Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice

Nature Neuroscience

Volumn 17, Issue 4, 2014, Pages 569-576

  Cazakoff, Brittany N ^a   Lau, Billy Y B ^a   Crump, Kerensa L ^a   Demmer, Heike S ^a   Shea, Stephen D ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADULT; ANIMAL EXPERIMENT; ARTICLE; BRAIN CORTEX; BREATHING; CONTROLLED STUDY; CORTICAL SYNCHRONIZATION; FACILITATION; GRANULE CELL; MALE; MOUSE; NONHUMAN; ODOR; OLFACTORY BULB; PRIORITY JOURNAL; WAKEFULNESS;

ANESTHESIA; ANIMALS; BEHAVIOR, ANIMAL; CELL RESPIRATION; MALE; MICE; MICE, INBRED C57BL; NEURAL INHIBITION; NEURONS; ODORS; OLFACTORY BULB; OLFACTORY PERCEPTION; PATCH-CLAMP TECHNIQUES; WAKEFULNESS;

EID: 84897082338     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3669     Document Type: Article

References (52)

1. Gilbert, C.D. & Sigman, M. Brain states: Top-down influences in sensory processing. Neuron 54, 677-696 (2007
2. Sohal, V.S., Zhang, F., Yizhar, O. & Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698-702 (2009
3. Cardin, J.A. et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 459, 663-667 (2009
4. Haider, B., Hausser, M. & Carandini, M. Inhibition dominates sensory responses in the awake cortex. Nature 493, 97-100 (2013
5. Gentet, L.J. et al. Unique functional properties of somatostatin- expressing GABAergic neurons in mouse barrel cortex. Nat. Neurosci. 15, 607-612 (2012
6. Polack, P.O., Friedman, J. & Golshani, P. Cellular mechanisms of brain state-dependent gain modulation in visual cortex. Nat. Neurosci. 16, 1331-1339 (2013
7. Rinberg, D., Koulakov, A. & Gelperin, A. Sparse odor coding in awake behaving mice. J. Neurosci. 26, 8857-8865 (2006
8. Davison, I.G. & Katz, L.C. Sparse and selective odor coding by mitral/tufted neurons in the main olfactory bulb. J. Neurosci. 27, 2091-2101 (2007
9. Cury, K.M. & Uchida, N. Robust odor coding via inhalation-coupled transient activity in the mammalian olfactory bulb. Neuron 68, 570-585 (2010
10. Shusterman, R., Smear, M.C., Koulakov, A.A. & Rinberg, D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039-1044 (2011
11. Kay, L.M. & Laurent, G. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat. Neurosci. 2, 1003-1009 (1999
12. Doucette, W. & Restrepo, D. Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 6, e258 (2008
13. Doucette, W. et al. Associative cortex features in the first olfactory brain relay station. Neuron 69, 1176-1187 (2011
14. Kato, H.K., Chu, M.W., Isaacson, J.S. & Komiyama, T. Dynamic sensory representations in the olfactory bulb: Modulation by wakefulness and experience. Neuron 76, 962-975 (2012
15. Mouret, A., Murray, K. & Lledo, P.M. Centrifugal drive onto local inhibitory interneurons of the olfactory bulb. Ann. NY Acad. Sci. 1170, 239-254 (2009
16. Boyd, A.M., Sturgill, J.F., Poo, C. & Isaacson, J.S. Cortical feedback control of olfactory bulb circuits. Neuron 76, 1161-1174 (2012
17. Markopoulos, F., Rokni, D., Gire, D.H. & Murthy, V.N. Functional properties of cortical feedback projections to the olfactory bulb. Neuron 76, 1175-1188 (2012
18. Fuentes, R.A., Aguilar, M.I., Aylwin, M.L. & Maldonado, P.E. Neuronal activity of mitral-tufted cells in awake rats during passive and active odorant stimulation. J. Neurophysiol. 100, 422-430 (2008
19. Abraham, N.M. et al. Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 65, 399-411 (2010
20. Isaacson, J.S. & Strowbridge, B.W. Olfactory reciprocal synapses: Dendritic signaling in the CNS. Neuron 20, 749-761 (1998
21. Jahr, C.E. & Nicoll, R.A. Dendrodendritic inhibition: Demonstration with intracellular recording. Science 207, 1473-1475 (1980
22. Giridhar, S. & Urban, N.N. Mechanisms and benefits of granule cell latency coding in the mouse olfactory bulb. Front. Neural Circuits 6, 40 (2012
23. Kay, L.M. et al. Olfactory oscillations: The what, how and what for. Trends Neurosci. 32, 207-214 (2009
24. Koulakov, A.A. & Rinberg, D. Sparse incomplete representations: A potential role of olfactory granule cells. Neuron 72, 124-136 (2011
25. Shepherd, G.M., Chen, W.R., Willhite, D., Migliore, M. & Greer, C.A. The olfactory granule cell: From classical enigma to central role in olfactory processing. Brain Res. Brain Res. Rev. 55, 373-382 (2007
