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PMID: 10516300 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Presynaptic inhibition of primary olfactory afferents mediated by different mechanisms in lobster and turtle.

Wachowiak M, Cohen LB

Abstract

Presynaptic regulation of transmission at the first olfactory synapse was investigated by selectively imaging axon terminals of receptor neurons in the lobster olfactory lobe and turtle olfactory bulb. In both species, action potential propagation into axon terminals after olfactory nerve stimulation was measured using voltage-sensitive dyes. In addition, in the turtle, calcium influx into terminals was measured by selectively labeling receptor neurons with dextran-conjugated calcium indicator dyes. In the lobster, application of the inhibitory transmitters GABA or histamine suppressed action potentials in the terminals. The suppression was blocked by picrotoxin and cimetidine, respective antagonists to lobster GABA and histamine receptors. These results suggest that previously characterized GABA and histaminergic interneurons regulate olfactory input by suppressing action potential propagation into axon terminals of olfactory afferents. In contrast, in the turtle olfactory bulb, neither GABA nor dopamine had any effect on receptor cell action potentials as measured with voltage-sensitive dyes. However, calcium influx into axon terminals was reduced by the GABA(B) agonist baclofen and the dopamine D(2) agonist quinpirole, and paired-pulse suppression of calcium influx was reduced by the GABA(B) antagonist saclofen. These results indicate that in the turtle, GABA and dopamine mediate presynaptic inhibition not by affecting action potentials directly, as in the lobster, but by reducing calcium influx via GABA(B) and dopamine D(2) receptors. Thus, although mediated by different cellular mechanisms, presynaptic regulation of olfactory input to the CNS, via dual synaptic pathways, is a feature common to vertebrates and invertebrates. This inhibition may be important in the processing of olfactory information.

MeSH Terms
Animals Axons/physiology Fluorescent Dyes Histamine/physiology Nephropidae/physiology Neural Inhibition/physiology Neurons, Afferent/physiology Neurotransmitter Agents/physiology Olfactory Bulb/physiology Olfactory Pathways/cytology,physiology Optics and Photonics Organic Chemicals Presynaptic Terminals/physiology Sodium Chloride/pharmacology Synaptic Transmission/drug effects Turtles/physiology gamma-Aminobutyric Acid/physiology
Chemicals
Fluorescent Dyes Neurotransmitter Agents Organic Chemicals calcium crimson Sodium Chloride gamma-Aminobutyric Acid Histamine
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Wachowiak M
Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut 06520, USA.
Cohen L B
References (34)
34 references, click to expand
  1. Synaptic organization in the olfactory glomerulus of the mouse.
    Brain Res. 1972 Feb 11;37(1):69-80 PMID: 4334289
  2. Local interneurons define functionally distinct regions within lobster olfactory glomeruli
    J Exp Biol. 1997;200(Pt 6):989-1001 PMID: 9318790
  3. The neuropil of the periglomerular region of the olfactory bulb.
    J Cell Sci. 1971 Sep;9(2):379-409 PMID: 5124504
  4. Presynaptic D2 dopaminergic receptors mediate inhibition of excitatory synaptic transmission in rat neostriatum.
    Brain Res. 1995 Sep 4;690(2):264-8 PMID: 8535848
  5. Ionotropic GABA receptor from lobster olfactory projection neurons.
    J Neurophysiol. 1997 May;77(5):2235-51 PMID: 9163355
  6. Optical monitoring of activity from many areas of the in vitro and in vivo salamander olfactory bulb: a new method for studying functional organization in the vertebrate central nervous system.
    J Neurosci. 1983 Nov;3(11):2251-62 PMID: 6631479
  7. Synaptic connections between identified neuron types in the antennal lobe glomeruli of the cockroach, Periplaneta americana: I. Uniglomerular projection neurons.
    J Comp Neurol. 1997 Feb 17;378(3):307-19 PMID: 9034893
  8. [Baclofen inhibition of synaptic transmission in glomeruli of the olfactory bulb of the frog].
    Neirofiziologiia. 1985;17(6):834-7 PMID: 3003600
  9. Presynaptic inhibition is mediated by histamine and GABA in the crustacean escape reaction.
    J Neurophysiol. 1994 Mar;71(3):1088-95 PMID: 8201404
  10. Olfactory bulb DA receptors may be located on terminals of the olfactory nerve.
    Neuroreport. 1991 Jan;2(1):9-12 PMID: 1722720
  11. Presynaptic inhibition of identified wind-sensitive afferents in the cercal system of the locust.
    J Neurosci. 1988 Aug;8(8):2748-57 PMID: 3411352
  12. Mechanisms of olfactory discrimination: converging evidence for common principles across phyla.
    Annu Rev Neurosci. 1997;20:595-631 PMID: 9056726
  13. Evidence for GABAB-mediated inhibition of transmission from the olfactory nerve to mitral cells in the rat olfactory bulb.
    Brain Res Bull. 1994;35(2):119-23 PMID: 7953767
  14. Monoamine synaptic structure and localization in the central nervous system.
    J Electron Microsc Tech. 1990 May;15(1):20-33 PMID: 2187068
  15. Functional organization of rat olfactory bulb glomeruli revealed by optical imaging.
    J Neurosci. 1998 Apr 1;18(7):2602-12 PMID: 9502819
  16. Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage-sensitive dyes.
    J Comp Neurol. 1996 Nov 04;375(1):89-108 PMID: 8913895
  17. A detailed mapping of dopamine D-2 receptors in rat central nervous system by autoradiography with [125I]iodosulpride.
    Neuroscience. 1987 Jan;20(1):117-55 PMID: 2882443
  18. Antennular projections to the midbrain of the spiny lobster. II. Sensory innervation of the olfactory lobe.
    J Comp Neurol. 1992 Apr 15;318(3):291-303 PMID: 1583164
  19. Presynaptic modulation of sensory afferents in the invertebrate and vertebrate nervous system.
    Comp Biochem Physiol Comp Physiol. 1992 Oct;103(2):227-39 PMID: 1359948
  20. Presynaptic receptors.
    Annu Rev Pharmacol Toxicol. 1998;38:201-27 PMID: 9597154
  21. Synaptic excitatory and inhibitory interactions at distal dendritic sites on mitral cells in the isolated turtle olfactory bulb.
    J Neurosci. 1984 Sep;4(9):2291-6 PMID: 6481448
  22. Dopaminergic periglomerular cells in the turtle olfactory bulb.
    Brain Res Bull. 1982 Jul-Dec;9(1-6):383-9 PMID: 6129042
  23. Presynaptic afferent inhibition of lobster olfactory receptor cells: reduced action-potential propagation into axon terminals.
    J Neurophysiol. 1998 Aug;80(2):1011-5 PMID: 9705490
  24. Evidence for glutamate as the olfactory receptor cell neurotransmitter.
    J Neurophysiol. 1994 Jun;71(6):2557-61 PMID: 7931535
  25. Presynaptic inhibition of elicited neurotransmitter release.
    Trends Neurosci. 1997 May;20(5):204-12 PMID: 9141196
  26. GABAA and GABAB receptor site distribution in the rat central nervous system.
    Neuroscience. 1987 Feb;20(2):365-83 PMID: 3035421
  27. Histamine-induced modulation of olfactory receptor neurones in two species of lobster, Panulirus argus and Homarus americanus.
    J Exp Biol. 1989 Sep;145:133-46 PMID: 2809493
  28. Depolarizing action of GABA (gamma-aminobutyric acid) on myelinated fibers of peripheral nerves.
    Brain Res. 1983 Nov 14;278(1-2):117-26 PMID: 6640304
  29. Presynaptic inhibition of muscle spindle and tendon organ afferents in the mammalian spinal cord.
    Trends Neurosci. 1990 Dec;13(12):499-505 PMID: 1703681
  30. Axonal GABA-receptors in mammalian peripheral nerve trunks.
    Brain Res. 1978 Nov 3;156(1):187-91 PMID: 212161
  31. Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging.
    Neuron. 1997 May;18(5):737-52 PMID: 9182799
  32. Invertebrate presynaptic inhibition and motor control.
    Exp Brain Res. 1996 Nov;112(2):163-80 PMID: 8951385
  33. Cortical point-spread function and long-range lateral interactions revealed by real-time optical imaging of macaque monkey primary visual cortex.
    J Neurosci. 1994 May;14(5 Pt 1):2545-68 PMID: 8182427
  34. Synaptic potentials in the central terminals of locust proprioceptive afferents generated by other afferents from the same sense organ.
    J Neurosci. 1993 Feb;13(2):808-19 PMID: 8426238
Article Info
Journal
The Journal of neuroscience : the official journal of the Society for Neuroscience
Abbr.
J Neurosci
ISSN
1529-2401
Published
1999-10-15
Pages
8808-17
Language
English
Region
United States
NLM ID
8102140
PMCID
PMC6782745
Subset
IM
Grants
NINDS NIH HHS · NS08437 · United States
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