Noradrenergic and cholinergic modulation of olfactory bulb sensory processing

Frontiers in Behavioral Neuroscience

Volumn , Issue AUGUST, 2012, Pages

  Devore, Sasha ^a   Linster, Christiane ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Acetylcholine; Neuromodulation; Noradrenaline; Olfactory bulb

Indexed keywords

4 AMINOBUTYRIC ACID; ACETYLCHOLINE; MUSCARINIC RECEPTOR; NORADRENALIN;

ATTENTION; CELL SYNCHRONIZATION; CHOLINERGIC SYSTEM; COGNITION; DIAGONAL BAND OF BROCA; GRANULE CELL; INHIBITORY POSTSYNAPTIC POTENTIAL; MITRAL CELL; NERVE CELL NETWORK; NEUROMODULATION; NONHUMAN; NORADRENERGIC SYSTEM; OLFACTORY BULB; OLFACTORY DISCRIMINATION; PERCEPTIVE DISCRIMINATION; REVIEW; SIGNAL NOISE RATIO; SMELLING;

EID: 84870821131     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (65)

1. Aston-Jones, G., and Cohen, J. D. (2005). An integrative theory of locus coeruleus-norepinephrine function: adaptive gain and optimal performance. Annu. Rev. Neurosci. 28, 403-450.
2. Bathellier, B., Lagier, S., Faure, P., and Lledo, P. M. (2006). Circuit properties generating gamma oscillations in a network model of the olfactory bulb. J. Neurophysiol. 95, 2678-2691.
3. Beshel, J., Kopell, N., and Kay, L. M. (2007). Olfactory bulb gamma oscillations are enhanced with task demands. J. Neurosci. 27, 8358-8365.
4. Brea, J. N., Kay, L. M., and Kopell, N. J. (2009). Biophysical model for gamma rhythms in the olfactory bulb via subthreshold oscillations. Proc. Natl. Acad. Sci. U.S.A. 106, 21954-21959.
5. Brennan, P. A., Schellinck, H. M., de la Riva, C., Kendrick, K. M., and Keverne, E. B. (1998). Changes in neurotransmitter release in the main olfactory bulb following an olfactory conditioning procedure in mice. Neuroscience 87, 583-590.
6. Butt, A. E., Chavez, C. M., Flesher, M. M., Kinney-Hurd, B. L., Araujo, G. C., Miasnikov, A. A., and Weinberger, N. M. (2009). Association learning-dependent increases in acetylcholine release in the rat auditory cortex during auditory classical conditioning. Neurobiol. Learn. Mem. 92, 400-409.
7. Castillo, P. E., Carleton, A., Vincent, J. D., and Lledo, P. M. (1999). Multiple and opposing roles of cholinergic transmission in the main olfactory bulb. J. Neurosci. 19, 9180-9191.
8. Chabaud, P., Ravel, N., Wilson, D. A., Mouly, A. M., Vigouroux, M., Farget, V., and Gervais, R. (2000). Exposure to behaviourally relevant odour reveals differential characteristics in rat central olfactory pathways as studied through oscillatory activities. Chem. Senses 25, 561-573.
9. Chaudhury, D., Escanilla, O., and Linster, C. (2009). Bulbar acetyl-choline enhances neural and perceptual odor discrimination. J. Neurosci. 29, 52-60.
10. Ciombor, K. J., Ennis, M., and Shipley, M. T. (1999). Norepinephrine increases rat mitral cell excitatory responses to weak olfactory nerve input via alpha-1 receptors in vitro. Neuroscience 90, 595-606.
11. Cleland, T. A., Johnson, B. A., Leon, M., and Linster, C. (2007). Relational representation in the olfactory system. Proc. Natl. Acad. Sci. U.S.A. 104, 1953-1958.
12. Cleland, T. A., and Linster, C. (2005). Computation in the olfactory system. Chem. Senses 30, 801-813.
13. Cleland, T. A., and Linster, C. (2012). On-Center/Inhibitory-surround decorrelation via intraglomerular inhibition in the olfactory bulb glomerular layer. Front. Integr. Neurosci. 6:5. doi:10.3389/fnint.2012.00005
14. Cleland, T. A., Morse, A., Yue, E. L., and Linster, C. (2002). Behavioral models of odor similarity. Behav. Neurosci. 116, 222-231.
15. Cleland, T. A., and Sethupathy, P. (2006). Non-topographical contrast enhancement in the olfactory bulb. BMC Neurosci. 7, 7.
16. Cools, R., Roberts, A. C., and Robbins, T. W. (2008). Serotoninergic regulation of emotional and behavioural control processes. Trends Cogn. Sci. 12, 31-40.
17. Davison, I. G., and Ehlers, M. D. (2011). Neural circuit mechanisms for pattern detection and feature combination in olfactory cortex. Neuron 70, 82-94.
18. D'Souza, R. D., and Vijayaraghavan, S. (2012). Nicotinic receptor-mediated filtering of mitral cell responses to olfactory nerve inputs involves the α3β4 subtype. J. Neurosci. 32, 3261-3266.
19. Elaagouby, A., and Gervais, R. (1992). ACh-induced long-lasting enhancement in excitability of the olfactory bulb. Neuroreport 3, 10-12.
