Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

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

Nature Neuroscience volume 17, pages 1208–1216 (2014)Cite this article

Subjects

This article has been updated

Abstract

Circuits in the brain possess the ability to orchestrate activities on different timescales, but the manner in which distinct circuits interact to sculpt diverse rhythms remains unresolved. The olfactory bulb is a classic example of a place in which slow theta and fast gamma rhythms coexist. Furthermore, inhibitory interneurons that are generally implicated in rhythm generation are segregated into distinct layers, neatly separating local and global motifs. We combined intracellular recordings in vivo with circuit-specific optogenetic interference to examine the contribution of inhibition to rhythmic activity in the mouse olfactory bulb. We found that the two inhibitory circuits controlled rhythms on distinct timescales: local, glomerular networks coordinated theta activity, regulating baseline and odor-evoked inhibition, whereas granule cells orchestrated gamma synchrony and spike timing. Notably, granule cells did not contribute to baseline rhythms or sniff-coupled odor-evoked inhibition. Thus, activities on theta and gamma timescales are controlled by separate, dissociable inhibitory networks in the olfactory bulb.

This is a preview of subscription content, access via your institution

Relevant articles

Open Access articles citing this article.

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

Learn more

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Efficiency and specificity of optogenetic silencing of granule cells in vitro and in vivo.
Figure 2: Glomerular layer inhibition structures the baseline theta rhythm.
Figure 3: Sniff coupling of distinct JGC populations.
Figure 4: GL inhibition, rather than GC lateral inhibition, underlies slow odor-evoked inhibition.
Figure 5: Feedforward circuit in the GL likely mediates the evoked inhibition.
Figure 6: Granule cells coordinate neuronal activities on a fast timescale.
Figure 7: GCs contribute to fast, but not slow, activities in awake animals.

Change history

  • 22 July 2014

    In the version of this article initially published, the first construct under "Virus generation and stereotaxic injections" in the Online Methods was given as AAV-EF1A-DIO-Chr2-GFP. The correct construct is AAV-EF1A-DIO-Chr2-EYFP. The error has been corrected in the HTML and PDF versions of the article.

References

  1. Wachowiak, M. All in a sniff: olfaction as a model for active sensing. Neuron 71, 962–973 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Smear, M., Shusterman, R., O'Connor, R., Bozza, T. & Rinberg, D. Perception of sniff phase in mouse olfaction. Nature 479, 397–400 (2011).

    Article  CAS  PubMed  Google Scholar 

  3. Haddad, R. et al. Olfactory cortical neurons read out a relative time code in the olfactory bulb. Nat. Neurosci. 16, 949–957 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Klausberger, T. & Somogyi, P. Neuronal diversity and temporal dynamics: the unity of hippocampal circuit operations. Science 321, 53–57 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Whittington, M.A. & Traub, R.D. Interneuron diversity series: inhibitory interneurons and network oscillations in vitro. Trends Neurosci. 26, 676–682 (2003).

    Article  CAS  PubMed  Google Scholar 

  9. Lisman, J.E. & Jensen, O. The theta-gamma neural code. Neuron 77, 1002–1016 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Kay, L.M. et al. Olfactory oscillations: the what, how and what for. Trends Neurosci. 32, 207–214 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Adrian, E.D. The electrical activity of the mammalian olfactory bulb. Electroencephalogr. Clin. Neurophysiol. 2, 377–388 (1950).

    Article  CAS  PubMed  Google Scholar 

  12. Macrides, F. & Chorover, S.L. Olfactory bulb units: activity correlated with inhalation cycles and odor quality. Science 175, 84–87 (1972).

