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

II. The olfactory pathway

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Abstract

Neurons in the olfactory deutocerebrum of the spiny lobster, Panulirus argus, were recorded intracellularly and filled with biocytin. Recorded neurons arborized in the olfactory lobe (OL), a glomerular neuropil innervated by olfactory and some presumptive mechanosensory antennular afferents. The neurons responded to chemosensory input from the lateral antennular flagellum bearing the olfactory sensilla but not the medial flagellum bearing many non-olfactory chemosensory sensilla. Many neurons received additional mechanosensory input. Thus the OL integrates specifically olfactory with mechanosensory input. OL neurons had multiglomerular arborizations restricted to one or two of the three horizontal layers of the columnar glomeruli. OL local interneurons comprised “core” neurons with tree-like neurites and terminals in the base of the glomeruli and “rim” neurons with neurites surrounding the OL and terminals in the cap/subcap. The somata of OL local interneurons lay in the medial soma cluster (100000 somata). OL projection neurons arborized in the base of the glomeruli and ascended via the olfactory glomerular tract to the lateral protocerebrum. A parallel projection pathway is constituted by projection neurons of the accessory lobe, a glomerular neuropil without afferent innervation but intimate links to the OL. The projection neuron somata constituted the lateral soma cluster (200000 somata).

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Abbreviations

AC :

anterior cluster (cluster 6,7)

AL :

accessory lobe

aMC :

anterior subcluster of medial cluster (cluster 9)

A lNv:

main antenna I (antennular) nerve

A lNM:

antenna I (antennular) motor nerve

A llNv:

main antenna II (antennal) nerve

CB :

central body

CL :

central layer of accessory lobe

DC :

deutocerebral commissure

DCN :

deutocerebral commissure neuropil

dDUMC :

dorsal subcluster of dorsal unpaired median cluster (cluster 17)

dMC :

dorsal subcluster of medial cluster (cluster 11)

dVPALC :

dorsal subcluster of ventral paired anterolateral cluster (cluster 8) G glomerulus

IDUMC :

lateral subcluster of dorsal unpaired median cluster (cluster 16)

LC :

lateral cluster (cluster 10)

LF :

lateral flagellum of antenna I (antennule)

LL :

lateral layer of accessory lobe

MF :

medial flagellum of antenna I (antennule)

ML :

medial layer of accessory lobe

MPN :

anterior and posterior median protocerebral neuropils

OGT :

olfactory globular tract

OGTN :

olfactory globular tract neuropil

OL :

olfactory lobe

OLALT :

olfactory lobe-accessory lobe tract

PB :

protocerebral bridge

pMC :

posterior subcluster of medial cluster (cluster 9)

PT :

protocerebral tract

TNv :

tegumentary nerve

VPMC :

ventral paired medial cluster (cluster 12)

VUMC :

ventral unpaired medial cluster (cluster 13)

vVPALC :

ventral subcluster of ventral paired anterolateral cluster (cluster 8)

ASW :

artificial sea water

M3 :

mixture 3

PRO :

L-proline

TM :

TetraMarin extract

References

  • 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: 231–241

    Google Scholar 

  • Bauchau AG, Passelecq-Gérin (1984) Ultrastructure des aesthetascs du crabe Carcinus maenas, L. Cahiers de Biologie Marine 25: 333–341

    Google Scholar 

  • 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: 493–519

    Google Scholar 

  • Boeckh J, Ernst KD, Sass H, Waldow U (1984) Anatomical and physiological characteristics of individual neurons in the central antennal pathway of insects. J Insect Physiol 30: 15–26

    Google Scholar 

  • Chambille I, Rospars JP (1985) Neurons and identified glomeruli of antennal lobes during postembryonic development in the cockroach Blaberus craniifer Burm. (Dictyoptera: Blaberidae). Int J Insect Morphol Embryol 14: 203–226

    Google Scholar 

  • Christensen TA, Hildebrand JG (1987) Male-specific, sex pheromone-selective projection neurons in the antennal lobes of the moth Manduca sexta. J Comp Physiol A 160: 553–569

    CAS  PubMed  Google Scholar 

  • Christensen TA, Waldrop BR, Harrow ID, Hildebrand JG (1993) Eocal interneurons and information processing in the olfactory glomeruli of the moth Manduca sexta. J Comp Physiol A 173: 385–399

    Google Scholar 

  • Devine DV, Atema J (1982) Function of chemoreceptor organs in spatial orientation of the lobster, Homarus americanus: differences and overlap. Biol Bull 163: 144–153

    Google Scholar 

  • Diebel CE, Ache BW (1993) Whole cell recordings from interneurons in the olfactory pathway of the CNS in the spiny lobster. Chem Senses 18: 544–545

    Google Scholar 

  • Ernst KD, Boeckh J (1983) A neuroanatomical study on the organization of the central antennal pathways in insects. III. Neuroanatomical characterization of physiologically defined response types of deutocerebral neurons in Periplaneta americana. Cell Tissue Res 229: 1–22

