Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb

Nature Neuroscience

Volumn 17, Issue 9, 2014, Pages 1208-1216

  Fukunaga, Izumi ^a,b   Herb, Jan T ^a,b,c   Kollo, Mihaly ^a,b   Boyden, Edward S ^d   Schaefer, Andreas T ^a,b,c,e  

^a MAX PLANCK INSTITUTE FOR MEDICAL RESEARCH   (Germany)

^b NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; VESICULAR INHIBITORY AMINO ACID TRANSPORTER;

ACTION POTENTIAL; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; BRAIN CORTEX; BREATHING; CELL LEVEL; CONTRAST ENHANCEMENT; CONTROLLED STUDY; EVOKED RESPONSE; GAMMA RHYTHM; GRANULE CELL; HIPPOCAMPUS; INHIBITORY POSTSYNAPTIC POTENTIAL; INTERNEURON; INTRACELLULAR RECORDING; MOUSE; NERVE CELL NETWORK; NONHUMAN; OLFACTORY BULB; PRIORITY JOURNAL; PROTEIN EXPRESSION; SYNAPTIC INHIBITION; THETA RHYTHM; WHOLE CELL PATCH CLAMP; ANIMAL; C57BL MOUSE; CYTOLOGY; NERVE CELL INHIBITION; ODOR; OPTOGENETICS; PATCH CLAMP TECHNIQUE; PHYSIOLOGY; TRANSGENIC MOUSE; WAKEFULNESS;

ANIMALS; EVOKED POTENTIALS; GAMMA RHYTHM; INTERNEURONS; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURAL INHIBITION; ODORS; OLFACTORY BULB; OPTOGENETICS; PATCH-CLAMP TECHNIQUES; SMELL; THETA RHYTHM; WAKEFULNESS;

EID: 84908443103     PISSN: 10976256     EISSN: 15461726     Source Type: Journal    
DOI: 10.1038/nn.3760     Document Type: Article

References (56)

