A two-layer biophysical model of cholinergic neuromodulation in olfactory bulb

Journal of Neuroscience

Volumn 33, Issue 7, 2013, Pages 3037-3058

  Li, Guoshi ^a   Cleland, Thomas A ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCARINIC RECEPTOR; NICOTINIC RECEPTOR;

ARTICLE; CHOLINERGIC ACTIVITY; CHOLINERGIC TRANSMISSION; COMPUTER MODEL; CONTROLLED STUDY; GRANULE CELL; HYPERPOLARIZATION; ION CURRENT; MITRAL CELL; NERVE CELL NETWORK; NERVE FIBER MEMBRANE CONDUCTANCE; NERVE POTENTIAL; NEUROMODULATION; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; RODENT; SPIKE WAVE; SYNAPTIC POTENTIAL;

ALGORITHMS; ANIMALS; BIOPHYSICAL PHENOMENA; BIOPHYSICS; CALCIUM SIGNALING; CELL MEMBRANE; COMPUTER SIMULATION; CYTOPLASMIC GRANULES; KINETICS; MEMBRANE POTENTIALS; MODELS, NEUROLOGICAL; NERVE NET; NEURAL CONDUCTION; NEURONS; ODORS; OLFACTORY BULB; PARASYMPATHETIC NERVOUS SYSTEM; RATS; RECEPTORS, MUSCARINIC; RECEPTORS, NICOTINIC; REPRODUCIBILITY OF RESULTS;

EID: 84873615897     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2831-12.2013     Document Type: Article

References (93)