26. Tsuno, Y., Kashiwadani, H. & Mori, K. Behavioral state regulation of dendrodendritic synaptic inhibition in the olfactory bulb. J. Neurosci. 28, 9227-9238 (2008
27. Vucinic, D., Cohen, L.B. & Kosmidis, E.K. Interglomerular center-surround inhibition shapes odorant-evoked input to the mouse olfactory bulb in vivo. J. Neurophysiol. 95, 1881-1887 (2006
28. Yokoi, M., Mori, K. & Nakanishi, S. Refinement of odor molecule tuning by dendrodendritic synaptic inhibition in the olfactory bulb. Proc. Natl. Acad. Sci. USA 92, 3371-3375 (1995
29. Cang, J. & Isaacson, J.S. In vivo whole-cell recording of odor-evoked synaptic transmission in the rat olfactory bulb. J. Neurosci. 23, 4108-4116 (2003
30. Tan, J., Savigner, A., Ma, M. & Luo, M. Odor information processing by the olfactory bulb analyzed in gene-targeted mice. Neuron 65, 912-926 (2010
31. Wellis, D.P. & Scott, J.W. Intracellular responses of identified rat olfactory bulb interneurons to electrical and odor stimulation. J. Neurophysiol. 64, 932-947 (1990
32. Pressler, R.T. & Strowbridge, B.W. Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49, 889-904 (2006
33. Niell, C.M. & Stryker, M.P. Modulation of visual responses by behavioral state in mouse visual cortex. Neuron 65, 472-479 (2010
34. Macrides, F. & Chorover, S.L. Olfactory bulb units: Activity correlated with inhalation cycles and odor quality. Science 175, 84-87 (1972
35. Meredith, M. Patterned response to odor in mammalian olfactory bulb: The influence of intensity. J. Neurophysiol. 56, 572-597 (1986
36. Chaput, M. & Holley, A. Single unit responses of olfactory bulb neurones to odour presentation in awake rabbits. J. Physiol. (Paris) 76, 551-558 (1980
37. Fukunaga, I., Berning, M., Kollo, M., Schmaltz, A. & Schaefer, A.T. Two distinct channels of olfactory bulb output. Neuron 75, 320-329 (2012
38. Berens, P. CircStat: A MATLAB toolbox for circular statistics. J. Stat. Softw. 31, 1-21 (2009
39. Dhawale, A.K., Hagiwara, A., Bhalla, U.S., Murthy, V.N. & Albeanu, D.F. Non-redundant odor coding by sister mitral cells revealed by light addressable glomeruli in the mouse. Nat. Neurosci. 13, 1404-1412 (2010
40. Fantana, A.L., Soucy, E.R. & Meister, M. Rat olfactory bulb mitral cells receive sparse glomerular inputs. Neuron 59, 802-814 (2008
41. Khan, A.G., Thattai, M. & Bhalla, U.S. Odor representations in the rat olfactory bulb change smoothly with morphing stimuli. Neuron 57, 571-585 (2008
42. Kato, H.K., Gillet, S.N., Peters, A.J., Isaacson, J.S. & Komiyama, T. Parvalbumin-expressing interneurons linearly control olfactory bulb output. Neuron 80, 1218-1231 (2013
43. Miyamichi, K. et al. Dissecting local circuits: Parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80, 1232-1245 (2013
44. Apicella, A., Yuan, Q., Scanziani, M. & Isaacson, J.S. Pyramidal cells in piriform cortex receive convergent input from distinct olfactory bulb glomeruli. J. Neurosci. 30, 14255-14260 (2010
45. Davison, I.G. & Ehlers, M.D. Neural circuit mechanisms for pattern detection and feature combination in olfactory cortex. Neuron 70, 82-94 (2011
46. Illig, K.R. & Haberly, L.B. Odor-evoked activity is spatially distributed in piriform cortex. J. Comp. Neurol. 457, 361-373 (2003
47. Sosulski, D.L., Bloom, M.L., Cutforth, T., Axel, R. & Datta, S.R. Distinct representations of olfactory information in different cortical centres. Nature 472, 213-216 (2011
48. Miyamichi, K. et al. Cortical representations of olfactory input by trans-synaptic tracing. Nature 472, 191-196 (2011
49. Haddad, R. et al. Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat. Neurosci. 16, 949-957 (2013
50. Miura, K., Mainen, Z.F. & Uchida, N. Odor representations in olfactory cortex: Distributed rate coding and decorrelated population activity. Neuron 74, 1087-1098 (2012
51. Shea, S.D., Katz, L.C. & Mooney, R. Noradrenergic induction of odor-specific neural habituation and olfactory memories. J. Neurosci. 28, 10711-10719 (2008
52. Hegde, J. & Van Essen, D.C. Temporal dynamics of shape analysis in macaque visual area V2. J. Neurophysiol. 92, 3030-3042 (2004