Postnatal development of the superficial layers in the rat superior colliculus: a study with Golgi-Cox and Klüver-Barrera techniques

SummaryThe postnatal development of the superficial (optic) layers of the rat superior colliculus has been studied using Klüver-Barrera staining and Golgi impregnation in rats aged 3–45 days. The Klüver-Barrera staining reveals that the SC of 3 day old rats is morphologically immature with no obvious lamination. It contains densely packed cells of uniform size. The packing density of the cells gradually decreases between 9 and 15 days as the thickness of the layers increases. The first myelinated fibres in the SC appear at 15 days but the stratum opticum is still not recognizable. By 30 days, the SC has a distinctly laminated appearance, but the thickness of the superficial layers continues to increase until day 45 postnatal. Golgi-Cox impregnation displays the range of neuronal types in the superficial layers of the SC previously described by Langer and Lund (1974). Using the morphological criteria of these authors for classification of the neurons, the developmental changes of the marginal cells, horizontal cells, ganglion cells types I, II, III and stellate cells have been followed. The SC of 3 day old rats contains immature neurons; only a few larger cells have branched dendrites. In 9 days old SC the neuronal types present in the adult are recognizable, although their appearances are still immature. By 15 days neurons have adult-looking dendritic trees but dendritic growth continues beyond 30 days. The visual part of the SC has a protracted period of postnatal development, the sequence of developmental changes being similar for the different types of collicular neurons. Features common to development are the increasing size of neuronal somata, the increasing length of dendrites and the acquisition of a complex pattern of dendritic arborization. Larger cells appear to commence development earlier than small cells, although the rate of developmental changes is different for each of the various types of collicular neurons.

[1]  A. Tokunaga,et al.  Dendritic patterns of neurons in the rat superior colliculus , 1976, Experimental Neurology.

[2]  J. Juraska The development of pyramidal neurons after eye opening in the visual cortex of hooded rats: A quantitative study , 1982, The Journal of comparative neurology.

[3]  J. Lund,et al.  Development of neurons in the visual cortex (area 17) of the monkey (Macaca nemestrina): A Golgi study from fetal day 127 to postnatal maturity , 1977, The Journal of comparative neurology.

[4]  G. Jeffery,et al.  Does the early exuberant retinal projection to the superior colliculus in the neonatal rat develop synaptic connections? , 1984, Brain research.

[5]  B. Cragg,et al.  The development of synapses in the visual system of the cat , 1975, The Journal of comparative neurology.

[6]  G. Brückner,et al.  Neurogenesis in the visual system of the rat. An autoradiographic investigation , 1976, The Journal of comparative neurology.

[7]  C. Mason Postnatal maturation of neurons in the cat's lateral geniculate nucleus , 1983, The Journal of comparative neurology.

[8]  E. Ramón-Moliner,et al.  The Golgi-Cox Technique , 1970 .

[9]  A. Harvey,et al.  Transplantation of tectal tissue in rats. II. Distribution of host neurons which project to transplants , 1981, The Journal of comparative neurology.

[10]  A. Harvey,et al.  Transplantation of tectal tissue in rats. IV. Maturation of transplants and development of host retinal projection. , 1984, Brain research.

[11]  R. Anker The prenatal development of some of the visual pathways in the cat , 1977, The Journal of comparative neurology.

[12]  J. Kaas,et al.  Retinal projections in adult and newborn grey squirrels. , 1982, Brain research.

[13]  T. Tsumoto,et al.  Postnatal development of corticotectal neurons in the kitten striate cortex: A quantitative study with the horseradish peroxidase technique , 1983, The Journal of comparative neurology.

[14]  S. Wise,et al.  Maturation of pyramidal cell form in relation to developing afferent and efferent connections of rat somatic sensory cortex , 1979, Neuroscience.

[15]  M. Murray,et al.  Naturally occurring neuron death in the optic layers of superior colliculus of the postnatal rat , 1980, Journal of neurocytology.

[16]  L H Mathers,et al.  Postnatal maturation of neurons in the rabbit superior Colliculus , 1977, The Journal of comparative neurology.

[17]  A. Peters,et al.  Maturation of rat visual cortex. II. A combined Golgi‐electron microscope study of pyramidal neurons , 1981, The Journal of comparative neurology.

[18]  M. Berry,et al.  Dendritic growth and the control of neuronal form. , 1980, Current topics in developmental biology.

[19]  H. Uylings,et al.  The growth of non-pyramidal neurons in the visual cortex of the rat: A morphometric study , 1980, Brain Research.

[20]  L. Fagan-Dubin,et al.  Developmental changes in neuron size and density in the visual cortex and superior colliculus of the postnatal golden hamster , 1974, The Journal of comparative neurology.

[21]  B E Stein,et al.  Sequence of changes in properties of neurons of superior colliculus of the kitten during maturation. , 1973, Journal of neurophysiology.

[22]  Michael Miller Maturation of rat visual cortex. I. A quantitative study of Golgi-impregnated pyramidal neurons , 1981, Journal of neurocytology.

[23]  L. Garey,et al.  Golgi studies of the normal development of neurons in the lateral geniculate nucleus of the monkey , 2004, Experimental Brain Research.

[24]  D. K. Morest,et al.  The Golgi Methods , 1981 .

[25]  T T Norton,et al.  Receptive-field properties of superior colliculus cells and development of visual behavior in kittens. , 1974, Journal of neurophysiology.

[26]  R. Lund,et al.  The upper layers of the superior colliculus of the rat: A Golgi study , 1974, The Journal of comparative neurology.

[27]  R. Lund,et al.  Histogenesis of the superior colliculus of the albino rat: A tritiated thymidine study , 1979, Brain Research.

[28]  A. Harvey,et al.  Transplantation of tectal tissue in rats. I. Organization of transplants and pattern of distribution of host afferents within them , 1981, The Journal of comparative neurology.

[29]  T. J. Cunningham,et al.  Naturally occurring neuron death in the ganglion cell layer of the neonatal rat: morphology and evidence for regional correspondence with neuron death in superior colliculus. , 1981, Brain research.

[30]  R. Lund,et al.  Prenatal development of the optic projection in albino and hooded rats. , 1983, Brain research.

[31]  J. Sprague,et al.  Anatomical organization of pretectal nuclei and tectal laminae in the cat , 1974, The Journal of comparative neurology.

[32]  J. Parnavelas,et al.  The postnatal development of neurons in the dorsal lateral geniculate nucleus of the rat: A Golgi study , 1977, The Journal of comparative neurology.

[33]  L K Laemle,et al.  Retinocollicular projections in the neonatal rat: an anatomical basis for plasticity. , 1982, Brain research.

[34]  H. Feirabend,et al.  Classic Methods in Neuroanatomy , 1981 .

[35]  E. Fifková,et al.  A Golgi study of the early postnatal development of the visual cortex of the hooded rat , 1979, The Journal of comparative neurology.

[36]  J. Altman,et al.  Time of origin of neurons of the rat superior colliculus in relation to other components of the visual and visuomotor pathways , 2004, Experimental Brain Research.

[37]  J. Lund,et al.  Development of synaptic patterns in the superior colliculus of the rat. , 1972, Brain research.

[38]  T. Tsumoto,et al.  Postnatal development of corticotectal neurons in the kitten striate cortex: an electrophysiological study. , 1983, Brain research.

[39]  R. Lund,et al.  Prenatal development of central optic pathways in albino rats , 1976, The Journal of comparative neurology.