Abstract
We have induced, by appropriate surgery in newborn ferrets, retinal projections into the medial geniculate nucleus, the principal auditory thalamic nucleus. In operated animals studied as adults, retinal ganglion cells that give rise to the projection have small and medium sized somata and heterogeneous dendrite morphologies. Each retina projects to the auditory thalamus in patchy fashion. Various nuclei in auditory thalamus project normally to auditory cortex. Visual cells in auditory thalamus have circular receptive fields and receive input from slowly conducting afferents characteristic of retinal W cells. Many visual cells in primary auditory cortex have oriented receptive fields that resemble those of complex cells in striate cortex. Primary auditory cortex also contains a two dimensional visual field map. Our results carry several implications for sensory cortical function. A parsimonious explanation for the visual receptive field properties in auditory cortex is that sensory cortex carries out certain stereotypical transformations on input regardless of modality. The response features of visual cells and the two dimensional visual field map in primary auditory cortex appear to be products of adaptive organization arising from a highly divergent thalamocortical projection characteristic of the auditory system.
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References
Aitkin, L.M., Irvine, D.R.F. & Webster, W.R. (1984) Central neural mechanisms of hearing. In: Handbook of Physiology: The Nervous System III, Amer. Physiol. Soc., Bethesda, MD, pp. 675–737.
Campbell, G. & Frost, D.O. (1987) Target-controlled differentiation of axon terminals and synaptic organization. Proc. Natl. Acad. Sci. USA, 84: 6929–6933.
Cucchiaro, J. & Guillery, R.W. (1984) The development of the retinogeniculate pathways in normal and albino ferrets. Proc. R. Soc. Lond. B. 223: 141–164.
Cunningham, T.J. (1976) Early eye removal produces extensive bilateral branching in the rat. Science. 194: 857–859. Devor, M. (1975) Neuroplasticity in the sparing or deterioration of function after early olfactory tract lesions. Science. 190: 998–1000.
Dreher, B., Leventhal A.G., & 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.
Edelman, G.M. (1978) Group selection and phasic reentrant signaling: a theory of higher brain function. In: The Mindful Brain. M.I.T. Press.
Edelman, G.M. and Finkel, L.H. (1984) Neuronal group selection in the cerebral cortex. In: Dynamic Aspects of Neocortical Function. ed. by G.M. Edelman, W.E. Gall, W.M. Cowan. Wiley-Interscience.
Ferster, D. & Lindstrom, S. (1983) An intracellular analysis of geniculocortical connectivity in area 17 of the cat. J. Physiol.. Lond.. 342: 181–215.
Finkel, L.H. and Edelman, G.M. (1987) Population rules for synapses in networks. In: Synaptic Function. ed. by G.M. Edelman, W.E. Gall and W.M. Cowan. Wiley-Interscience.
Finlay, B.L., Wilson K.G., & Schneider, G.E. (1979) Anomalous ipsilateral retinotectal projections in Syrian hamsters with early lesions: Topography and functional capacity. J. Comp. Neurol., 183: 721–740.
Frost, D.O. (1981) Ordered anomalous retinal projections to the medial geniculate, ventrobasal and lateral posterior nuclei. J. Comp. Neurol., 203: 227–256.
Frost, D.O. (1986) Development of anomalous retinal projections to nonvisual thalamic nuclei in Syrian hamsters: a quantitative study. J. Comp. Neurol., 252: 95–105.
Frost, D.O. & Metin, C. (1985) Induction of functional retinal projections to the somatosensory system. Nature, 317: 162–164.
Gilbert, C D. & Wiesel, T.N. (1979) Morphology and intracortical projections of functionally characterized neurones in cat visual cortex. Nature, 3: 120–125.
Graziadei, P.P.C., Levine, R.R. & Monti-Graziadei, G.A. (1979) Plasticity of connections of the olfactory sensory neuron: regeneration into the forebrain following bulbectomy in the neonatal mouse. Neuroscience, 4: 713–727.
Hoffmann, K.-P. (1973) Conduction velocity in pathways from retina to superior colliculus in the cat: a correlation with receptive field properties. J. Neurophysiol., 36: 409–424.
Imig, T.J. and Adrian, H.O. (1977) Binaural columns in the primary field (Al) of cat auditory cortex. Brain Res. 138: 241–257.
Jones, E.G. (1984) Identification and classification of intrinsic circuit elements in the neocortex. In: Dynamic Aspects of Neocortical Function, ed. by G.M. Edelman, W.E. Gall, W.M. Cowan. Wiley-Interscience.
Jones, E.G. (1985) The Thalamus. Plenum.
Kelly, J.G., Judge, P.W. & Phillips, D.P. (1986) Representation of the cochlea in primary auditory cortex of the ferret (Mustela putorius). Hearing Res. 24: 111–115.
