Olfactory consciousness and gamma oscillation couplings across the olfactory bulb, olfactory cortex, and orbitofrontal cortex

Frontiers in Psychology

Volumn 4, Issue OCT, 2013, Pages

  Mori, Kensaku ^a,b   Manabe, Hiroyuki ^a,b   Narikiyo, Kimiya ^a,b   Onisawa, Naomi ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Gamma synchronization; Olfactory bulb; Olfactory consciousness; Olfactory cortex; Orbitofrontal cortex; Tufted and mitral cells

Indexed keywords

EID: 84900794993     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2013.00743     Document Type: Article

References (100)

1. Adrian, E. D. (1942). Olfactory reactions in the brain of the hedgehog. J. Physiol. 100, 459-473
2. Allison, A. C., and Warwick, R. T. (1949). Quantitative observations on the olfactory system of the rabbit. Brain 72, 186-197. doi: 10.1093/brain/72.2.186
3. Baars, B. J. (2002). The conscious access hypothesis: origins and recent evidence. Trends Cogn. Sci. 6, 47-52. doi: 10.1016/S1364-6613(00)01819-2
4. Barkai, E., Bergman, R. E., Horwitz, G., and Hasselmo, M. E. (1994). Modulation of associative memory function in a biophysical simulation of rat piriform cortex. J. Neurophysiol. 72, 659-677
5. Barkai, E., and Hasselmo, M. E. (1994). Modulation of the input/output function of rat piriform cortex pyramidal cells. J. Neurophysiol. 72, 644-658
6. Bekkers, J. M. S. N. (2013). Neurons and circuits for odor processing in the piriform cortex. Trends Neurosci. 36, 429-438. doi: 10.1016/j.tins.2013.04.005
7. Bennett, M. V., and Zukin, R. S. (2004). Electrical coupling and neuronal synchronization in the Mammalian brain. Neuron 41, 495-511. doi: 10.1016/S0896-6273(04)00043-1
8. Beshel, J., Kopell, N., and Kay, L. M. (2007). Olfactory bulb gamma oscillations are enhanced with task demands. J. Neurosci. 27, 8358-8365. doi: 10.1523/JNEUROSCI.1199-07.2007
9. Bressler, S. L. (1984). Spatial organization of EEGs from olfactory bulb and cortex. Electroencephalogr. Clin. Neurophysiol. 57, 270-276. doi: 10.1016/0013-4694(84)90128-7
10. Brunjes, P. C., Kay, R. B., and Arrivillaga, J. P. (2011). The mouse olfactory peduncle. J. Comp. Neurol. 519, 2870-2886. doi: 10.1002/cne.22662
11. Buck, L., and Axel, R. (1991). A novel multigene family may encode odorant receptors: a molecular basis for odor recognition. Cell 65, 175-187. doi: 10.1016/0092-8674(91)90418-X
12. Buonviso, N., Amat, C., Litaudon, P., Roux, S., Royet, J. P., Fargot, V., et al. (2003). Rhythm sequence through the olfactory bulb layers during the time window of a respiratory cycle. Eur. J. Neurosci. 17, 1811-1819. doi: 10.1046/j.1460-9568.2003.02619.x
13. Buzsaki, G., and Wang, X. J. (2012). Mechanisms of gamma oscillations. Annu. Rev. Neurosci. 35, 203-225. doi: 10.1146/annurev-neuro-062111-150444
14. Cardin, J. A., Carlen, M., Meletis, K., Knoblich, U., Zhang, F., Deisseroth, K., et al. (2009). Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663-667. doi: 10.1038/nature08002
15. Cenier, T., Amat, C., Litaudon, P., Garcia, S., Lafaye de Micheaux, P., Liquet, B., et al. (2008). Odor vapor pressure and quality modulate local field potential oscillatory patterns in the olfactory bulb of the anesthetized rat. Eur. J. Neurosci. 27, 1432-1440. doi: 10.1111/j.1460-9568.2008.06123.x
