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.

  • Letter
  • Published:

A synaptic memory trace for cortical receptive field plasticity

Abstract

Receptive fields of sensory cortical neurons are plastic, changing in response to alterations of neural activity or sensory experience1,2,3,4,5,6,7,8,9,10,11,12. In this way, cortical representations of the sensory environment can incorporate new information about the world, depending on the relevance or value of particular stimuli1,6,9. Neuromodulation is required for cortical plasticity, but it is uncertain how subcortical neuromodulatory systems, such as the cholinergic nucleus basalis, interact with and refine cortical circuits13,14,15,16,17,18,19,20,21,22,23,24. Here we determine the dynamics of synaptic receptive field plasticity in the adult primary auditory cortex (also known as AI) using in vivo whole-cell recording. Pairing sensory stimulation with nucleus basalis activation shifted the preferred stimuli of cortical neurons by inducing a rapid reduction of synaptic inhibition within seconds, which was followed by a large increase in excitation, both specific to the paired stimulus. Although nucleus basalis was stimulated only for a few minutes, reorganization of synaptic tuning curves progressed for hours thereafter: inhibition slowly increased in an activity-dependent manner to rebalance the persistent enhancement of excitation, leading to a retuned receptive field with new preference for the paired stimulus. This restricted period of disinhibition may be a fundamental mechanism for receptive field plasticity, and could serve as a memory trace9,25 for stimuli or episodes that have acquired new behavioural significance.

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: Synaptic modifications induced by nucleus basalis pairing.
Figure 2: Rapid suppression of inhibition during nucleus basalis pairing.
Figure 3: Nucleus basalis pairing altered intracortical connections.
Figure 4: Temporal dynamics of synaptic receptive field plasticity.

Similar content being viewed by others

References

  1. Buonomano, D. V. & Merzenich, M. M. Cortical plasticity: from synapses to maps. Annu. Rev. Neurosci. 21, 149–186 (1998)

    Article  CAS  Google Scholar 

  2. Debanne, D., Shulz, D. E. & Fregnac, Y. Activity-dependent regulation of 'on' and 'off' responses in cat visual cortical receptive fields. J. Physiol. (Lond.) 508, 523–548 (1998)

    Article  CAS  Google Scholar 

  3. Gilbert, C. D. Adult cortical dynamics. Physiol. Rev. 78, 467–485 (1998)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  5. Chang, E. F. & Merzenich, M. M. Environmental noise retards auditory cortical development. Science 300, 498–502 (2003)

    Article  ADS  CAS  Google Scholar 

  6. Fritz, J., Shamma, S., Elhilali, M. & Klein, D. Rapid task-related plasticity of spectrotemporal receptive fields in primary auditory cortex. Nature Neurosci. 6, 1216–1223 (2003)

    Article  CAS  Google Scholar 

  7. Suga, N. & Ma, X. Multiparametric corticofugal modulation and plasticity in the auditory system. Nature Rev. Neurosci. 4, 783–794 (2003)

    Article  CAS  Google Scholar 

  8. Malenka, R. C. & Bear, M. F. LTP and LTD: an embarrassment of riches. Neuron 44, 5–21 (2004)

    Article  CAS  Google Scholar 

  9. Weinberger, N. M. Specific long-term memory traces in primary auditory cortex. Nature Rev. Neurosci. 5, 279–290 (2004)

    Article  CAS  Google Scholar 

  10. Chang, E. F., Bao, S., Imaizumi, K., Schreiner, C. E. & Merzenich, M. M. Development of spectral and temporal response selectivity in the auditory cortex. Proc. Natl Acad. Sci. USA 102, 16460–16465 (2005)

    Article  ADS  CAS  Google Scholar 

  11. Karmarkar, U. R. & Dan, Y. Experience-dependent plasticity in adult visual cortex. Neuron 52, 577–585 (2006)

    Article  CAS  Google Scholar 

  12. de Villers-Sidani, E., Chang, E. F., Bao, S. & Merzenich, M. M. Critical period window for spectral tuning defined in the primary auditory cortex (A1) in the rat. J. Neurosci. 27, 180–189 (2007)

    Article  CAS  Google Scholar 

  13. Bear, M. F. & Singer, W. Modulation of visual cortical plasticity by acetylcholine and noradrenaline. Nature 320, 172–176 (1986)

    Article  ADS  CAS  Google Scholar 

  14. Everitt, B. J. & Robbins, T. W. Central cholinergic systems and cognition. Annu. Rev. Psychol. 48, 649–684 (1997)

    Article  CAS  Google Scholar 

  15. Sarter, M., Hasselmo, M. E., Bruno, J. P. & Givens, B. Unraveling the attentional functions of cortical cholinergic inputs: interactions between signal-driven and cognitive modulation of signal detection. Brain Res. Brain Res. Rev. 48, 98–111 (2005)