Linsker, R. (1986) From basic network principles to neural architecture: Emergence of orientation-selective cells. Proc. Natl. Acad. Sci. USA. 83: 8390–8394.
Lorente de No, R. (1938) Physiology of the Nervous System. Oxford Univ. Press.
Lund, R.D. (1969) Synaptic patterns of the superficial layers of the superior colliculus of the rat. J. Comp. Neurol. 135: 179–208.
Lund, R.D. & Lund, J.S. (1976) Plasticity in the developing visual system: the effects of retinal lesions made in young rats. J. Comp. Neurol., 169: 133–154.
McConnell, S.K. & LeVay, S. (1986) Anatomical organization of the visual system of the mink, Mustela vison. J. Comp. Neurol. 250: 109–132.
Mendelson, J.R. & Cynader, M.S. (1985) Sensitivity of cat primary auditory cortex (A1) neurons to the direction and rate of frequency modulation. Brain Res. 327: 331–335.
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: Dynamic Aspects of Neocortical Function, ed. by G.M. Edelman, W.E. Gall, W.M. Cowan. Wiley-Interscience.
Merzenich, M.M., Kaas, J.H., Wall, J., Nelson, R.J., Sur, M., & Felleman, D. (1983) Topographic reorganization of somatosensory cortical areas 3B and 1 in adult monkeys following restricted deafferentation. Neuroscience, 8: 33–55.
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.
Mitani, A., Shimokouchi, M., Itoh, K., Nomura, S., Kudo, M. & 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.
Mountcastle, V.B. (1978) An organizing principle for cerebral function: the unit module and the distributed system. In: The Mindful Brain. M.I.T. Press.
Palay, S.L. and Chan-Palay, V. (1974) Cerebellar Cortex: Cytology and Organization. Springer.
Roe, A.W., Garraghty, P.E. & Sur, M. (1987) Retinotectal W cell plasticity: experimentally induced retinal projections to auditory thalamus in ferrets. Soc. Neurosci. Abst., 13: 1023.
Schneider, G.E. (1973) Early lesions of the superior colliculus: factors affecting the formation of abnormal retinal projections. Brain Behav. Evol., 8: 73–109.
Shatz, C.J. (1983) The prenatal development of the cat’s retinogeniculate pathway. J. Neurosci., 3: 482–499.
Shepherd, G. (1979) The Synaptic Organization of the Brain. Oxford Univ. Press, 2nd ed.
Sherman, S.M. & Spear, P.D. (1982) Organization of visual pathways in normal and visually deprived cats. Physiol. Rev., 62: 738–855.
So, K.-F., Campbell, G., & Lieberman, A.R. (1985) Synaptic organization of the dorsal lateral geniculate nucleus in the adult hamster. Anat. Embryol., 171: 223–234.
Suga, N. (1984) The extent to which biosonar information is represented in the bat auditory cortex. In: Dynamic Aspects of Neocortical Function, ed. by G.M. Edelman, W.E. Gall, W.M. Cowan. Wiley-Interscience.
Sur, M. & Garraghty, P.E. (1986) Experimentally induced visual responses from auditory thalamus and cortex. Soc. Neuroscience Abst., 12: 592.
Sur, M., Garraghty, P.E., & Roe, A.W. (1988) Experimentally induced visual projections into auditory thalamus and cortex. Submitted for publication.
Sur, M., Roe, A.W. & Garraghty, P.E. (1987) Evidence for early specificity of the retinogeniculate X cell pathway. Soc. Neurosci. Abstr., 13: 590.
Sur, M. & Sherman, S.M. (1982) Linear and nonlinear W cells in C-laminae of the cat’s lateral geniculate nucleus. J. Neurophysiol., 47: 869–884.
Tong, L, Spear, P.D., Kalil, R.E., & Callahan, E.C. (1982) Loss of retinal X-cells in cats with neonatal or adult visual cortex damage. Science. 217: 72–75.
Vitek, D.J., Schall, J.D., & Leventhal, A.G. (1985) Morphology, central projections, and dendritic field orientation of retinal ganglion cells in the ferret. J. Comp. Neurol., 241: 1–11.
Whitfield, I.C. & Evans, E.F. (1965) Responses of auditory cortical neurons to stimuli of changing frequency. J. Neurophysiol., 28: 655–672.
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Sur, M. (1989). Visual Plasticity in the Auditory Pathway: Visual Inputs Induced into Auditory Thalamus and Cortex Illustrate Principles of Adaptive Organization in Sensory Systems. In: Arbib, M.A., Amari, Si. (eds) Dynamic Interactions in Neural Networks: Models and Data. Research Notes in Neural Computing, vol 1. Springer, New York, NY. https://doi.org/10.1007/978-1-4612-4536-0_3
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DOI: https://doi.org/10.1007/978-1-4612-4536-0_3
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