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Sensory experience modifies the short-term dynamics of neocortical synapses

Nature volume 400, pages 367–371 (1999)Cite this article

Abstract

Many representations of sensory stimuli in the neocortex are arranged as topographic maps. These cortical maps are not fixed, but show experience-dependent plasticity1,2. For instance, sensory deprivation causes the cortical area representing the deprived sensory input to shrink, and neighbouring spared representations to enlarge, in somatosensory3, auditory4 or visual cortex5. In adolescent and adult animals, changes in cortical maps are most noticeable in the supragranular layers at the junction of deprived and spared cortex6,7,8,9. However, the cellular mechanisms of this experience-dependent plasticity are unclear. Long-term potentiation and depression have been implicated10,11,12, but have not been proven to be necessary or sufficient for cortical map reorganization. Short-term synaptic dynamics have not been considered. We developed a brain slice preparation involving rat whisker barrel cortex in vitro. Here we report that sensory deprivation alters short-term synaptic dynamics in both vertical and horizontal excitatory pathways within the supragranular cortex. Moreover, modifications of horizontal pathways amplify changes in the vertical inputs. Our findings help to explain the functional cortical reorganization that follows persistent changes of sensory experience.

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Figure 1: ‘Across whisker barrel row’ brain slice preparation.
Figure 2: Short-term synaptic dynamics of horizontal pathways.
Figure 3: Short-term synaptic dynamics of vertical pathways.
Figure 4: Sensory deprivation changes synaptic strength and synaptic efficacy.

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

    Article  ADS  CAS  Google Scholar 

  3. Merzenich, M. M.et al. Progression of changes following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience 10, 639–665 (1983).

    Article  CAS  Google Scholar 

  4. Robertson, D. & Irvine, D. Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J. Comp. Neurol. 282, 456–471 (1989).

    Article  CAS  Google Scholar 

  5. Kaas, J. H.et al. Reorganization of retinotopic cortical maps in adult mammals after lesions of the retina. Science 248, 229–231 (1990).

    Article  ADS  CAS  Google Scholar 

  6. Glazewski, S. & Fox, K. Time course of experience-dependent synaptic potentiation and depression in barrel cortex of adolescent rats. J. Neurophysiol. 75, 1714–1729 (1996).

    Article  CAS  Google Scholar 

  7. Gilbert, C. D. & Wiesel, T. N. Receptive field dynamics in adult primary visual cortex. Nature 356, 150–152 (1992).

    Article  ADS  CAS  Google Scholar 

  8. Fox, K. Acritical period for experience-dependent synaptic plasticity in rat barrel cortex. J. Neurosci. 12, 1826–1838 (1992).

    Article  CAS  Google Scholar 

  9. Diamond, M. E., Huang, W. & Ebner, F. F. Laminar comparison of somatosensory cortical plasticity. Science 265, 1885–1888 (1994).

    Article  ADS  CAS  Google Scholar 

  10. Kirkwood, A., Rioult, M. C. & Bear, M. F. Experience-dependent modification of synaptic plasticity in visual cortex. Nature 381, 526–528 (1996).

    Article  ADS  CAS  Google Scholar 

  11. Glazewski, S., Chen, C.-M., Silva, A. & Fox, K. Requirement for α-CaMKII in experience-dependent plasticity of the barrel cortex. Science 272, 421–423 (1996).

    Article  ADS  CAS  Google Scholar 

  12. Garraghty, P. E. & Muja, N. NMDA receptors and plasticity in adult primate somatosensory cortex. J. Comp. Neurol. 367, 319–326 (1996).

    Article  CAS  Google Scholar 

  13. Carvell, G. E. & Simons, D. J. Biometric analyses of vibrissal tactile discrimination in the rat. J. Neurosci. 10, 2638–2648 (1990).

    Article  CAS  Google Scholar 

  14. Welker, C. & Woolsey, T. A. Structure of layer IV in the somatosensory neocortex of the rat: description and comparison with the mouse. J. Comp. Neurol. 158, 437–454 (1974).

    Article  CAS  Google Scholar 

  15. Markram, H. & Tsodyks, M. Redistribution of synaptic efficacy between neocortical pyramidal cells. Nature 382, 807–810 (1996).

    Article  ADS  CAS  Google Scholar 

  16. Abbot, L. F., Varela, J. A., Sen, K. & Nelson, S. B. Synaptic depression and cortical gain control. Science 275, 220–224 (1997).

