SpringerLink
Log in

Plasticity of Sniffing Pattern and Neural Activity in the Olfactory Bulb of Behaving Mice During Odor Sampling, Anticipation, and Reward

  • Original Article
  • Published:
Neuroscience Bulletin Aims and scope Submit manuscript

Abstract

The olfactory bulb (OB) is the first relay station in the olfactory system. In the OB, mitral/tufted cells (M/Ts), which are the main output neurons, play important roles in the processing and representation of odor information. Recent studies focusing on the function of M/Ts at the single-cell level in awake behaving mice have demonstrated that odor-evoked firing of single M/Ts displays transient/long-term plasticity during learning. Here, we tested whether the neural activity of M/Ts and sniffing patterns are dependent on anticipation and reward in awake behaving mice. We used an odor discrimination task combined with in vivo electrophysiological recordings in awake, head-fixed mice, and found that, while learning induced plasticity of spikes and beta oscillations during odor sampling, we also found plasticity of spikes, beta oscillation, sniffing pattern, and coherence between sniffing and theta oscillations during the periods of anticipation and/or reward. These results indicate that the activity of M/Ts plays important roles not only in odor representation but also in salience-related events such as anticipation and reward.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Germany)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Zhang W, Sun C, Shao Y, Zhou Z, Hou Y, Li A. Partial depletion of dopaminergic neurons in the substantia nigra impairs olfaction and alters neural activity in the olfactory bulb. Sci Rep 2019, 9: 254.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  2. ** H, Zhang JR, Shen Y, Liu CF. Clinical significance of REM sleep behavior disorders and other non-motor symptoms of Parkinsonism. Neurosci Bull 2017, 33: 576–584.

    Article  PubMed  PubMed Central  Google Scholar 

  3. Fullard ME, Morley JF, Duda JE. Olfactory dysfunction as an early biomarker in Parkinson’s disease. Neurosci Bull 2017, 33: 515–525.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Li A, Rao X, Zhou Y, Restrepo D. Complex neural representation of odour information in the olfactory bulb. Acta Physiol (Oxf) 2020, 228: e13333.

  5. Li A, Gire DH, Bozza T, Restrepo D. Precise detection of direct glomerular input duration by the olfactory bulb. J Neurosci 2014, 34: 16058–16064.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Roland B, Deneux T, Franks KM, Bathellier B, Fleischmann A. Odor identity coding by distributed ensembles of neurons in the mouse olfactory cortex. Elife 2017, 6.

  7. Chong E, Rinberg D. Behavioral readout of spatio-temporal codes in olfaction. Curr Opin Neurobiol 2018, 52: 18–24.

    Article  CAS  PubMed  Google Scholar 

  8. Wen P, Rao X, Xu L, Zhang Z, Jia F, He X, et al. Cortical organization of centrifugal afferents to the olfactory bulb: mono- and trans-synaptic tracing with recombinant neurotropic viral tracers. Neurosci Bull 2019, 35: 709–723.

    Article  PubMed  Google Scholar 

  9. Fletcher ML, Chen WR. Neural correlates of olfactory learning: Critical role of centrifugal neuromodulation. Learn Mem 2010, 17: 561–570.

    Article  PubMed  PubMed Central  Google Scholar 

  10. Linster C, Cleland TA. Neuromodulation of olfactory transformations. Curr Opin Neurobiol 2016, 40: 170–177.

    Article  CAS  PubMed  Google Scholar 

  11. Lizbinski KM, Dacks AM. Intrinsic and extrinsic neuromodulation of olfactory processing. Front Cell Neurosci 2017, 11: 424.

    Article  PubMed  CAS  Google Scholar 

  12. Restrepo D, Doucette W, Whitesell JD, McTavish TS, Salcedo E. From the top down: flexible reading of a fragmented odor map. Trends Neurosci 2009, 32: 525–531.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Li A, Gire DH, Restrepo D. Upsilon spike-field coherence in a population of olfactory bulb neurons differentiates between odors irrespective of associated outcome. J Neurosci 2015, 35: 5808–5822.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chu MW, Li WL, Komiyama T. Balancing the robustness and efficiency of odor representations during learning. Neuron 2016, 92: 174–186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gire DH, Restrepo D, Sejnowski TJ, Greer C, De Carlos JA, Lopez-Mascaraque L. Temporal processing in the olfactory system: can we see a smell? Neuron 2013, 78: 416–432.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Abraham NM, Vincis R, Lagier S, Rodriguez I, Carleton A. Long term functional plasticity of sensory inputs mediated by olfactory learning. Elife 2014, 3: e02109.

