Skip to main content
SpringerLink
Log in

Morphology and physiology of multiglomerular olfactory projection neurons in the spiny lobster

  • Original Paper
  • Published:
Journal of Comparative Physiology A Aims and scope Submit manuscript

Abstract

Whole-cell patch-clamp recording was used to characterize olfactory projection neurons in an isolated brain preparation of the spiny lobster, Panulirus argus. Responses to electrical stimulation of the olfactory afferents were recorded from projection neuron somata using biocytin-filled electrodes. All projection neurons were multiglomerular, innervating up to 80% of all olfactory lobe glomeruli, but the innervation was heterogeneous. Most neurons densely innervated only 3–4 glomeruli; the remaining glomeruli in their dendritic arbor were sparsely innervated, thereby creating two distinct patterns of intraglomerular branching. Projection neurons responded to orthodromic stimulation with an initial depolarization and spiking followed by a 1–3 s hyperpolarization. The inhibitory phase of the response was lower in threshold and longer in latency than the excitatory phase, a response pattern also reported in olfactory projection neurons of insects and vertebrates. The somata of the projection neurons supported voltage-activated currents and TTX-sensitive action potentials, suggesting that the soma, although spatially separated from the axon and dendrites, may play a significant functional role in these cells. Dye coupling between some projection neurons correlated with the presence of multiple amplitude action potentials, suggesting that at least some projection neurons may be coupled via gap junctions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ache BW (1991) Phylogeny of smell and taste. In: Getchell TV, Doty RL, Bartoshuk LM, Snow JB (eds) Smell and taste in health and disease. Raven Press, New York, pp 3–18

    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 Crustacean Biol 8: 493–519

    Google Scholar 

  • Boeckh J, Distler P, Ernst KD, Hösl M, Malun D (1990) Olfactory bulb and antennal lobe. In: Schild D (ed) Chemosensory information processing. Springer, Berlin, pp 201–227

    Google Scholar 

  • Bufler J, Zufall F, Franke C, Halt H (1992) Patch-clamp recordings of spiking and non-spiking interneurons from rabbit olfactory bulb slices: membrane properties and ionic currents. J Comp Physiol A 170: 145–152

    Google Scholar 

  • Carlson SD (1987) Ultrastructure of the arthropod neuroglia and neuropil. In: Gupta AP (ed) Arthropod brain. John Wiley and Sons, New York, pp 323–346

    Google Scholar 

  • Christensen TA, Hildebrand JG (1987a) 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, Hildebrand JG (1987b) Functions, organization, and physiology of the olfactory pathways in the lepidopteran brain. In: Gupta AP (ed) Arthropod brain: its evolution, development, structure, and functions. John Wiley and Sons, New York, pp 457–484

    Google Scholar 

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

    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 (Abstract)

    Google Scholar 

  • Ezeh P, Wellis DP, Scott JW (1993) Organization of inhibition in the rat olfactory bulb external plexiform layer. J Neurophysiol 70: 263–274

    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 

  • Gascuel JG, Masson C (1991) A quantitative ultrastructural study of the honeybee antennal lobe. Tissue Cell 23: 341–355

    Google Scholar 

  • Gupta AP (1987) Evolutionary trends in the central and mushroom bodies of the arthropod brain: a dilemma. In: Gupta AP (ed) Arthropod brain. John Wiley & Sons, New York, pp 27–42

    Google Scholar 

  • Guthrie KM, Andersen AJ, Leon M, Gall C (1993) Odor-induced increases in c-fos mRNA expression reveal an anatomical “unit” for odor-processing in olfactory bulb. Proc Natl Acad Sci USA 90: 3329–3333

    Google Scholar 

  • Hamilton KA, Kauer JS (1988) Responses of mitral/tufted cells to orthodromic and antidromic electrical stimulation in the olfactory bulb of the tiger salamander. J Neurophysiol 59: 1736–1755

    Google Scholar 

  • Homberg U, Montague RA, Hildebrand JG (1988) Anatomy of antenno-cerebral pathways in the brain of the sphinx moth Manduca sexta. Cell Tissue Res 254: 255–281

    CAS  PubMed  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 

  • Jahr CE, Nicoll RA (1982) An intracellular analysis of dendrodendritic inhibition in the turtle in vitro olfactory bulb. J Physiol (Lond) 326: 213–234

    Google Scholar 

  • Jiang T, Holley A (1992) Morphological variations among output neurons of the olfactory bulb in the frog (Rana ridibunda). J Comp Neurol 320: 86–96

    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 

  • Kosaka T, Hama K (1982) Structure of the mitral cell in the olfactory bulb of the goldfish (Carassius auratus). J Comp Neurol 212: 365–384

    Google Scholar 

  • Malun D (1991) Synaptic relationships between GABA-immunoreactive neurons and an identified uniglomerular projection neuron in the antennal lobe of Periplaneta americana: a double-labeling electron microscopic study. Histochemistry 96: 197–207

    Google Scholar 

  • Malun D, Waldow U, Kraus D, Boeckh J (1993) Connections between the deutocerebrum and the protocerebrum, and neuroanatomy of several classes of deutocerebral projection neurons in the brain of male Periplaneta americana. J Comp Neurol 329: 143–162