1. Arevian AC, Kapoor V, Urban NN (2008) Activity-dependent gating of lateral inhibition in the mouse olfactory bulb. Nat Neurosci 11:80-87. CrossRef Medline
2. 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. CrossRef Medline
3. Balu R, Larimer P, Strowbridge BW (2004) Phasic stimuli evoke precisely timed spikes in intermittently discharging mitral cells. J Neurophysiol 92:743-753. CrossRef Medline
4. Barkai E, Hasselmo ME (1994) Modulation of the input/output function of rat piriform cortex pyramidal cells. J Neurophysiol 72:644-658. Medline
5. Bathellier B, Lagier S, Faure P, Lledo PM (2006) Circuit properties generating gamma oscillations in a network model of the olfactory bulb. J Neurophysiol 95:2678-2691. Medline
6. Bhalla US, Bower JM (1993) Exploring parameter space in detailed single neuron models: simulations of the mitral and granule cells of the olfactory bulb. J Neurophysiol 69:1948-1965. Medline
7. Brea JN, Kay LM, Kopell NJ (2009) Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations. Proc Natl Acad Sci USA106:21954-21959. CrossRefMedline
8. Brunel N, Wang XJ (2003) What determines the frequency of fast network oscillations with irregular neural discharges? I. Synaptic dynamics and excitation-inhibition balance. J Neurophysiol 90:415-430. CrossRef Medline
9. Buhl EH, Tamás G, Fisahn A (1998) Cholinergic activation and tonic excitation induce persistent gamma oscillations in mouse somatosensory cortex in vitro. J Physiol 513:117-126. Medline
10. Cadetti L, Belluzzi O (2001) Hyperpolarisation-activated current in glomerular cells of the rat olfactory bulb. Neuroreport 12:3117-3120. CrossRef Medline
11. 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. Medline
12. Carnevale NT, Hines ML (2006) The neuron book. Cambridge, UK: Cambridge UP.
13. Castillo PE, Carleton A, Vincent JD, Lledo PM (1999) Multiple and opposing roles of cholinergic transmission in the main olfactory bulb. J Neurosci 19:9180-9191. Medline
14. Chaudhury D, Escanilla O, Linster C (2009) Bulbar acetylcholine enhances neural and perceptual odor discrimination. J Neurosci 29:52-60. CrossRef Medline
15. Chen WR, Shepherd GM (1997) Membrane and synaptic properties of mitral cells in slices of rat olfactory bulb. Brain Res 745:189-196. CrossRef Medline
16. Cleland TA (2010) Early transformations in odor representation. Trends Neurosci 33:130-139. CrossRef Medline
17. Cleland TA, Linster C (2002) How synchronization properties among second-order sensory neurons can mediate stimulus salience. Behav Neurosci 116:212-221. CrossRef Medline
18. Cleland TA, Linster C (2012) On-center/inhibitory-surround decorrelation via intraglomerular inhibition in the olfactory bulb glomerular layer. Front Integr Neurosci 6:5. CrossRef Medline
19. Cleland TA, Sethupathy P (2006) Non-topographical contrast enhancement in the olfactory bulb. BMC Neurosci 7:7. Medline
20. Cleland TA, Johnson BA, Leon M, Linster C (2007) Relational representation in the olfactory system. Proc Natl Acad Sci U S A 104:1953-1958. CrossRef Medline
21. Cleland TA, Narla VA, Boudadi K (2009) Multiple learning parameters differentially regulate olfactory generalization. Behav Neurosci 123:26-35. CrossRef Medline
22. David F, Linster C, Cleland TA (2008) Lateral dendritic shunt inhibition can regularize mitral cell spike patterning. J Comp Neurosci 25:25-38. CrossRef Medline
23. David FO, Hugues E, Cenier T, Fourcaud-Trocmé N, Buonviso N (2009) Specific entrainment of mitral cells during gamma oscillation in the rat olfactory bulb. PLoS Comp Biol 5:e1000551. CrossRef Medline
24. Davison AP, Feng J, Brown D (2000) A reduced compartmental model of the mitral cell for use in network models of the olfactory bulb. Brain Res Bull 51:393-399. CrossRef Medline
25. Davison AP, Feng J, Brown D (2003) Dendrodendritic inhibition and simulated odor responses in a detailed olfactory bulb network model. J Neurophysiol 90:1921-1935. CrossRef Medline
26. 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. Medline
27. Doty RL, Bagla R, Kim N (1999) Physostigmine enhances performance on an odor mixture discrimination test. Physiol Behav 65:801-804. Medline
28. D'Souza RD, Vijayaraghavan S (2012) Nicotinic receptor-mediated filtering of mitral cell responses to olfactory nerve inputs involves the 3 4 subtype. J Neurosci 32:3261-3266. CrossRef Medline
29. Durand M, Coronas V, Jourdan F, Quirion R (1998) Developmental and aging aspects of the cholinergic innervation of the olfactory bulb. Int J Dev Neurosci 16:777-785. CrossRef Medline
30. Fantana AL, Soucy ER, Meister M (2008) Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59:802-814. CrossRef Medline
31. Finelli LA, Haney S, Bazhenov M, Stopfer M, Sejnowski TJ (2008) Synaptic learning rules and sparse coding in a model sensory system. PLoS Comp Biol 4:e1000062. CrossRef Medline
32. Fisahn A, Pike FG, Buhl EH, Paulsen O (1998) Cholinergic induction of network oscillations at 40 Hz in the hippocampus in vitro. Nature 394: 186-189. CrossRef Medline
33. Friedrich RW, Stopfer M (2001) Recent dynamics in olfactory population coding. Curr Opin Neurobiol 11:468-474. CrossRef Medline
34. Fries P, Nikolić D, Singer W (2007) The gamma cycle. Trends Neurosci 30:309-316. CrossRef Medline