16. Chen, S., Murakami, K., Oda, S., and Kishi, K. (2003). Quantitative analysis of axon collaterals of single cells in layer III of the piriform cortex of the guinea pig. J. Comp. Neurol. 465, 455-465. doi: 10.1002/cne.10844
17. Choi, G. B., Stettler, D. D., Kallman, B. R., Bhaskar, S. T., Fleischmann, A., and Axel, R. (2011). Driving opposing behaviors with ensembles of piriform neurons. Cell 146, 1004-1015. doi: 10.1016/j.cell.2011.07.041
18. Christie, J. M., Bark, C., Hormuzdi, S. G., Helbig, I., Monyer, H., and Westbrook, G. L. (2005). Connexin36 mediates spike synchrony in olfactory bulb glomeruli. Neuron 46, 761-772. doi: 10.1016/j.neuron.2005.04.030
19. Crick, F. C., and Koch, C. (2005). What is the function of the claustrum? Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 1271-1279. doi: 10.1098/rstb.2005.1661
20. Davison, I. G., and Ehlers, M. D. (2011). Neural circuit mechanisms for pattern detection and feature combination in olfactory cortex. Neuron 70, 82-94. doi: 10.1016/j.neuron.2011.02.047
21. Ekstrand, J. J., Domroese, M. E., Johnson, D. M., Feig, S. L., Knodel, S. M., Behan, M., et al. (2001). A new subdivision of anterior piriform cortex and associated deep nucleus with novel features of interest for olfaction and epilepsy. J. Comp. Neurol. 434, 289-307. doi: 10.1002/cne.1178
22. Engel, A. K., Fries, P., and Singer, W. (2001). Dynamic predictions: oscillations and synchrony in top-down processing. Nat. Rev. Neurosci. 2, 704-716. doi: 10.1038/35094565
23. Freeman, W. J. (1975). Mass Action in the Nervous System. New York, NY: Academic
24. Friedman, D., and Strowbridge, B. W. (2003). Both electrical and chemical synapses mediate fast network oscillations in the olfactory bulb. J. Neurophysiol. 89, 2601-2610. doi: 10.1152/jn.00887.2002
25. Fries, P. (2009). Neuronal gamma-band synchronization as a fundamental process in cortical computation. Annu. Rev. Neurosci. 32, 209-224. doi: 10.1146/annurev.neuro.051508.135603
26. Galarreta, M., and Hestrin, S. (2001). Electrical synapses between GABA-releasing interneurons. Nat. Rev. Neurosci. 2, 425-433. doi: 10.1038/35077566
27. Gautam, S. H., and Verhagen, J. V. (2012). Retronasal odor representations in the dorsal olfactory bulb of rats. J. Neurosci. 32, 7949-7959. doi: 10.1523/JNEUROSCI.1413-12.2012
28. Gellman, R. L., and Aghajanian, G. K. (1993). Pyramidal cells in piriform cortex receive a convergence of inputs from monoamine activated GABAergic interneurons. Brain Res. 600, 63-73. doi: 10.1016/0006-8993(93)90402-9
29. Ghosh, S., Larson, S. D., Hefzi, H., Marnoy, Z., Cutforth, T., Dokka, K., et al. (2011). Sensory maps in the olfactory cortex defined by long-range viral tracing of single neurons. Nature 472, 217-220. doi: 10.1038/nature09945
30. Gottfried, J. A. (2007). What can an orbitofrontal cortex-endowed animal do with smells? Ann. N.Y. Acad. Sci. 1121, 102-120. doi: 10.1196/annals.1401.018
31. Gray, C. M., Konig, P., Engel, A. K., and Singer, W. (1989). Oscillatory responses in cat visual cortex exhibit inter-columnar synchronization which reflects global stimulus properties. Nature 338, 334-337. doi: 10.1038/338334a0
32. Greer, C. A. (1987). Golgi analyses of dendritic organization among denervated olfactory bulb granule cells. J. Comp. Neurol. 257, 442-452. doi: 10.1002/cne.902570311
