Greater excitability and firing irregularity of tufted cells underlies distinct afferent-evoked activity of olfactory bulb mitral and tufted cells

Journal of Physiology

Volumn 592, Issue 10, 2014, Pages 2097-2118

  Burton, Shawn D ^a   Urban, Nathaniel N ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTION POTENTIAL; AFTERHYPERPOLARIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EXCITATION; FEMALE; LATENT PERIOD; MALE; MITRAL CELL; MOUSE; NERVE CELL; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; REPOLARIZATION; SYNAPSE; TUFTED CELL; ANIMAL; C57BL MOUSE; CELL CULTURE; CLASSIFICATION; COMPARATIVE STUDY; CYTOLOGY; EVOKED SOMATOSENSORY RESPONSE; EXCITATORY POSTSYNAPTIC POTENTIAL; OLFACTORY BULB; PHYSIOLOGY; REACTION TIME; SENSORY NERVE CELL;

ACTION POTENTIALS; ANIMALS; CELLS, CULTURED; EVOKED POTENTIALS, SOMATOSENSORY; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; MALE; MICE; MICE, INBRED C57BL; OLFACTORY BULB; REACTION TIME; SENSORY RECEPTOR CELLS;

EID: 84900505040     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.269886     Document Type: Article

References (101)

1. Angelo K & Margrie TW (2011). Population diversity and function of hyperpolarization-activated current in olfactory bulb mitral cells. Sci Rep 1, 50.
2. Angelo K, Rancz EA, Pimentel D, Hundahl C, Hannibal J, Fleischmann A, Pichler B & Margrie TW (2012). A biophysical signature of network affiliation and sensory processing in mitral cells. Nature 488, 375-378.
3. Antal M, Eyre M, Finklea B & Nusser Z (2006). External tufted cells in the main olfactory bulb form two distinct subpopulations. Eur J Neurosci 24, 1124-1136.
4. Arevian AC, Kapoor V & Urban NN (2008). Activity-dependent gating of lateral inhibition in the mouse olfactory bulb. Nat Neurosci 11, 80-87.
5. Balu R, Larimer P & Strowbridge BW (2004). Phasic stimuli evoke precisely timed spikes in intermittently discharging mitral cells. J Neurophysiol 92, 743-753.
6. Balu R, Pressler RT & Strowbridge BW (2007). Multiple modes of synaptic excitation of olfactory bulb granule cells. J Neurosci 27, 5621-5632.
7. Bathellier B, Buhl DL, Accolla R & Carleton A (2008). Dynamic ensemble odor coding in the mammalian olfactory bulb: sensory information at different timescales. Neuron 57, 586-598.
8. Bathellier B, Gschwend O & Carleton A (2010). Temporal coding in olfaction. In The Neurobiology of Olfaction, ed. Menini A, pp. 329-348. CRC Press, Boca Raton, FL.
9. Blauvelt DG, Sato TF, Wienisch M, Knöpfel T & Murthy VN (2013). Distinct spatiotemporal activity in principal neurons of the mouse olfactory bulb in anesthetized and awake states. Front Neural Circuits 7, 46.
10. Boyd AM, Sturgill JF, Poo C & Isaacson JS (2012). Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161-1174.
11. Buonviso N, Amat C, Litaudon P, Roux S, Royet J-P, Farget V & Sicard G (2003). Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur J Neurosci 17, 1811-1819.
12. Burton SD, Ermentrout GB& Urban NN (2012). Intrinsic heterogeneity in oscillatory dynamics limits correlation-induced neural synchronization. J Neurophysiol 108, 2115-2133.
13. Cajal SR (1911). Histologie du système nerveux de l'homme et des vertébrés, Vol. 2, pp. 891-942. Maloine, Paris.
14. Cang J & Isaacson JS (2003). In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J Neurosci 23, 4108-4116.
15. Carey RM & Wachowiak M (2011). Effect of sniffing on the temporal structure of mitral/tufted cell output from the olfactory bulb. J Neurosci 31, 10615-10626.
16. Carlson GC, Shipley MT & Keller A (2000). Long-lasting depolarizations in mitral cells of the rat olfactory bulb. J Neurosci 20, 2011-2021.
17. Chen WR & Shepherd GM (1997). Membrane and synaptic properties of mitral cells in slices of rat olfactory bulb. Brain Res 745, 189-196.
18. Christie JM, Schoppa NE & Westbrook GL (2001). Tufted cell dendrodendritic inhibition in the olfactory bulb is dependent on NMDA receptor activity. J Neurophysiol 85, 169-173.
19. Cury KM & Uchida N (2010). Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-585.
20. D'Souza RD & Vijayaraghavan S (2012). Nicotinic receptor-mediated filtering of mitral cell responses to olfactory nerve inputs involves the α3β4 subtype. J Neurosci 32, 3261-3266.
