Complementary postsynaptic activity patterns elicited in olfactory bulb by stimulation of mitral/tufted and centrifugal fiber inputs to granule cells

Journal of Neurophysiology

Volumn 97, Issue 1, 2007, Pages 296-306

  Laaris, Nora ^a   Puche, Adam ^b   Ennis, Matthew ^c  

^a UNIVERSITY OF MARYLAND   (United States)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF TENNESSEE HEALTH SCIENCE CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR ANTAGONIST; GLUTAMATE RECEPTOR; MAGNESIUM; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CENTRIFUGATION; CONTROLLED STUDY; ELECTRIC POTENTIAL; EVOKED CORTICAL RESPONSE; GRANULE CELL; MOUSE; NERVE TRACT; NONHUMAN; OLFACTORY BULB; OLFACTORY TRACT; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL;

ACTION POTENTIALS; ANIMALS; CARBOCYANINES; DENDRITES; ELECTRIC STIMULATION; EXCITATORY AMINO ACID ANTAGONISTS; GLUTAMIC ACID; INTERNEURONS; MAGNESIUM; MICE; MICE, INBRED C57BL; NEURAL PATHWAYS; OLFACTORY BULB; OLFACTORY PATHWAYS; ORGAN CULTURE TECHNIQUES; PRESYNAPTIC TERMINALS; PYRIDINIUM COMPOUNDS; RECEPTORS, GLUTAMATE; SMELL; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 33846418817     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00823.2006     Document Type: Article

References (79)

