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Manipulating critical period closure across different sectors of the primary auditory cortex

Nature Neuroscience volume 11, pages 957–965 (2008)Cite this article

Abstract

During early brain development and through 'adult' experience-dependent plasticity, neural circuits are shaped to represent the external world with high fidelity. When raised in a quiet environment, the rat primary auditory cortex (A1) has a well-defined 'critical period', lasting several days, for its representation of sound frequency. The addition of environmental noise extends the critical period duration as a variable function of noise level. It remains unclear whether critical period closure should be regarded as a unified, externally gated event that applies for all of A1 or if it is controlled by progressive, local, activity-driven changes in this cortical area. We found that rearing rats in the presence of a spectrally limited noise band resulted in the closure of the critical period for A1 sectors representing the noise-free spectral bands, whereas the critical period appeared to remain open in noise-exposed sectors, where the cortex was still functionally and physically immature.

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Figure 1: Effect of notched noise and BLN exposure on A1 characteristic frequency maps.
Figure 2: Slowing of temporal processing restricted to noise-exposed neurons.
Figure 3: BLN exposure selectively decreases neural synchrony in A1.
Figure 4: BLN exposure reduced the number of parvalbumin-positive cells selectively in the central region of A1.
Figure 5: Delaying critical period closure selectively in the low-frequency sector of A1.
Figure 6: Recovery of spectral and temporal processing in A1 after BLN exposure.

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References

  1. Kilgard, M.P. et al. Sensory input directs spatial and temporal plasticity in primary auditory cortex. J. Neurophysiol. 86, 326–338 (2001).

    Article  CAS  PubMed  Google Scholar 

  2. Goodman, J.C. & Nusbaum, H.C. The Development of Speech Perception: The Transition from Speech Sounds to Spoken Words (MIT Press, Cambridge, Massachusetts, 1994).

    Google Scholar 

  3. Moore, D.R., Hutchings, M.E. & Meyer, S.E. Binaural masking level differences in children with a history of otitis media. Audiology 30, 91–101 (1991).

    Article  CAS  PubMed  Google Scholar 

  4. Rice, F.L. & Van der Loos, H. Development of the barrels and barrel field in the somatosensory cortex of the mouse. J. Comp. Neurol. 171, 545–560 (1977).

    Article  CAS  PubMed  Google Scholar 

  5. Schlaggar, B.L. & O'Leary, D.D. Patterning of the barrel field in somatosensory cortex with implications for the specification of neocortical areas. Perspect. Dev. Neurobiol. 1, 81–91 (1993).

    CAS  PubMed  Google Scholar 

  6. 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  PubMed  PubMed Central  Google Scholar 

  7. Fagiolini, M., Pizzorusso, T., Berardi, N., Domenici, L. & Maffei, L. Functional postnatal development of the rat primary visual cortex and the role of visual experience: dark rearing and monocular deprivation. Vision Res. 34, 709–720 (1994).

    Article  CAS  PubMed  Google Scholar 

  8. Berardi, N., Pizzorusso, T. & Maffei, L. Critical periods during sensory development. Curr. Opin. Neurobiol. 10, 138–145 (2000).

    Article  CAS  PubMed  Google Scholar 

  9. Berardi, N., Pizzorusso, T., Ratto, G.M. & Maffei, L. Molecular basis of plasticity in the visual cortex. Trends Neurosci. 26, 369–378 (2003).

    Article  CAS  PubMed  Google Scholar 

  10. Stern, E.A., Maravall, M. & Svoboda, K. Rapid development and plasticity of layer 2/3 maps in rat barrel cortex in vivo. Neuron 31, 305–315 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. Crair, M.C., Gillespie, D.C. & Stryker, M.P. The role of visual experience in the development of columns in cat visual cortex. Science 279, 566–570 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  13. 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  PubMed  PubMed Central  Google Scholar 

  14. Pearson, H.E., Berman, N. & Murphy, E.H. Stroboscopic rearing reduces direction selectivity in rabbit visual cortex. Brain Res. 227, 127–131 (1981).

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  16. Zheng, W. & Knudsen, E.I. Functional selection of adaptive auditory space map by GABAA-mediated inhibition. Science 284, 962–965 (1999).

