function in the spiny lobster, Panulirus argus. Z Vergl Physiol 46: 515–540Google Scholar
  22. Mellon D Jr (1977) Central and peripheral features of crayfish oculomotor organization. In: Hoyle G (ed) Identified neurons and behavior of arthropods. Plenum Press, New York London, pp 149–166Google Scholar
  23. Mellon D Jr, Alones V (1993) Cellular organization and growthrelated plasticity of the crayfish olfactory midbrain. Microsc Res Tech 24: 231–259Google Scholar
  24. Mellon D Jr, Munger SD (1990) Nontopographic projection of olfactory sensory neurons in the crayfish brain. J Comp Neurol 296: 253–262Google Scholar
  25. Mellon D Jr, Alones V, Lawrence MD (1992) Anatomy and fine structure of neurons in the deutocerebral projection pathway of the crayfish olfactory system. J Comp Neurol 321: 93–111Google Scholar
  26. Michel WC, Trapido-Rosenthal HG, Chao ET, Wachowiak M (1993) Stereoselective detection of amino acids by lobster olfactory receptor neurons. J Comp Physiol A 171: 705–712Google Scholar
  27. Nakagawa H, Hisada M (1989) Morphology of descending statocyst interneurons in the crayfish Procambarus clarkii Girard. Cell Tissue Res 255: 539–551Google Scholar
  28. Nakagawa H, Hisada M (1990) A vibration-sensitive descending statocyst interneurone in the crayfish Procambarus clarkii. J Exp Biol 149: 361–378Google Scholar
  29. Nakagawa H, Hisada M (1991) Inhibitory connections underlying the directional sensitivity of the equilibrium system in the crayfish Procambarus clarkii. J Exp Biol 152: 305–312Google Scholar
  30. Nakagawa H, Hisada M (1992) Local spiking interneurons controlling the equilibrium response in the crayfish Procambarus clarkii. J Comp Physiol A 170: 291–302Google Scholar
  31. Neil DM (1982) Compensatory eye movements. In: Sandeman DC, Atwood HL (eds) The biology of Crustacea, vol. 4. Neural integration and behavior. Acad Press, New York London, pp 133–163Google Scholar
  32. Patton ML, Grove RF (1992) The response of statocyst receptors of the lobster, Homarus americanus, to movements of statolith hairs. Comp Biochem Physiol 101A: 249–257Google Scholar
  33. Rospars JP (1988) Structure and development of the insect antennodeutocerebral system. Int J Insect Morphol Embryol 17: 243–294Google Scholar
  34. Roye DB (1975) The physiological basis for pitch-induced antennule movements in the blue crab, Callinectes sapidus. Comp Biochem Physiol 62A: 475–484Google Scholar
  35. Roye DB (1986) The central distribution of movement sensitive afferent fibers from the antennular short hair sensilla of Callinectes sapidus. Mar Behav Physiol 12: 181–196Google Scholar
  36. Roye DB, Dillaman RM (1982) Morphological and physiological characteristics of the antennular short hair sensilla of the blue crab, Callinectes sapidus. Mar Behav Physiol 9: 59–71Google Scholar
  37. Sandeman DC, Denburg JL (1976) The central projections of chemoreceptor axons in the crayfish revealed by axoplasmic transport. Brain Res 115: 492–496Google Scholar
  38. Sandeman DC, Luff SE (1973) The structural organization of glomerular neuropile in the olfactory and accessory lobes of an Australian freshwater crayfish, Cherax destructor. Z Zellforsch 142: 37–61Google Scholar
  39. Sandeman DC, Okajima A (1972) Statocyst-induced eye movements in the crab Scylla serrata. I. The sensory input from the statocyst. J Exp Biol 57: 187–204Google Scholar
  40. Sandeman DC, Okajima A (1973) Statocyst-induced eye movements in the crab Scylla serrata. III. The anatomical projections of sensory and motor neurones and the responses of the motor neurones. J Exp Biol 59: 17–38Google Scholar
