The Neocortex pp 205-218 | Cite as

Cross-Modal Plasticity in Sensory Cortex

Visual Responses in Primary Auditory Cortex in Ferrets with Induced Retinal Projections to the Medial Geniculate Nucleus
  • Sarah L. Pallas
Part of the NATO ASI Series book series (NSSA, volume 200)


The evolution of the mammalian brain has involved marked degrees of encephalization, and this trend is particularly spectacular in the neocortex (see Jenson, Finlay, this volume). An important question in understanding neocortical evolution is how this expansion may be exploited by structures which form afferent connections with the expanded cortical populations. For example, what happens when additional cortical processing circuitry becomes available to sensory inputs as a result of mutation or duplication? Does the newly acquired circuitry replicate the existing mode(s) of information processing, or does it process sensory input in a new way? The latter change would be more likely to increase the animal’s behavioral repertoire and hence reproductive “fitness”. Certainly in the visual system, the number of separable visual cortical areas increases from hedgehogs to rats to cats and monkeys (Kaas et al., 1970; see Kaas, 1987 for review), and there is a large body of evidence that the different areas perform different transformations on their sensory input. Whether this segregation of function derives from differences inherent in cortical circuitry, or from parcellation of subtypes of afferent input (or both) is unknown from either an evolutionary or developmental perspective.


Visual Cortex Superior Colliculus Auditory Cortex Sensory Epithelium Primary Auditory Cortex 
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  1. Andersen, R.A., Knight, P.L., and Merzenich, M.M. (1980) The thalamocortical and corticotha-lamic connections of AI, AII, and the anterior auditory field (AAF) in the cat: Evidence for two largely segregated systems of connections. J. Comp. Neurol., 194: 663–701.PubMedCrossRefGoogle Scholar
  2. Bronchti, G., Heil, P., Scheich, H., and Wollberg, Z. (1989a) Auditory pathway and auditory activation of primary visual targets in the blind mole rat (Spalax ehrenbergi): I. 2-deoxyglucose study of subcortical centers. J. Comp. Neurol., 284: 253–274.PubMedCrossRefGoogle Scholar
  3. Bronchti, G., Heil, P., Scheich, H., and Wollberg, Z. (1989c) Auditory activation of cortical visual fields in the blind mole rat. Proc. 2nd Intl. Cong. NeuroethoL, Abstract # 147.Google Scholar
  4. Bronchti, G., Rado, R., Terkel, J., and Wollberg, Z. (1989b) Ontogenetic degeneration of retinal projections in the blind mole rat (Spalax ehrenbergi). Proc. 2nd Intl. Cong. Neuroethol., Abstract #201.Google Scholar
  5. Brunso-Bechtold, J.K., and Casagrande, V.A. (1981) Effect of bilateral enucleation on the development of layers in the dorsal lateral geniculate nucleus. Neuroscience, 6: 2579–2586.PubMedCrossRefGoogle Scholar
  6. Chun, J.J.M., Nakamura, M.J., and Shatz, C.J. (1987) Transient cells of the developing mammalian cerebral telencephalon are peptide-immunoreactive neurons. Nature., 325: 617–620.PubMedCrossRefGoogle Scholar
  7. Chun, J.J.M., and Shatz, C.J. (1988) Redistribution of synaptic vesicle antigens is correlated with the disappearance of a transient synaptic zone in the developing cerebral cortex. Neuron, 1: 297–310.PubMedCrossRefGoogle Scholar
  8. Chun, J.J.M., and Shatz, C.J. (1989) The earliest-generated neurons of the cerebral cortex: Characterization by MAP2 and neurotransmitter immunohistochemistry during fetal life. J. Neurosci., 9: 1648–1667.PubMedGoogle Scholar