    Article  CAS  PubMed  Google Scholar 

  13. Shusterman, R., Smear, M.C., Koulakov, A.A. & Rinberg, D. Precise olfactory responses tile the sniff cycle. Nat. Neurosci. 14, 1039–1044 (2011).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Fukunaga, I., Berning, M., Kollo, M., Schmaltz, A. & Schaefer, A.T. Two distinct channels of olfactory bulb output. Neuron 75, 320–329 (2012).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Luo, M. & Katz, L.C. Response correlation maps of neurons in the mammalian olfactory bulb. Neuron 32, 1165–1179 (2001).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  22. Cleland, T.A. & Sethupathy, P. Non-topographical contrast enhancement in the olfactory bulb. BMC Neurosci. 7, 7 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  23. MacLeod, K. & Laurent, G. Distinct mechanisms for synchronization and temporal patterning of odor-encoding neural assemblies. Science 274, 976–979 (1996).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Lepousez, G. & Lledo, P.-M. Odor discrimination requires proper olfactory fast oscillations in awake mice. Neuron 80, 1010–1024 (2013).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Vong, L. et al. Leptin action on GABAergic neurons prevents obesity and reduces inhibitory tone to POMC neurons. Neuron 71, 142–154 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  32. Kiyokage, E. et al. Molecular identity of periglomerular and short axon cells. J. Neurosci. 30, 1185–1196 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Rinberg, D., Koulakov, A. & Gelperin, A. Sparse odor coding in awake behaving mice. J. Neurosci. 26, 8857–8865 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  38. Isaacson, J.S. & Strowbridge, B.W. Olfactory reciprocal synapses: dendritic signaling in the CNS. Neuron 20, 749–761 (1998).

    Article  CAS  PubMed  Google Scholar 

  39. 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).

    Article  CAS  PubMed  Google Scholar 

  40. Miyamichi, K. et al. Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80, 1232–1245 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  Google Scholar 

  44. Livneh, Y., Adam, Y. & Mizrahi, A. Odor processing by adult-born neurons. Neuron 81, 1097–1110 (2014).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Abraham, N.M. et al. Synaptic inhibition in the olfactory bulb accelerates odor discrimination in mice. Neuron 65, 399–411 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. MacLeod, K., Backer, A. & Laurent, G. Who reads temporal information contained across synchronized and oscillatory spike trains? Nature 395, 693–698 (1998).

    Article  CAS  PubMed  Google Scholar 

  48. Huxter, J., Burgess, N. & O'Keefe, J. Independent rate and temporal coding in hippocampal pyramidal cells. Nature 425, 828–832 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Tsai, H.-C. et al. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324, 1080–1084 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  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).

    Article  CAS  PubMed  Google Scholar 

  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).

    Article  PubMed  PubMed Central  Google Scholar 

  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).

Download references

Acknowledgements

We thank M. Kaiser, E. Stier and G. Matthies for technical assistance, A. Balz and S. Martin for stereotactic injections, S. Belanca for morphological reconstructions, J. Reinert for virus characterization, A. Schmaltz and M. Abdelhamid for help with setting up the head-fixed awake preparation, G. Giese and A. Scherbarth for glass brain preparation and imaging, B. Lowell, L. Vong and V. Murthy (Harvard University) for providing Vgat-IRES-Cre knock-in mice, R. Sprengel (MPI for Medical Research) for the Cre antibody, T. Margrie, T. Cleland and W. Denk for discussion, and T. Margrie, D. Burdakov, H. Monyer, R. Jordan, A. Grabska-Barwiń´ska and M. Helmstaedter for comments on earlier versions of the manuscript. This work was supported by the Max Planck Society, the DFG-SPP1392, the Federal Ministry of Education and Research (US-German collaboration computational neuroscience), the Alexander von Humbold Foundation (AvH), the Medical Research Council (MC_UP_1202/5), the ExcellenzCluster CellNetworks, and the Gottschalk foundation.

