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.

  • Article
  • Published:

A critical period for auditory thalamocortical connectivity

Nature Neuroscience volume 14, pages 1189–1194 (2011)Cite this article

Subjects

Abstract

Neural circuits are shaped by experience during periods of heightened brain plasticity in early postnatal life. Exposure to acoustic features produces age-dependent changes through largely unresolved cellular mechanisms and sites of origin. We isolated the refinement of auditory thalamocortical connectivity by in vivo recordings and day-by-day voltage-sensitive dye imaging in an acute brain slice preparation. Passive tone-rearing modified response strength and topography in mouse primary auditory cortex (A1) during a brief, 3-d window, but did not alter tonotopic maps in the thalamus. Gene-targeted deletion of a forebrain-specific cell-adhesion molecule (Icam5) accelerated plasticity in this critical period. Consistent with its normal role of slowing spinogenesis, loss of Icam5 induced precocious stubby spine maturation on pyramidal cell dendrites in neocortical layer 4 (L4), identifying a primary locus of change for the tonotopic plasticity. The evolving postnatal connectivity between thalamus and cortex in the days following hearing onset may therefore determine a critical period for auditory processing.

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

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

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

Figure 1: Developmental cortical map reorganization in mouse A1.
Figure 2: Thalamic tonotopy remains stable despite reorganization of A1 maps.
Figure 3: Topography and developmental window for A1 response strengthening at P12–15.
Figure 4: Critical period for experience-dependent topographic refinement at P12–15.
Figure 5: Columnar shift of thalamocortical connectivity up to L4 through the critical period.
Figure 6: Forebrain-specific gene deletion accelerates thalamocortical plasticity.
Figure 7: Stubby spine density increases through the critical period.

Similar content being viewed by others

References

  1. Hensch, T.K. Critical period regulation. Annu. Rev. Neurosci. 27, 549–579 (2004).

    Article  CAS  Google Scholar 

  2. Keuroghlian, A.S. & Knudsen, E.I. Adaptive auditory plasticity in developing and adult animals. Prog. Neurobiol. 82, 109–121 (2007).

    Article  Google Scholar 

  3. Werker, J.F. & Tees, R.C. Speech perception as a window for understanding plasticity and commitment in language systems of the brain. Dev. Psychobiol. 46, 233–251 (2005).

    Article  Google Scholar 

  4. Sanes, D.H. & Bao, S. Tuning up the developing auditory CNS. Curr. Opin. Neurobiol. 19, 188–199 (2009).

    Article  CAS  Google Scholar 

  5. 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 

  6. Insanally, M.N., Kover, H., Kim, H. & Bao, S. Feature-dependent sensitive periods in the development of complex sound representation. J. Neurosci. 29, 5456–5462 (2009).

    Article  CAS  Google Scholar 

  7. King, A.J. & Nelken, I. Unraveling the principles of auditory cortical processing: can we learn from the visual system? Nat. Neurosci. 12, 698–701 (2009).

    Article  CAS  Google Scholar 

  8. Wiesel, T.N. & Hubel, D.H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J. Neurophysiol. 28, 1029–1040 (1965).

    Article  CAS  Google Scholar 

  9. Hensch, T.K. Critical period plasticity in local cortical circuits. Nat. Rev. Neurosci. 6, 877–888 (2005).

    Article  CAS  Google Scholar 

  10. Winer, J.A., Miller, L.M., Lee, C.C. & Schreiner, C.E. Auditory thalamo-cortical transformation: structure and function. Trends Neurosci. 28, 255–263 (2005).

    Article  CAS  Google Scholar 

  11. Cruikshank, S.J., Rose, H.J. & Metherate, R. Auditory thalamocortical synaptic transmission in vitro. J. Neurophysiol. 87, 361–384 (2002).

    Article  Google Scholar 

  12. Zhang, L.I., Bao, S. & Merzenich, M.M. Disruption of primary auditory cortex by synchronous auditory inputs during a critical period. Proc. Natl. Acad. Sci. USA 99, 2309–2314 (2002).

    Article  CAS  Google Scholar 

  13. Hackett, T.A., Rinaldi Barkat, T., O'Brien, B.J., Hensch, T.K. & Polley, D.B. Linking topography to tonotopy in mouse auditory cortex. J. Neurosci. 31, 2983–2995 (2011).

    Article  CAS  Google Scholar 

  14. Winer, J.A., Sally, S.L., Larue, D.T. & Kelly, J.B. Origins of medial geniculate body projections to physiologically defined zones of rat primary auditory cortex. Hear. Res. 130, 42–61 (1999).

    Article  CAS  Google Scholar 

  15. Kaur, S., Rose, H.J., Lazar, R., Liang, K. & Metherate, R. Spectral integration in primary auditory cortex: laminar processing of afferent input, in vivo and in vitro. Neuroscience 134, 1033–1045 (2005).

    Article  CAS  Google Scholar 

  16. Alford, B.R. & Ruben, R.J. Physiological, behavioral and anatomical correlates of the development of hearing in the mouse. Ann. Otol. Rhinol. Laryngol. 72, 237–247 (1963).

