Skip to main content
Log in

Auditory compensation of the effects of visual deprivation in the cat's superior colliculus

  • Published:
Experimental Brain Research Aims and scope Submit manuscript

Summary

Neurones in the superior colliculus of normal and visually deprived cats were analyzed for their responses to visual, auditory and somatosensory stimuli. The percentage of auditory-responsive cells throughout all layers had increased from 11% to 42% after binocular deprivation. Some auditory responses were found even in superficial layers. The number of somatosensory responses, though not systematically tested, was also higher in the visually deprived animals. Visually responsive units did not significantly decrease in number, thus resulting in an increased proportion of multisensory neurones. The vigour of auditory responses had increased after visual deprivation, while the vigour of visual responses had decreased significantly. In addition to the auditory effects of visual deprivation found, our study confirms previous findings on the visual effects of visual deprivation in the superior colliculus. Since only qualitative changes of visual responses, but no suppression of visual by non-visual activity was found, the neuronal mechanisms responsible for these changes may be different from competition as present in the visual cortex.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abeles M, Goldstein MH (1972) Responses of single units in the primary auditory cortex of the cat to tones and to tone pairs. Brain Res 42: 337–352

    Google Scholar 

  • Axelrod S (1959) Effects of early blindness. American Foundation for the Blind, New York

    Google Scholar 

  • Barlow HB (1981) Critical limiting factors in the design of the eye and visual cortex. Proc R Soc Lond [Biol] 212: 1–34

    Google Scholar 

  • Berman N, Cynader M (1972) Comparison of receptive-field organization of the superior colliculus in Siamese and normal cats. J Physiol (Lond) 224: 363–389

    Google Scholar 

  • Blakemore C, Cooper GF (1970) Development of the brain depends on the visual environment. Nature 228: 477–478

    Google Scholar 

  • Blakemore C, van Sluyters RC (1974) Reversal of the physiological effects of monocular deprivation in kittens: Further evidence for a sensitive period. J Physiol (Lond) 237: 195–216

    Google Scholar 

  • Blakemore C (1976) The conditions required for the maintenance of binocularity in the kitten's visual cortex. J Physiol (Lond) 261: 423–444

    Google Scholar 

  • Cynader M (1979) Competitive interactions in postnatal development. In: Freeman RD (ed) Developmental neurobiology of vision. Plenum Press, New York, pp 109–120

    Google Scholar 

  • Dews PB, Wiesel TN (1970) Consequences of monocular deprivation on visual behaviour in kittens. J Physiol (Lond) 206: 437–455

    Google Scholar 

  • Dräger UC, Hubel DH (1975) Responses to visual stimulation and relationship between visual, auditory, and somatosensory inputs in mouse superior colliculus. J Neurophysiol 38: 690–713

    Google Scholar 

  • Dreher B, Hoffmann K-P (1973) Properties of excitatory and inhibitory regions in the receptive fields of single units in the cat's superior colliculus. Exp Brain Res 16: 333–353

    Google Scholar 

  • Edwards SB, Ginsburgh CL, Henkel CK, Stein BE (1979) Sources of subcortical projections to the superior colliculus in the cat. J Comp Neurol 184: 309–330

    Google Scholar 

  • Feldon S, Feldon P, Kruger L (1970) Topography of the retinal projection upon the superior colliculus of the cat. Vision Res 10: 135–143

    Google Scholar 

  • Goldberg JM, Brown PB (1968) Functional organization of the dog superior olivary complex: an anatomical and electrophysiological study. J Neurophysiol 31: 639–656

    Google Scholar 

  • Gordon B (1973) Receptive fields in deep layers of cat superior colliculus. J Neurophysiol 38: 1049–1059

    Google Scholar 

  • Griesbach H (1899) Vergleichende Untersuchungen über die Sinnesschärfe Blinder und Sehender. Pflügers Arch 74: 577–638

    Google Scholar 

  • Guillery RW (1972) Binocular competition in the control of geniculate cell growth. J Comp Neurol 144: 117–127

    Google Scholar 

  • Harris LR (1980) The superior colliculus and movements of the head and eyes in cats. J Physiol (Lond) 300: 367–391

    Google Scholar 

  • Harris LR, Blakemore C, Donaghy M (1980) Integration of visual and auditory space in the mammalian superior colliculus. Nature 288: 56–59

    Google Scholar 

  • Hirsch HVB, Spinelli DN (1970) Visual experience modifies distribution of horizontally and vertically oriented receptive fields in cats. Science 168: 869–871

    Google Scholar 

  • Hirsch HVB (1972) Visual perception in cats after environmental surgery. Exp Brain Res 15: 405–423

    Google Scholar 

  • Hoffmann K-P, Sherman SM (1975) Effects of early binocular deprivation on visual input to cat superior colliculus. J Neurophysiol 38: 1049–1059

    Google Scholar 

  • Hoffmann K-P, Cynader M (1976) Visual responses and direction selectivity in cells of superficial and deep laminae in the cat's superior colliculus. Exp Brain Res [Suppl] I: 537–540

    Google Scholar 

  • Hubel DH, Wiesel TN (1965) Binocular interaction in striate cortex of kittens reared with artificial squint. J Neurophysiol 28: 1041–1059

    Google Scholar 

  • Hubel DH, Wiesel TN (1970) The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J Physiol (Lond) 206: 419–436