  17. Koldaeva A, Schaefer AT, Fukunaga I. Rapid task-dependent tuning of the mouse olfactory bulb. Elife 2019, 8: e43558.

  18. Rinberg D, Koulakov A, Gelperin A. Sparse odor coding in awake behaving mice. J Neurosci 2006, 26: 8857–8865.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Li A, Gong L, Xu F. Brain-state-independent neural representation of peripheral stimulation in rat olfactory bulb. Proc Natl Acad Sci U S A 2011, 108: 5087–5092.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Li A, Guthman EM, Doucette WT, Restrepo D. Behavioral status influences the dependence of odorant-induced change in firing on prestimulus firing rate. J Neurosci 2017, 37: 1835–1852.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Doucette W, Restrepo D. Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol 2008, 6: e258.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  22. Kay LM, Laurent G. Odor- and context-dependent modulation of mitral cell activity in behaving rats. Nat Neurosci 1999, 2: 1003–1009.

    Article  CAS  PubMed  Google Scholar 

  23. Jordan R, Fukunaga I, Kollo M, Schaefer AT. Active sampling state dynamically enhances olfactory bulb odor representation. Neuron 2018, 98: 1214–1228.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Sun C, Tang K, Wu J, Xu H, Zhang W, Cao T, et al. Leptin modulates olfactory discrimination and neural activity in the olfactory bulb. Acta Physiol (Oxf) 2019: e13319.

  26. Jeanne JM, Sharpee TO, Gentner TQ. Associative learning enhances population coding by inverting interneuronal correlation patterns. Neuron 2013, 78: 352–363.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Zhou Y, Wang X, Cao T, Xu J, Wang D, Restrepo D, et al. Insulin modulates neural activity of pyramidal neurons in the anterior piriform cortex. Front Cell Neurosci 2017, 11: 378.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  28. Slotnick B, Restrepo D. Olfactometry with mice. Curr Protoc Neurosci 2005, Chapter 8: Unit 8 20.

  29. Doucette W, Gire DH, Whitesell J, Carmean V, Lucero MT, Restrepo D. Associative cortex features in the first olfactory brain relay station. Neuron 2011, 69: 1176–1187.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Khan AG, Sarangi M, Bhalla US. Rats track odour trails accurately using a multi-layered strategy with near-optimal sampling. Nat Commun 2012, 3: 703.

    Article  PubMed  CAS  Google Scholar 

  31. Nguyen Chi V, Muller C, Wolfenstetter T, Yanovsky Y, Draguhn A, Tort AB, et al. Hippocampal respiration-driven rhythm distinct from theta oscillations in awake mice. J Neurosci 2016, 36: 162–177.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Ravel N, Chabaud P, Martin C, Gaveau V, Hugues E, Tallon-Baudry C, et al. Olfactory learning modifies the expression of odour-induced oscillatory responses in the gamma (60–90 Hz) and beta (15–40 Hz) bands in the rat olfactory bulb. Eur J Neurosci 2003, 17: 350–358.

    Article  PubMed  Google Scholar 

  33. Martin C, Gervais R, Hugues E, Messaoudi B, Ravel N. Learning modulation of odor-induced oscillatory responses in the rat olfactory bulb: a correlate of odor recognition? J Neurosci 2004, 24: 389–397.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Martin C, Ravel N. Beta and gamma oscillatory activities associated with olfactory memory tasks: different rhythms for different functional networks? Front Behav Neurosci 2014, 8: 218.

    PubMed  PubMed Central  Google Scholar 

  35. Kay LM. Olfactory system oscillations across phyla. Curr Opin Neurobiol 2015, 31: 141–147.

    Article  CAS  PubMed  Google Scholar 

  36. Kato HK, Chu MW, Isaacson JS, Komiyama T. Dynamic sensory representations in the olfactory bulb: modulation by wakefulness and experience. Neuron 2012, 76: 962–975.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Ross JM, Fletcher ML. Learning-dependent and -independent enhancement of mitral/tufted cell glomerular odor responses following olfactory fear conditioning in awake mice. J Neurosci 2018, 38: 4623–4640.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Fontanini A, Katz DB. Behavioral states, network states, and sensory response variability. J Neurophysiol 2008, 100: 1160–1168.

