Olfactory Bulb Glomeruli: External Tufted Cells Intrinsically Burst at Theta Frequency and Are Entrained by Patterned Olfactory Input

Journal of Neuroscience

Volumn 24, Issue 5, 2004, Pages 1190-1199

  Hayar, Abdallah ^a,b   Karnup, Sergei ^a   Shipley, Michael T ^a   Ennis, Matthew ^a,b  

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

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

Author keywords

Bursting; Coefficient of variation; Entrainment; External tufted; Persistent sodium current; Synchrony

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; IONOTROPIC RECEPTOR; SODIUM CHANNEL BLOCKING AGENT; SODIUM ION;

ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CELL FUNCTION; CELL STRUCTURE; CELL TYPE; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; HYPERPOLARIZATION; JUXTAGLOMERULAR CELL; JUXTAGLOMERULAR NEURON; MEMBRANE POTENTIAL; NERVE CELL; NERVE CELL NECROSIS; NERVE CELL NETWORK; NONHUMAN; OLFACTORY BULB; OLFACTORY GLOMERULUS; OLFACTORY NERVOUS SYSTEM; PRIORITY JOURNAL; RAT; SNIFFING; SODIUM CURRENT; SYNAPSE; SYNAPTIC MEMBRANE; THETA RHYTHM;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNEL BLOCKERS; CALCIUM SIGNALING; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GABA ANTAGONISTS; MALE; NEURONS; OLFACTORY BULB; PATCH-CLAMP TECHNIQUES; PERIODICITY; RATS; RATS, SPRAGUE-DAWLEY; SMELL; SODIUM CHANNEL BLOCKERS; SYNAPTIC TRANSMISSION; THETA RHYTHM;

EID: 0842282117     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4714-03.2004     Document Type: Article

References (50)

