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.

Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity

Abstract

Learning to adapt to a complex and fluctuating environment requires the ability to adjust neural representations of sensory stimuli. Through pattern completion processes, cortical networks can reconstruct familiar patterns from degraded input patterns, whereas pattern separation processes allow discrimination of even highly overlapping inputs. Here we show that the balance between pattern separation and completion is experience dependent. Rats given extensive training with overlapping complex odorant mixtures showed improved behavioral discrimination ability and enhanced piriform cortical ensemble pattern separation. In contrast, behavioral training to disregard normally detectable differences between overlapping mixtures resulted in impaired piriform cortical ensemble pattern separation (enhanced pattern completion) and impaired discrimination. This bidirectional effect was not found in the olfactory bulb; it may be due to plasticity within olfactory cortex itself. Thus pattern recognition, and the balance between pattern separation and completion, is highly malleable on the basis of task demands and occurs in concert with changes in perceptual performance.

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

Access options

Rent or buy this article

Prices vary by article type

from$1.95

to$39.95

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

Figure 1: Sensory acuity in the naive rat.
Figure 2: Learned enhancement in sensory acuity.
Figure 3: Experience increases cortical pattern completion.
Figure 4: Learned enhancement in sensory generalization.
Figure 5: Transient decrease in sensory acuity associated with poor behavioral performance.

Similar content being viewed by others

References

  1. Lee, I., Yoganarasimha, D., Rao, G. & Knierim, J.J. Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430, 456–459 (2004).

    Article  CAS  Google Scholar 

  2. Leutgeb, S., Leutgeb, J.K., Treves, A., Moser, M.B. & Moser, E.I. Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305, 1295–1298 (2004).

    Article  CAS  Google Scholar 

  3. Barnes, D.C., Hofacer, R.D., Zaman, A.R., Rennaker, R.L. & Wilson, D.A. Olfactory perceptual stability and discrimination. Nat. Neurosci. 11, 1378–1380 (2008).

    Article  CAS  Google Scholar 

  4. Haberly, L.B. Parallel-distributed processing in olfactory cortex: new insights from morphological and physiological analysis of neuronal circuitry. Chem. Senses 26, 551–576 (2001).

    Article  CAS  Google Scholar 

  5. Wilson, D.A. & Stevenson, R.J. The fundamental role of memory in olfactory perception. Trends Neurosci. 26, 243–247 (2003).

    Article  CAS  Google Scholar 

  6. McClelland, J.L. & Goddard, N.H. Considerations arising from a complementary learning systems perspective on hippocampus and neocortex. Hippocampus 6, 654–665 (1996).

    Article  CAS  Google Scholar 

  7. Wesson, D.W., Donahou, T.N., Johnson, M.O. & Wachowiak, M. Sniffing behavior of mice during performance in odor-guided tasks. Chem. Senses 33, 581–596 (2008).

    Article  Google Scholar 

  8. Fletcher, M.L. & Chen, W.R. Neural correlates of olfactory learning: Critical role of centrifugal neuromodulation. Learn. Mem. 17, 561–570 (2010).

    Article  Google Scholar 

  9. Restrepo, D., Doucette, W., Whitesell, J.D., McTavish, T.S. & Salcedo, E. From the top down: flexible reading of a fragmented odor map. Trends Neurosci. 32, 525–531 (2009).

    Article  CAS  Google Scholar 

  10. Kadohisa, M. & Wilson, D.A. Separate encoding of identity and similarity of complex familiar odors in piriform cortex. Proc. Natl. Acad. Sci. USA 103, 15206–15211 (2006).

    Article  CAS  Google Scholar 

  11. Saar, D., Grossman, Y. & Barkai, E. Reduced synaptic facilitation between pyramidal neurons in the piriform cortex after odor learning. J. Neurosci. 19, 8616–8622 (1999).

    Article  CAS  Google Scholar 

  12. Saar, D. & Barkai, E. Long-term modifications in intrinsic neuronal properties and rule learning in rats. Eur. J. Neurosci. 17, 2727–2734 (2003).

    Article  Google Scholar 

  13. Martin, C., Beshel, J. & Kay, L.M. An olfacto-hippocampal network is dynamically involved in odor-discrimination learning. J. Neurophysiol. 98, 2196–2205 (2007).