    Google Scholar 

  • Flanagan D, Mercer AR (1989) Morphology and response characteristics of neurones in the deutocerebrum of the brain of the honeybee Apis mellifera. J Comp Physiol A 164: 483–494

    Google Scholar 

  • Fonta C, Sun X-J, Masson C (1993) Morphology and spatial distribution of bee antennal lobe interneurones responsive to odours. Chem Senses 18: 101–119

    Google Scholar 

  • Fuzessery ZM (1978) Quantitative stimulation of antennular chemoreceptors of the spiny lobster, Panulirus argus. Comp Biochem Physiol 60: 303–308

    Google Scholar 

  • Grünert U, Ache BW (1988) Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster, Panulirus argus. Cell Tissue Res 251: 95–103

    Google Scholar 

  • Hanström B (1968) Vergleichende Anatomie des Nervensystems der wirbellosen Tiere. A. Asher & Co., Amsterdam

    Google Scholar 

  • Helluy S, Sandeman R, Beltz B, Sandeman D (1993) Comparative brain ontogeny of the crayfish and clawed lobster: Implications of direct and larval development. J Comp Neurol 335: 343–354

    Google Scholar 

  • Helm F (1928) Vergleichend-anatomische Untersuchungen über das Gehirn, insbesondere das “Antennalganglion” der Dekapoden. Z Morph Ökol Tiere 12: 70–134

    Google Scholar 

  • Homberg U (1984) Processing of antennal information in extrinsic mushroom body neurons of the bee brain. J Comp Physiol A 154: 825–836

    Google Scholar 

  • Homberg U, Christensen TA, Hildebrand JG (1989) Structure and function of the deutocerebrum in insects. Annu Rev Entomol 34: 477–501

    Google Scholar 

  • Johansson KUI (1991) Identification of different types of serotoninlike immunoreactive olfactory interneurons in four infraorders of decapod crustaceans. Cell Tissue Res 264: 357–362

    Google Scholar 

  • Kanzaki R, Arbas EA, Strausfeld NJ, Hildebrand JG (1989) Physiology and morphology of projection neurons in the antennal lobe of the male moth Manduca sexta. J Comp Physiol A 165: 427–453

    Google Scholar 

  • Koontz MA, Schneider D (1987) Sexual dimorphism in neuronal projections from the antennae of silk moths (Bombyx mori, Antheraea polyphemus) and the gypsy moth (Lymantria dispar). Cell Tissue Res 249: 39–50

    Google Scholar 

  • Laurent G, Naraghi M (1994) Odorant-induced oscillations in the mushroom bodies of the locust. J Neurosci 14: 2993–3004

    Google Scholar 

  • Laverack MS (1964) The antennular sense organs of Panulirus argus. Comp Biochem Physiol 13: 301–321

    Google Scholar 

  • Laverack MS, Ardill DJ (1965) The innervation of the aesthetasc hairs of Panulirus argus. Quart J MICR Sci 106: 45–60

    Google Scholar 

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

    Google Scholar 

  • Macrides F, Chorover SL (1972) Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175: 84–87

    Google Scholar 

  • Matsumoto SG, Hildebrand JG (1981) Olfactory mechanisms in the moth Manduca sexta: response characteristics and morphology of central neurons in the antennal lobes. Proc R Soc Lond B 213: 249–277

    Google Scholar 

  • Mellon D Jr, Alones V (1993) Cellular organization and growthrelated plasticity of the crayfish olfactory midbrain. Microsc Res Tech 24: 231–259

    Google Scholar 

  • Mellon D Jr, Munger SD (1990) Nontopographic projection of olfactory sensory neurons in the crayfish brain. J Comp Neurol 296: 253–262

    Google Scholar 

  • Mellon D Jr, Alones V, Lawrence MD (1992a) Anatomy and fine structure of neurons in the deutocerebral projection pathway of the crayfish olfactory system. J Comp Neurol 321: 93–111

    Google Scholar 

  • Mellon D Jr, Sandeman DC, Sandeman RE (1992b) Characterization of oscillatory olfactory interneurones in the protocerebrum of the crayfish. J Exp Biol 167: 15–38

    Google Scholar 

  • Orona E, Ache BW (1992) Physiological and pharmacological evidence for histamine as a neurotransmitter in the olfactory CNS of the spiny lobster. Brain Res 590: 136–143

    Google Scholar 

  • Reeder PB, Ache BW (1980) Chemotaxis in the Florida spiny lobster, Panulirus argus. Anim Behav 28: 831–839

    Google Scholar 

  • Sandeman DC, Denburg JL (1976) The central projections of chemoreceptor axons in the crayfish revealed by axoplasmic transport. Brain Res 115: 492–496

    Google Scholar 

  • 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: 37–61

    Google Scholar 

  • Sandeman RE, Sandeman DC (1987) Serotonin-like immunoreactivity of giant olfactory interneurons in the crayfish brain. Brain Res 403: 371–374