35. Ghatpande AS, Gelperin A (2009) Presynaptic muscarinic receptors enhance glutamate release at the mitral/tufted to granule cell dendrodendritic synapse in the rat main olfactory bulb. J Neurophysiol 101:2052-2061. CrossRef Medline
36. Gire DH, Schoppa NE (2009) Control of on/off glomerular signaling by a local GABAergic microcircuit in the olfactory bulb. Soc Neurosci Abstr 29:13454-13464.
37. Gschwend O, Beroud J, Carleton A (2012) Encoding odorant identity by spiking packets of rate-invariant neurons in awake mice. PLoS One 7:e30155. CrossRef Medline
38. Hall BJ, Delaney KR (2002) Contribution of a calcium-activated nonspecific conductance to NMDA receptor-mediated synaptic potentials in granule cells of the frog olfactory bulb. J Physiol 543:819-834. CrossRef Medline
39. Hodgkin AL, Huxley AF (1952) A quantitative description of membrane current and its application to conduction and excitation in nerve. J Physiol 117:500-544. Medline
40. Inoue T, Strowbridge BW (2008) Transient activity induces a long-lasting increase in the excitability of olfactory bulb interneurons. J Neurophysiol 99:187-199. CrossRef Medline
41. Isaacson JS, Strowbridge BW (1998) Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20:749-761. CrossRef Medline
42. Jahr CE, Nicoll RA (1980) Dendrodendritic inhibition: demonstration with intracellular recording. Science 207:1473-1475. CrossRef Medline
43. Kashiwadani H, Sasaki YF, Uchida N, Mori K (1999) Synchronized oscillatory discharges of mitral/tufted cells with different molecular receptive ranges in the rabbit olfactory bulb. J Neurophysiol 82:1786-1792. Medline
44. Kim DH, Phillips ME, Chang AY, Patel HK, Nguyen KT, Willhite DC (2011) Lateral connectivity in the olfactory bulb is sparse and segregated. Front Neural Circuits 5:5. CrossRef Medline
45. Kosaka K, Kosaka T (2005) Synaptic organization of the glomerulus in the main olfactory bulb: compartments of the glomerulus and heterogeneity of the periglomerular cells. Anat Sci Int 80:80-90. CrossRef Medline
46. Lagier S, Carleton A, Lledo PM (2004) Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J Neurosci 24:4382-4392. CrossRef Medline
47. Lagier S, Panzanelli P, Russo RE, Nissant A, Bathellier B, Sassoè-Pognetto M, Fritschy JM, Lledo PM (2007) GABAergic inhibition at dendrodendritic synapses tunes gamma oscillations in the olfactory bulb. Proc Natl Acad Sci U S A 104:7259-7264. CrossRef Medline
48. Le Jeune H, Aubert I, Jourdan F, Quirion R (1995) Comparative laminar distribution of various autoradiographic cholinergic markers in adult main olfactory bulb. J Chem Neuroanat 9:99-112. CrossRef Medline
49. Linster C, Cleland TA (2001) How spike synchronization among olfactory neurons can contribute to sensory discrimination. J Comp Neurosci 10: 187-193. Medline
50. Linster C, Cleland TA (2010) Decorrelation of odor representations via spike timing-dependent plasticity. Front Comp Neurosci 4:157. CrossRef Medline
51. Linster C, Garcia PA, Hasselmo ME, Baxter MG (2001) Selective loss of cholinergic neurons projecting to the olfactory system increases perceptual generalization between similar, but not dissimilar, odorants. Behav Neurosci 115:826-833. CrossRef Medline
52. Luo M, Katz LC (2001) Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32:1165-1179. CrossRef Medline
53. 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. CrossRef Medline
54. Macrides F, Davis BJ, Youngs WM, Nadi NS, Margolis FL (1981) Cholinergic and catecholaminergic afferents to the olfactory bulb in the hamster: a neuroanatomical, biochemical, and histochemical investigation. J Comp Neurol 203:495-514. CrossRef Medline
55. Madison DV, Lancaster B, Nicoll RA (1987) Voltage clamp analysis of cholinergic action in the hippocampus. J Neurosci 7:733-741. Medline
56. Mandairon N, Linster C (2009) Odor perception and olfactory bulb plasticity in adult mammals. J Neurophysiol 101:2204-2209. CrossRef Medline
57. Mandairon N, Ferretti CJ, Stack CM, Rubin DB, Cleland TA, Linster C (2006) Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats. Eur J Neurosci 24:3234-3244. CrossRef Medline
58. Mandairon N, Peace ST, Boudadi K, Boxhorn CE, Narla VA, Suffis SD, Cleland TA (2011) Compensatory responses to age-related decline in odor quality acuity: cholinergic neuromodulation and olfactory enrichment. Neurobiol Aging 32:2254-2265. CrossRef Medline
59. McQuiston AR, Katz LC (2001) Electrophysiology of interneurons in the glomerular layer of the rat olfactory bulb. J Neurophysiol 86:1899-1907. Medline
60. McTavish TS, Migliore M, Shepherd GM, Hines ML (2012) Mitral cell spike synchrony modulated by dendrodendritic synapse location. Front Comp Neurosci 6:3. CrossRef Medline
61. Migliore M, Shepherd GM (2008) Dendritic action potentials connect distributed dendrodendritic microcircuits. J Comp Neurosci 24:207-221. CrossRef Medline
62. Migliore M, Hines ML, Shepherd GM (2005) The role of distal dendritic gap junctions in synchronization of mitral cell axonal output. J Comp Neurosci 18:151-161. CrossRef Medline
63. Neville KR, Haberly LB (2003) Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J Neurophysiol 90:3921-3930. CrossRef Medline