  9. Crandall, J.E., and Caviness, V.S. (1984) Thalamocortical connections in newborn mice. J. Comp. Neurol., 228: 542–556.PubMedCrossRefGoogle Scholar
  10. Dawson, D.R., and Killackey, H.P. (1985) Distinguishing topography and somatotopy in the thalamocortical projections of the developing rat. Dev. Brain Res., 17: 309–313.CrossRefGoogle Scholar
  11. Dreher, B., Leventhal, A.G., and Hale, P.T. (1980) Geniculate input to cat visual cortex: a comparison of area 19 with areas 17 and 18. J. Neurophysiol., 44: 804–826.PubMedGoogle Scholar
  12. Duysens, J., Orban, G.A., van der Glas, H.W., and de Zegher, F.E. (1982a) Functional properties of Area 19 as compared to Area 17 of the cat. Brain Res., 231: 279–291.PubMedCrossRefGoogle Scholar
  13. Duysens, J., Orban, G.A., van der Glas, H.W., and Maes, H. (1982b) Receptive field structure of Area 19 as compared to Area 17 of the cat. Brain Res., 231: 293–308.PubMedCrossRefGoogle Scholar
  14. Edelman, G.M., and Finkel, L.H. (1984) Neuronal group selection in the cerebral cortex. In G.M. Edelman, W.E. Gall, and W.M. Cowan (eds.): Dynamic Aspects of Neocortical Function. New York, NY: Neurosciences Research Foundation, pp. 653–695.Google Scholar
  15. Ferster, D., and Lindstrom, S. (1983) An intracellular analysis of geniculo-cortical connectivity in Area 17 of the cat. J. Physiol., (Lond.) 342: 181–215.Google Scholar
  16. Finlay, B.L., and Pallas, S.L. (1989) Control of cell number in the developing mammalian visual system. Prog. Neurobiol., 32: 207–234.PubMedCrossRefGoogle Scholar
  17. Frost, D.O. (1981) Orderly anomalous retinal projections to the medial geniculate, ventrobasal, and lateral posterior nuclei of the hamster. J. Comp. Neurol., 203: 227–256.PubMedCrossRefGoogle Scholar
  18. Fukuda, Y., Hsiao, C.-F., Watanabe, M., and lto, H. (1984) Morphological correlates of physiologically identified Y-, X-, and W-cells in cat retina. J. Neurophysiol., 52: 999–1013.PubMedGoogle Scholar
  19. Ghosh, A., Antonini, A., McConnell, S.K., and Shatz, C.J. (1989) Ablation of subplate neurons alters the development of geniculocortical axons. Soc. Neurosci. Abstr., 15: 960.Google Scholar
  20. Gilbert, C.D., and Wiesel, T.N. (1979) Morphology and intracortical projections of functionally characterized neurones in the cat visual cortex. Nature, (Lond.) 280: 120–125.CrossRefGoogle Scholar
  21. Goldberg, J.M., and Brown, P.B. (1969) Response of binaural neurons of dog superior olivary complex to dichotic tonal stimuli: Some physiological mechanisms of sound localization. J. Neurophysiol., 32: 613–636.PubMedGoogle Scholar
  22. Hahm, J., and Sur, M. (1988) The development of individual retinogeniculate axons during laminar and sublaminar segregation in the ferret LGN. Soc. Neurosci. Abstr., 14:460.Google Scholar
  23. Hutchins, B., and Updyke, B.V. (1989) Retinotopic organization within the lateral posterior complex of the cat. J. Comp. Neurol., 285: 350–398.PubMedCrossRefGoogle Scholar
  24. Imig, T.J., and Reale, R.A. (1980) Patterns of cortico-cortical connections related to tonotopic maps in cat auditory cortex. J. Comp. Neurol., 192: 293–332.PubMedCrossRefGoogle Scholar
  25. Innocenti, G.M. (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science, 212: 824–827.PubMedCrossRefGoogle Scholar
  26. Innocenti, G.M., and Caminiti, R. (1980) Postnatal shaping of callosal connections from sensory areas. Exptl. Brain Res., 38: 381–394.CrossRefGoogle Scholar
  27. Innocenti, G.M., Fiore, L., and Caminiti, R. (1977) Exuberant projection into the corpus callo-sum from the visual cortex of newborn cats. Neurosci. Lett., 4: 237–242.PubMedCrossRefGoogle Scholar