    Google Scholar 

  • Hyvärinen J (1981) Early visual deprivation alters modality of neuronal responses in area 19 of monkey cortex. Neurosci Lett 26: 239–243

    Google Scholar 

  • Kellogg WN (1962) Sonar system of the blind. Science 137: 399–404

    Google Scholar 

  • McIlwain JT, Fields HL (1970) Superior colliculus: single unit responses to stimulation of visual cortex in the cat. Science 170: 1426–1428

    Google Scholar 

  • Niemeyer W, Starlinger I (1981) Do the blind hear better? Investigations on auditory processing in congenital or early acquired blindness. II. Central functions. Audiology 20: 510–515

    Google Scholar 

  • Norton TT (1974) Receptive field properties of superior colliculus cells and development of visual behavior in kittens. J Neurophysiol 37: 674–690

    Google Scholar 

  • Paula-Barbosa MM, Sousa-Pinto (1973) Auditory cortical projections to the superior colliculus in the cat. Brain Res 50: 47–61

    Google Scholar 

  • Pettigrew JD (1978) The paradox of the critical period for striate cortex. In: Cotman CW (ed) Neuronal plasticity. Raven Press, New York, pp 311–330

    Google Scholar 

  • Rauschecker JP (1979) Orientation-dependent changes in response properties of neurons in the kitten's visual cortex. In: Freeman RD (ed) Developmental neurobiology of vision. Plenum Press, New York, pp 121–133

    Google Scholar 

  • Rauschecker JP, Singer W (1979) Changes in the circuitry of the kitten's visual cortex are gated by postsynaptic activity. Nature 280: 58–60

    Google Scholar 

  • Rauschecker JP, Harris LR (1981) Multimodal responses in the superior colliculus of binocularly deprived cats. Neurosci Lett [Suppl] 7: 203

    Google Scholar 

  • Rauschecker JP, Singer W (1981) The effects of early visual experience on the cat's visual cortex and their possible explanation by Hebb Synapses. J Physiol (Lond) 310: 215–239

    Google Scholar 

  • Rauschecker JP, Singer W, von Grünau MW (1981) Effects of monocular stroboscopic experience on the kitten's visual cortex. In: Szentágothai J, Hámori J, Palkovits M (eds) Adv Physiol Sci 2: Regulatory functions of the CNS. Subsystems. Akadémiai Kiadó, Budapest, pp 31–39

    Google Scholar 

  • Rauschecker JP (1982) Instructive changes in the kitten's visual cortex and their limitation. Exp Brain Res 48: 301–305

    Google Scholar 

  • Rauschecker JP, Singer W (1982) Binocular deprivation can erase the effects of preceding monocular or binocular vision in kitten cortex. Dev Brain Res 4: 495–498

    Google Scholar 

  • Sherman SM, Guillery RW, Kaas JH, Sanderson KJ (1974) Behavioral, electrophysiological and morphological studies of binocular competition in development of the geniculo-cortical pathway of cats. J Comp Neurol 158: 1–18

    Google Scholar 

  • Sprague JM, Berlucchi G, Rizzolatti G (1973) The role of the superior colliculus and pretectum in vision and visually guided behavior. In: Jung R (ed) Handbook of sensory physiology, vol VII/3B. Springer, Berlin Heidelberg New York, pp 27–102

    Google Scholar 

  • Stein BE, Labos E, Kruger L (1973) Sequence of changes in properties of neurons of superior colliculus of the kitten during maturation. J Neurophysiol 36: 667–679

    Google Scholar 

  • Sterling P, Wickelgren BG (1969) Visual receptive fields in the superior colliculus of the cat. J Neurophysiol 32: 1–15

    Google Scholar 

  • Vidyasagar TR (1978) Possible plasticity in the rat superior colliculus. Nature 275: 140–141

    Google Scholar 

  • Wickelgren BG, Sterling P (1969) Influence of visual cortex on receptive fields in cat superior colliculus. J Neurophysiol 32: 16–23

    Google Scholar 

  • Wickelgren BG (1971) Superior colliculus: Some receptive field properties of bimodally responsive cells. Science 173: 69–72

    Google Scholar 

  • Wiesel TN, Hubel DH (1963) Single-cell responses in striate cortex of kittens deprived of vision in one eye. J Neurophysiol 26: 1003–1017

    Google Scholar 

  • Wiesel TN, Hubel DH (1965) Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol 28: 1029–1040

    Google Scholar 

  • Woelfflin E (1909) Untersuchungen über den Fernsinn der Blinden. Z Sinnesphysiol 43: 187–198

    Google Scholar 

  • Wurtz RH, Mohler CW (1976) Organization of monkey superior colliculus: Enhanced visual response of superficial layer cells. J Neurophysiol 39: 745–765

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Supported partly by the Deutsche Forschungsgemeinschaft (SFB 50 Kybernetik). L.R. Harris received a visiting scholarship from the Max-Planck-Society. Part of the present work was done at the Max-Planck-Institute for Psychiatry, Dept. of Neurophysiology, Munich

Addison Wheeler Fellow

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rauschecker, J.P., Harris, L.R. Auditory compensation of the effects of visual deprivation in the cat's superior colliculus. Exp Brain Res 50, 69–83 (1983). https://doi.org/10.1007/BF00238233

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00238233

Key words

Navigation