    Article  CAS  Google Scholar 

  17. Allendoerfer, K.L. & Shatz, C.J. The subplate, a transient neocortical structure: its role in the development of connections between thalamus and cortex. Annu. Rev. Neurosci. 17, 185–218 (1994).

    Article  CAS  Google Scholar 

  18. Kanold, P.O. & Luhmann, H.J. The subplate and early cortical circuits. Annu. Rev. Neurosci. 33, 23–48 (2010).

    Article  CAS  Google Scholar 

  19. Zhao, C., Kao, J.P.Y. & Kanold, P.O. Functional excitatory microcircuits in neonatal cortex connect thalamus and layer 4. J. Neurosci. 29, 15479–15488 (2009).

    Article  CAS  Google Scholar 

  20. Nakamura, K. et al. Enhancement of hippocampal LTP, reference memory and sensorimotor gating in mutant mice lacking a telencephalon-specific cell adhesion molecule. Eur. J. Neurosci. 13, 179–189 (2001).

    Article  CAS  Google Scholar 

  21. Matsuno, H. et al. Telencephalin slows spine maturation. J. Neurosci. 26, 1776–1786 (2006).

    Article  CAS  Google Scholar 

  22. de Villers-Sidani, E. et al. Manipulating critical period closure across different sectors of the primary auditory cortex. Nat. Neurosci. 11, 957–965 (2008).

    Article  CAS  Google Scholar 

  23. Richardson, R.J., Blundon, J.A., Bayazitov, I.T. & Zakharenko, S.S. Connectivity patterns revealed by mapping of active inputs on dendrites of thalamo-recipient neurons in the auditory cortex. J. Neurosci. 29, 6406–6417 (2009).

    Article  CAS  Google Scholar 

  24. Simons, D.J. Response properties of vibrissa units in rat SI somatosensory neocortex. J. Neurophysiol. 41, 798–820 (1978).

    Article  CAS  Google Scholar 

  25. Masino, S.A., Kwon, M.C., Dory, Y. & Frostig, R.D. Characterization of functional organization within rat barrel cortex using intrinsic signal optical imaging through a thinned skull. Proc. Natl. Acad. Sci. USA 90, 9998–10002 (1993).

    Article  CAS  Google Scholar 

  26. Kleinfeld, D. & Delaney, K.R. Distributed representation of vibrissa movement in the upper layers of somatosensory cortex revealed with voltage-sensitive dyes. J. Comp. Neurol. 375, 89–108 (1996).

    Article  CAS  Google Scholar 

  27. Petersen, C.C., Grinvald, A. & Sakmann, B. Spatiotemporal dynamics of sensory responses in layer 2/3 of rat barrel cortex measured in vivo by voltage-sensitive dye imaging combined with whole-cell voltage recordings and neuron reconstructions. J. Neurosci. 23, 1298–1309 (2003).

    Article  CAS  Google Scholar 

  28. Mataga, N., Mizuguchi, Y. & Hensch, T.K. Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44, 1031–1041 (2004).

    Article  CAS  Google Scholar 

  29. Morishita, H. & Hensch, T.K. Critical period revisited: impact on vision. Curr. Opin. Neurobiol. 18, 101–107 (2008).

    Article  CAS  Google Scholar 

  30. Kandler, K., Clause, A. & Noh, J. Tonotopic reorganization of developing auditory brainstem circuits. Nat. Neurosci. 12, 711–717 (2009).

    Article  CAS  Google Scholar 

  31. Han, Y.K., Köver, H., Insanally, M.N., Semerdjian, J.H. & Bao, S. Early experience impairs perceptual discrimination. Nat. Neurosci. 10, 1191–1197 (2007).

    Article  CAS  Google Scholar 

  32. Dorrn, A.L., Yavan, K., Barker, A.J., Schreiner, C.E. & Froemke, R.C. Developmental sensory experience balances cortical excitation and inhibition. Nature 465, 932–936 (2010).

    Article  CAS  Google Scholar 

  33. Sun, Y.J. et al. Fine-tuning of pre-balanced excitation and inhibition during auditory cortical development. Nature 465, 927–931 (2010).

    Article  CAS  Google Scholar 

  34. Oviedo, H.V., Bureau, I., Svoboda, K. & Zador, A.M. The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits. Nat. Neurosci. 13, 1413–1420 (2010).

    Article  CAS  Google Scholar 

  35. Harris, J.A. & Rubel, E.W. Afferent regulation of neuron number in the cochlear nucleus: cellular and molecular analyses of a critical period. Hear. Res. 216–217, 127–137 (2006).

    Article  Google Scholar 

  36. Smith, Z.D., Gray, L. & Rubel, E.W. Afferent influences on brainstem auditory nuclei of the chicken: n. laminaris dendritic length following monaural conductive hearing loss. J. Comp. Neurol. 220, 199–205 (1983).

    Article  CAS  Google Scholar 

  37. Seidl, A.H. & Grothe, B. Development of sound localization mechanisms in the mongolian gerbil is shaped by early acoustic experience. J. Neurophysiol. 94, 1028–1036 (2005).