    Article  CAS  PubMed  Google Scholar 

  17. 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  CAS  PubMed  PubMed Central  Google Scholar 

  18. Gordon, J.A. & Stryker, M.P. Experience-dependent plasticity of binocular responses in the primary visual cortex of the mouse. J. Neurosci. 16, 3274–3286 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Eggermont, J.J. Correlated neural activity as the driving force for functional changes in auditory cortex. Hear. Res. 229, 69–80 (2007).

    Article  PubMed  Google Scholar 

  20. Zhang, L.I. & Poo, M.M. Electrical activity and development of neural circuits. Nat. Neurosci. 4 Suppl, 1207–1214 (2001).

    Article  CAS  PubMed  Google Scholar 

  21. Xu, H., Kotak, V.C. & Sanes, D.H. Conductive hearing loss disrupts synaptic and spike adaptation in developing auditory cortex. J. Neurosci. 27, 9417–9426 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Pallas, S.L. Intrinsic and extrinsic factors that shape neocortical specification. Trends Neurosci. 24, 417–423 (2001).

    Article  CAS  PubMed  Google Scholar 

  23. de Venecia, R.K. & McMullen, N.T. Single thalamocortical axons diverge to multiple patches in neonatal auditory cortex. Brain Res. Dev. Brain Res. 81, 135–142 (1994).

    Article  CAS  PubMed  Google Scholar 

  24. Feldman, D.E., Nicoll, R.A., Malenka, R.C. & Isaac, J.T. Long-term depression at thalamocortical synapses in developing rat somatosensory cortex. Neuron 21, 347–357 (1998).

    Article  CAS  PubMed  Google Scholar 

  25. Alonso, J.M. & Swadlow, H.A. Thalamocortical specificity and the synthesis of sensory cortical receptive fields. J. Neurophysiol. 94, 26–32 (2005).

    Article  PubMed  Google Scholar 

  26. Daw, M.I., Ashby, M.C. & Isaac, J.T. Coordinated developmental recruitment of latent fast spiking interneurons in layer IV barrel cortex. Nat. Neurosci. 10, 453–461 (2007).

    Article  CAS  PubMed  Google Scholar 

  27. Gao, W.J. & Pallas, S.L. Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections. J. Neurosci. 19, 7940–7950 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. McGee, A.W., Yang, Y., Fischer, Q.S., Daw, N.W. & Strittmatter, S.M. Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309, 2222–2226 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. del Rio, J.A., de Lecea, L., Ferrer, I. & Soriano, E. The development of parvalbumin-immunoreactivity in the neocortex of the mouse. Brain Res. Dev. Brain Res. 81, 247–259 (1994).

    Article  CAS  PubMed  Google Scholar 

  30. Gao, W.J., Wormington, A.B., Newman, D.E. & Pallas, S.L. Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: immunocytochemical localization of calbindin- and parvalbumin-containing neurons. J. Comp. Neurol. 422, 140–157 (2000).

    Article  CAS  PubMed  Google Scholar 

  31. Hendrickson, A.E., Van Brederode, J.F., Mulligan, K.A. & Celio, M.R. Development of the calcium-binding protein parvalbumin and calbindin in monkey striate cortex. J. Comp. Neurol. 307, 626–646 (1991).

    Article  CAS  PubMed  Google Scholar 

  32. Beierlein, M., Gibson, J.R. & Connors, B.W. A network of electrically coupled interneurons drives synchronized inhibition in neocortex. Nat. Neurosci. 3, 904–910 (2000).

    Article  CAS  PubMed  Google Scholar 

  33. Bi, G. & Poo, M. Synaptic modification by correlated activity: Hebb's postulate revisited. Annu. Rev. Neurosci. 24, 139–166 (2001).

    Article  CAS  PubMed  Google Scholar 

  34. Marco, P., Sola, R.G., Ramon y Cajal, S. & DeFelipe, J. Loss of inhibitory synapses on the soma and axon initial segment of pyramidal cells in human epileptic peritumoural neocortex: implications for epilepsy. Brain Res. Bull. 44, 47–66 (1997).

    Article  CAS  PubMed  Google Scholar 

  35. Somogyi, P., Tamas, G., Lujan, R. & Buhl, E.H. Salient features of synaptic organisation in the cerebral cortex. Brain Res. Brain Res. Rev. 26, 113–135 (1998).