33. Haberly, L. B. (2001). Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26, 551-576. doi: 10.1093/chemse/26.5.551
34. Haberly, L. B., and Presto, S. (1986). Ultrastructural analysis of synaptic relationships of intracellularly stained pyramidal cell axons in piriform cortex. J. Comp. Neurol. 248, 464-474. doi: 10.1002/cne.902480403
35. Haberly, L. B., and Price, J. L. (1977). The axonal projection patterns of the mitral and tufted cells of the olfactory bulb in the rat. Brain Res. 129, 152-157. doi: 10.1016/0006-8993(77)90978-7
36. Haberly, L. B., and Price, J. L. (1978). Association and commissural fiber systems of the rat. II. Systems originating in the olfactory peduncle. J. Comp. Neurol. 181, 781-807. doi: 10.1002/cne.901810407
37. Hameroff, S. (2010). The "conscious pilot"-dendritic synchrony moves through the brain to mediate consciousness. J. Biol. Phys. 36, 71-93. doi: 10.1007/s10867-009-9148-x
38. Hasselmo, M. E., and Barkai, E. (1995). Cholinergic modulation of activity-dependent synaptic plasticity in the piriform cortex and associative memory function in a network biophysical simulation. J. Neurosci. 15, 6592-6604
39. Herculano-Houzel, S., Munk, M. H., Neuenschwander, S., and Singer, W. (1999). Precisely synchronized oscillatory firing patterns require electroencephalographic activation. J. Neurosci. 19, 3992-4010
40. Igarashi, K. M., Ieki, N., An, M., Yamaguchi, Y., Nagayama, S., Kobayakawa, K., et al. (2012). Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32, 7970-7985. doi: 10.1523/JNEUROSCI.0154-12.2012
41. Illig, K. R., and Haberly, L. B. (2003). Odor-evoked activity is spatially distributed in piriform cortex. J. Comp. Neurol. 457, 361-373. doi: 10.1002/cne.10557
42. Johnson, D. M., Illig, K. R., Behan, M., and Haberly, L. B. (2000). New features of connectivity in piriform cortex visualized by intracellular injection of pyramidal cells suggest that "primary" olfactory cortex functions like "association" cortex in other sensory systems. J. Neurosci. 20, 6974-6982
43. Jones, E. G. (2001). The thalamic matrix and thalamocortical synchrony. Trends Neurosci. 24, 595-601. doi: 10.1016/S0166-2236(00)01922-6
44. Jones, E. G. (2009). Synchrony in the interconnected circuitry of the thalamus and cerebral cortex. Ann. N.Y. Acad. Sci. 1157, 10-23. doi: 10.1111/j.1749-6632.2009.04534.x
45. Kashiwadani, H., Sasaki, Y. F., Uchida, N., and 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
46. Kay, L. M. (2003). Two species of gamma oscillations in the olfactory bulb: dependence on behavioral state and synaptic interactions. J. Integr. Neurosci. 2, 31-44. doi: 10.1142/S0219635203000196
47. Kikuta, S., Fletcher, M. L., Homma, R., Yamasoba, T., and Nagayama, S. (2013). Odorant response properties of individual neurons in an olfactory glomerular module. Neuron 77, 1122-1135. doi: 10.1016/j.neuron.2013.01.022
48. Kikuta, S., Kashiwadani, H., and Mori, K. (2008). Compensatory rapid switching of binasal inputs in the olfactory cortex. J. Neurosci. 28, 11989-11997. doi: 10.1523/JNEUROSCI.3106-08.2008
49. Kosaka, T., Deans, M. R., Paul, D. L., and Kosaka, K. (2005). Neuronal gap junctions in the mouse main olfactory bulb: morphological analyses on transgenic mice. Neuroscience 134, 757-769. doi: 10.1016/j.neuroscience.2005.04.057