Author information

Authors and Affiliations

  1. Behavioural Neurophysiology, Max Planck Institute for Medical Research, Heidelberg, Germany

    Izumi Fukunaga, Jan T Herb, Mihaly Kollo & Andreas T Schaefer

  2. Division of Neurophysiology, MRC National Institute for Medical Research, London, UK

    Izumi Fukunaga, Jan T Herb, Mihaly Kollo & Andreas T Schaefer

  3. Department Anatomy and Cell Biology, Faculty of Medicine, University of Heidelberg, Heidelberg, Germany

    Jan T Herb & Andreas T Schaefer

  4. Media Lab, Synthetic Neurobiology Group, Massachusetts Institute of Technology, Cambridge, Massachusetts, USA

    Edward S Boyden

  5. Department of Neuroscience, Physiology and Pharmacology, University College London, London, UK

    Andreas T Schaefer

Authors
  1. Izumi Fukunaga
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jan T Herb
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mihaly Kollo
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Edward S Boyden
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andreas T Schaefer
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

I.F. and A.T.S. conceived and designed the experiments and wrote the paper with inputs from all authors. I.F. performed in vivo experiments in anesthetized and awake animals. J.H. performed in vitro physiology experiments and made and characterized AAV. M.K. contributed data from awake animals. E.S.B. provided ArchT viral constructs and assisted with the design of the optogenetic experiments.

Corresponding authors

Correspondence to Izumi Fukunaga or Andreas T Schaefer.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Integrated supplementary information

Supplementary Figure 1 Schematic of how inhibition in the OB structures the timing of activities.

(a) Simplified OB circuitry: glutamatergic inputs from the olfactory nerve (ON) are transmitted to principal neurons within glomeruli in the glomerular layer (GL). In the GL, juxtaglomerular cells (JGC) mediate largely local inhibition. Granule cells (GC) in the granule cell layer (GCL) inhibit the lateral dendrites of principal neurons across larger distances. (b) Inhibition in the OB establishes a phase-shift in sniff-coupled activities between MCs (pink) and TCs (blue) at rest16. Gray trace (bottom) represents the nasal airflow, with lighter gray indicating inhalation. (c) Odor presentation frequently results in slow inhibition of M/TCs13,19,20,34, causing a pause in their action potential discharge. (d) Faster, gamma range activities in the OB or its insect analogue are evoked by odors and require inhibition4,10,11. (e) Schematic of the finding. Glomerular layer interneurons (orange) structure activities on the theta timescale, setting phase preferences and modulate amplitudes of sniff-coupled activities. Theta activities are regulated during baseline period, as well as during responses to odors. Activities on a faster timescale, here in the gamma frequency range, are observed often nested in theta rhythms, and are controlled by the circuits in the granule cell layer (blue). Thus the OB outputs are highly regulated in both theta and gamma range frequencies by actions of dissociable circuits in the glomerular layer and GC layer.

Supplementary Figure 2 GC silencing at different depths.

Optogenetic manipulations in vivo require light to penetrate thicker tissues to achieve sufficiently high light intensities at relevant light activatable receptors. Plots here show light evoked Vm deviation in GCs recorded at various depths (vertical distance from the OB surface) for Gad2-Cre animals (anaesthetized) and Vgat-Cre animals (awake, head-fixed) injected into the GCL with AAV-FLEX-ArchT. Each data point corresponds to one GC.

Supplementary Figure 3 Sniff-coupled inhibition is reduced with glomerular layer silencing in both Gad2-Cre and Vgat-Cre mice.

(a) Example of local infection with glomerular injection of AAV-FLEX-ArchT in a Gad2-Cre animal. Scale bars = 1 mm (left) and 0.1 mm (right). Less than <0.05% of GCL interneurons were infected with glomerular injection (n = 2 OB). (b) Example high-resolution image from another animal. (c) Odor-evoked hyperpolarization under control (odor only) conditions and with light application (+LED) in Gad2-Cre (blue; n = 3 cells) and Vgat-Cre (brown; n = 4 cells) animals with glomerular layer injection of AAV-FLEX-ArchT.

Supplementary Figure 4 Possible involvement of GL feedforward circuit in evoked inhibition.