    Google Scholar 

  17. Tsodyks, M. V. & Markram, H. The neural code between neocortical pyramidal neurons depends on neurotransmitter release probability. Proc. Natl Acad. Sci. USA 94, 719–723 (1997).

    Article  ADS  CAS  Google Scholar 

  18. McCasland, J. S. & Woolsey, T. A. High-resolution 2-deoxyglucose mapping of functional cortical columns in mouse barrel cortex. J. Comp. Neurol. 278, 555–569 (1988).

    Article  CAS  Google Scholar 

  19. Armstrong-James, M. Diamond, M. E. & Ebner, F. F. An innocuous bias in whisker use in adult rats modifies receptive fields of barrel cortex neurons. J. Neurosci. 14, 6978–6991 (1994).

    Article  CAS  Google Scholar 

  20. Darian-Smith, C. & Gilbert, C. D. Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature 368, 737–740 (1994).

    Article  ADS  CAS  Google Scholar 

  21. Florence, S. L., Taub, H. B. & Kaas, J. H. Large-scale sprouting of cortical connections after peripheral injury in adult macaque monkeys. Science 282, 1117–1121 (1998).

    Article  ADS  CAS  Google Scholar 

  22. Mason, A., Nicoll, A. & Stratford, K. Synaptic transmission between individual pyramidal neurons of the rat visual cortex in vitro. J. Neurosci. 11, 72–84 (1991).

    Article  CAS  Google Scholar 

  23. Nicolelis, M. A. L., Baccala, L. A., Lin, R. C. S. & Chapin, J. K. Sensorimotor encoding by synchronous neural ensemble activity at multiple levels of the somatosensory system. Science 268, 1353–1358 (1995).

    Article  ADS  CAS  Google Scholar 

  24. Stuart, G. & Sakmann, B. Amplification of EPSPs by axosomatic sodium channels in neocortical pyramidal neurons. Neuron 15, 1065–1076 (1995).

    Article  CAS  Google Scholar 

  25. Connors, B. W., Malenka, R. C. & Silva, L. R. Two inhibitory postsynaptic potentials, and GABAAreceptor-mediated responses in neocortex of rat and cat. J. Physiol. (Lond.) 406, 443–468 (1988).

    Article  CAS  Google Scholar 

  26. Dobrunz, L. E. & Stevens, C. F. Heterogeneity of release probability, facilitation, and depletion at central synapses. Neuron 18, 995–1008 (1997).

    Article  CAS  Google Scholar 

  27. Raastad, M., Storm, J. F. & Andersen, P. Putative single quantum and single fibre excitatory postsynaptic currents show similar amplitude range and variability in rat hippocampal slices. Eur. J. Neurosci. 4, 113–117 (1992).

    Article  Google Scholar 

  28. Volgushev, M., Voronin, L. L., Chistiakova, M., Artola, A. & Singer, W. All-or-none excitatory postsynaptic potentials in the rat visual cortex. Eur. J. Neurosci. 7, 1751–1760 (1995).

    Article  CAS  Google Scholar 

  29. Cash, S. & Yuste, R. Input summation by cultured pyramidal neurons is linear and position-independent. J. Neurosci. 18, 10–15 (1998).

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by a Wellcome Trust Advanced Training Fellowship to G.T.F. and a grant to B.W.C. from NIH. We thank S. Patrick for technical assistance with histology; A.Akima for discussions on the optimal slicing angle; D. Pinto for checking the mathematics; and M.Bear, J. Gibson, M. Beierlein and D. Pinto for helpful comments on a earlier version of the manuscript. G.T.F. thanks R. Jones and D. Smith for encouragement with the current project.

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  1. Gerald T. Finnerty

    Present address: Department of Physiology, School of Medical Sciences, University Walk, Bristol, BS81TD, UK

Authors and Affiliations

  1. Department of Neuroscience, Brown University, Providence, 02912, Rhode Island, USA

    Gerald T. Finnerty, Langdon S. E. Roberts & Barry W. Connors

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Correspondence to Barry W. Connors.

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Finnerty, G., Roberts, L. & Connors, B. Sensory experience modifies the short-term dynamics of neocortical synapses. Nature 400, 367–371 (1999). https://doi.org/10.1038/22553

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