    Article  CAS  PubMed  Google Scholar 

  36. Micheva, K.D. & Beaulieu, C. Neonatal sensory deprivation induces selective changes in the quantitative distribution of GABA-immunoreactive neurons in the rat barrel field cortex. J. Comp. Neurol. 361, 574–584 (1995).

    Article  CAS  PubMed  Google Scholar 

  37. Jiao, Y., Zhang, C., Yanagawa, Y. & Sun, Q.Q. Major effects of sensory experiences on the neocortical inhibitory circuits. J. Neurosci. 26, 8691–8701 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Daw, N.W., Fox, K., Sato, H. & Czepita, D. Critical period for monocular deprivation in the cat visual cortex. J. Neurophysiol. 67, 197–202 (1992).

    Article  CAS  PubMed  Google Scholar 

  39. Desai, N.S., Cudmore, R.H., Nelson, S.B. & Turrigiano, G.G. Critical periods for experience-dependent synaptic scaling in visual cortex. Nat. Neurosci. 5, 783–789 (2002).

    Article  CAS  PubMed  Google Scholar 

  40. Goel, A. & Lee, H.K. Persistence of experience-induced homeostatic synaptic plasticity through adulthood in superficial layers of mouse visual cortex. J. Neurosci. 27, 6692–6700 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Hooks, B.M. & Chen, C. Critical periods in the visual system: changing views for a model of experience-dependent plasticity. Neuron 56, 312–326 (2007).

    Article  CAS  PubMed  Google Scholar 

  42. Bartoletti, A., Medini, P., Berardi, N. & Maffei, L. Environmental enrichment prevents effects of dark-rearing in the rat visual cortex. Nat. Neurosci. 7, 215–216 (2004).

    Article  CAS  PubMed  Google Scholar 

  43. Cang, J. et al. Development of precise maps in visual cortex requires patterned spontaneous activity in the retina. Neuron 48, 797–809 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Bao, S., Chang, E.F., Davis, J.D., Gobeske, K.T. & Merzenich, M.M. Progressive degradation and subsequent refinement of acoustic representations in the adult auditory cortex. J. Neurosci. 23, 10765–10775 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Kilgard, M.P. & Merzenich, M.M. Distributed representation of spectral and temporal information in rat primary auditory cortex. Hear. Res. 134, 16–28 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Bao, S., Chang, E.F., Woods, J. & Merzenich, M.M. Temporal plasticity in the primary auditory cortex induced by operant perceptual learning. Nat. Neurosci. 7, 974–981 (2004).

    Article  CAS  PubMed  Google Scholar 

  47. Brosch, M. & Schreiner, C.E. Correlations between neural discharges are related to receptive field properties in cat primary auditory cortex. Eur. J. Neurosci. 11, 3517–3530 (1999).

    Article  CAS  PubMed  Google Scholar 

  48. Eggermont, J.J. Neural interaction in cat primary auditory cortex. Dependence on recording depth, electrode separation and age. J. Neurophysiol. 68, 1216–1228 (1992).

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank T. Babcock, J. Zhang for technical support and J. Li for comments on the manuscript. This research was supported by US National Institutes of Health Grants grant NS-10414 and PO2 NS34835-09, the Sandler Fund and the Fonds de Recherche en Santé du Québec.

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Authors and Affiliations

  1. Department of Otolaryngology, W.M. Keck Center for Integrative Neuroscience, Coleman Laboratory, University of California, San Francisco, 513 Parnassus Avenue, Room HSE-808, Box 0732, San Francisco, 94143, California, USA

    Etienne de Villers-Sidani & Michael M Merzenich

  2. Departments of Anatomy, Psychiatry & Human Behavior, University of Mississippi Medical Center, 2500 North State Street, Jackson, 39216, Mississippi, USA

    Kimberly L Simpson, Y-F Lu & Rick C S Lin

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  1. Etienne de Villers-Sidani
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Contributions

E.d.V.-S. contributed to the experimental design, electrophysiological data collection, analysis and writing of the manuscript. K.L.S., Y.-F.L. and R.C.S.L. performed the histological analysis and edited the text. M.M.M. participated in experimental design and writing.

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Correspondence to Etienne de Villers-Sidani.

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de Villers-Sidani, E., Simpson, K., Lu, YF. et al. Manipulating critical period closure across different sectors of the primary auditory cortex. Nat Neurosci 11, 957–965 (2008). https://doi.org/10.1038/nn.2144

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