(a) An example recording from an M/TC, where an odor evoked inhibition. Pink arrowhead indicates the preferred phase of hyperpolarization for this example cell. The dotted line indicates the onset of first inhalation after valve opening. Sniff cycle 1 is the first complete cycle after the opening of the odor valve. (b) An example of whole-cell recording from a PGo with an excitatory response to an odor. Pink arrowhead is the preferred phase of M/TC hyperpolarization as in (a). PGo was identified as described in Fig 3. (c) Summary PSTH from all action potential times recorded from all PGo cell – odor pairs where an excitatory response was observed (n= 3 PGo cells). Time = 0 is the inhalation onset. Pink arrowhead is the preferred phase of M/TC hyperpolarization as in (a). (d) Polar histogram of individual AP phase from the 3 PGo cells. The range shown in pink is the preferred phase of inhibition evoked in all M/TCs (n=31 cells) during sniff cycle 1 (a). Ticks indicate the 25, 50 & 75 percentiles. Scale bar = π/6 radians, corresponding to 33.7 ms when calibrated to the average sniff cycle length. (e) In some cells, as shown in this example, increasing the concentration of odor that at low concentrations evoked hyperpolarization resulted in emergence of excitatory responses. No drugs were applied for this experiment. Values on the left are the concentrations of isoamylacetate presented (% of saturated vapour). (f) Data from Fig 5b is replotted, also as histograms (blue = hyperpolarizing response during control; black = no detectable response during control). (g) Histogram of evoked Vm in M/TCs recorded only in the GABAA-clamp condition, without paired control showing similar distribution to (f). (h) Conversion to depolarization in GABAA-clamp was often strong enough to elicit action potentials. Cell-odor pairs here showed evoked inhibition during control. n = 11 cells (same cells and odor as in Fig 5b). Each data point is the average of 2-6 repeated trials. (i) Top: Two example cells with odor-evoked activity during control and GABAA-clamp. Below: Relationship of odor-evoked depolarization/hyperpolarization between control and GABAA-clamp. Note the inverse relationship between responses evoked during control and unmasked with GABAA-clamp. r = -0.56, p = 0.01, n = 20 cells.

Supplementary Figure 5 Fast inhibitory transients are reduced during GCL silencing.

(a) Experimental configuration: whole-cell recordings were made in vitro from MCs in OB slices cut from Gad2-Cre animals with GC layer injection of AAV- FLEX-ArchT. Depolarising current was injected to elicit bursts of APs in MCs, which evoke recurrent inhibition in the recorded cell. (b) In addition to slow recurrent hyperpolarization, individual, fast recurrent IPSPs can be resolved (detected events indicated by gray arrowheads). (c) Same cell and conditions as in (b) but with light-evoked silencing of GCs. (+LED, green). Scale bars = 1 mV, 10 ms. (d) Summary histograms of the change in IPSP count due to light-mediated GCL silencing. (n = 25 cells).

Supplementary Figure 6 GC silencing does not cause significant change in firing rates.

(a) Experimental configuration: odors were presented to anaesthetized Vgat-Cre mice injected with AAV-FLEX-ArchT into the GC layer while whole-cell recordings from TCs were made. GCs were silenced for intermittent trials. (b) Examples of evoked depolarizing response to odor during control condition (above, black trace) and during GC silencing (below, green). Scale bars = 5 mV, 50 ms, same example as in Fig. 6e,f on a magnified scale. (c) Scatter plot of instantaneous firing rates for control (black dots) and during GC silencing (green). Each dot is the reciprocal of the interval between an action potential that occurs at time indicated (x axis) and the next action potential, in Hz. (Same cell as in b, n = 6 trials each for control and +LED). (d) Histogram of instantaneous firing rates for all cells (n = 9 TCs; the same as shown in Fig. 6). (e) Summary data showing average instantaneous firing rate for individual cells.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–6 (PDF 2342 kb)

Supplementary Methods Checklist (PDF 384 kb)

Extent of GCL infection imaged with light sheet.

Extent of GFP expression following GCL injection in the left olfactory bulb was imaged in a cleared tissue using a light sheet microscopy (courtesy of Guenter Giese and AnneMarie Scherbarth). Image was taken every 5 m to produce this z-stack. (MOV 5311 kb)

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fukunaga, I., Herb, J., Kollo, M. et al. Independent control of gamma and theta activity by distinct interneuron networks in the olfactory bulb. Nat Neurosci 17, 1208–1216 (2014). https://doi.org/10.1038/nn.3760

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.3760

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing