Dopamine inhibits mitral/tufted→granule cell synapses in the frog olfactory bulb

Journal of Neuroscience

Volumn 24, Issue 37, 2004, Pages 8057-8067

  Davison, Ian G ^a,b   Boyd, Jamie D ^a   Delaney, Kerry R ^a  

^a SIMON FRASER UNIVERSITY   (Canada)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

D2; Feedback inhibition; Lateral dendrite; Mitral cell; Rana pipiens; Reciprocal synapse

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR STIMULATING AGENT; CALCIUM ION; DOPAMINE; DOPAMINE 2 RECEPTOR STIMULATING AGENT; GLUTAMIC ACID; POTASSIUM CHANNEL; POTASSIUM ION; QUINPIROLE;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DENDRITE; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; EVOKED RESPONSE; FROG; GRANULE CELL; MALE; MITRAL CELL; NEUROMODULATION; NONHUMAN; ODOR; OLFACTORY BULB; POSTSYNAPTIC POTENTIAL; POTASSIUM CURRENT; PRIORITY JOURNAL; SYNAPSE;

4-AMINOPYRIDINE; ACTION POTENTIALS; ANIMALS; CALCIUM; CALCIUM CHANNELS; DENDRITES; DEPRESSION, CHEMICAL; DOPAMINE; DOPAMINE AGONISTS; EVOKED POTENTIALS; FEEDBACK, BIOCHEMICAL; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; ION TRANSPORT; MALE; MAMMALS; NEURONS; ODORS; OLFACTORY BULB; PATCH-CLAMP TECHNIQUES; POTASSIUM; POTASSIUM CHANNELS; QUINPIROLE; RANA PIPIENS; RECEPTORS, DOPAMINE D2; RECEPTORS, GABA-A; SMELL; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 4644343698     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2138-04.2004     Document Type: Article

References (70)