  28. Ivy, G.O., and Killackey, H.P. (1982) Ontogenetic changes in the projections of neocortical neurons. J. Neurosci., 2: 735–743.PubMedGoogle Scholar
  29. Jackson, CA., Peduzzi, J.D., and Hickey, T.L. (1989) Visual cortex development in the ferret. I. Genesis and migration of visual cortical neurons. J. Neurosci., 9: 1242–1253.PubMedGoogle Scholar
  30. Kaas, J.H. (1987) The organization of neocortex in mammals: Implications for theories of brain function. Ann. Rev. Psychol., 38: 129–151.CrossRefGoogle Scholar
  31. Kaas, J.H., Hall, W.C., and Diamond, I.T. (1970) Cortical visual areas I and II in the hedgehog: Relation between evoked potential maps and architectonic subdivisions. J. Neurophysiol., 33: 595–615.PubMedGoogle Scholar
  32. Kaiserman-Abramof, I.R., Graybiel, A.M., and Nauta, W.J.H. (1980) The thalamic projection to cortical area 17 in a congenitally anopthalmic mouse strain. Neuroscience, 5: 41–52.PubMedCrossRefGoogle Scholar
  33. Kelly, J.B., Judge, P.W., and Phillips, D.P. (1986) Representation of the cochlea in primary auditory cortex of the ferret (Mustela putorius). Hearing Res., 24: 111–115.CrossRefGoogle Scholar
  34. Kimura, M., Shiida, T., Tanaka, K., and Toyama, K. (1980) Three classes of area 19 cortical cells characterized by their neuronal connectivity and photic responsiveness. Vision Res., 20: 69–77.PubMedCrossRefGoogle Scholar
  35. King, A.J., and Hutchings, M.E. (1987) Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: a map of auditory space. J. Neurophysiol., 57: 596–624.PubMedGoogle Scholar
  36. Knudsen, E.I., and Konishi, M. (1978) A neural map of auditory space in the owl. Science, 200: 795–797.PubMedCrossRefGoogle Scholar
  37. Leventhal, A.G., Rodieck, R.W., and Dreher, B. (1985) Central projections of cat retinal gan-glion cells. J. Comp. Neurol., 237: 216–226.PubMedCrossRefGoogle Scholar
  38. Linden, D.C., Guillery, R.W., and Cucchiaro, J. (1981) The dorsal lateral geniculate nucleus of the normal ferret and its postnatal development. J. Comp. Neurol., 203: 189–211.PubMedCrossRefGoogle Scholar
  39. Lund, R.D., and Mustari, M.J. (1977) Development of the geniculocortical pathway in rats. J. Comp. Neurol., 173: 289–306.PubMedCrossRefGoogle Scholar
  40. Luskin, M.B., and Shatz, C.J. (1985a) Studies of the earliest generated cells of the cat’s visual cortex: cogeneration of subplate and marginal zones. J. Neurosci., 5: 1062–1075.PubMedGoogle Scholar
  41. Luskin, M.B., and Shatz, C.J. (1985b) Neurogenesis of the cat’s primary visual cortex. J.Comp. Neurol., 242: 611–631.PubMedCrossRefGoogle Scholar
  42. Mason, C.A., and Robson, J.A. (1979) Morphology of retino-geniculate axons in the cat. Neu-roscience, 4: 79–97.Google Scholar
  43. McConnell, S.K., Ghosh, A., and Shatz, C.J. (1989) Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science, 245: 978–982.PubMedCrossRefGoogle Scholar
  44. Mendelson, J.R., and Cynader, M.S. (1985) Sensitivity of cat primary auditory cortex (AI) neurons to the direction and rate of frequency modulation. Brain Res., 327: 331–335.PubMedCrossRefGoogle Scholar
  45. Merzenich, M.M., Jenkins, W.M., and Middlebrooks, J.C. (1984) Observations and hypotheses on special organizational features of the central auditory nervous system. In G.M. Edelman, W.E. Gall, and W.M. Cowan (eds.): Dynamic Aspects of Neocortical Function. New York, NY: Neurosciences Research Foundation, pp. 397–424.Google Scholar
  46. Merzenich, M.M., Knight, P.L., and Roth, G.L. (1975) Representation of cochlea within primary auditory cortex in the cat. J. Neurophysiol., 38: 231–249.PubMedGoogle Scholar
  47. Middlebrooks, J.C., Dykes, R.W., and Merzenich, M.M. (1980) Binaural response-specific bands in primary auditory cortex (AI) of the cat: Topographical organization orthogonal to isofrequency contours. Brain Res., 181: 31–48.PubMedCrossRefGoogle Scholar
  48. Middlebrooks, J.C., and Knudsen, E.I. (1984) A neural code for auditory space in the cat’s superior colliculus. J. Neurosci., 4: 2621–2634.PubMedGoogle Scholar
  49. Middlebrooks, J.C., and Zook, J.M. (1983) Intrinsic organization of the cat’s medial geniculate body identified by projections to binaural response-specific bands in the primary auditory cortex. J. Neurosci., 3: 203–224.PubMedGoogle Scholar
  50. Mitani, A., and Shimokouchi, M. (1985) Neuronal connections in the primary auditory cortex: An electrophysiological study in the cat. J. Comp. Neurol., 235: 417–429.PubMedCrossRefGoogle Scholar
  51. Mitani, A., Shimokouchi, M., Itoh, K., Nomura, S., Kudo, M., and Mizuno, N. (1985) Morphology and laminar organization of electrophysiologically identified neurons in the primary auditory cortex in the cat. J. Comp. Neurol., 235: 430–447.PubMedCrossRefGoogle Scholar
  52. Pallas, S.L., Hahm, J.-O., and Sur, M. (1989) Retinal axon arbors in a novel target: Morphology of ganglion cell axons induced to arborize in the medial geniculate nucleus of ferrets. Soc. Neurosci. Abstr., 15: 495.Google Scholar
  53. Pallas, S.L., Roe, A.W., and Sur, M. (1988) Retinal projections induced into auditory thalamus in ferrets: Changes in inputs and outputs of primary auditory cortex. Soc. Neurosci. Abstr., 14: 460.Google Scholar
  54. Pallas, S.L., Roe, A.W., and Sur, M. (in press) Visual projections induced into the auditory pathway of ferrets: I. Novel inputs to primary auditory cortex (AI) from the LP/Pulvinar complex and the topography of the MGN-AI projection. J. Comp. Neurol. Google Scholar
  55. Pearson, H.E., Labar, D.R., Payne, B.R., Cornwaell, P., and Aggarwal, N. (1981) Transneuronal retrograde degeneration in the cat following neonatal ablation of visual cortex. Brain Res., 212: 470–475.PubMedCrossRefGoogle Scholar
  56. Perry, V.H., and Cowey, A. (1979) The effects of unilateral cortical and tectal lesions on retinal ganglion cells in rats. Exp. Brain Res., 35: 97–108.PubMedGoogle Scholar
  57. Phillips, D.P., Judge, P.W., and Kelly, J.B. (1988) Primary auditory cortex in the ferret (Mustela putorius): neural response properties and topographic organization. Brain Res., 443: 281–294.PubMedCrossRefGoogle Scholar
  58. Raabe, J.I., Windrem, M.S., and Finlay, B.L. (1986) Control of cell number in the developing visual system. II. Visual cortex ablation. Devel. Brain. Res., 28: 1–11.CrossRefGoogle Scholar
  59. Rakic, P. (1976) Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature, 261: 467–471.PubMedCrossRefGoogle Scholar
  60. Rakic, P. (1977) Prenatal development of the visual system in rhesus monkey. Phil. Trans. Roy. Soc., (Lond.) B 278: 245–260.CrossRefGoogle Scholar
  61. Roe, A.W., Garraghty, P.E., and Sur, M. (1987) Retinotectal W-cell plasticity: Experimentally induced retinal projections to auditory thalamus in ferrets. Soc. Neurosci. Abstr., 13: 1023.Google Scholar
  62. Roe A.W., Pallas, S.L., Hahm, J., Kwon, Y.H., and Sur, M. (1988) Retinal projections induced into auditory thalamus in ferrets: Visual topography in primary auditory cortex. Soc. Neu-rosci. Abstr., 14: 460.Google Scholar
  63. Schneider, G.E. (1973) Early lesions of the superior colliculus: Factors affecting the formation of abnormal retinal projections. Brain, Behav. Evol., 8: 73–109.CrossRefGoogle Scholar