50. Kosaka, T., and Kosaka, K. (2005). Intraglomerular dendritic link connected by gap junctions and chemical synapses in the mouse main olfactory bulb: electron microscopic serial section analyses. Neuroscience 131, 611-625. doi: 10.1016/j.neuroscience.2004.11.050
51. Lagier, S., Carleton, A., and Lledo, P. M. (2004). Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J. Neurosci. 24, 4382-4392. doi: 10.1523/JNEUROSCI.5570-03.2004
52. Lei, H., Mooney, R., and Katz, L. C. (2006). Synaptic integration of olfactory information in mouse anterior olfactory nucleus. J. Neurosci. 26, 12023-12032. doi: 10.1523/JNEUROSCI.2598-06.2006
53. Li, W., Lopez, L., Osher, J., Howard, J. D., Parrish, T. B., and Gottfried, J. A. (2010). Right orbitofrontal cortex mediates conscious olfactory perception. Psychol. Sci. 21, 1454-1463. doi: 10.1177/0956797610382121
54. Litaudon, P., Amat, C., Bertrand, B., Vigouroux, M., and Buonviso, N. (2003). Piriform cortex functional heterogeneity revealed by cellular responses to odours. Eur. J. Neurosci. 17, 2457-2461. doi: 10.1046/j.1460-9568.2003.02654.x
55. Litaudon, P., Mouly, A. M., Sullivan, R., Gervais, R., and Cattarelli, M. (1997). Learning-induced changes in rat piriform cortex activity mapped using multisite recording with voltage sensitive dye. Eur. J. Neurosci. 9, 1593-1602. doi: 10.1111/j.1460-9568.1997.tb01517.x
56. Llinas, R., Ribary, U., Contreras, D., and Pedroarena, C. (1998). The neuronal basis for consciousness. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1841-1849. doi: 10.1098/rstb.1998.0336
57. Luskin, M. B., and Price, J. L. (1983). 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. doi: 10.1002/cne.902160305
58. Manabe, H., and Mori, K. (2013). Sniffrhythm-paced fast and slow gamma oscillations in the olfactory bulb: relation to tufted and mitral cells and behavioral states. J. Neurophysiol. 110, 1593-1599. doi: 10.1152/jn.00379.2013
59. Marr, D. (1971). Simple memory: a theory for archicortex. Philos. Trans. R. Soc. Lond. B Biol. Sci. 262, 23-81. doi: 10.1098/rstb.1971.0078
60. McCormick, D. A., and Bal, T. (1997). Sleep and arousal: thalamocortical mechanisms. Annu. Rev. Neurosci. 20, 185-215. doi: 10.1146/annurev.neuro.20.1.185
61. Migliore, M., Hines, M. L., and Shepherd, G. M. (2005). The role of distal dendritic gap junctions in synchronization of mitral cell axonal output. J. Comput. Neurosci. 18, 151-161. doi: 10.1007/s10827-005-6556-1
62. Mitsui, S., Igarashi, K. M., Mori, K., and Yoshihara, Y. (2011). Genetic visualization of the secondary olfactory pathway in Tbx21 transgenic mice. Neural Syst. Circuits 1:5. doi: 10.1186/2042-1001-1-5
63. Miyamichi, K., Amat, F., Moussavi, F., Wang, C., Wickersham, I., Wall, N. R., et al. (2011). Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191-196. doi: 10.1038/nature09714
64. Mori, K., Kishi, K., and 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. doi: 10.1002/cne.902190308
65. Mori, K., Mataga, N., and Imamura, K. (1992). Differential specificities of single mitral cells in rabbit olfactory bulb for a homologous series of fatty acid odor molecules. J. Neurophysiol. 67, 786-789