1. Wachowiak, M. All in a sniff: olfaction as a model for active sensing. Neuron 71, 962-973 (2011).
2. Smear, M., Shusterman, R., O'Connor, R., Bozza, T. & Rinberg, D. Perception of sniff phase in mouse olfaction. Nature 479, 397-400 (2011).
3. Haddad, R. et al. Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat. Neurosci. 16, 949-957 (2013).
4. Freeman, W.J. III. 1972 Waves, Pulses, and the Theory of Neural Masses (Academic Press, 1972).
5. Sohal, V.S., Zhang, F., Yizhar, O. & Deisseroth, K. Parvalbumin neurons and gamma rhythms enhance cortical circuit performance. Nature 459, 698-702 (2009).
6. Royer, S. et al. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 15, 769-775 (2012).
7. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53-57 (2008).
8. Whittington, M.A. & Traub, R.D. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci. 26, 676-682 (2003).
9. Lisman, J.E. & Jensen, O. The theta-gamma neural code. Neuron 77, 1002-1016 (2013).
10. Kay, L.M. et al. Olfactory oscillations: the what, how and what for. Trends Neurosci. 32, 207-214 (2009).
11. Adrian, E.D. The electrical activity of the mammalian olfactory bulb. Electroencephalogr. Clin. Neurophysiol. 2, 377-388 (1950).
12. Macrides, F. & Chorover, S.L. Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175, 84-87 (1972).
13. Shusterman, R., Smear, M.C., Koulakov, A.A. & Rinberg, D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039-1044 (2011).
14. Margrie, T.W. & Schaefer, A.T. Theta oscillation coupled spike latencies yield computational vigour in a mammalian sensory system. J. Physiol. (Lond.) 546, 363-374 (2003).
15. Igarashi, K.M. et al. Parallel mitral and tufted cell pathways route distinct odor information to different targets in the olfactory cortex. J. Neurosci. 32, 7970-7985 (2012).
16. Fukunaga, I., Berning, M., Kollo, M., Schmaltz, A. & Schaefer, A.T. Two distinct channels of olfactory bulb output. Neuron 75, 320-329 (2012).
17. Phillips, M.E., Sachdev, R.N.S., Willhite, D.C. & Shepherd, G.M. Respiration drives network activity and modulates synaptic and circuit processing of lateral inhibition in the olfactory bulb. J. Neurosci. 32, 85-98 (2012).
18. 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).
19. Luo, M. & Katz, L.C. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32, 1165-1179 (2001).
20. 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).
21. 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. Rev. 55, 373-382 (2007).
22. Cleland, T.A. & Sethupathy, P. Non-topographical contrast enhancement in the olfactory bulb. BMC Neurosci. 7, 7 (2006).
23. MacLeod, K. & Laurent, G. Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274, 976-979 (1996).
24. Lagier, S., Carleton, A. & Lledo, P.-M. Interplay between local GABAergic interneurons and relay neurons generates gamma oscillations in the rat olfactory bulb. J. Neurosci. 24, 4382-4392 (2004).
25. Lepousez, G. & Lledo, P.-M. Odor discrimination requires proper olfactory fast oscillations in awake mice. Neuron 80, 1010-1024 (2013).
26. Bathellier, B., Lagier, S., Faure, P. & Lledo, P.-M. Circuit properties generating gamma oscillations in a network model of the olfactory bulb. J. Neurophysiol. 95, 2678-2691 (2006).
27. Nusser, Z., Kay, L.M., Laurent, G., Homanics, G.E. & Mody, I. Disruption of GABAA receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J. Neurophysiol. 86, 2823-2833 (2001).
28. Han, X. et al. A high-light sensitivity optical neural silencer: development and application to optogenetic control of non-human primate cortex. Front. Syst. Neurosci. 5, 18 (2011).
29. Taniguchi, H. et al. A resource of cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995-1013 (2011).
30. Vong, L. et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71, 142-154 (2011).
31. Parrish-Aungst, S., Shipley, M.T., Erdelyi, F., Szabo, G. & Puche, A.C. Quantitative analysis of neuronal diversity in the mouse olfactory bulb. J. Comp. Neurol. 501, 825-836 (2007).
32. Kiyokage, E. et al. Molecular identity of periglomerular and short axon cells. J. Neurosci. 30, 1185-1196 (2010).
33. Najac, M., De Saint Jan, D., Reguero, L., Grandes, P. & Charpak, S. Monosynaptic and polysynaptic feed-forward inputs to mitral cells from olfactory sensory neurons. J. Neurosci. 31, 8722-8729 (2011).
34. Margrie, T.W., Sakmann, B. & Urban, N.N. 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. USA 98, 319-324 (2001).
35. 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).
36. Rinberg, D., Koulakov, A. & Gelperin, A. Sparse odor coding in awake behaving mice. J. Neurosci. 26, 8857-8865 (2006).
37. Cazakoff, B.N., Lau, B.Y.B., Crump, K.L., Demmer, H.S. & Shea, S.D. Broadly tuned and respiration-independent inhibition in the olfactory bulb of awake mice. Nat. Neurosci. 17, 569-576 (2014).
38. Isaacson, J.S. & Strowbridge, B.W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20, 749-761 (1998).
39. Kato, H.K., Gillet, S.N., Peters, A.J., Isaacson, J.S. & Komiyama, T. Parvalbuminexpressing interneurons linearly control olfactory bulb output. Neuron 80, 1218-1231 (2013).
40. Miyamichi, K. et al. Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80, 1232-1245 (2013).
41. Labarrera, C., London, M. & Angelo, K. Tonic inhibition sets the state of excitability in olfactory bulb granule cells. J. Physiol. (Lond.) 591, 1841-1850 (2013).
42. Pressler, R.T. & Strowbridge, B.W. Blanes cells mediate persistent feedforward inhibition onto granule cells in the olfactory bulb. Neuron 49, 889-904 (2006).
43. Manabe, H. & Mori, K. Sniff rhythm-paced fast and slow gamma-oscillations in the olfactory bulb: relation to tufted and mitral cells and behavioral states. J. Neurophysiol. 110, 1593-1599 (2013).
44. Livneh, Y., Adam, Y. & Mizrahi, A. Odor processing by adult-born neurons. Neuron 81, 1097-1110 (2014).
45. Shimshek, D.R. et al. Enhanced odor discrimination and impaired olfactory memory by spatially controlled switch of ampa receptors. PLoS Biol. 3, e354 (2005).
46. Abraham, N.M. et al. Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 65, 399-411 (2010).
47. MacLeod, K., Backer, A. & Laurent, G. Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395, 693-698 (1998).
48. Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828-832 (2003).
49. Akam, T.E. & Kullmann, D.M. Efficient 'communication through coherence' requires oscillations structured to minimize interference between signals. PLoS Comput. Biol. 8, e1002760 (2012).
50. Tsai, H.-C. et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080-1084 (2009).
51. During, M., Young, D., Baer, K., Lawlor, P. & Klugmann, M. Development and optimization of adeno-associated virus vector transfer into the central nervous system. in Viral Vectors for Gene Therapy, Vol. 76. Methods in Molecular Medicine (ed. Machida, C.A.) 221-236 (Humana Press, 2003).
52. Marx, M., Gunter, R.H., Hucko, W., Radnikow, G. & Feldmeyer, D. Improved biocytin labeling and neuronal 3D reconstruction. Nat. Protoc. 7, 394-407 (2012).
53. Fisher, N.I. Statistical Analysis of Circular Data (Cambridge University Press, 1996).
54. Mitra, P. & Bokil, H. 2007 Observed Brain Dynamics (Oxford University Press, USA, 2007).
55. Kay, L.M. & Lazzara, P. How global are olfactory bulb oscillations? J. Neurophysiol. 104, 1768-1773 (2010).
56. Gabbiani, F. & Koch, C. Principles of spike train analysis. in Methods In Neuronal Modeling: From Synapses To Networks (eds. Koch, C. & Segev, I.) 313-360 (MIT Press, 1998).