    Article  Google Scholar 

  14. Cohen-Matsliah, S.I., Rosenblum, K. & Barkai, E. Olfactory-learning abilities are correlated with the rate by which intrinsic neuronal excitability is modulated in the piriform cortex. Eur. J. Neurosci. 30, 1339–1348 (2009).

    Article  Google Scholar 

  15. Brosh, I. & Barkai, E. Learning-induced enhancement of feedback inhibitory synaptic transmission. Learn. Mem. 16, 413–416 (2009).

    Article  Google Scholar 

  16. Hasselmo, M.E., Anderson, B.P. & Bower, J.M. Cholinergic modulation of cortical associative memory function. J. Neurophysiol. 67, 1230–1246 (1992).

    Article  CAS  Google Scholar 

  17. Nakazawa, K. et al. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science 297, 211–218 (2002).

    Article  CAS  Google Scholar 

  18. Freeman, W.J. & Schneider, W. Changes in spatial patterns of rabbit olfactory EEG with conditioning to odors. Psychophysiology 19, 44–56 (1982).

    Article  CAS  Google Scholar 

  19. Fletcher, M.L. & Wilson, D.A. Olfactory bulb mitral-tufted cell plasticity: odorant-specific tuning reflects previous odorant exposure. J. Neurosci. 23, 6946–6955 (2003).

    Article  CAS  Google Scholar 

  20. Doucette, W. & Restrepo, D. Profound context-dependent plasticity of mitral cell responses in olfactory bulb. PLoS Biol. 6, e258 (2008).

    Article  Google Scholar 

  21. Doucette, W. et al. Associative cortex features in the first olfactory brain relay station. Neuron 69, 1176–1187 (2011).

    Article  CAS  Google Scholar 

  22. Jones, S.V., Choi, D.C., Davis, M. & Ressler, K.J. Learning-dependent structural plasticity in the adult olfactory pathway. J. Neurosci. 28, 13106–13111 (2008).

    Article  CAS  Google Scholar 

  23. Bakin, J.S., Lepan, B. & Weinberger, N.M. Sensitization induced receptive field plasticity in the auditory cortex is independent of CS-modality. Brain Res. 577, 226–235 (1992).

    Article  CAS  Google Scholar 

  24. Kilgard, M.P. & Merzenich, M.M. Cortical map reorganization enabled by nucleus basalis activity. Science 279, 1714–1718 (1998).

    Article  CAS  Google Scholar 

  25. Chen, C.F., Barnes, D.C. & Wilson, D.A. Generalized versus stimulus-specific learned fear differentially modifies stimulus encoding in primary sensory cortex of awake rats. J. Neurophysiol. doi:10.1152/jn.00721.2011 (14 September 2011).

  26. Suzuki, N. & Bekkers, J.M. Inhibitory neurons in the anterior piriform cortex of the mouse: classification using molecular markers. J. Comp. Neurol. 518, 1670–1687 (2010).

    Article  CAS  Google Scholar 

  27. Stokes, C.C. & Isaacson, J.S. From dendrite to soma: dynamic routing of inhibition by complementary interneuron microcircuits in olfactory cortex. Neuron 67, 452–465 (2010).

    Article  CAS  Google Scholar 

  28. Suzuki, N. & Bekkers, J.M. Two layers of synaptic processing by principal neurons in piriform cortex. J. Neurosci. 31, 2156–2166 (2011).

    Article  CAS  Google Scholar 

  29. Resnik, J., Sobel, N. & Paz, R. Auditory aversive learning increases discrimination thresholds. Nat. Neurosci. 14, 791–796 (2011).

    Article  CAS  Google Scholar 

  30. Li, F., Wang, L.P., Shen, X. & Tsien, J.Z. Balanced dopamine is critical for pattern completion during associative memory recall. PLoS ONE 5, e15401 (2010).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  32. Barnes, D.C., Chapuis, J., Chaudhury, D. & Wilson, D.A. Odor fear conditioning modifies piriform cortex local field potentials both during conditioning and during post-conditioning sleep. PLoS ONE 6, e18130 (2011).

    Article  CAS  Google Scholar 

  33. Beshel, J., Kopell, N. & Kay, L.M. Olfactory bulb gamma oscillations are enhanced with task demands. J. Neurosci. 27, 8358–8365 (2007).