    Google Scholar 

  • 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: 130–144

    Google Scholar 

  • Sandeman DC, Sandeman RE, Aitken AR (1988) Atlas of serotonin-containing neurons in the optic lobes and the brain of the crayfish, Cherax destructor. J Comp Neurol 269: 465–478

    Google Scholar 

  • 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: 304–326

    Google Scholar 

  • Sandeman DC, Scholtz G, Sandeman RE (1993) Brain evolution in decapod Crustacea. J Exp Zool 265: 112–133

    Google Scholar 

  • Schildberger K (1984) Multimodal interneurons in the cricket brain: properties of identified extrinsic mushroom body cells. J Comp Physiol A 154: 71–79

    Google Scholar 

  • Schmidt M, Ache BW (1991) FMRFamide-like immunoreactivity in the olfactory brain of the spiny lobster, Panulirus argus. Chem Senses 16: 408

    Google Scholar 

  • Schmidt M, Ache BW (1992) Antennular projections to the midbrain of the spiny lobster. II. Sensory innervation of the olfactory lobe. J Comp Neurol 318: 291–303

    Google Scholar 

  • Schmidt M, Ache BW (1993) Antennular projections to the midbrain of the spiny lobster. III. Central arborizations of motoneurons. J Comp Neurol 336: 583–594

    Google Scholar 

  • Schmidt M, Ache BW (1994) Descending neurons with dopamninelike or with substance P/FMRF-like immunoreactivity target the somata of olfactory interneurons in the brain of the spiny lobster, Panulirus argus. Cell Tissue Res 278: 337–352

    Google Scholar 

  • Schmidt M, Ache BW (1996) 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. J Comp Physiol A

  • Schmidt M, Orona E, Waechter S, Batelle B-A, Ache BW (1990) Serotonin in the central olfactory system of the spiny lobster Panulirus argus. Chem Senses 15: 634–635

    Google Scholar 

  • Schmidt M, Orona E, Ache BW (1991) Parallel processing of chemosensory input in the brain of the spiny lobster. Soc Neurosci Abstr 17: 1018

    Google Scholar 

  • 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: 277–290

    Google Scholar 

  • Schmitt BC, Ache BW (1979) Olfaction: Responses of a decapod crustacean are enhanced by flicking. Science 205: 204–206

    Google Scholar 

  • Spencer M (1986) The innervation and chemical sensitivity of single aesthetasc hairs. J Comp Physiol A 158: 59–68

    Google Scholar 

  • 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: 69–80

    Google Scholar 

  • Stocker RF, Lienhard MC, Borst A, Fischbach K-F (1990) Neuronal architecture of the antennal lobe in Drosophila melanogaster. Cell Tissue Res 262: 9–34

    Google Scholar 

  • Strausfeld NJ (1976) Atlas of an insect brain. Springer, Berlin Heidelberg, New York

    Google Scholar 

  • Sun X-J, Fonta C, Masson C (1993) Odour quality processing by the antennal lobe interneurons. Chem Senses 18: 355–377

    Google Scholar 

  • Takami S, Graziadei PPC (1990) Morphological complexity of the glomerulus in the rat accessory olfactory bulb-A Golgi study. Brain Res 510: 339–342

    Google Scholar 

  • Tierney AJ, Thompson CS, Dunham DW (1986) Fine structure of aesthetasc chemoreceptors in the crayfish Orconectes propinquus. Can J Zool 64: 392–399

    Google Scholar 

  • Wachowiak M, Ache BW (1993) Whole-cell recording from multiglomerular projection neurons in the olfactory lobe of the spiny lobster. Chem Senses 18: 645–646

    Google Scholar 

  • Wachowiak M, Ache BW (1994) Morphology and physiology of multiglomerular olfactory projection neurons in the spiny lobster. J Comp Physiol A 175: 35–48

    Google Scholar 

  • Waldow U (1975) Multimodale Neurone im Deutocerebrum von Periplaneta americana. J Comp Physiol 101: 329–341

    Google Scholar 

  • Weissburg MJ, Zimmer-Faust RK (1993) Life and death in moving fluids: Hydrodynamic effects on chemosensory-mediated predation. Ecology 74: 1428–1443

    Google Scholar 

  • Witthöft W (1967) Absolute Anzahl und Verteilung der Zellen im Hirn der Honigbiene. Z Morph Ökol Tiere 61: 160–184

    Google Scholar 

  • Young SJ, Royer SM, Groves PM, Kinnamon JC (1987) Threedimensional reconstructions from serial micrographs using the IBM PC. J Electron Microsc Tech 6: 207–217

    Google Scholar 

  • Zippel HP, Voigt R, Wächter T, Kühling-Thees J (1986) Goldfish olfactory bulb neurons respond to mechano- thermo- and nonolfactory stimuli applied to the olfactory mucosa. Chem Senses 11: 683

    Google Scholar 

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Schmidt, M., Ache, B.W. Processing of antennular input in the brain of the spiny lobster, Panulirus argus . J Comp Physiol A 178, 605–628 (1996). https://doi.org/10.1007/BF00227375

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