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Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity

Abstract

Following restricted peripheral damage, reorganization of adult sensory or motor cortex is believed to depend on loss of surround inhibition, which unmasks latent inputs to the deprived cortex. Here I demonstrate that limited damage to auditory receptors causes loss of functional surround inhibition in the cortex, unmasking of latent inputs and significantly altered neural coding. However, these changes do not lead to plasticity of the cortical map, defined by the most sensitive input from the receptor surface to each cortical location. Thus, in sensory cortex, loss of surround inhibition as a consequence of receptor organ damage does not necessarily result in cortical map plasticity.

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Figure 1: Restricted cochlear hearing losses result in a near-absence of cortical surround inhibition, which alters neuronal response patterns shaped by inhibition.
Figure 2: Loss of surround inhibition unmasks inputs.
Figure 3: Loss of surround inhibition does not alter cochleotopic CF maps in A1.

References

  1. Merzenich, M.M. et al. Topographic reorganization of somatosensory cortical areas 3b and 1 in adult monkeys following restricted deafferentation. Neuroscience 8, 33–55 (1983)

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  3. Darian-Smith, C. & Gilbert, C.D. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci. 15, 1631–1647 (1995)

    CAS  Article  Google Scholar 

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

    CAS  Article  Google Scholar 

  5. Rajan, R., Irvine, D.R.F., Wise, L.Z. & Heil, P. Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex. J. Comp. Neurol. 338, 17–49 ( 1993)

    CAS  Article  Google Scholar 

  6. Sanes, J.N., Suner, S. & Donoghue, J.P. Dynamic organization of primary motor cortex output to target muscles in adult rats. I. Long-term patterns of reorganization following motor or mixed peripheral nerve lesions. Exp. Brain Res. 79, 479–491 (1990)

    CAS  Article  Google Scholar 

  7. Hendry, S.H.C. & Jones, E.G. Reduction in number of immunostained GABAergic neurones in deprived-eye dominance columns of monkey area 17. Nature 320, 750–753 ( 1986)

    CAS  Article  Google Scholar 

  8. Hendry, S.H.C. & Kennedy, M.B. Immunoreactivity for a calmodulin-dependent protein kinase is selectively increased in macaque striate cortex after monocular deprivation. Proc. Natl Acad. Sci. USA. 83, 1536–1540 (1986)

    CAS  Article  Google Scholar 

  9. Warren, R., Tremblay, N. & Dykes, R.W. Quantitative study of glutamic acid decarboxylase-immunoreactive neurones and cytochrome oxidase activity in normal and partially deafferented rat hindlimb somatosensory cortex. J. Comp. Neurol. 288, 583–592 (1989)

    CAS  Article  Google Scholar 

  10. Welker, E., Soriano, E. & van der Loos, H. Plasticity in the barrel cortex of the adult mouse: effects of peripheral deprivation on GAD-immunoreactivity. Exp. Brain Res. 74, 441–452 ( 1989)

    CAS  Article  Google Scholar 

  11. Hendry, S.H.C., Fuchs, J., deBlas, A.L. & Jones, E.G. Distribution and plasticity of immunocytochemically localized GABAA receptors in adult monkey visual cortex. J. Neurosci. 10, 2438–2450 (1990)

    CAS  Article  Google Scholar 

  12. Garraghty, P.E., LaChica, E.A. & Kaas, J.H. Injury-induced reorganization of somatosensory cortex is accompanied by reductions in GABA staining. Somatosens. Motor Res. 8, 347–354 ( 1991)

    CAS  Article  Google Scholar 

  13. Calford, M.B. & Tweedale, R. Immediate and chronic changes in responses of somatosensory cortex in adult flying-fox after digit amputation . Nature 332, 446–448 (1988)

    CAS  Article  Google Scholar 

  14. Jacobs, K.M. & Donoghue, J.P. Reshaping the cortical motor map by unmasking latent intracortical connections. Science 251, 944–947 (1991)

    CAS  Article  Google Scholar 

  15. Wall, J.T. Variable organization in cortical maps of the skin as an indication of the lifelong adaptive capacities of circuits in the mammalian brain. Trends Neurosci. 11, 549–557 (1988)

    CAS  Article  Google Scholar 

  16. Rausell, E., Cusick, C.G., Taub, E. & Jones, E.G. Chronic deafferentation in monkeys differentially affects nociceptive and nonnociceptive pathways distinguished by specific calcium-binding proteins and down-regulates γ-aminobutyric acid type A receptors at thalamic levels. Proc. Natl Acad. Sci. USA 89, 2571–2575 ( 1992)

    CAS  Article  Google Scholar 

  17. Rasmusson, D.D., Webster, H.H. & Dykes, R.W. Neuronal response properties within subregions of raccoon somatosensory cortex 1 week after digit amputation. Somat. Motor Res. 9, 279–289 ( 1992)

    CAS  Article  Google Scholar 

  18. Jones, E.G. GABAergic neurones and their role in cortical plasticity in primates. Cereb. Cortex 3, 361–372 ( 1993)

    CAS  Article  Google Scholar 

  19. Donoghue, J.P. Plasticity of adult sensorimotor representations. Curr. Opin. Neurobiol. 5, 749–754 (1995)

    CAS  Article  Google Scholar 

  20. D'Amelio, F., Fox, R.A., Wu, L.C. & Daunton, N.G. Quantitative changes of GABA-immunoreactive neurons in the hindlimb representation of the rat somatosensory cortex after 14-day hindlimb unloading by tail suspension . J. Neurosci. Res. 44, 532– 539 (1996)