    Article  CAS  Google Scholar 

  34. Kay, L.M. & Beshel, J. A beta oscillation network in the rat olfactory system during a 2-alternative choice odor discrimination task. J. Neurophysiol. 104, 829–839 (2010).

    Article  Google Scholar 

  35. Fell, J. & Axmacher, N. The role of phase synchronization in memory processes. Nat. Rev. Neurosci. 12, 105–118 (2011).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  37. Chapuis, J. et al. The way an odor is experienced during aversive conditioning determines the extent of the network recruited during retrieval: a multisite electrophysiological study in rats. J. Neurosci. 29, 10287–10298 (2009).

    Article  CAS  Google Scholar 

  38. Cenier, T. et al. Respiration-gated formation of gamma and beta neural assemblies in the mammalian olfactory bulb. Eur. J. Neurosci. 29, 921–930 (2009).

    Article  Google Scholar 

  39. Nusser, Z., Kay, L.M., Laurent, G., Homanics, G.E. & Mody, I. Disruption of GABA(A) receptors on GABAergic interneurons leads to increased oscillatory power in the olfactory bulb network. J. Neurophysiol. 86, 2823–2833 (2001).

    Article  CAS  Google Scholar 

  40. Seckinger, R.A. et al. Olfactory identification and WAIS-R performance in deficit and nondeficit schizophrenia. Schizophr. Res. 69, 55–65 (2004).

    Article  Google Scholar 

  41. Murphy, C. Loss of olfactory function in dementing disease. Physiol. Behav. 66, 177–182 (1999).

    Article  CAS  Google Scholar 

  42. Tanila, H., Shapiro, M., Gallagher, M. & Eichenbaum, H. Brain aging: changes in the nature of information coding by the hippocampus. J. Neurosci. 17, 5155–5166 (1997).

    Article  CAS  Google Scholar 

  43. Tanila, H., Sipila, P., Shapiro, M. & Eichenbaum, H. Brain aging: impaired coding of novel environmental cues. J. Neurosci. 17, 5167–5174 (1997).

    Article  CAS  Google Scholar 

  44. Barnes, C.A., Suster, M.S., Shen, J. & McNaughton, B.L. Multistability of cognitive maps in the hippocampus of old rats. Nature 388, 272–275 (1997).

    Article  CAS  Google Scholar 

  45. Wesson, D.W., Levy, E., Nixon, R.A. & Wilson, D.A. Olfactory dysfunction correlates with amyloid-beta burden in an Alzheimer's disease mouse model. J. Neurosci. 30, 505–514 (2010).

    Article  CAS  Google Scholar 

  46. Li, W., Howard, J.D. & Gottfried, J.A. Disruption of odour quality coding in piriform cortex mediates olfactory deficits in Alzheimer's disease. Brain 133, 2714–2726 (2010).

    Article  Google Scholar 

  47. Wilson, D.A. Single-unit activity in piriform cortex during slow-wave state is shaped by recent odor experience. J. Neurosci. 30, 1760–1765 (2010).

    Article  CAS  Google Scholar 

  48. Fletcher, M.L., Smith, A.M., Best, A.R. & Wilson, D.A. High-frequency oscillations are not necessary for simple olfactory discriminations in young rats. J. Neurosci. 25, 792–798 (2005).

    Article  CAS  Google Scholar 

  49. Smith, D.V. & Travers, J.B. A metric for the breadth of tuning of gustatory neurons. Chem. Senses 4, 215–229 (1979).

    Article  Google Scholar 

  50. Preacher, K.J. Calculation for the test of the difference between two independent correlation coefficients. <http://quantpsy.org/> (2002).

Download references

Acknowledgements

This work was supported by US National Institutes of Health grants DC003906 and DC008982 to D.A.W. and a Fyssen Foundation post-doctoral grant to J.C.

Author information

Authors and Affiliations

Authors

Contributions

D.A.W. and J.C. designed the research. J.C. collected data. J.C. and D.A.W. analyzed and interpreted data. J.C. and D.A.W. wrote the paper.

Corresponding authors

Correspondence to Julie Chapuis or Donald A Wilson.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–3, Supplementary Table 1, Supplementary Results and Discussion (PDF 667 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chapuis, J., Wilson, D. Bidirectional plasticity of cortical pattern recognition and behavioral sensory acuity. Nat Neurosci 15, 155–161 (2012). https://doi.org/10.1038/nn.2966

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2966

This article is cited by

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