21. D'Souza RD, Parsa PV & Vijayaraghavan S (2013). Nicotinic receptors modulate olfactory bulb external tufted cells via an excitation-dependent inhibitory mechanism. J Neurophysiol 110, 1544-1553.
22. De Saint Jan D, Hirnet D, Westbrook GL & Charpak S (2009). External tufted cells drive the output of olfactory bulb glomeruli. J Neurosci 29, 2043-2052.
23. Del Punta K, Puche A, Adams NC, Rodriguez I & Mombaerts P (2002). A divergent pattern of sensory axonal projections is rendered convergent by second-order neurons in the accessory olfactory bulb. Neuron 35, 1057-1066.
24. Desmaisons D, Vincent JD & Lledo PM (1999). Control of action potential timing by intrinsic subthreshold oscillations in olfactory bulb output neurons. J Neurosci 19, 10727-10737.
25. Devore S & Linster C (2012). Noradrenergic and cholinergic modulation of olfactory bulb sensory processing. Front Behav Neurosci 6, 52.
26. Ezeh PI, Wellis DP & Scott JW (1993). Organization of inhibition in the rat olfactory bulb external plexiform layer. J Neurophysiol 70, 263-274.
27. Fadool DA, Tucker K & Pedarzani P (2011). Mitral cells of the olfactory bulb perform metabolic sensing and are disrupted by obesity at the level of the Kv1.3 ion channel. PLoS ONE 6, e24921.
28. Fadool DA, Tucker K, Phillips JJ & Simmen JA (2000). Brain insulin receptor causes activity-dependent current suppression in the olfactory bulb through multiple phosphorylation of Kv1.3. J Neurophysiol 83, 2332-2348.
29. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, Nerbonne JM, Lichtman JW & Sanes JR (2000). Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41-51.
30. Friedman D & Strowbridge BW (2000). Functional role of NMDA autoreceptors in olfactory mitral cells. J Neurophysiol 84, 39-50.
31. Friedrich RW (2006). Mechanisms of odor discrimination: neurophysiological and behavioral approaches. Trends Neurosci 29, 40-47.
32. Fukunaga I, Berning M, Kollo M, Schmaltz A & Schaefer AT (2012). Two distinct channels of olfactory bulb output. Neuron 75, 320-329.
33. Ghosh S, Larson SD, Hefzi H, Marnoy Z, Cutforth T, Dokka K & Baldwin KK (2011). Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472, 217-220.
34. Gire DH & Schoppa NE (2009). Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. J Neurosci 29, 13454-13464.
35. Gire DH, Franks KM, Zak JD, Tanaka KF, Whitesell JD, Mulligan AA, Hen R & Schoppa NE (2012). Mitral cells in the olfactory bulb are mainly excited through a multistep signaling path. J Neurosci 32, 2964-2975.
36. Giridhar S & Urban NN (2012). Mechanisms and benefits of granule cell latency coding in the mouse olfactory bulb. Front Neural Circuits 6, 40.
37. Golomb D, Donner K, Shacham L, Shlosberg D, Amitai Y & Hansel D (2007). Mechanisms of firing patterns in fast-spiking cortical interneurons. PLoS Comput Biol 3, e156.
38. Golowasch J, Thomas G, Taylor AL, Patel A, Pineda A, Khalil C & Nadim F (2009). Membrane capacitance measurements revisited: dependence of capacitance value on measurement method in nonisopotential neurons. J Neurophysiol 102, 2161-2175.
39. Gracia-Llanes FJ, Crespo C, Blasco-Ibáñez JM, Nácher J, Varea E, Rovira-Esteban L & Martínez-Guijarro FJ (2010). GABAergic basal forebrain afferents innervate selectively GABAergic targets in the main olfactory bulb. Neuroscience 170, 913-922.
40. Griff ER, Mafhouz M & Chaput MA (2008). Comparison of identified mitral and tufted cells in freely breathing rats: II. Odor-evoked responses. Chem Senses 33, 793-802.
41. Haddad R, Lanjuin A, Madisen L, Zeng H, Murthy VN & Uchida N (2013). Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat Neurosci 16, 949-957.
42. Hayar A, Karnup S, Shipley MT & Ennis M (2004). Olfactory bulb glomeruli: external tufted cells intrinsically burst at theta frequency and are entrained by patterned olfactory input. J Neurosci 24, 1190-1199.
43. Holt GR, Softky WR, Koch C & Douglas RJ (1996). Comparison of discharge variability in vitro and in vivo in cat visual cortex neurons. J Neurophysiol 75, 1806-1814.
44. Huang L, Garcia I, Jen HI& Arenkiel BR (2013). Reciprocal connectivity between mitral cells and external plexiform layer interneurons in the mouse olfactory bulb. Front Neural Circuits 7, 32.
45. Igarashi KM, Ieki N, An M, Yamaguchi Y, Nagayama S, Kobayakawa K, Kobayakawa R, Tanifuji M, Sakano H, Chen WR & Mori K (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J Neurosci 32, 7970-7985.