    Article  CAS  Google Scholar 

  16. Zhang, Y., Hamilton, S. E., Nathanson, N. M. & Yan, J. Decreased input-specific plasticity of the auditory cortex in mice lacking M1 muscarinic acetylcholine receptors. Cereb. Cortex 16, 1258–1265 (2006)

    Article  Google Scholar 

  17. Rasmusson, D. D. The role of acetylcholine in cortical synaptic plasticity. Behav. Brain Res. 115, 205–218 (2000)

    Article  CAS  Google Scholar 

  18. Yu, A. J. & Dayan, P. Uncertainty, neuromodulation, and attention. Neuron 46, 681–692 (2005)

    Article  CAS  Google Scholar 

  19. Metherate, R., Cox, C. L. & Ashe, J. H. Cellular bases of neocortical activation: modulation of neural oscillations by the nucleus basalis and endogenous acetylcholine. J. Neurosci. 12, 4701–4711 (1992)

    Article  CAS  Google Scholar 

  20. Lee, M. G., Hassani, O. K., Alonso, A. & Jones, B. E. Cholinergic basal forebrain neurons burst with theta during waking and paradoxical sleep. J. Neurosci. 25, 4365–4369 (2005)

    Article  CAS  Google Scholar 

  21. Richardson, R. T. & DeLong, M. R. A reappraisal of the functions of the nucleus basalis of Meynert. Trends Neurosci. 11, 264–267 (1988)

    Article  CAS  Google Scholar 

  22. Woody, C. D. & Gruen, E. Acetylcholine reduces net outward currents measured in vivo with single electrode voltage clamp techniques in neurons of the motor cortex of cats. Brain Res. 424, 193–198 (1987)

    Article  CAS  Google Scholar 

  23. Xiang, Z., Huguenard, J. R. & Prince, D. A. Cholinergic switching within neocortical inhibitory networks. Science 281, 985–988 (1998)

    Article  ADS  CAS  Google Scholar 

  24. Metherate, R. et al. Spectral integration in auditory cortex: mechanisms and modulation. Hear. Res. 206, 146–158 (2005)

    Article  Google Scholar 

  25. Thompson, R. F. In search of memory traces. Annu. Rev. Psychol. 56, 1–23 (2005)

    Article  Google Scholar 

  26. Wehr, M. & Zador, A. M. Balanced inhibition underlies tuning and sharpens spike timing in auditory cortex. Nature 426, 442–446 (2003)

    Article  ADS  CAS  Google Scholar 

  27. Tan, A. Y. Y., Zhang, L. I., Merzenich, M. M. & Schreiner, C. E. Tone-evoked excitatory and inhibitory synaptic conductances of primary auditory cortex neurons. J. Neurophysiol. 92, 630–643 (2004)

    Article  Google Scholar 

  28. Gritti, I., Manns, I. D., Mainville, L. & Jones, B. E. Parvalbumin, calbindin, or calretinin in cortically projecting and GABAergic, cholinergic, or glutamatergic basal forebrain neurons of the rat. J. Comp. Neurol. 458, 11–31 (2003)

    Article  Google Scholar 

  29. DeWeese, M. R., Wehr, M. & Zador, A. M. Binary spiking in auditory cortex. J. Neurosci. 23, 7940–7949 (2003)

    Article  CAS  Google Scholar 

  30. Hromadka, T. & Zador, A. M. Towards the mechanisms of auditory attention. Hear. Res. 229, 180–185 (2007)

    Article  Google Scholar 

Download references

Acknowledgements

We thank K. L. Arendt, T. Babcock, Y. Dan, E. de Villers-Sidani, M. R. DeWeese, M. P. Kilgard, D. Polley, L. Wilbrecht and J. A. Winer for comments and discussions, and S. Bao, W. Huang, K. Imaizumi, A. Tan and C.-L. Teng for technical assistance. D. Bliss created the artwork in Figs 1a and 3a. This work was supported by the NIDCD, the Conte Center for Neuroscience Research at UCSF, Hearing Research Inc., and the John C. and Edward Coleman Fund. R.C.F. is a recipient of the Jane Coffin Childs Postdoctoral Research Fellowship and the Sandler Translational Research Fellowship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Robert C. Froemke.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Suppplementary Information

The file contains Supplementary Figures S1-S6 and their Legends. (PDF 523 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Froemke, R., Merzenich, M. & Schreiner, C. A synaptic memory trace for cortical receptive field plasticity. Nature 450, 425–429 (2007). https://doi.org/10.1038/nature06289

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature06289

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

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