64. Panhuber H, Laing DG, Willcox ME, Eagleson GK, Pittman EA (1985) The distribution of the size and number of mitral cells in the olfactory bulb of the rat. J Anat 140:297-308. Medline
65. Panzeri S, Brunel N, Logothetis NK, Kayser C (2010) Sensory neural codes using multiplexed temporal scales. Trends Neurosci 33:111-120. CrossRef Medline
66. Pinato G, Midtgaard J (2003) Regulation of granule cell excitability by a low-threshold calcium spike in turtle olfactory bulb. J Neurophysiol 90: 3341-3351. CrossRef Medline
67. Pressler RT, Inoue T, Strowbridge BW (2007) Muscarinic receptor activation modulates granule cell excitability and potentiates inhibition onto mitral cells in the rat olfactory bulb. J Neurosci 27:10969-10981. CrossRef Medline
68. Rall W, Shepherd GM, Reese TS, Brightman MW (1966) Dendrodendritic synaptic pathway for inhibition in the olfactory bulb. Exp Neurol 14:44-56. CrossRef Medline
69. Rinberg D, Koulakov A, Gelperin A (2006) Sparse odor coding in awake behaving mice. J Neurosci 26:8857-8865. CrossRef Medline
70. Rodriguez R, Kallenbach U, Singer W, Munk MH (2004) Short and long term effects of cholinergic modulation on gamma oscillations and response synchronization in the visual cortex. J Neurosci 24:10369-10378. CrossRef Medline
71. Rojas-Líbano D, Kay LM (2008) Olfactory system gamma oscillations: the physiological dissection of a cognitive neural system. Cognit Neurodynam 2:179-194. CrossRef Medline
72. Roman FS, Simonetto I, Soumireu-Mourat B (1993) Learning and memory of odor-reward association: selective impairment following horizontal diagonal band lesions. Behav Neurosci 107:72-81. CrossRef Medline
73. Rubin DB, Cleland TA (2006) Dynamical mechanisms of odor processing in olfactory bulb mitral cells. J Neurophysiol 96:555-568. CrossRef Medline
74. Schoppa NE (2006) Synchronization of olfactory bulb mitral cells by precisely timed inhibitory inputs. Neuron 49:271-283. CrossRef Medline
75. Schoppa NE, Westbrook GL (1999) Regulation of synaptic timing in the olfactory bulb by an A-type potassium current. Nat Neurosci 2:1106-1113. CrossRef Medline
76. Shao Z, Puche AC, Kiyokage E, Szabo G, Shipley MT (2009) Two GABAergic intraglomerular circuits differentially regulate tonic and phasic presynaptic inhibition of olfactory nerve terminals. J Neurophysiol 101: 1988-2001. CrossRef Medline
77. Shen GY, Chen WR, Midtgaard J, Shepherd GM, Hines ML (1999) Computational analysis of action potential initiation in mitral cell soma and dendrites based on dual patch recordings. J Neurophysiol 82: 3006-3020. Medline
78. Shepherd GM, Wei RC, Greer CA (2004) Olfactory bulb. In: The synaptic organization of the brain (Shepherd GM, ed), pp 165-216. New York: Oxford UP.
79. Smith RS, Araneda RC (2010) Cholinergic modulation of neuronal excitability in the accessory olfactory bulb. J Neurophysiol 104:2963-2974. CrossRef Medline
80. Stopfer M, Bhagavan S, Smith BH, Laurent G (1997) Impaired odour discrimination on desynchronization of odour-encoding neural assemblies. Nature 390:70-74. CrossRef Medline
81. Sultan S, Mandairon N, Kermen F, Garcia S, Sacquet J, Didier A (2010) Learning-dependent neurogenesis in the olfactory bulb determines longterm olfactory memory. FASEB J 24:2355-2363. CrossRef Medline
82. Takahashi Y, Kaba H (2010) Muscarinic receptor type 1 (M1) stimulation, probably through KCNQ/Kv7 channel closure, increases spontaneous GABA release at the dendrodendritic synapse in the mouse accessory olfactory bulb. Brain Res 1339:26-40. CrossRef Medline
83. Traub RD, Whittington MA, Colling SB, Buzsáki G, Jeffreys JG (1996) Analysis of gamma rhythms in the rat hippocampus in vitro and in vivo. J Physiol 493:471-484. Medline
84. Wang XJ (1993) Ionic basis for intrinsic 40 Hz neuronal oscillations. Neuroreport 5:221-224. CrossRef Medline
85. Wang XJ (1999) Fast burst firing and short-term synaptic plasticity: a model of neocortical chattering neurons. Neuroscience 89:347-362. CrossRef Medline
86. Wang XJ, Buzsáki G (1996) Gamma oscillation by synaptic inhibition in a hippocampal interneuronal network model. J Neurosci 16:6402-6413. Medline
87. Wang XY, McKenzie JS, Kemm RE (1996) Whole-cell K currents in identified olfactory bulb output neurones of rats. J Physiol 490:63-77.
88. Wellis DP, Scott JW (1990) Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J Neurophysiol 64: 932-947. Medline
89. Wellis DP, Kauer JS (1994) GABAergic and glutamatergic synaptic input to identified granule cells in salamander olfactory bulb. J Physiol 475: 419-430. Medline
90. Wilson DA, Fletcher ML, Sullivan RM (2004) Acetylcholine and olfactory perceptual learning. Learn Mem 11:28-34. CrossRef Medline
91. Yokoi M, Mori K, Nakanishi S (1995) Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc Natl Acad Sci U S A 92:3371-3375. CrossRef Medline
92. Záborszky L, Carlsen J, Brashear HR, Heimer L (1986) Cholinergic and GABAergic afferents to the olfactory bulb in the rat with special emphasis on the projection neurons in the nucleus of the horizontal limb of the diagonal band. J Comp Neurol 243:488-509. CrossRef Medline
93. Zador A, Koch C, Brown TH (1990) Biophysical model of a Hebbian synapse. Proc Natl Acad Sci U S A 87:6718-6722. CrossRef Medline