1. Aroniadou-Anderjaska V, Ennis M, Shipley MT. Current-source density analysis in the rat olfactory bulb: laminar distribution of kainate/AMPA and NMDA receptor-mediated currents. J Neurophysiol 81: 15-28, 1999.
2. Buonviso N, Chaput M. Olfactory experience decreases responsiveness of the olfactory bulb in the adult rat. Neuroscience 95: 325-32, 2000.
3. Cajal RSY. Histologie du Systeme Nerveux de l'Hommes et des Vertebres. Paris: Maloine, 1911.
4. Carlson GC, Shipley MT, Keller A. Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20: 2011-21, 2000.
5. Chaput M. Effects of olfactory peduncle sectioning on the single unit responses of olfactory bulb neurons to odor presentation in awake rabbits. Chem Senses 8: 161-177, 1983.
6. Chen WR, Xiong W, Shepherd GM. Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron 25: 625-633, 2000.
7. Christie JM, Bark C, Hormuzdi SG, Helbig I, Monyer H, Westbrook GL. Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 46: 761-772, 2005.
8. Collinridge GL, Bliss TVP. Memories of NMDA receptors and LTP. Trends Neurosci 18: 54-56, 1995.
9. Coopersmith R, Leon M. Enhanced neural response by adult rats to odors experienced early in life. Brain Res 371: 400-403, 1986.
10. Davis BJ, Macrides F. The organization of centrifugal projections from the anterior olfactory nucleus, ventral hippocampal rudiment, and piriform cortex to the main olfactory bulb in the hamster: an autoradiographic study. J Comp Neurol 203: 475-493, 1981.
11. De Saint Jan D, Westbrook GL. Detecting activity in olfactory bulb glomeruli with astrocyte recording. J Neurosci 25: 2917-2924, 2005.
12. Djurisic M, Antic S, Chen WR, Zecevic D. Voltage imaging from dendrites of mitral cells: EPSP attenuation and spike trigger zones. J Neurosci 24: 6703-6714, 2004.
13. Egger V, Svoboda K, Mainen ZF. Dendrodendritic synaptic signals in olfactory bulb granule cells: local spine boost and global low-threshold spike. J Neurosci 25: 3521-3530, 2005.
14. Ennis M, Hamilton KA, Hayar A. Neurochemistry of the main olfactory system. In: Handbook of Neurochemistry and Molecular Neurobiology. (3rd ed.), edited by Lajtha A. New York: Springer In press.
15. Fallon JH, Moore RY. Catecholamine innervation of the basal forebrain. III. Olfactory bulb, anterior olfactory nuclei, olfactory tubercle and piriform cortex. J Comp Neurol 180: 533-554, 1978.
16. Fletcher ML, Wilson DA. Olfactory bulb mitral-tufted cell plasticity: odorant-specific tuning reflects previous odorant exposure. J Neurosci 23: 6946-6955, 2003.
17. Frazier LL, Brunjes PC. Unilateral odor deprivation: early postnatal changes in olfactory bulb cell density and number. J Comp Neurol 269: 355-370, 1988.
18. Friedman D, Strowbridge BW. Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 84: 39-50, 2000.
19. Gray CM, Skinner JE. Centrifugal regulation of olfactory bulb of the waking rabbit as revealed by reversible cryogenic blockade. Exp Brain Res 69: 378-386, 1988.
20. Grinvald A, Frostig RD, Lieke E, Hildesheim R. Optical imaging of neuronal activity. Physiol Rev 68: 1285-1366, 1988.
21. Haberly LB, Price JL. Association and commissural fiber systems of the olfactory cortex of the rat. I. Systems originating in the piriform cortex and adjacent areas. J Comp Neurol 178: 711-740, 1978.
22. Halabisky B, Friedman D, Radojicic M, Strowbridge BW. Calcium influx through NMDA receptors directly evokes GABA release in olfactory bulb granule cells. J Neurosci 20: 5124-34, 2000.
23. Heinbockel T, Heyward PM, Ennis M. Potent regulation of main olfactory bulb mitral cell excitability by metabotropic glutamate receptor mGluR1. J Neurophysiol 92: 3085-3096, 2004.
24. Isaacson JS. Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 23: 377-384, 1999.
25. Isaacson JS. Mechanisms governing dendritic gamma-aminobutyric acid (GABA) release in the rat olfactory bulb. Proc Natl Acad Sci 98: 337-342, 2001.
26. Isaacson JS, Strowbridge BW. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20: 749-761, 1998.
27. 14C]2- deoxyglucose uptake in the glomerular layer of the rat olfactory bulb following early odor preference learning. J Comp Neurol 376: 557-566, 1996.
28. Keller A, Yagodin S, Aroniadou-Anderjaska A, Zimmer LA, Ennis M, Sheppard NF, Shipley MT. Functional organization of rat olfactory bulb glomeruli revealed by optical imaging. J Neurosci 18: 2602-2612, 1998.
29. Kerr DIB, Hagbarth KE. An investigation of the olfactory centrifugal system. J Neurophysiol 18: 362-374, 1955.
30. Kiselycznyk CL, Zhang S, Linster C. Role of centrifugal projections to the olfactory bulb in olfactory processing. Learn Mem 13: 575-579, 2006.
31. Konnerth A, Obaid AL, Salzberg DM. Optical recording of electrical activity from parallel fibers and other cell types in skate cerebellar slices in vitro. J Physiol 393: 681-702, 1987.
32. Laaris N, Carlson GC, Keller A. Thalamic-evoked synaptic interactions in barrel cortex revealed by optical imaging. J Neurosci 20: 1529-1537, 2000.
33. Luo M, Katz LC. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32: 1165-1179, 2001.
34. Luskin MB, Price JL. The topographic organization of associational fibers of the olfactory system in the rat, including centrifugal fibers to the olfactory bulb. J Comp Neurol 216: 264-291, 1983.
35. Macrides F, Davis BJ, Youngs WM, Nadi NS, Margolis FL. Cholinergic and catecholaminergic afferents to the olfactory bulb in the hamster: a neuroanatomical, biochemical, and histochemical investigation. J Comp Neurol 203: 495-514, 1981.
36. Mandairon N, Stack C, Kiselycznyk C, Linster C. Broad activation of the olfactory bulb produces long-lasting changes in odor perception. Proc Natl Acad Sci USA 101: 13543-13548, 2006a.
37. Mandairon N, Stack C, Kiselycznyk C, Linster C. Enrichment to odors improves olfactory discrimination in adult rats. Behav Neurosci 120: 173-179, 2006b.
38. Martin C, Gervais R, Hugues E, Messaoudi B, Ravel N. Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: a correlate of odor recognition? J Neurosci 24: 389-397, 2004.
39. Martin C, Gervais R, Messaoudi B, Ravel N. Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur J Neurosci 23: 1801-1810, 2006.
