The Maturation of the Superior Collicular Map of Auditory Space in the Guinea Pig is Disrupted by Developmental Visual Deprivation

In the normal guinea pig a map of auditory space appears, in the deeper layers of the superior colliculus, at 32 days after birth (DAB). The animal is unable to construct this collicular map of auditory space in the absence of developmental visual experience. Auditory receptive fields of animals dark‐reared from birth are typically large, occupying most of the contralateral hemifield. There is no topographic relationship between the collicular location of the recording electrode and the spatial position from which auditory stimuli elicit a maximal response. The fields of dark‐reared animals resemble, in their tuning parameters, the spatially undifferentiated fields typical of young postnatal normal guinea pigs. To investigate the time‐course during which visual experience is required for map emergence, animals received normal visual experience until either 18 or 26 DAB and were then dark‐reared until the terminal mapping experiment. Maps developed in neither group. Animals provided with a normal visual environment until 30 DAB, and then placed in the dark did, however, construct topographically organized spatial maps with discrete spatial receptive fields. Maps also failed to emerge in animals receiving normal visual experience both before and after a 4‐day period of visual deprivation between 26 and 30 DAB. We conclude that this 4‐day period, or part of it, constitutes a ‘crucial’ period during which visual experience is required for the normal elaboration of the collicular map of auditory space.

[1]  D. Hubel,et al.  Physiology of visual cells in mouse superior colliculus and correlation with somatosensory and auditory input , 1975, Nature.

[2]  Trichur Raman Vidyasagar,et al.  Possible plasticity in the rat superior colliculus , 1978, Nature.

[3]  E I Knudsen,et al.  Early blindness results in a degraded auditory map of space in the optic tectum of the barn owl. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[4]  J. Olavarria,et al.  The projection from striate and extrastriate cortical areas to the superior colliculus in the rat , 1982, Brain Research.

[5]  K E Binns,et al.  The developmental emergence of a map of auditory space in the superior colliculus of the guinea pig. , 1990, Brain research. Developmental brain research.

[6]  R. Lund The occipitotectal pathway of the rat. , 1966, Journal of anatomy.

[7]  J. Popelář,et al.  Effect of noise on auditory evoked responses in awake guina pigs , 1987, Hearing Research.

[8]  S D Esterly,et al.  A critical period for the recovery of sound localization accuracy following monaural occlusion in the barn owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[9]  M. Berry,et al.  Preferential orientation of stellate cell dendrites in the visual cortex of the dark-reared rat , 1976, Brain Research.

[10]  D. Sparks,et al.  Sensory and motor maps in the mammalian superior colliculus , 1987, Trends in Neurosciences.

[11]  E D Young,et al.  Rate responses of auditory nerve fibers to tones in noise near masked threshold. , 1986, The Journal of the Acoustical Society of America.

[12]  D. Creel,et al.  Differential susceptibility to noise-induced permanent threshold shift between albino and pigmented guinea pigs , 1986, Hearing Research.

[13]  J. Servière,et al.  Deoxyglucose demonstration of in-utero hearing in the guinea pig foetus , 1987, Hearing Research.

[14]  C. Blakemore,et al.  Developmental plasticity in the visual and auditory representations in the mammalian superior colliculus , 1988, Nature.

[15]  P. Marler,et al.  Role of auditory feedback in canary song development. , 1977, Journal of comparative and physiological psychology.

[16]  E I Knudsen,et al.  Computational maps in the brain. , 1987, Annual review of neuroscience.

[17]  Eric I. Knudsen,et al.  The role of auditory experience in the development and maintenance of sound localization , 1984, Trends in Neurosciences.

[18]  L. Aitkin,et al.  Rearing in an acoustically unusual environment — effects on neural auditory responses , 1975, Neuroscience Letters.

[19]  M. Keating,et al.  Visual experience and the maturation of the ipsilateral visuotectal projection inXenopus laevis , 1987, Neuroscience.

[20]  H. Killackey,et al.  Differential effect of enucleation on two populations of layer V pyramidal cells , 1975, Brain Research.

[21]  T. Raslear The use of the cochlear microphonic response as an indicant of auditory sensitivity: review and evaluation. , 1974, Psychological bulletin.

[22]  D. Hubel,et al.  RECEPTIVE FIELDS OF CELLS IN STRIATE CORTEX OF VERY YOUNG, VISUALLY INEXPERIENCED KITTENS. , 1963, Journal of neurophysiology.

[23]  M. A. Matthews,et al.  The postnatal development of the rat primary visual cortex during optic nerve impulse blockade by intraocular tetrodotoxin: a quantitative electron microscopic analysis. , 1985, Brain research.

[24]  S D Esterly,et al.  Monaural occlusion alters sound localization during a sensitive period in the barn owl , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  J. Haseman,et al.  Noise‐induced inner ear damage in newborn and adult guinea pigs , 1974, The Laryngoscope.

[26]  J. Blauert Spatial Hearing: The Psychophysics of Human Sound Localization , 1983 .

[27]  D. Sparks,et al.  Population coding of saccadic eye movements by neurons in the superior colliculus , 1988, Nature.

[28]  Frank H. Duffy,et al.  Comparison of the effects of dark rearing and binocular suture on development and plasticity of cat visual cortex , 1981, Brain Research.

[29]  D. Hubel,et al.  Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. , 1965, Journal of neurophysiology.

[30]  A R Palmer,et al.  Cells responsive to free‐field auditory stimuli in guinea‐pig superior colliculus: distribution and response properties. , 1983, The Journal of physiology.

[31]  B. J. Hammond,et al.  Signal processing technique to extract neuronal activity from noise , 1987, Journal of Neuroscience Methods.

[32]  J. Schmidt,et al.  Stroboscopic illumination and dark rearing block the sharpening of the regenerated retinotectal map in goldfish , 1985, Neuroscience.

[33]  M. Freire Effects of dark rearing on dendritic spines in layer IV of the mouse visual cortex. A quantitative electron microscopical study. , 1978, Journal of anatomy.

[34]  J. C. Middlebrooks,et al.  A neural code for auditory space in the cat's superior colliculus , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[35]  A J King,et al.  Spatial response properties of acoustically responsive neurons in the superior colliculus of the ferret: a map of auditory space. , 1987, Journal of neurophysiology.

[36]  K. E. Binns,et al.  The Maturation of the Superior Collicular Map of Auditory Space in the Guinea Pig is Disrupted by Developmental Auditory Deprivation , 1990, The European journal of neuroscience.

[37]  E. Knudsen,et al.  Vision calibrates sound localization in developing barn owls , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[38]  M. Berry,et al.  The effects of dark rearing on the development of the visual cortex of the rat , 1978, The Journal of comparative neurology.

[39]  E I Knudsen,et al.  Monaural occlusion shifts receptive-field locations of auditory midbrain units in the owl. , 1980, Journal of neurophysiology.

[40]  M. Keating,et al.  Visual deprivation and the maturation of the retinotectal projection in Xenopus laevis. , 1986, Journal of embryology and experimental morphology.

[41]  L. Chalupa,et al.  Receptive field characteristics of superior colliculus neurons and visually guided behavior in dark‐reared hamsters , 1978, The Journal of comparative neurology.

[42]  L. Chalupa,et al.  Responses of visual, somatosensory, and auditory neurones in the golden hamster's superior colliculus , 1977, The Journal of physiology.