1. Alonso JR, Covenas R, Lara J, Arevalo R, De Leon M, Aijon J (1989) Tyrosine hydroxylase immunoreactivity in a subpopulation of granule cells in the olfactory bulb of teleost fish. Brain Behav Evol 34:318-324.
2. B heteroreceptors. J Neurophysiol 84:1194-1203.
3. Aungst JL, Heyward PM, Puche AC, Karnup SV, Hayar A, Szabo G, Shipley MT (2003) Centre-surround inhibition among olfactory bulb glomeruli. Nature 426:623-629.
4. Baker H, Kawano T, Margolis FL, Joh TH (1983) Transneuronal regulation of tyrosine hydroxylase expression in olfactory bulb of mouse and rat. J Neurosci 3:69-78.
5. Bazhenov M, Stopfer M, Rabinovich M, Abarbanel HD, Sejnowski TJ, Laurent G (2001) Model of cellular and network mechanisms for odor-evoked temporal patterning in the locust antennal lobe. Neuron 30:569-581.
6. Berkowicz DA, Trombley PQ (2000) Dopaminergic modulation at the olfactory nerve synapse. Brain Res 855:90-99.
7. Boyd JB, Delaney KR (2002) Tyrosine-hydroxylase-reactive interneurons in the olfactory bulb of the frogs Rana pipiens and Xenopus laevis. J Comp Neurol 454:42-57.
8. Brunjes PC, Smith-Crafts LK, McCarty R (1985) Unilateral odor deprivation: effects on the development of olfactory bulb catecholamines and behavior. Brain Res 354:1-6.
9. Buck LB (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100:611-618.
10. Christie JM, Westbrook GL (2003) Regulation of backpropagating action potentials in mitral cell lateral dendrites by A-type potassium currents. J Neurophysiol 89:2466-2472.
11. Coronas V, Srivistava LK, Liang JJ, Jourdan F, Moyse E (1997) Identification and localization of dopamine receptor subtypes in rat olfactory mucosa and bulb: a combined in situ hybridization and ligand binding autoradiographic approach. J Chem Neuroanat 12:243-257.
12. Czesnik D, Rossler W, Kirchner F, Gennerich A, Schild D (2003) Neuronal representation of odourants in the olfactory bulb of Xenopus laevis tadpoles. Eur J Neurosci 17:113-118.
13. Davila NG, Blakemore LJ, Trombley PQ (2003) Dopamine modulates synaptic transmission between olfactory bulb neurons in culture. J Neurophysiol 90:395-404.
14. Debarbieux F, Audinat E, Charpak S (2003) Action potential propagation in dendrites of rat mitral cells in vivo. J Neurosci 23:5553-5560.
15. Delaney KR, Hall BJ (1996) An in vitro preparation of frog nose and brain for the study of odour-evoked oscillatory activity. J Neurosci Methods 68:193-202.
16. Dittman JS, Regehr WG (1996) Contributions of calcium-dependent and calcium-independent mechanisms to presynaptic inhibition at a cerebellar synapse. J Neurosci 16:1623-1633.
17. Doty RL, Risser JM (1989) Influence of the D-2 dopamine receptor agonist quinpirole on the odor detection performance of rats before and after spiperone administration. Psychopharmacology 98:310-315.
18. Duchamp-Viret P, Coronas V, Delaleu JC, Moyse E, Duchamp A (1997) Dopaminergic modulation of mitral cell activity in the frog olfactory bulb: a combined radioligand-electrophysiological study. Neuroscience 79:203-216.
19. Ennis M, Zhou FM, Ciombor KJ, Aroniadou-Anderjaska V, Hayar A, Borrelli E, Zimmer LA, Margolis F, Shipley MT (2001) Dopamine D2 receptor-mediated presynaptic inhibition of olfactory nerve terminals. J Neurophysiol 86:2986-2997.
20. + channels control action potential backpropagation. J Physiol (Lond) 551:40-65.
21. Gonzalez A, Smeets WJ (1991) Comparative analysis of dopamine and tyrosine hydroxylase immunoreactivities in the brain of two amphibians, the anuran Rana ridibunda and the urodele Pleurodeles waltlii. J Comp Neurol 303:457-477.
22. Halasz N, Johansson O, Hokfelt T, Ljungdahl A, Goldstein M (1981) Immunohistochemical identification of two types of dopamine neuron in the rat olfactory bulb as seen by serial sectioning. J Neurocytol 10:251-259.
23. 3H]dopa uptake in the turtle olfactory bulb. Neuroscience 8:705-715.
24. Hall BJ, Delaney KR (2002) Contribution of a calcium-activated non-specific conductance to NMDA receptor-mediated synaptic potentials in granule cells of the frog olfactory bulb. J Physiol (Lond) 543:P819-P834.
25. Hamilton KA, Kauer JS (1989) Patterns of intracellular potentials in salamander mitral/tufted cells in response to odor stimulation. J Neurophysiol 62:609-625.
26. Hoffman DA, Johnston D (1999) Neuromodulation of dendritic action potentials. J Neurophysiol 81:408-411.
27. + channel regulation of signal propagation in dendrites of hippocampal pyramidal neurons. Nature 387:869-875.
28. Hsia AY, Vincent JD, Lledo PM (1999) Dopamine depresses synaptic inputs to the olfactory bulb. J Neurophysiol 82:1082-1085.
29. Huguenard JR, Coulter DA, Prince JR (1991) A fast transient potassium current in thalamic relay neurons: kinetics of activation and inactivation. J Neurophysiol 66:1304-1315.
30. Isaacson JS, Strowbridge BW (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20:749-761.
31. Jahr CE, Nicoll RA (1982) Noradrenergic modulation of dendrodendritic inhibition in the olfactory bulb. Nature 297:227-229.
32. Johnston D, Huffman DA, Magee JC, Poolos NP, Watanabe S, Colbert CM, Migliore M (2000) Dendritic potassium channels in hippocampal pyramidal neurons. J Physiol (Lond) 525:75-81.
33. Kaba H, Hayashi Y, Higuchi T, Nakanishi S (1994) Induction of an olfactory memory by the activation of a metabotropic glutamate receptor. Science 265:262-264.
34. Kim K-M, Nakajima Y, Nakajima S (1995) G-protein-coupled inward rectifier modulated by dopamine agonists in cultured substantia nigra neurons. Neuroscience 69:1145-1158.