46. Kato HK, Chu MW, Isaacson JS & Komiyama T (2012). Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 76, 962-975.
47. Kato HK, Gillet SN, Peters AJ, Isaacson JS & Komiyama T (2013). Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80, 1218-1231.
48. Kikuta S, Fletcher ML, Homma R, Yamasoba T & Nagayama S (2013). Odorant response properties of individual neurons in an olfactory glomerular module. Neuron 77, 1122-1135.
49. King JD & Meriney SD (2005). Proportion of N-type calcium current activated by action potential stimuli. J Neurophysiol 94, 3762-3770.
50. Kishi K, Mori K & Ojima H (1984). Distribution of local axon collaterals of mitral, displaced mitral, and tufted cells in the rabbit olfactory bulb. J Comp Neurol 225, 511-526.
51. Labarrera C, London M & Angelo K (2013). Tonic inhibition sets the state of excitability in olfactory bulb granule cells. J Physiol 591, 1841-1850.
52. Liu S & Shipley MT (2008). Multiple conductances cooperatively regulate spontaneous bursting in mouse olfactory bulb external tufted cells. J Neurosci 28, 1625-1639.
53. Livneh Y, Adam Y & Mizrahi A (2014). Odor processing by adult-born neurons. Neuron 81, 1097-1110.
54. Ma JJ & Lowe GG (2010). Correlated firing in tufted cells of mouse olfactory bulb. Neuroscience 169, 1715-1738.
55. Ma M & Luo M (2012). Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. J Neurosci 32, 10105-10116.
56. 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.
57. Macrides F, Schoenfeld TA, Marchand JE & Clancy AN (1985). Evidence for morphologically, neurochemically and functionally heterogeneous classes of mitral and tufted cells in the olfactory bulb. Chem Senses 10, 175-202.
58. Margrie TW & Schaefer AT (2003). Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J Physiol 546, 363-374.
59. 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 U S A 98, 319-324.
60. Markopoulos F, Rokni D, Gire DH & Murthy VN (2012). Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76, 1175-1188.
61. Markram H, Toledo-Rodriguez M, Wang Y, Gupta A, Silberberg G & Wu C (2004). Interneurons of the neocortical inhibitory system. Nat Rev Neurosci 5, 793-807.
62. McGann JP (2013). Presynaptic inhibition of olfactory sensory neurons: new mechanisms and potential functions. Chem Senses 38, 459-474.
63. Migliore M & Shepherd GM (2002). Emerging rules for the distributions of active dendritic conductances. Nat Rev Neurosci 3, 362-370.
64. Miyamichi K, Shlomai-Fuchs Y, Shu M, Weissbourd BC, Luo L & Mizrahi A (2013). Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80, 1232-1245.
65. Mori K & Sakano H (2011). How is the olfactory map formed and interpreted in the mammalian brain? Annu Rev Neurosci 34, 467-499.
66. 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.
67. Nagayama S, Enerva A, Fletcher ML, Masurkar AV, Igarashi KM, Mori K & Chen WR (2010). Differential axonal projection of mitral and tufted cells in the mouse main olfactory system. Front Neural Circuits 4, 120.
68. Nagayama S, Takahashi YK, Yoshihara Y & Mori K (2004). Mitral and tufted cells differ in the decoding manner of odor maps in the rat olfactory bulb. J Neurophysiol 91, 2532-2540.
69. Najac M, De Saint Jan D, Reguero L, Grandes P & Charpak S (2011). Monosynaptic and polysynaptic feed-forward inputs to mitral cells from olfactory sensory neurons. J Neurosci 31, 8722-8729.
70. Nunez-Parra A, Maurer RK, Krahe K, Smith RS & Araneda RC (2013). Disruption of centrifugal inhibition to olfactory bulb granule cells impairs olfactory discrimination. Proc Natl Acad Sci U S A 110, 14777-14782.
71. Orona E, Rainer EC & Scott JW (1984). Dendritic and axonal organization of mitral and tufted cells in the rat olfactory bulb. J Comp Neurol 226, 346-356.
72. Oswald A-M & Urban NN (2012a). There and back again: the corticobulbar loop. Neuron 76, 1045-1047.
73. Oswald A-MM & Urban NN (2012b). Interactions between behaviorally relevant rhythms and synaptic plasticity alter coding in the piriform cortex. J Neurosci 32, 6092-6104.
74. Padmanabhan K & Urban NN (2010). Intrinsic biophysical diversity decorrelates neuronal firing while increasing information content. Nat Neurosci 13, 1276-1282.