66. Mori, K., Nagao, H., and Yoshihara, Y. (1999). The olfactory bulb: coding and processing of odor molecule information. Science 286, 711-715. doi: 10.1126/science.286.5440.711
67. Mori, K., and Sakano, H. (2011). How is the olfactory map formed and interpreted in the mammalian brain? Annu. Rev. Neurosci. 34, 467-499. doi: 10.1146/annurev-neuro-112210-112917
68. Mori, K., and Takagi, S. F. (1977). "Inhibition in the olfactory bulb: dendrodendritic interaction and their relation to the induced waves," in Food Intake and Chemical Senses, ed K. Katsuki, M. Sato, S. F. Takagi, and Y. Oomura, (Tokyo: University of Tokyo Press), 33-43
69. Mori, K., Takahashi, Y. K., Igarashi, K. M., and Yamaguchi, M. (2006). Maps of odorant molecular features in the Mammalian olfactory bulb. Physiol. Rev. 86, 409-433. doi: 10.1152/physrev.00021.2005
70. Murakami, M., Kashiwadani, H., Kirino, Y., and Mori, K. (2005). State-dependent sensory gating in olfactory cortex. Neuron 46, 285-296. doi: 10.1016/j.neuron.2005.02.025
71. Nagayama, S., Takahashi, Y. K., Yoshihara, Y., and 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. doi: 10.1152/jn.01266.2003
72. Neville, K. R., and Haberly, L. B. (2003). Beta and gamma oscillations in the olfactory system of the urethane-anesthetized rat. J. Neurophysiol. 90, 3921-3930. doi: 10.1152/jn.00475.2003
73. Neville, K. R., and Haberly, L. B. (2004). "Olfactory cortex," in The Synaptic Organization of the Brain, ed G. M. Shepherd (New York, NY: Oxford University Press), 415-454. doi: 10.1093/acprof:oso/9780195159561.003.0010
74. Orona, E., Scott, J. W., and Rainer, E. C. (1983). Different granule cell populations innervate superficial and deep regions of the external plexiform layer in rat olfactory bulb. J. Comp. Neurol. 217, 227-237. doi: 10.1002/cne.902170209
75. Plailly, J., Howard, J. D., Gitelman, D. R., and Gottfried, J. A. (2008). Attention to odor modulates thalamocortical connectivity in the human brain. J. Neurosci. 28, 5257-5267. doi: 10.1523/JNEUROSCI.5607-07.2008
76. Poo, C., and Isaacson, J. S. (2011). A major role for intracortical circuits in the strength and tuning of odor-evoked excitation in olfactory cortex. Neuron 72, 41-48. doi: 10.1016/j.neuron.2011.08.015
77. Price, J. L. (2007). Definition of the orbital cortex in relation to specific connections with limbic and visceral structures and other cortical regions. Ann. N.Y. Acad. Sci. 1121, 54-71. doi: 10.1196/annals.1401.008
78. Rall, W., and Shepherd, G. M. (1968). Theoretical reconstruction of field potentials and dendrodendritic synaptic interactions in olfactory bulb. J. Neurophysiol. 31, 884-915
79. Rennaker, R. L., Chen, C. F., Ruyle, A. M., Sloan, A. M., and Wilson, D. A. (2007). Spatial and temporal distribution of odorant-evoked activity in the piriform cortex. J. Neurosci. 27, 1534-1542. doi: 10.1523/JNEUROSCI.4072-06.2007
80. Rolls, E. T. (2006). Brain mechanisms underlying flavour and appetite. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361, 1123-1136. doi: 10.1098/rstb.2006.1852
81. Rolls, E. T., and Baylis, L. L. (1994). Gustatory, olfactory, and visual convergence within the primate orbitofrontal cortex. J. Neurosci. 14, 5437-5452
82. Rosero, M. A., and Aylwin, M. L. (2011). Sniffing shapes the dynamics of olfactory bulb gamma oscillations in awake behaving rats. Eur. J. Neurosci. 34, 787-799. doi: 10.1111/j.1460-9568.2011.07800.x
