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.

  • Correspondence
  • Published:

The sensory immune system: a neural twist to the antigenic discontinuity theory

Nature Reviews Immunology volume 14, page 280 (2014)Cite this article

Subjects

Access through your institution
Buy or subscribe

In their recent Essay (The speed of change: towards a discontinuity theory of immunity? Nature Rev. Immunol. 13, 764–769 (2013))1, Pradeu et al. proposed that rather than antigens per se, antigenic discontinuity is a major determinant of immune responses. However, the immune system is currently viewed as a complex network of cells and molecules that are endowed with the unique ability to discriminate self from non-self and to recognize specific molecular patterns associated with pathogens or damaged tissues2,3,4,5. To reconcile those two partially divergent theories, I argue that our current theoretical conception of immunity is possibly biased by an incomplete picture of the so-called 'immune recognition' process. Indeed, although Jerne6 was the first to enrich the immunological lexicon with neuroscience-derived terms, such as 'recognition', 'learning' and 'memory' (Refs 4,6), this analogy-based reasoning may have missed some important aspects of neurophysiology and neurocognitive science.

As an example, depending on our auditory attention and the level of background noise accompanying a given auditory input, the auditory processing (integration) step may or may not permit the discrimination of meaningful auditory objects from meaningless ones7,8. Also, although the rhythmicity of an auditory input is one of a number of signal-dependent features that drives our perception of this particular signal, this perception may be in fine shaped by signal-independent factors that comprise our auditory attention and by the presence of superimposed auditory inputs9,10,11. On this basis, a parallel could be established between the sensory nervous system and the afferent arm of immunity, and we propose the term 'immune perception' to describe the function of 'immune recognition'. In this conception of a sensory immune system, perception of immune signals would not only be determined by their intrinsic nature (for example, their antigenic structure, and the presence of danger-associated molecular patterns (DAMPs) or pathogen-associated molecular patterns (PAMPs)) and the rhythmicity of their occurrence (antigenic discontinuity) but also by signal-independent parameters that would condition the integration step of immune perception. These would notably include age12, gender13, metabolic status14 and gut microbiota composition15. In all likelihood, such an integration step would essentially take place in secondary lymphoid organs and would be shaped by systemic blood-circulating factors (Fig. 1b).

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

Access options

Access through your institution

Buy this article

  • Purchase on SpringerLink
  • Instant access to full article PDF
Buy now

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

Figure 1: Comparison of the sensory nervous and immune systems.

References

  1. Pradeu, T., Jaeger, S. & Vivier, E. The speed of change: towards a discontinuity theory of immunity? Nature Rev. Immunol. 13, 764–769 (2013).

    Article  CAS  Google Scholar 

  2. Burnet, F. M. & Fenner, F. The Production of Antibodies 2nd edn (Macmillan and Co., 1949).

    Google Scholar 

  3. Tauber, A. I. The Immune Self: Theory or Metaphor? (Cambridge Univ. Press, 1994).

    Book  Google Scholar 

  4. Tauber, A. in The Stanford Encyclopedia of Philosophy (ed. Zalta, E. N.) [online], (2012).

    Google Scholar 

  5. Matzinger, P. The danger model: a renewed sense of self. Science 296, 301–305 (2002).

    Article  CAS  Google Scholar 

  6. Jerne, N. K. Towards a network theory of the immune system. Ann. Immunol. (Paris) 125C, 373–389 (1974).

    CAS  Google Scholar 

  7. Rabinowitz, N. C., Willmore, B. D., King, A. J. & Schnupp, J. W. Constructing noise-invariant representations of sound in the auditory pathway. PLoS Biol. 11, e1001710 (2013).

    Article  Google Scholar 

  8. Bar-Yosef, O., Rotman, Y. & Nelken, I. Responses of neurons in cat primary auditory cortex to bird chirps: effects of temporal and spectral context. J. Neurosci. 22, 8619–8632 (2002).

    Article  CAS  Google Scholar 

  9. Lakatos, P. et al. The spectrotemporal filter mechanism of auditory selective attention. Neuron 77, 750–761 (2013).

    Article  CAS  Google Scholar 

  10. Okamoto, H., Teismann, H., Keceli, S., Pantev, C. & Kakigi, R. Differential effects of temporal regularity on auditory-evoked response amplitude: a decrease in silence and increase in noise. Behav. Brain Funct. 9, 44 (2013).

    Article  Google Scholar 

  11. Seydell-Greenwald, A., Greenberg, A. S. & Rauschecker, J. P. Are you listening? Brain activation associated with sustained nonspatial auditory attention in the presence and absence of stimulation. Hum. Brain Mapp. http://dx.doi.org/10.1002/hbm.22323 (2013).

  12. Anderson, C. C. & Matzinger, P. Immunity or tolerance: opposite outcomes of microchimerism from skin grafts. Nature Med. 7, 80–87 (2001).

    Article  CAS  Google Scholar 

  13. Zhao, G., Moore, D. J. & Kim, J. I. Inhibition of transplantation tolerance by immune senescence is reversed by endocrine modulation. Sci. Transl Med. 3, 87ra52 (2011).

    Article  Google Scholar 

  14. Procaccini, C., De Rosa, V. & Galgani, M. An oscillatory switch in mTOR kinase activity sets regulatory T cell responsiveness. Immunity 33, 929–941 (2010).

    Article  CAS  Google Scholar 

  15. Iida, N., Dzutsev, A. & Stewart, C. A. Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342, 967–970 (2013).

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Serge Nataf is at the Lyon Neuroscience Research Center, INSERM 1028 CNRS UMR5292, University Lyon-1, Banque de tissus et de cellules, Hôpital Edouard Herriot, Lyon University Hospital (Hospices Civils de Lyon), Lyon F-69000, France.,

    Serge Nataf

Authors
  1. Serge Nataf
    View author publications

    Search author on:PubMed Google Scholar

Corresponding author

Correspondence to Serge Nataf.

Ethics declarations

Competing interests

The author declares no competing financial interests.

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nataf, S. The sensory immune system: a neural twist to the antigenic discontinuity theory. Nat Rev Immunol 14, 280 (2014). https://doi.org/10.1038/nri3521-c1

Download citation

  • Published:

  • Issue date:

  • DOI: https://doi.org/10.1038/nri3521-c1

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