75. Parrish-Aungst S, Shipley MT, Erdelyi F, Szabo G & Puche AC (2007). Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J Comp Neurol 501, 825-836.
76. Patterson MA, Lagier S & Carleton A (2013). Odor representations in the olfactory bulb evolve after the first breath and persist as an odor afterimage. Proc Natl Acad Sci U S A 110, E3340-E3349.
77. Petzold GC, Hagiwara A & Murthy VN (2009). Serotonergic modulation of odor input to the mammalian olfactory bulb. Nat Neurosci 12, 784-791.
78. Phillips ME, Sachdev RNS, Willhite DC & Shepherd GM (2012). Respiration drives network activity and modulates synaptic and circuit processing of lateral inhibition in the olfactory bulb. J Neurosci 32, 85-98.
79. Potter SM, Zheng C, Koos DS, Feinstein P, Fraser SE & Mombaerts P (2001). Structure and emergence of specific olfactory glomeruli in the mouse. J Neurosci 21, 9713-9723.
80. Rinzel J & Ermentrout GB (1989). Analysis of neural excitability and oscillations. In Methods in Neuronal Modeling, eds Koch C & Segev I, pp. 135-169. MIT Press, Cambridge, MA.
81. Rush ME & Rinzel J (1995). The potassium A-current, low firing rates and rebound excitation in Hodgkin-Huxley models. Bull Math Biol 57, 899-929.
82. Schaefer AT & Margrie TW (2007). Spatiotemporal representations in the olfactory system. Trends Neurosci 30, 92-100.
83. Schaefer AT & Margrie TW (2012). Psychophysical properties of odor processing can be quantitatively described by relative action potential latency patterns in mitral and tufted cells. Front Syst Neurosci 6, 30.
84. Schaefer AT, Angelo K, Spors H & Margrie TW (2006). Neuronal oscillations enhance stimulus discrimination by ensuring action potential precision. PLoS Biol 4, e163.
85. 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.
86. Schoppa NE (2006). Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs. Neuron 49, 271-283.
87. Schoppa NE & Urban NN (2003). Dendritic processing within olfactory bulb circuits. Trends Neurosci 26, 501-506.
88. Schoppa NE & Westbrook GL (2002). AMPA autoreceptors drive correlated spiking in olfactory bulb glomeruli. Nat Neurosci 5, 1194-1202.
89. Shao Z, Puche AC & Shipley MT (2013). Intraglomerular inhibition maintains mitral cell response contrast across input frequencies. J Neurophysiol 110, 2185-2191.
90. Shao Z, Puche AC, Liu S & Shipley MT (2012). Intraglomerular inhibition shapes the strength and temporal structure of glomerular output. J Neurophysiol 108, 782-793.
91. Shusterman R, Smear MC, Koulakov AA & Rinberg D (2011). Precise olfactory responses tile the sniff cycle. Nat Neurosci 14, 1039-1044.
92. Smear M, Resulaj A, Zhang J, Bozza T & Rinberg D (2013). Multiple perceptible signals from a single olfactory glomerulus. Nat Neurosci 16, 1687-1691.
93. Stiefel KM, Englitz B & Sejnowski TJ (2013). Origin of intrinsic irregular firing in cortical interneurons. Proc Natl Acad Sci U S A 110, 7886-7891.
94. Tepper JMJ & Bolam JPJ (2004). Functional diversity and specificity of neostriatal interneurons. Curr Opin Neurobiol 14, 685-692.
95. Tripathy SJ, Padmanabhan K, Gerkin RC & Urban NN (2013). Intermediate intrinsic diversity enhances neural population coding. Proc Natl Acad Sci U S A 110, 8248-8253.
96. Tucker K & Fadool DA (2002). Neurotrophin modulation of voltage-gated potassium channels in rat through TrkB receptors is time and sensory experience dependent. J Physiol 542, 413-429.
97. Tucker K, Cho S, Thiebaud N, Henderson MX & Fadool DA (2013). Glucose sensitivity of mouse olfactory bulb neurons is conveyed by a voltage-gated potassium channel. J Physiol 591, 2541-2561.
98. Urban NN & Sakmann B (2002). Reciprocal intraglomerular excitation and intra- and interglomerular lateral inhibition between mouse olfactory bulb mitral cells. J Physiol 542, 355-367.
99. Wachowiak M (2011). All in a sniff: olfaction as a model for active sensing. Neuron 71, 962-973.
100. Wachowiak M, Economo MN, Díaz-Quesada M, Brunert D, Wesson DW, White JA & Rothermel M (2013). Optical dissection of odor information processing in vivo using GCaMPs expressed in specified cell types of the olfactory bulb. J Neurosci 33, 5285-5300.
101. Wellis DP, Scott JW & Harrison TA (1989). Discrimination among odorants by single neurons of the rat olfactory bulb. J Neurophysiol 61, 1161-1177.