    Article  PubMed  PubMed Central  Google Scholar 

  39. Carlson KS, Gadziola MA, Dauster ES, Wesson DW. Selective attention controls olfactory decisions and the neural encoding of odors. Curr Biol 2018, 28: 2195–2205.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yamada Y, Bhaukaurally K, Madarasz TJ, Pouget A, Rodriguez I, Carleton A. Context- and output layer-dependent long-term ensemble plasticity in a sensory circuit. Neuron 2017, 93: 1198–1212.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Gourevitch B, Kay LM, Martin C. Directional coupling from the olfactory bulb to the hippocampus during a go/no-go odor discrimination task. J Neurophysiol 2010, 103: 2633–2641.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Frederick DE, Brown A, Tacopina S, Mehta N, Vujovic M, Brim E, et al. Task-dependent behavioral dynamics make the case for temporal integration in multiple strategies during odor processing. J Neurosci 2017, 37: 4416–4426.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Abraham NM, Guerin D, Bhaukaurally K, Carleton A. Similar odor discrimination behavior in head-restrained and freely moving mice. PLoS One 2012, 7: e51789.

  44. Rojas-Libano D, Frederick DE, Egana JI, Kay LM. The olfactory bulb theta rhythm follows all frequencies of diaphragmatic respiration in the freely behaving rat. Front Behav Neurosci 2014, 8: 214.

    PubMed  PubMed Central  Google Scholar 

  45. Calu DJ, Roesch MR, Stalnaker TA, Schoenbaum G. Associative encoding in posterior piriform cortex during odor discrimination and reversal learning. Cereb Cortex 2007, 17: 1342–1349.

    Article  PubMed  Google Scholar 

  46. Roesch MR, Stalnaker TA, Schoenbaum G. Associative encoding in anterior piriform cortex versus orbitofrontal cortex during odor discrimination and reversal learning. Cereb Cortex 2007, 17: 643–652.

    Article  PubMed  Google Scholar 

  47. Gelperin A, Ghatpande A. Neural basis of olfactory perception. Ann N Y Acad Sci 2009, 1170: 277–285.

    Article  PubMed  Google Scholar 

  48. Ogg MC, Ross JM, Bendahmane M, Fletcher ML. Olfactory bulb acetylcholine release dishabituates odor responses and reinstates odor investigation. Nat Commun 2018, 9: 1868.

    Google Scholar 

  49. Ma M, Luo M. Optogenetic activation of basal forebrain cholinergic neurons modulates neuronal excitability and sensory responses in the main olfactory bulb. J Neurosci 2012, 32: 10105–10116.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Liu ZX, Zhou JF, Li Y, Hu F, Lu Y, Ma M, et al. Dorsal raphe neurons signal reward through 5-HT and glutamate. Neuron 2014, 81: 1360–1374.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Luo M, Li Y, Zhong W. Do dorsal raphe 5-HT neurons encode “beneficialness”? Neurobiol Learn Mem 2016, 135: 40–49.

    Article  CAS  PubMed  Google Scholar 

  52. Moberly AH, Schreck M, Bhattarai JP, Zweifel LS, Luo W, Ma M. Olfactory inputs modulate respiration-related rhythmic activity in the prefrontal cortex and freezing behavior. Nat Commun 2018, 9: 1528.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. Fukunaga I, Berning M, Kollo M, Schmaltz A, Schaefer AT. Two distinct channels of olfactory bulb output. Neuron 2012, 75: 320–329.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (31571082, 31872771 and 31700895), the Natural Science Foundation of the Jiangsu Higher Education Institutions of China (16KJA180007), and the Natural Science Foundation of Jiangsu Province (BK20170260). We thank Siqi **g and Lingzhi Zhang for technical assistance.

Author information

Author notes

  1. Penglai Liu and Tiantian Cao have contributed equally to this work.

Authors and Affiliations

  1. Jiangsu Key Laboratory of Brain Disease and Bioinformation, Research Center for Biochemistry and Molecular Biology, Xuzhou Medical University, Xuzhou, 221004, China

    Penglai Liu, Tiantian Cao, **shan Xu, **ngfeng Mao, Dejuan Wang & Anan Li

Authors
  1. Penglai Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tiantian Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. **shan Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. **ngfeng Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dejuan Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anan Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Anan Li.

Ethics declarations

Conflict of interest

The authors declare that they have no competing financial interests.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 467 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, P., Cao, T., Xu, J. et al. Plasticity of Sniffing Pattern and Neural Activity in the Olfactory Bulb of Behaving Mice During Odor Sampling, Anticipation, and Reward. Neurosci. Bull. 36, 598–610 (2020). https://doi.org/10.1007/s12264-019-00463-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12264-019-00463-9

Keywords

Search

Navigation