20. Elaagouby, A., Ravel, N., and Gervais, R. (1991). Cholinergic modulation of excitability in the rat olfactory bulb: effect of local application of cholinergic agents on evoked field potentials. Neuroscience 45, 653-662.
21. Escanilla, O., Alperin, S., Youssef, M., Ennis, M., and Linster, C. (2011). Noradrenergic modulation in the olfactory bulb influences detection and discrimination thresholds at low odor concentrations. Abstr. Soc. Neurosci. 2011, Washington DC, P374.08.
22. Escanilla, O., Arrellanos, A., Karnow, A., Ennis, M., and Linster, C. (2010). Noradrenergic modulation of behavioral odor detection and discrimination thresholds in the olfactory bulb. Eur. J. Neurosci. 32, 458-468.
23. Franks, K. M., and Isaacson, J. S. (2006). Strong single-fiber sensory inputs to olfactory cortex: implications for olfactory coding. Neuron 49, 357-363.
24. Freeman, W. J., and Schneider, W. (1982). Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiology 19, 44-56.
25. Ghatpande, A. S., Sivaraaman, K., and Vijayaraghavan, S. (2006). Store calcium mediates cholinergic effects on mIPSCs in the rat main olfactory bulb. J. Neurophysiol. 95, 1345-1355.
26. Gire, D. H., and Schoppa, N. E. (2008). Long-term enhancement of synchronized oscillations by adren-ergic receptor activation in the olfactory bulb. J. Neurophysiol. 99, 2021-2025.
27. Heimer, L., Zahm, D. S., and Schmued, L. C. (1990). The basal forebrain projection to the region of the nuclei gemini in the rat; a combined light and electron microscopic study employing horseradish per-oxidase, fluorescent tracers and Phaseolus vulgaris-leucoagglutinin. Neuroscience 34, 707-731.
28. Jiang, M., Griff, E. R., Ennis, M., Zimmer, L. A., and Shipley, M. T. (1996). Activation of locus coeruleus enhances the responses of olfactory bulb mitral cells to weak olfactory nerve input. J. Neurosci. 16, 6319-6329.
29. Levy, F., Gervais, R., Kindermann, U., Orgeur, P., and Piketty, V. (1990). Importance of beta-noradrenergic receptors in the olfactory bulb of sheep for recognition of lambs. Behav. Neurosci. 104, 464-469.
30. Linster, C., and Cleland, T. A. (2001). How spike synchronization among olfactory neurons can contribute to sensory discrimination. J. Comput. Neurosci. 10, 187-193.
31. Linster, C., and Cleland, T. A. (2002). Cholinergic modulation of sensory representations in the olfactory bulb. Neural Netw. 15, 709-717.
32. Linster, C., and Cleland, T. A. (2009). Glomerular microcircuits in the olfactory bulb. Neural Netw. 22, 1169-1173.
33. Linster, C., and Cleland, T. A. (2012). Decorrelation of odor representations via spike timing-dependent plasticity. Front. Comput. Neurosci. 4:157. doi: 10.3389/fncom.2010.00157
34. Linster, C., and Hasselmo, M. (1997). Modulation of inhibition in a model of olfactory bulb reduces overlap in the neural representation of olfactory stimuli. Behav. Brain Res. 84, 117-127.
35. Linster, C., and Hasselmo, M. E. (1999). Behavioral responses to aliphatic aldehydes can be predicted from known electrophysiological responses of mitral cells in the olfactory bulb. Physiol. Behav. 66, 497-502.
36. Linster, C., Johnson, B. A., Morse, A., Yue, E., and Leon, M. (2002). Spontaneous versus reinforced olfactory discriminations. J. Neurosci. 22, 6842-6845.
37. Linster, C., Johnson, B. A., Yue, E., Morse, A., Xu, Z., Hingco, E. E., Choi, Y., Choi, M., Messiha, A., and Leon, M. (2001). Perceptual correlates of neural representations evoked by odorant enantiomers. J. Neurosci. 21, 9837-9843.
38. Linster, C., Nai, Q., and Ennis, M. (2010). Nonlinear effects of nora-drenergic modulation of olfactory bulb function in adult rodents. J. Neurophysiol. 105, 1432-1443.
39. Mandairon, N., Ferretti, C. J., Stack, C. M., Rubin, D. B., Cleland, T. A., and Linster, C. (2006). Cholinergic modulation in the olfactory bulb influences spontaneous olfactory discrimination in adult rats. Eur. J. Neurosci. 24, 3234-3244.
40. Mandairon, N., and Linster, C. (2009). Odor perception and olfactory bulb plasticity in adult mammals. J. Neurophysiol. 101, 2204-2209.
41. Mandairon, N., Peace, S., Karnow, A., Kim, J., Ennis, M., and Linster, C. (2008). Noradrenergic modulation in the olfactory bulb influences spontaneous and reward-motivated discrimination, but not the formation of habituation memory. Eur. J. Neurosci. 27, 1210-1219.
42. Martin, C., Gervais, R., Hugues, E., Messaoudi, B., and Ravel, N. (2004). Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: a correlate of odor recognition? J. Neurosci. 24, 389-397.
43. Martin, C., Gervais, R., Messaoudi, B., and Ravel, N. (2006). Learning-induced oscillatory activities correlated to odour recognition: a network activity. Eur. J. Neurosci. 23, 1801-1810.
44. McLean, J. H., Shipley, M. T., Nickell, W. T., Aston-Jones, G., and Reyher, C. K. (1989). Chemoanatomical organization of the noradrenergic input from locus coeruleus to the olfactory bulb of the adult rat. J. Comp. Neurol. 285, 339-349.
45. Migliore, M., and Shepherd, G. M. (2008). Dendritic action potentials connect distributed dendro-dendritic microcircuits. J. Comput. Neurosci. 24, 207-221.
46. Nai, Q., Dong, H. W., Hayar, A., Linster, C., and Ennis, M. (2009). Noradrenergic regulation of GABAergic inhibition of main olfactory bulb mitral cells varies as a function of concentration and receptor subtype. J. Neurophysiol. 101, 2472-2484.
47. Nai, Q., Dong, H. W., Linster, C., and Ennis, M. (2010). Activation of alpha1 and alpha2 noradrener-gic receptors exert opposing effects on excitability of main olfactory bulb granule cells. Neuroscience 169, 882-892.
48. Nusser, Z., Kay, L. M., Laurent, G., Homanics, G. E., and Mody, I. (2001). Disruption of GABA(A) receptors on GABAergic interneu-rons leads to increased oscillatory power in the olfactory bulb network. J. Neurophysiol. 86, 2823-2833.
49. Okutani, F., Kaba, H., Takahashi, S., and Seto, K. (1998). The biphasic effects of locus coeruleus noradren-ergic activation on dendrodendritic inhibition in the rat olfactory bulb. Brain Res. 783, 272-279.
50. Pressler, R. T., Inoue, T., and Strowbridge, B. W. (2007). Muscarinic receptor activation modulates granule cell excitability and potentiates inhibition onto mitral cells in the rat olfactory bulb. J. Neurosci. 27, 10969-10981.
51. Ravel, N., Akaoka, H., Gervais, R., and Chouvet, G. (1990). The effect of acetylcholine on rat olfactory bulb unit activity. Brain Res. Bull. 24, 151-155.
52. Ravel, N., Elaagouby, A., and Gervais, R. (1994). Scopolamine injection into the olfactory bulb impairs short-term olfactory memory in rats. Behav. Neurosci. 108, 317-324.
53. Roberts, M. J., Zinke, W., Guo, K., Robertson, R., McDonald, J. S., and Thiele, A. (2005). Acetylcholine dynamically controls spatial integration in marmoset primary visual cortex. J. Neurophysiol. 93, 2062-2072.
54. Sarter, M., and Bruno, J. P. (1997). Cognitive functions of cortical acetylcholine: toward a unifying hypothesis. Brain Res. Brain Res. Rev. 23, 28-46.
55. Sarter, M., Hasselmo, M. E., Bruno, J. P., and Givens, B. (2005). Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res. Brain Res. Rev. 48, 98-111.
56. Schultz, W., Dayan, P., and Montague, P. R. (1997). A neural substrate of prediction and reward. Science 275, 1593-1599.
57. Shea, S. D., Katz, L. C., and Mooney, R. (2008). Noradrenergic induction of odor-specific neural habituation and olfactory memories. J. Neurosci. 28, 10711-10719.
58. Shipley, M. T., and Ennis, M. (1996). Functional organization of olfactory system. J. Neurobiol. 30, 123-176.
59. Spors, H., and Grinvald, A. (2002). Spatio-temporal dynamics of odor representations in the mammalian olfactory bulb. Neuron 34, 301-315.
60. Stopfer, M., Bhagavan, S., Smith, B. H., and Laurent, G. (1997). Impaired odour discrimination on desyn-chronization of odour-encoding neural assemblies. Nature 390, 70-74.
61. Tsuno, Y., Kashiwadani, H., and Mori, K. (2008). Behavioral state regulation of dendrodendritic synaptic inhibition in the olfactory bulb. J. Neurosci. 28, 9227-9238.
62. Urban, N. N. (2002). Lateral inhibition in the olfactory bulb and in olfaction. Physiol. Behav. 77, 607-612.
63. Usher, M., Cohen, J. D., Servan-Schreiber, D., Rajkowski, J., and Aston-Jones, G. (1999). The role of locus coeruleus in the regulation of cognitive performance. Science 283, 549-554.
64. Weinberger, N. M. (2003). The nucleus basalis and memory codes: auditory cortical plasticity and the induction of specific, associative behavioral memory. Neurobiol. Learn. Mem. 80, 268-284.
65. Zaborszky, L., Carlsen, J., Brashear, H. R., and Heimer, L. (1986). Cholinergic and GABAergic affer-ents 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.