    CAS  Article  Google Scholar 

  21. Sillito, A.M. The contribution of inhibitory mechanisms to the receptive field properties of neurones in the striate cortex of the cat. J. Physiol. 250, 305–329 (1975)

    CAS  Article  Google Scholar 

  22. Ramoa, A.S., Paradiso, M.A. & Freeman, R.D. Blockade of intracortical inhibition in kitten striate cortex: effects on receptive field properties and associated loss of ocular dominance plasticity. Exp. Brain Res. 73, 285–296 (1988)

    CAS  Article  Google Scholar 

  23. Dykes, R.W., Landry, P., Metherate, R. & Hicks, T.P. Functional role of GABA in cat primary somatosensory cortex: shaping receptive fields of cortical neurons. J. Neurophysiol. 52, 1066– 1093 (1984)

    CAS  Article  Google Scholar 

  24. Batuev, A.S., Alexandrov, A.A., Scheynikov, N.A., Kcharazia, V.N. & An, C.C. The role of inhibitory processes in the formation of functional properties of neurons in vibrissal projection zone of the cat somatosensory cortex. Exp. Brain Res. 76, 198–206 (1989)

    CAS  Article  Google Scholar 

  25. Alloway, K.D., Rosenthal, P. & Burton, H. Quantitative measurements of receptive field changes during antagonism of GABAergic transmission in primary somatosensory cortex of cats. Exp. Brain Res. 78, 514–532 (1989)

    CAS  Article  Google Scholar 

  26. Rajan, R., Irvine, D.R.F. & Cassell, J.F. Normative N1 audiogram data for the barbiturate-anaesthetised domestic cat. Hearing Res. 53, 153– 158 (1991)

    CAS  Article  Google Scholar 

  27. Volkov, I.O. & Galazjuk, A.V. Formation of spike response to sound tones in cat auditory cortex neurons: interaction of excitatory and inhibitory effects. Neuroscience 43, 307 –321 (1991)

    CAS  Article  Google Scholar 

  28. Schreiner, C.E. & Mendelson, J.R. Functional topography of cat primary auditory cortex: distribution of integrated excitation. J. Neurophysiol. 64, 1442–1459 (1990)

    CAS  Article  Google Scholar 

  29. Vater, M., Habbicht, H., Kössl, M. & Grothe, B. The functional role of GABA and glycine in monaural and binaural processing in the inferior colliculus of horseshoe bats. J. Comp. Physiol. A 171 , 541–553 (1992)

    CAS  Article  Google Scholar 

  30. Yang, L., Pollak G.D. & Resler, C. GABAergic circuits sharpen tuning curves and modify response properties in the mustache bat inferior colliculus. J. Neurophysiol. 68, 1760–1774 (1992)

    CAS  Article  Google Scholar 

  31. Pollak G.D. & Park, T.J. The effects of GABAergic inhibition on monaural response properties of neurons in the mustache bat's inferior colliculus. Hearing Res. 65, 99– 117 (1993)

    CAS  Article  Google Scholar 

  32. Calford, M.B. & Semple, M.N. Monaural inhibition in cat auditory cortex. J. Neurophysiol. 73, 1876– 1891 (1995)

    CAS  Article  Google Scholar 

  33. Calford M.B. & Tweedale, R. Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox. J. Neurophysiol. 65, 178– 187 (1991)

    CAS  Article  Google Scholar 

  34. Calford M.B. & Tweedale, R. C-fibres provide a source of masking inhibition to primary somatosensory cortex. Proc. Royal Soc. Lond. B 243, 269–275 ( 1991)

    CAS  Article  Google Scholar 

  35. Rasmusson, D.D., Louw, D.F. & Northgrave, S.A. The immediate effects of peripheral denervation on inhibitory mechanisms in the somatosensory thalamus. Somatosens. Motor Res. 10, 69–80 ( 1993)

    CAS  Article  Google Scholar 

  36. Kiang, N.Y.-S., Watanabe, T., Thomas, E.C. & Clark, L.F. Discharge Patterns of Single Fibers in the Cat's Auditory Nerve (M.I.T. Press, Cambridge, Massachusetts, 1965)

    Google Scholar 

  37. Liberman, M.C. Auditory-nerve response from cats raised in a low-noise chamber. J. Acoustic Soc. Am. 63, 442–455 ( 1978)

    CAS  Article  Google Scholar 

  38. Evans, E.F. & Palmer, A.R. Relationship between the dynamic range of cochlear nerve fibres and their spontaneous activity. Exp. Brain Res. 40, 115–118 (1980)

    CAS  Article  Google Scholar 

  39. Liberman, M.C. Physiology of cochlear efferent and afferent neurons: direct comparisons in the same animal. Hearing Res. 34, 179– 192 (1988)

    CAS  Article  Google Scholar 

  40. Manley, G.A. & Robertson, D. Analysis of spontaneous activity of auditory neurones in the spiral ganglion of the guinea-pig cochlea. J. Physiol. 258, 323–336 (1976)

    CAS  Article  Google Scholar 

  41. Schmiedt, R.A. Spontaneous rates, thresholds and tuning of auditory-nerve fibers in the gerbil: comparisons to cat data. Hearing Res. 42, 23– 36 (1989)

    CAS  Article  Google Scholar 

Download references

Acknowledgements

This study was supported by grant No. 941006 from the National Health and Medical Research Council of Australia.

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Correspondence to R. Rajan.

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Rajan, R. Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat Neurosci 1, 138–143 (1998). https://doi.org/10.1038/388

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