    Google Scholar 

  • Masson C, Mustaparta H (1990) Chemical information processing in the olfactory system of insects. Physiol Rev 70: 199–245

    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, 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 interneurones in the protocerebrum of the crayfish. J Exp Biol 167: 15–38

    Google Scholar 

  • Meredith M (1986) Patterned responses to odor in mammalian olfactory bulb: the influence of intensity. J Neurophysiol 56: 572–597

    Google Scholar 

  • Mittman S, Flaming DG, Copenhagen DR, Belgum JH (1987) Bubble pressure measurement of micropipet tip outer diameter. J Neurosci Methods 22: 161–166

    Google Scholar 

  • Mon K (1987) Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog Neurobiol 29: 275–320

    Google Scholar 

  • Mori K, Nowycky MC, Shepherd GM (1981a) Electrophysiological analysis of mitral cells in the isolated turtle olfactory bulb. J Physiol (Lond) 314: 281–294

    Google Scholar 

  • Mori K, Nowycky MC, Shepherd GM (1981b) Analysis of synaptic potentials in mitral cells in isolated turtle olfactory bulb. J Physiol (Lond) 314: 295–309

    Google Scholar 

  • Mori K, Nowycky MC, Shepherd GM (1982) Impulse activity in presynaptic dendrites: analysis of mitral cells in the isolated turtle olfactory bulb. J Neurosci 2: 497–502

    Google Scholar 

  • Mori K, Nowycky MC, Shepherd GM (1984) Synaptic excitatory and inhibitory interactions at distal dendritic sites on mitral cells in the isolated turtle olfactory bulb. J Neurosci 4: 2291–2296

    Google Scholar 

  • Nickell WT, Shipley MT (1992) Neurophysiology of the olfactory bulb. In: Serby MJ, Chobor KL (eds) Science of olfaction.Springer, New York, pp 172–212

    Google Scholar 

  • Nickell WT, Behbehani MM, Shipley MT (1993) Whole cell patch clamp recording of olfactory bulb mitral cells from in vitro slices: membrane properties and synaptic responses to stimulation of the olfactory nerve. Chem Senses 18: 607 (Abstract)

    Google Scholar 

  • Nowycky MC, Mori K, Shepherd GM (1981) Blockade of synaptic inhibition reveals long-lasting excitation in isolated turtle olfactory bulb. J. Neurophysiol. 46: 649–658

    Google Scholar 

  • Oka Y (1983) Golgi, electron-microscopic and combined Golgielectron-microscopic studies of the mitral cells in the goldfish olfactory bulb. Neuroscience 8: 723–742

    Google Scholar 

  • Onoda N (1992) Odor-induced fos-like immunoreactivity in the rat olfactory bulb. Neurosci Lett 137: 157–160

    Google Scholar 

  • Orona E, Guthrie KM, Gall CM, Fadool JM, Greenberg RM, Ache BW (1992) Functional activity maps in the olfactory CNS of the lobster. Chem Senses 17: 681 (Abstract)

    Google Scholar 

  • Saint Marie RL, Carlson SD (1985) Interneuronal and glial-neuronal gap junctions in the lamina ganglionaris of the compound eye of the housefly, Musca domestica. Cell Tissue Res 241: 43–52

    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 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 

  • 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: 277–290

    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 (Abstract)

    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: 291–303

    Google Scholar 

  • Schneider SP, Scott JW (1983) Orthodromic response properties of rat olfactory bulb mitral and tufted cells correlate with their projection patterns. J Neurophysiol 50: 358–378

    Google Scholar 

  • Scott JW (1991) Central processing of olfaction. J Steroid Biochem Mol Biol 39: 593–600

    Google Scholar 

  • Scott JW, Wellis DP, Priddy B (1991) Properties of olfactory bulb mitral, tufted and periglomerular neurons studied by electrical stimulation of the olfactory nerve layer. Chem Senses 16: 578–579 (Abstract)

    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 

  • Tolbert LP, Hildebrand JG (1981) Organization and synaptic ultrastructure of glomeruli in the antennal lobes of the moth Manduca sexta: a study using thin sections and freeze-fracture. Proc R Soc Lond B 213: 279–301

    Google Scholar 

  • Tsvileneva VA, Titova VA (1985) On the brain structures of decapods. Zool Jb Anat 113: 217–266

    Google Scholar 

  • Vaney DI (1991) Many diverse types of retinal neurons show tracer coupling when injected with biocytin or neurobiotin. Neurosci Lett 125: 187–190

    Google Scholar 

  • Wellis DP, Kauer JS (1991) Patch-clamp recordings in the salamander olfactory bulb. Chem Senses 16: 599 (Abstract)

    Google Scholar 

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

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Whitney Laboratory, 9505 Ocean Shore Blvd., 32086, St. Augustine, FL, USA

    M. Wachowiak & B. W. Ache

Authors
  1. M. Wachowiak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. B. W. Ache
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wachowiak, M., Ache, B.W. Morphology and physiology of multiglomerular olfactory projection neurons in the spiny lobster. J Comp Physiol A 175, 35–48 (1994). https://doi.org/10.1007/BF00217435

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00217435

Key words

Search

Navigation