40. Martinez DP, Freeman WJ. Periglomerular cell action on mitral cells in olfactory bulb shown by current source density analysis. Brain Res 308: 223-233, 1984.
41. McLean JH, Shipley MT. Serotonergic afferents to the rat olfactory bulb. I. Origins and laminar specificity of serotonergic inputs in the adult rat. J Neurosci 7: 3016-3028, 1987.
42. McLean JH, Shipley MT, Nickell WT, Aston-Jones G, Reyher CK. Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J Comp Neurol 285: 339-349, 1989.
43. Meisami E. A proposed relationship between increases in the number of olfactory receptor neurons, convergence ratio and sensitivity in the developing rat. Brain Res Dev Brain Res 46: 9-19, 1989.
44. Montag-Sallaz M, Buonviso N. Altered odor-induced expression of c-fos and arg 3.1 immediate early genes in the olfactory system after familiarization with an odor. J Neurobiol 52: 61-72, 2002.
45. Mori K, Takagi SF. Activation and inhibition of olfactory bulb neurones by anterior commissure volleys in the rabbit. J Physiol 279: 589-604, 1978.
46. Moyano HF, Molina JC. Axonal projections and conduction properties of olfactory peduncle neurons in the rat. Exp Brain Res 39: 241-248, 1980.
47. Nakashima M, Mori K, Takagi SF. Centrifugal influence on olfactory bulb activity in the rabbit. Brain Res 154: 301-316, 1978.
48. Neville KR, Haberly LB. Beta and gamma oscillations in the olfactory system of the urethan-anesthetized rat. J Neurophysiol 90: 3921-3930, 2003.
49. Nickell WT, Shipley MT. Neurophysiology of the Olfactory Bulb. In: Science of Olfaction, edited by Serby MJ, Chobor KL. New York: Springer-Verlag, 1992, p. 172-212.
50. Nickell WT, Shipley MT. Evidence for presynaptic inhibition of the olfactory commissural pathway by cholinergic agonists and stimulation of the nucleus of the diagonal band. J Neurosci 13: 650-659, 1993.
51. Nicoll RA. Pharmacological evidence for GABA as the transmitter in granule cell inhibition in the olfactory bulb. Brain Res 35: 137-149, 1971.
52. Patneau DK, Stripling JS. Functional correlates of selective long-term potentiation in the olfactory cortex and olfactory bulb. Brain Res 585: 219-228, 1992.
53. Paxinos G, Franklin KBJ. The Mouse Brain in Stereotaxic Coordinates (2nd ed.). San Diego, CA: Academic, 2001.
54. Pinato G, Midtgaard J. Regulation of granule cell excitability by a low-threshold calcium spike in turtle olfactory bulb. J Neurophysiol 90: 3341-3351, 2003.
55. Pinato G, Midtgaard J. Dendritic sodium spikelets and low-threshold calcium spikes in turtle olfactory bulb granule cells. J Neurophysiol 93: 1285-1294, 2005.
56. Pinching AJ, Powell TPS. The termination of centrifugal fibres in the glomerular layer of the olfactory bulb. J Cell Sci 10: 621-635, 1972.
57. Pressler RT, Strowbridge BW. Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49: 889-904, 2006.
58. Price JL, Powell TPS. An electron-microscopic study of the termination of the afferent fibres to the olfactory bulb from the cerebral hemisphere. J Cell Sci 7: 157-187, 1970.
59. Rall W, Shepherd GM, Reese TS, Brightman MW. Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp Neurol 14: 44-56, 1966.
60. Ravel N, Chabaud P, Martin C, Hugues E, Tallon-Baudry, Bertand O, Gervais R. Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60-90 Hz) and beta (15-40 Hz) bands in the rat olfactory bulb. Eur J Neurosci 17: 350-358, 2003.
61. Salcedo E, Zhang C, Kronberg E, Restrepo D. Analysis of training-induced changes in ethyl acetate odor maps using a new computational tool to map the glomerular layer of the olfactory bulb. Chem Senses 30: 615-626, 2005.
62. Salin PA, Lledo PM, Vincent JD, Charpak S. Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J Neurophysiol 85: 1275-1282, 2001.
63. Salzberg BM, Davila HV, Cohen LB. Optical recording of impulses in individual neurons of an invertebrate central nervous system. Nature 246: 508-509, 1973.
64. Satou M, Anzai S, Huruno M. Long-term potentiation and olfactory memory formation in the carp (Cyprinus carpio L.) olfactory bulb. J Comp Physiol 191: 421-434, 2005.
65. Schoppa NE, Kinzie JM, Sahara Y, Segerson TP, Westbrook GL. Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci 18: 6790-6802, 1998.
66. Schoppa NE, Westbrook GL. Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat Neurosci 2: 1106-1113, 1999.
67. Schoppa NE, Westbrook GL. AMPA receptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 5: 1194-1202, 2002.
68. Schwob JE, Haberly LB, Price JP. The development of physiological responses of the piriform cortex in rats to stimulation of the lateral olfactory tract. J Comp Neurol 223: 223-237, 1984.
69. Stripling JS, Patneau DK, Gramlich CA. Characterization and anatomical distribution of selective long-term potentiation in the olfactory forebrain. Brain Res 542: 107-122, 1991.
70. Urban NN, Sakmann B. Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J Physiol 542: 355-367, 2002.
71. Wellis DP, Kauer JS. GABAA and glutamate receptor involvement in dendrodendritic synaptic interactions from salamander olfactory bulb. J Physiol 469: 315-339, 1993.
72. Wilson DA, Leon M. Spatial patterns of olfactory bulb single-unit responses to learned olfactory cues in young rats. J Neurophysiol 59: 1770-1782, 1988.
73. Wu J-Y, Cohen LB. Fast multisite optical measurement of membrane potential. In: Fluorescent and Luminescent Probes for Biological Activity, edited by Mason WT, London: Academic, 1993, p. 389-404.
74. Xiong W, Chen WR. Dynamic gating of spike propagation in the mitral cell lateral dendrites. Neuron 34: 115-126, 2002.
75. Yamamoto C, Yamamoto T, Iwama K. The inhibitory systems in the olfactory bulb studied by intracellular recording. J Neurophysiol 26: 403-415, 1963.
76. Yokoi M, Mori K, Nakanishi S. refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci USA 92: 3371-3375, 1995.
77. Yuan Q, Harley CW, McLean JH, Knopfel T. Optical imaging of odor preference memory in the rat olfactory bulb. J Neurophysiol 87: 3156-3159, 2002.
78. Yuste R, Tank DW, Kleinfeld D. Functional study of the rat cortical microcircuitry with voltage-sensitive dye imaging of neocortical slices. Cereb Cortex 7: 546-558, 1997.
79. +-dependent dendritic spikes in olfactory granule cells. J Neurosci 26: 30-40, 2006.