  41. Sandeman DC, Sandeman RE (1994) Electrical responses and synaptic connections of giant serotonin-immunoreactive neurons in crayfish olfactory and accessory lobes. J Comp Neurol 341: 130–144Google Scholar
  42. Sandeman D, Sandeman R, Derby C, Schmidt M (1992) Morphology of the brain of crayfish, crabs, and spiny lobsters: A common nomenclature for homologous structures. Biol Bull 183: 304–326Google Scholar
  43. Schmidt M, Ache BW (1992) Antennular projections to the midbrain of the spiny lopbster. II. Sensory innervation of the olfactory lobe. J Comp Neurol 318: 291–303Google Scholar
  44. Schmidt M, Ache BW (1993) Antennular projections to the midbrain of the spiny lopbster. III. Central arborizations of motoneurons. J Comp Neurol 336: 583–594Google Scholar
  45. Schmidt M, Ache BW (1996) Processing of antennular input in the brain of the spiny lobster, Panulirus argus. II. The olfactory pathway. J Comp Physiol AGoogle Scholar
  46. Schmidt M, Orona E, Ache BW (1991) Parallel processing of chemosensory input in the brain of the spiny lobster. Soc Neurosci Abstr 17: 1018Google Scholar
  47. Schmidt M, Van Ekeris L, Ache BW (1992) Antennular projections to the midbrain of the spiny lobster. I. Sensory innervation of the lateral and medial antennular neuropils. J Comp Neurol 318: 277–290Google Scholar
  48. Silvey GE, Sandeman DC (1976) Integration between statocyst sensory neurons and oculomotor neurons in the crab Scylla serrata. III. The sensory to motor synapse. J Comp Physiol 108: 53–65Google Scholar
  49. Silvey GE, Dunn PA, Sandeman DC (1976) Integration between statocyst sensory neurons and oculomotor neurons in the crab Scylla serrata. II. The thread hair sensory receptors. J Comp Physiol 108: 45–52Google Scholar
  50. Snow PJ (1973) The antennular activities of the hermit crab, Pagurus a/askensis (Benedikt). J Exp Biol 58: 745–765Google Scholar
  51. Snow PJ (1974) Surface structures of the antennular flagella of the hermit crab Pagurus alaskensis (Benedict): A light and scanning electron microscopy study. J Morphol 144: 195–216Google Scholar
  52. Spencer M (1986) The innervation and chemical sensitivity of single aesthetasc hairs. J Comp Physiol A 158: 59–68Google Scholar
  53. Spencer M, Linberg KA (1986) Ultrastructure of aesthetasc innervation and external morphology of the lateral antennule setae of the spiny lobster Panulirus interruptus (Randall). Cell Tissue Res 245: 69–80Google Scholar
  54. Tautz J (1987) Interneurons in the tritocerebrum of the crayfish. Brain Res 407: 230–239Google Scholar
  55. Tautz J, Erber J, Ache B (1986) Chemosensitive interneurons ascend in the optic nerve in the crayfish. Naturwissenschaften 73: 154–155Google Scholar
  56. Tierney AJ, Voigt R, Atema J (1988) Response properties of chemoreceptors from the medial antennular filament of the lobster Homarus americanus. Biol Bull 174: 364–372Google Scholar
  57. Wachowiak M, Ache BW (1994) Morphology and physiology of olfactory projection neurons in the spiny lobster: J Comp Physiol A 175: 35–48Google Scholar
  58. Wyse GA, Maynard DM (1965) Joint receptors in the antennule of Panulirus argus Latreille. J Exp Biol 42: 521–535Google Scholar
  59. Yoshino M, Kondoh Y, Hisada M (1983) Projection of statocyst sensory neurons associated with crescent hairs in the crayfish Procambarus clarkii Girard. Cell Tissue Res 230: 37–48Google Scholar

Copyright information

© Springer-Verlag 1996

Authors and Affiliations

  • M. Schmidt
    • 1
    • 2
  • B. W. Ache
    • 2
    • 3
  1. 1.Institut für Biologie, TU BerlinBerlinGermany
  2. 2.Whitney Laboratory, University of FloridaSt. AugustineUSA
  3. 3.Departments of Zoology and Neuroscience, University of FloridaSt. AugustineUSA

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