83. Schoenbaum, G., Saddoris, M. P., and Stalnaker, T. A. (2007). Reconciling the roles of orbitofrontal cortex in reversal learning and the encoding of outcome expectancies. Ann. N.Y. Acad. Sci. 1121, 320-335. doi: 10.1196/annals.1401.001
84. Shepherd, G. M. (2006). Smell images and the flavour system in the human brain. Nature 444, 316-321. doi: 10.1038/nature05405
85. Shepherd, G. M. (2007). Perspectives on olfactory processing, conscious perception, and orbitofrontal cortex. Ann. N.Y. Acad. Sci. 1121, 87-101. doi: 10.1196/annals.1401.032
86. Shepherd, G. M., Chen, W. R., and Greer, C. A. (2004). "Olfactory bulb," in The Synaptic Organization of the Brain, ed G. M. Shepherd (New York, NY: Oxford University Press), 165-216. doi: 10.1093/acprof:oso/9780195159561.001.1
87. Shipley, M. T., and Ennis, M. (1996). Functional organization of olfactory system. J. Neurobiol. 30, 123-176. doi: 10.1002/(SICI)1097-4695(199605)30:1<123::AID-NEU11>3.0.CO;2-N
88. Singer, W. (1998). Consciousness and the structure of neuronal representations. Philos. Trans. R. Soc. Lond. B Biol. Sci. 353, 1829-1840. doi: 10.1098/rstb.1998.0335
89. Singer, W. (1999). Neurobiology. Striving for coherence. Nature 397, 391, 393
90. Singer, W., and Gray, C. M. (1995). Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555-586. doi: 10.1146/annurev.ne.18.030195.003011
91. Sosulski, D. L., Bloom, M. L., Cutforth, T., Axel, R., and Datta, S. R. (2011). Distinct representations of olfactory information in different cortical centres. Nature 472, 213-216. doi: 10.1038/nature09868
92. Steriade, M. (2000). Corticothalamic resonance, states of vigilance and mentation. Neuroscience 101, 243-276. doi: 10.1016/S0306-4522(00)00353-5
93. Stettler, D. D., and Axel, R. (2009). Representations of odor in the piriform cortex. Neuron 63, 854-864. doi: 10.1016/j.neuron.2009.09.005
94. Tononi, G., and Edelman, G. M. (1998). Consciousness and complexity. Science 282, 1846-1851. doi: 10.1126/science.282.5395.1846
95. Tsuno, Y., Kashiwadani, H., and Mori, K. (2008). Behavioral state regulation of dendrodendritic synaptic inhibition in the olfactory bulb. J. Neurosci. 28, 9227-9238. doi: 10.1523/JNEUROSCI.1576-08.2008
96. van Wingerden, M., Vinck, M., Lankelma, J. V., and Pennartz, C. M. (2010). Learning-associated gamma-band phase-locking of action-outcome selective neurons in orbitofrontal cortex. J. Neurosci. 30, 10025-10038. doi: 10.1523/JNEUROSCI.0222-10.2010
97. Wallis, J. D. (2007). Orbitofrontal cortex and its contribution to decision-making. Annu. Rev. Neurosci. 30, 31-56. doi: 10.1146/annurev.neuro.30.051606.094334
98. Wilson, D. A., and Sullivan, R. M. (2011). Cortical processing of odor objects. Neuron 72, 506-519. doi: 10.1016/j.neuron.2011.10.027
99. Yang, J., Ul Quraish, A., Murakami, K., Ishikawa, Y., Takayanagi, M., Kakuta, S., et al. (2004). Quantitative analysis of axon collaterals of single neurons in layer IIa of the piriform cortex of the guinea pig. J. Comp. Neurol. 473, 30-42. doi: 10.1002/cne.20104
100. Yoshida, I., and Mori, K. (2007). Odorant category profile selectivity of olfactory cortex neurons. J. Neurosci. 27, 9105-9114. doi: 10.1523/JNEUROSCI.2720-07.2007