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Cross-Modal Plasticity in Sensory Cortex

Visual Responses in Primary Auditory Cortex in Ferrets with Induced Retinal Projections to the Medial Geniculate Nucleus

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The Neocortex

Part of the book series: NATO ASI Series ((NSSA,volume 200))

Abstract

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.

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References

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Crandall, J.E., and Caviness, V.S. (1984) Thalamocortical connections in newborn mice. J. Comp. Neurol., 228: 542–556.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    CAS  Google Scholar 

  • Finlay, B.L., and Pallas, S.L. (1989) Control of cell number in the developing mammalian visual system. Prog. Neurobiol., 32: 207–234.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • Hutchins, B., and Updyke, B.V. (1989) Retinotopic organization within the lateral posterior complex of the cat. J. Comp. Neurol., 285: 350–398.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Innocenti, G.M. (1981) Growth and reshaping of axons in the establishment of visual callosal connections. Science, 212: 824–827.

    Article  PubMed  CAS  Google Scholar 

  • Innocenti, G.M., and Caminiti, R. (1980) Postnatal shaping of callosal connections from sensory areas. Exptl. Brain Res., 38: 381–394.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Ivy, G.O., and Killackey, H.P. (1982) Ontogenetic changes in the projections of neocortical neurons. J. Neurosci., 2: 735–743.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Kaas, J.H. (1987) The organization of neocortex in mammals: Implications for theories of brain function. Ann. Rev. Psychol., 38: 129–151.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Knudsen, E.I., and Konishi, M. (1978) A neural map of auditory space in the owl. Science, 200: 795–797.

    Article  PubMed  CAS  Google Scholar 

  • Leventhal, A.G., Rodieck, R.W., and Dreher, B. (1985) Central projections of cat retinal gan-glion cells. J. Comp. Neurol., 237: 216–226.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Lund, R.D., and Mustari, M.J. (1977) Development of the geniculocortical pathway in rats. J. Comp. Neurol., 173: 289–306.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • Luskin, M.B., and Shatz, C.J. (1985b) Neurogenesis of the cat’s primary visual cortex. J.Comp. Neurol., 242: 611–631.

    Article  PubMed  CAS  Google Scholar 

  • Mason, C.A., and Robson, J.A. (1979) Morphology of retino-geniculate axons in the cat. Neu-roscience, 4: 79–97.

    CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  Google Scholar 

  • Rakic, P. (1976) Prenatal genesis of connections subserving ocular dominance in the rhesus monkey. Nature, 261: 467–471.

    Article  PubMed  CAS  Google Scholar 

  • Rakic, P. (1977) Prenatal development of the visual system in rhesus monkey. Phil. Trans. Roy. Soc., (Lond.) B 278: 245–260.

    Article  CAS  Google Scholar 

  • 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 

  • 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 

  • Schneider, G.E. (1973) Early lesions of the superior colliculus: Factors affecting the formation of abnormal retinal projections. Brain, Behav. Evol., 8: 73–109.

    Article  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    CAS  Google Scholar 

  • Sherman, S.M., and Spear, P.D. (1982) Organization of visual pathways in normal and visually deprived cats. Physiol. Rev., 62: 738–855.

    PubMed  CAS  Google Scholar 

  • Singer, W. (1977) Effects of monocular deprivation on excitatory and inhibitory pathways in cat striate cortex. Exptl. Brain Res., 134: 568–572.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • Stanford, L.R. (1987) W-cells in the cat retina: Correlated morphological and physiological evidence for two distinct classes. J. Neurophysiol, 57: 218–244.

    PubMed  CAS  Google Scholar 

  • Sur, M., Garraghty, P.E., and Roe, A.W. (1988) Experimentally induced visual projections into auditory thalamus and cortex. Science, 242: 1437–1441.

    Article  PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    PubMed  CAS  Google Scholar 

  • Swadlow, H.A. (1983) Efferent systems of primary visual cortex: A review of structure and function. Brain Res. Rev., 6: 1–24.

    Article  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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.

    PubMed  CAS  Google Scholar 

  • 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 

  • 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.

    Article  PubMed  CAS  Google Scholar 

  • 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.

    Article  PubMed  CAS  Google Scholar 

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Pallas, S.L. (1991). Cross-Modal Plasticity in Sensory Cortex. In: Finlay, B.L., Innocenti, G., Scheich, H. (eds) The Neocortex. NATO ASI Series, vol 200. Springer, Boston, MA. https://doi.org/10.1007/978-1-4899-0652-6_19

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