  64. Schreiner, C.E., and Cynader, M.S. (1984) Basic functional organization of second auditory cortical field (AII) of the cat. J. Neurophysiol., 51: 1284–1305.PubMedGoogle Scholar
  65. Shatz, C.J., and Luskin, M.B. (1986) The relationship between the geniculocortical afferents and their cortical target cells during development of the cat’s primary visual cortex. J. Neurosci., 6: 3655–3668.PubMedGoogle Scholar
  66. Shatz, C.J., and Stryker, M.P. (1978) Ocular dominance in layer IV of the cat’s visual cortex and the effects of monocular deprivation. J. Physiol., (Lond.) 281: 267–283.Google Scholar
  67. Sherman, S.M., and Spear, P.D. (1982) Organization of visual pathways in normal and visually deprived cats. Physiol. Rev., 62: 738–855.PubMedGoogle Scholar
  68. Singer, W. (1977) Effects of monocular deprivation on excitatory and inhibitory pathways in cat striate cortex. Exptl. Brain Res., 134: 568–572.CrossRefGoogle Scholar
  69. Stanfield, B.B., and O’Leary, D.D.M. (1985) The transient corticospinal projection from the occipital cortex during the postnatal development of the rat. J. Comp. Neurol., 238: 236–248.PubMedCrossRefGoogle Scholar
  70. Stanfield, B.B., O’Leary, D.D.M., and Fricks, C. (1982) Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones. Nature, 298: 371–373.PubMedCrossRefGoogle Scholar
  71. Stanford, L.R. (1987) W-cells in the cat retina: Correlated morphological and physiological evidence for two distinct classes. J. Neurophysiol, 57: 218–244.PubMedGoogle Scholar
  72. Sur, M., Garraghty, P.E., and Roe, A.W. (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science, 242: 1437–1441.PubMedCrossRefGoogle Scholar
  73. Sur, M., Roe, A.W., and Garraghty, P.E. (1987) Evidence for early specificity of the retinogen-iculate X cell pathway. Soc. Neurosci. Abstr., 13: 590.Google Scholar
  74. Sur, M., and Sherman, S.M. (1982) Linear and nonlinear W cells in C-laminae of the cat’s lateral geniculate nucleus. J. Neurophysiol., 47: 869–884.PubMedGoogle Scholar
  75. Swadlow, H.A. (1983) Efferent systems of primary visual cortex: A review of structure and function. Brain Res. Rev., 6: 1–24.CrossRefGoogle Scholar
  76. Tong, L., Spear, P.D., Kalil, R.E., and Callahan, E.C. (1982) Loss of retinal X-cells in cats with neonatal or adult visual cortex damage. Science, 217: 72–75.PubMedCrossRefGoogle Scholar
  77. Wiesel, T.N., and Hubel, D.H. (1963) Single cell responses in striate cortex of kittens deprived of vision in one eye. J. Neurophysiol., 26: 1003–1017.PubMedGoogle Scholar
  78. Wiesel, T.N., and Hubel, D.H. (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unti responses in kittens. J. Neurophysiol., 28: 1029–1040.PubMedGoogle Scholar
  79. Wilson, J.R., and Sherman, S.M. (1977) Differential effects of early monocular deprivation on binocular and monocular segments of the cat striate cortex. J. Neurophysiol., 40: 892–903.Google Scholar
  80. Winguth, S.D., and Winer, J.A. (1986) Corticocortical connections of cat primary auditory cortex (AI): Laminar organization and identification of supragranular neurons projecting to Area AH. J. Comp. Neurol., 248: 36–56.PubMedCrossRefGoogle Scholar
  81. Wise, S.P., Hendry, S.H.C., and Jones, E.G. (1977) Prenatal development of sensory-motor cortical projections in cats. Brain Res., 138: 538–544.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1991

Authors and Affiliations

  • Sarah L. Pallas
    • 1
  1. 1.Department of Brain and Cognitive Sciences, E25-618Massachusetts Institute of TechnologyCambridgeUSA

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