1. Adrian ED (1950) The electrical activity of the olfactory bulb. Electroencephalogr Clin Neurophysiol 2:377-388.
2. Alreja M, Aghajanian GK (1995) Use of the whole-cell patch-clamp method in studies on the role of cAMP in regulating the spontaneous firing of locus coeruleus neurons. J Neurosci Methods 59:67-75.
3. Aroniadou-Anderjaska V, Ennis M, Shipley MT (1999) Dendrodendritic recurrent excitation in mitral cells of the rat olfactory bulb. J Neurophysiol 82:489-494.
4. Aroniadou-Anderjaska V, Zhou FM, Priest CA, Ennis M, Shipley MT (2000) Tonic and synaptically evoked presynaptic inhibition of sensory input to the rat olfactory bulb via GABA(B) heteroreceptors. J Neurophysiol 84:1194-1203.
5. Azouz R, Jensen MS, Yaari Y (1996) Ionic basis of spike after-depolarization and burst generation in adult rat hippocampal CA1 pyramidal cells. J Physiol (Lond) 492:211-223.
6. Bardoni R, Magherini PC, Belluzzi O (1995) Sodium current in periglomerular cells of frog olfactory bulb in vitro. Brain Res 703:19-25.
7. Belluscio L, Katz LC (2001) Symmetry, stereotypy, and topography of odorant representations in mouse olfactory bulbs. J Neurosci 21:2113-2122.
8. Brumberg JC, Nowak LG, McCormick DA (2000) Ionic mechanisms underlying repetitive high-frequency burst firing in supragranular cortical neurons. J Neurosci 20:4829-4843.
9. Carlson GC, Shipley MT, Keller A (2000) Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20:2011-2021.
10. Christodoulou C, Bugmann G (2001) Coefficient of variation (CV) vs mean interspike interval (ISI) curves: what do they tell us about the brain? Neurocomputing 38-40:1141-1149.
11. Cinelli AR, Hamilton KA, Kauer JS (1995) Salamander olfactory bulb neuronal activity observed by video rate, voltage-sensitive dye imaging. III. Spatial and temporal properties of responses evoked by odorant stimulation. J Neurophysiol 73:2053-2071.
12. Del Negro CA, Koshiya N, Butera Jr RJ, Smith JC (2002) Persistent sodium current, membrane properties and bursting behavior of pre-botzinger complex inspiratory neurons in vitro. J Neurophysiol 88:2242-2250.
13. DiFrancesco D (1993) Pacemaker mechanisms in cardiac tissue. Annu Rev Physiol 55:455-472.
14. Eeckinan FH, Freeman WJ (1990) Correlations between unit firing and EEG in the rat olfactory system. Brain Res 528:238-244.
15. 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.
16. Fox AP, Nowycky MC, Tsien RW (1987) Kinetic and pharmacological properties distinguishing three types of calcium currents in chick sensory neurones. J Physiol (Lond) 394:149-172.
17. Friedman D, Strowbridge BW (2000) Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 84:39-50.
18. Getchell TV, Shepherd GM (1975) Synaptic actions on mitral and tufted cells elicited by olfactory nerve volleys in the rabbit. J Physiol (Lond) 251:497-522.
19. Hayar A, Karnup S, Shipley MT, Ennis M (2001) Synchronous activity among juxtaglomerular neurons of the rat main olfactory bulb in vitro. Soc Neurosci Abst 27:459.4.
20. Isaacson JS (1999) Glutamate spillover mediates excitatory transmission in the rat olfactory bulb. Neuron 23:377-384.
21. Johnson BA, Leon M (2000a) Modular representations of odorants in the glomerular layer of the rat olfactory bulb and the effects of stimulus concentration. J Comp Neurol 422:496-509.
22. Johnson BA, Leon M (2000b) Odorant molecular length: one aspect of the olfactory code. J Comp Neurol 426:330-338.
23. Jourdan F, Duveau A, Astic L, Holley A (1980) Spatial distribution of [14C]2-deoxyglucose uptake in the olfactory bulbs of rats stimulated with two different odours. Brain Res 188:139-154.
24. Karnup S, Stelzer A (1999) Temporal overlap of excitatory and inhibitory afferent input in guinea-pig CA1 pyramidal cells. J Physiol (Lond) 516:485-504.
25. Kauer JS (1998) Olfactory processing: a time and place for everything. Curr Biol 8:R282-R283.
26. Kay LM (2003) A challenge to chaotic intinerancy from brain dynamics. Chaos 13:1057-1066.
27. Kay LM, Laurent G (1999) Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 2:1003-1009.
28. Kinzie JM, Shinohara MM, van den Pol AN, Westbrook GL, Segerson TP (1997) Immunolocalization of metabotropic glutamate receptor 7 in the rat olfactory bulb. J Comp Neurol 385:372-384.
29. Komisaruk BR (1970) Synchrony between limbic system theta activity and rhythmical behavior in rats. J Comp Physiol Psychol 70:482-492.
30. Laurent G (2002) Olfactory network dynamics and the coding of multidimensional signals. Nat Rev Neurosci 3:884-895.
31. Lüthi A, McCormick DA (1998) H-current: properties of a neuronal and network pacemaker. Neuron 21:9-12.
32. Macrides F, Schneider SP (1982) Laminar organization of mitral and tufted cells in the main olfactory bulb of the adult hamster. J Comp Neurol 208:419-430.
33. Macrides F, Eichenbaum HB, Forbes WB (1982) Temporal relationship between sniffing and the limbic Θ rhythm during odor discrimination and reversal learning. J Neurosci 2:1705-1717.
34. McQuiston AR, Katz LC (2001) Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J Neurophysiol 86:1899-1907.
35. Ohishi H, Akazawa C, Shigemoto R, Nakanishi S, Mizuno N (1995) Distributions of the mRNAs for L-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J Comp Neurol 360:555-570.
36. Pape HC (1996) Queer current and pacemaker: the hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58:299-327.
37. Perkel DH, Gerstein GL, Moore GP (1967) Neuronal spike trains and stochastic point processes. I. The single spike train. Biophys J 7:391-418.
38. Pinching AJ, Powell TP (1971a) The neuron types of the glomerular layer of the olfactory bulb. J Cell Sci 9:305-345.
39. Pinching AJ, Powell TP (1971b) The neuropil of the glomeruli of the olfactory bulb. J Cell Sci 9:347-377.
40. Puopolo M, Belluzzi O (1996) Sodium current in periglomerular cells of rat olfactory bulb in vitro. NeuroReport 7:1846-1850.
41. Puopolo M, Belluzzi O (1998) Inhibitory synapses among interneurons in the glomerular layer of rat and frog olfactory bulbs. J Neurophysiol 80:344-349.
42. Sahara Y, Kubota T, Ichikawa M (2001) Cellular localization of metabotropic glutamate receptors mGluR1, 2/3, 5 and 7 in the main and accessory olfactory bulb of the rat. Neurosci Lett 312:59-62.
43. Salin PA, Lledo PM, Vincent JD, Charpak S (2001) Dendritic glutamate autoreceptors modulate signal processing in rat mitral cells. J Neurophysiol 85:1275-1282.
44. Schoppa NE, Westbrook GL (2001) Glomerulus-specific synchronization of mitral cells in the olfactory bulb. Neuron 31:639-651.
45. Shipley MT, Mclean JH, Zimmer LA, Ennis M (1996) The olfactory system. In: Handbook of chemical neuroanatomy, Vol 12, Integrated systems of the CNS, Pt III (Björklund A, Hökfelt T, Swanson LW, eds), pp 469-573. Amsterdam: Elsevier.
46. Su H, Alroy G, Kirson ED, Yaari Y (2001) Extracellular calcium modulates persistent sodium current-dependent burst-firing in hippocampal pyramidal neurons. J Neurosci 21:4173-4182.
47. Uchida N, Mainen ZF (2003) Speed and accuracy of olfactory discrimination in the rat. Nat Neurosci 6:1224-1229.
48. Wehr M, Laurent G (1996) Odour encoding by temporal sequences of firing in oscillating neural assemblies. Nature 384:162-166.
49. Welker WI (1964) Analysis of sniffing of the albino rat. Behaviour 22:223-244.
50. Wellis DP, Scott JW (1990) Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J Neurophysiol 64:932-947.