35. Kloppenburg P, Levini RM, Harris-Warrick RM (1999) Dopamine modulates two potassium currents and inhibits the intrinsic firing properties of an identified motor neuron in a central pattern generator network. J Neurophysiol 81:29-38.
36. Kosaka T, Hataguchi Y, Hama K, Nagatsu I, Wu YJ (1985) Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine. Brain Res 343:166-171.
37. Koster NL, Norman AB, Richtand NM, Nickell WT, Puche AC, Pixley SK, Shipley MT (1999) Olfactory receptor neurons express D2 dopamine receptors. J Comp Neurol 411:666-673.
38. Lacey MG, Mercuri NB, North RA (1987) Dopamine acts on D2 receptors to increase potassium conductance in neurones of the rat substantia nigra zona compacta. J Physiol (Lond) 392:397-416.
39. Lagier S, Carleton A, Lledo P-M (2004) Interplay between local GABAergic interneurons and relay neurons generates γ oscillations in the rat olfactory bulb. J Neurosci 24:4382-4392.
40. Lowe G (2002) Inhibition of backpropagating action potentials in mitral cell secondary dendrites. J Neurophysiol 88:64-85.
41. Luo M, Katz LC (2001) Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32:1165-1179.
42. MacLeod K, Backer A, Laurent G (1998) Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395:693-698.
43. Margrie TW, Sakmann B, Urban NN (2001) Action potential propagation in mitral cell lateral dendrites is decremental and controls recurrent and lateral inhibition in the mammalian olfactory bulb. Proc Natl Acad Sci USA 98:319-324.
44. McLeod K, Laurent G (1996) Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274: 976-979.
45. + conductance in the back-propagation of action potentials in the dendrites of hippocampal pyramidal neurons. J Comput Neurosci 7:5-15.
46. 1-like dopaminergic receptors. J Neurosci 16:7505-7512.
47. Mori K, Nowycky MC, Shepherd GM (1981) Analysis of synaptic potentials in mitral cells in the isolated turtle olfactory bulb. J Physiol (Lond) 314:295-309.
48. Mori K, Kishi K, Ojima H (1983) Distribution of dendrites of mitral, displaced mitral, tufted, and granule cells in the rabbit olfactory bulb. J Comp Neurol 219:339-355.
49. Nowycky MC, Mori K, Shepherd GM (1981) GABAergic mechanisms of dendrodendritic synapses in isolated turtle olfactory bulb. J Neurophysiol 46:639-648.
50. A receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J Neurophysiol 86:2823-2833.
51. B receptor-mediated inhibition of mitral/tufted cell activity in the rat olfactory bulb: a whole-cell patch-clamp study in vitro. Neuroscience 111:241-250.
52. Rumsey JD, Darby-King A, Harley CW, McLean JH (2001) Infusion of the metabotropic receptor agonist, DCG-IV, into the main olfactory bulb induces olfactory preference learning in rat pups. Brain Res Dev Brain Res 128:177-179.
53. Sachse S, Galizia CG (2002) Role of inhibition for temporal and spatial odor representation in olfactory output neurons: a calcium imaging study. J Neurophysiol 87:1106-1117.
54. Schoppa NE, Westbrook GL (1999) Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat Neurosci 2:1041-1043.
55. Schoppa NE, Kinzie JM, Sahara Y, Segerson TP, Westbrook GL (1998) Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18:6790-6802.
56. Spruston N, Jaffe DB, Williams SH, Johnston D (1993) Voltage-and space-clamp errors associated with the measurement of electrotonically remote synaptic events. J Neurophysiol 70:781-801.
57. Spruston N, Schiller Y, Stuart G, Sakmann B (1995) Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites. Science 268:297-300.
58. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70-74.
59. Sullivan RM, Stackenwalt G, Nasr F, Lemon C, Wilson DA (2000) Association of an odor with activation of olfactory bulb noradrenergic β-receptors or locus coeruleus stimulation is sufficient to produce learned approach responses to that odor in neonatal rats. Behav Neurosci 114:957-962.
60. Svoboda K, Denk W, Kleinfeld D, Tank DW (1997) In vivo dendritic calcium dynamics in neocortical pyramidal neurons. Nature 385:161-165.
61. Tago H, Kimura H, Maeda T (1986) Visualization of detailed acetylcholinesterase fiber and neuron staining in rat brain by a sensitive histochemical procedure. J Histochem Cytochem 34:1431-1438.
62. Trombley PQ (1992) Norepinephrine inhibits calcium currents and EPSPs via a G-protein-coupled mechanism in olfactory bulb neurons. J Neurosci 12:3992-3998.
63. Tsubokawa H, Ross WN (1997) Muscarinic modulation of spike back-propagation in the apical dendrites of hippocampal CA1 pyramidal neurons. J Neurosci 17:5782-5791.
64. Wachowiak M, Cohen LB (1999) Presynaptic inhibition of primary olfactory afferents mediated by different mechanisms in lobster and turtle. J Neurosci 19:8808-8817.
65. + channels contribute to spike-timing dependent long-term potentiation in hippocampal pyramidal neurons. Proc Natl Acad Sci USA 99:8366-8371.
66. Wilson DA, Sullivan RM (1991) Olfactory associative conditioning in infant rats with brain stimulation as reward: II. Norepinephrine mediates a specific component of the bulb response to reward. Behav Neurosci 105:843-849.
67. Wilson DA, Sullivan RM (1995) The D2 antagonist spiperone mimics the effects of olfactory deprivation on mitral/tufted cell odor response patterns. J Neurosci 15:5574-5581.
68. Wu L-G, Saggau P (1997) Presynaptic inhibition of elicited transmitter release. Trends Neurosci 20:204-212.
69. Xiong W, Chen WR (2002) Dynamic gating of spike propagation in the mitral cell lateral dendrites. Neuron 34:115-126.
70. Yokoi M, Mori K, Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA 92:3371-3375.