    Article  Google Scholar 

  38. Sanes, D.H. & Constantine-Paton, M. Altered activity patterns during development reduce neural tuning. Science 221, 1183–1185 (1983).

    Article  CAS  Google Scholar 

  39. Mogdans, J. & Knudsen, E.I. Site of auditory plasticity in the brain stem (VLVp) of the owl revealed by early monaural occlusion. J. Neurophysiol. 72, 2875–2891 (1994).

    Article  CAS  Google Scholar 

  40. Yan, W. & Suga, N. Corticofugal modulation of the midbrain frequency map in the bat auditory system. Nat. Neurosci. 1, 54–58 (1998).

    Article  CAS  Google Scholar 

  41. Bajo, V.M., Nodal, F.R., Moore, D.R. & King, A.J. The descending corticocollicular pathway mediates learning-induced auditory plasticity. Nat. Neurosci. 13, 253–260 (2010).

    Article  CAS  Google Scholar 

  42. Popescu, M.V. & Polley, D.B. Monaural deprivation disrupts development of binaural selectivity in auditory midbrain and cortex. Neuron 65, 718–731 (2010).

    Article  CAS  Google Scholar 

  43. Razak, K.A., Richardson, M.D. & Fuzessery, Z.M. Experience is required for the maintenance and refinement of FM sweep selectivity in the developing auditory cortex. Proc. Natl. Acad. Sci. USA 105, 4465–4470 (2008).

    Article  CAS  Google Scholar 

  44. Stiebler, I., Neulist, R., Fichtel, I. & Ehret, G. The auditory cortex of the house mouse: left-right differences, tonotopic organization and quantitative analysis of frequency representation. J. Comp. Physiol. [A] 181, 559–571 (1997).

    Article  CAS  Google Scholar 

  45. Grinvald, A. & Hildesheim, R. VSDI: a new era in functional imaging of cortical dynamics. Nat. Rev. Neurosci. 5, 874–885 (2004).

    Article  CAS  Google Scholar 

  46. Ferezou, I., Bolea, S. & Petersen, C.C.H. Visualizing the cortical representation of whisker touch: voltage-sensitive dye imaging in freely moving mice. Neuron 50, 617–629 (2006).

    Article  CAS  Google Scholar 

  47. Zhou, X., Nagarajan, N., Mossop, B.J. & Merzenich, M.M. Influences of un-modulated acoustic inputs on functional maturation and critical-period plasticity of the primary auditory cortex. Neuroscience 154, 390–396 (2008).

    Article  CAS  Google Scholar 

  48. Kim, H. & Bao, S. Selective increase in representations of sounds repeated at an ethological rate. J. Neurosci. 29, 5163–5169 (2009).

    Article  CAS  Google Scholar 

  49. Geissler, D.B. & Ehret, G. Auditory perception vs. recognition: representation of complex communication sounds in the mouse auditory cortical fields. Eur. J. Neurosci. 19, 1027–1040 (2004).

    Article  Google Scholar 

  50. Gan, W.B., Grutzendler, J., Wong, W.T., Wong, R.O. & Lichtman, J.W. Multicolor 'DiOlistic' labeling of the nervous system using lipophilic dye combinations. Neuron 27, 219–225 (2000).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

Icam5−/− mice and antibody were kindly provided by M. Mishina (University of Tokyo) and Y. Yoshihara (RIKEN BSI), respectively. We thank M. Nakamura, A. Takesian, N. Gogolla, E.-J. Yang, K. Quast, M. Marcotrigiano, M. Kelly, R. Pavlyuk, B. Jones O'Brien and V. Khatri for technical assistance and comments. This work was supported by Core Research for Evolutional Science and Technology, Japan Science and Technology Agency (T.K.H.), the Human Frontiers Science Program (T.K.H.), the National Institute on Deafness and Other Communication Disorders (grant 009836, D.B.P.) and the Harvard Society of Fellows (T.R.B.).

Author information

Authors and Affiliations

  1. Department of Molecular and Cellular Biology, Center for Brain Science, Harvard University, Cambridge, Massachusetts, USA

    Tania Rinaldi Barkat & Takao K Hensch

  2. Department of Otology and Laryngology, Eaton-Peabody Laboratory, Massachusetts Eye and Ear Infirmary, Harvard Medical School, Boston, Massachusetts, USA

    Daniel B Polley

Authors
  1. Tania Rinaldi Barkat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Daniel B Polley
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takao K Hensch
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

T.R.B. performed all of the in vitro experiments and analysis. D.B.P. performed or supervised the in vivo experiments and analysis. T.R.B., D.B.P. and T.K.H. designed the study and wrote the paper.

Corresponding author

Correspondence to Takao K Hensch.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Text and Figures

Supplementary Figures 1–7 (PDF 445 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Barkat, T., Polley, D. & Hensch, T. A critical period for auditory thalamocortical connectivity. Nat Neurosci 14, 1189–1194 (2011). https://doi.org/10.1038/nn.2882

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nn.2882

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