The development of the corpus callosum in cats: A light‐ and electron‐ microscopic study

Changes in the size and shape of the corpus callosum (CC)–and in number, size, and structure of callosal axons–between embryonic day 38 E38 and postnatal day 150 (P150) were studied by light and electron microscope in 25 kittens. The development of the CC was divided into three phases: Embryonic development (E38, 53, 58): At E38, only part of the body of the CC was formed. At E53 and E58, the CC was still very short, but its different parts genu, body, and splenium) had formed. The cross‐sectional callosal area (CCA) was 5.4 mm2 at E53 and 5.6 mm2 at E58. The CC contained 46.3 and 56.4 million axons at E53 and E58 respectively. Mean axon diameters were 0.26 μm at E53 and 0.27 μm at E58. Early postnatal development (P4, 9, 15, 18, 21, 26): The CC at P4 was much longer than at E58 and still slightly elongated during this phase; CCA reached 8.55 mm2 at P4 and 8.88 mm2 at P26. There was a substantial axonal loss (66.8 million at P4 and 52.6 million at P26). From P15 onward, premyelinated and myelinated axons were seen. Mean axon diameter increased from 0.30 μm at P4 to 0.33 μm at P26. Late postnatal development (P39, 57, 92, 107, 150). The CC grew dramatically in both length and thickness, the latter especially in the genu. CCA was 10.1 mm2 at P39 and 15.3 mm2 at P150. The number of axons still decreased (46.5 million at P39 and 31.9 million at P150). The growth of the CCA paralleled the increase of myelinated axons (0.5% a t P26 and 29.6% at P150 and in the mean axon diameters (0.34 μm at P39 and 0.42 μm at P150). A number of axonal ultrastructural peculiarities (electron‐dense bodies, large vacuoles, lamellated bodies, etc., including those mentioned below) were noticed; their frequency at different ages was estimated as the percent of total axons. Interestingly, accumulations of vesicles inside axons increased from 4.1% a t E53 to 8.9% at P26, dropped to 0.2% at P39, and remained below 1% thereafter. Swollen mitochondria increased from 0.2% at E53 to 0.9% a t P26 and dropped to 0.06% (on the average) from P39 onward. Accumulations of vesicles and swollen mitochondria increased during the phase of rapid axonal elimination; thus, they may indicate axonal retraction and/or degeneration. Microglia‐gitter cells and astrocytes showing signs of phagocytosis were found during the embryonic and early postnatal development and may be involved in axon elimination.

[1]  J. Stone,et al.  The optic nerve of the cat: appearance and loss of axons during normal development. , 1982, Brain research.

[2]  R. Friede,et al.  The fine structure of stumps of transected nerve fibers in subserial sections , 1980, Journal of the Neurological Sciences.

[3]  G. Looney,et al.  Myelination of the corpus callosum in the cat: Time course, topography, and functional implications , 1986, The Journal of comparative neurology.

[4]  C. Hildebrand,et al.  Changing relation between onset of myelination and axon diameter range in developing feline white matter , 1982, Journal of the Neurological Sciences.

[5]  K. Kalil,et al.  Development of the pyramidal tract in the hamster. II. An electron microscopic study , 1982, The Journal of comparative neurology.

[6]  L. Landmesser,et al.  Fate of ganglionic synapses and ganglion cell axons during normal and induced cell death , 1976, The Journal of cell biology.

[7]  H. Naito,et al.  Diameters of callosal fibers interconnecting cat sensorimotor cortex. , 1971, Brain research.

[8]  P. Lampert A COMPARATOVE ELECTRON MICROSCOPIC STUDY OF REACTIVE, DEGENERATING, REGENERATING, AND DYSTROPHIC AXONS , 1967, Journal of neuropathology and experimental neurology.

[9]  B. Berger Etude Ultrastructurale de la Dégénérescence Wallérienne Experimentale d'un Nerf Entièrement Amyélinique: le Nerf Olfactif: I. Modifications axonales , 1971 .

[10]  S G Waxman,et al.  Small-diameter nonmyelinated axons in the primate corpus callosum. , 1980, Archives of neurology.

[11]  Giorgio M. Innocenti,et al.  Exuberant projection into the corpus callosum from the visual cortex of newborn cats , 1977, Neuroscience Letters.

[12]  R. Iman,et al.  Rank Transformations as a Bridge between Parametric and Nonparametric Statistics , 1981 .

[13]  J Bullier,et al.  Callosal connectivity of areas V1 and V2 in the newborn monkey , 1986, The Journal of comparative neurology.

[14]  Thomas S. Reese,et al.  FINE STRUCTURAL LOCALIZATION OF A BLOOD-BRAIN BARRIER TO EXOGENOUS PEROXIDASE , 1967, The Journal of cell biology.

[15]  R. Williams,et al.  Prenatal development of retinocollicular projections in the cat: an anterograde tracer transport study , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[16]  G. Innocenti,et al.  Development of projections from auditory to visual areas in the cat , 1988, The Journal of comparative neurology.

[17]  R. Coggeshall,et al.  Postnatal loss of axons in normal rat sciatic nerve , 1986, The Journal of comparative neurology.

[18]  Brent B. Stanfield,et al.  Selective collateral elimination in early postnatal development restricts cortical distribution of rat pyramidal tract neurones , 1982, Nature.

[19]  R. Coggeshall,et al.  Numbers of rat dorsal root axons and ganglion cells during postnatal development. , 1986, Brain research.

[20]  G. Shaw,et al.  Differential expression of neurofilament triplet proteins in brain development , 1982, Nature.

[21]  S. Waxman,et al.  Postnatal differentiation of rat optic nerve fibers: Electron microscopic observations on the development of nodes of Ranvier and axoglial relations , 1984, The Journal of comparative neurology.

[22]  G. Innocenti,et al.  Is there a genuine exuberancy of callosal projections in development? A quantitative electron microscopic study in the cat , 1983, Neuroscience Letters.

[23]  G. Innocenti General Organization of Callosal Connections in the Cerebral Cortex , 1986 .

[24]  Stephen G. Waxman,et al.  Ultrastructure of visual callosal axons in the rabbit , 1976, Experimental Neurology.

[25]  H. Killackey,et al.  Differential distribution of callosal projection neurons in the neonatal and adult rat , 1979, Brain Research.

[26]  Meyerson Ba Ontogeny of interhemispheric functions. An electrophysiological study in pre- and postnatal sheep. , 1968 .

[27]  John F. Brugge,et al.  Postnatal development of auditory callosal connections in the kitten , 1983 .

[28]  R. Doty,et al.  Forebrain Commissures and Vision , 1973 .

[29]  G M Innocenti,et al.  Growth and reshaping of axons in the establishment of visual callosal connections. , 1981, Science.

[30]  H. Killackey,et al.  Ontogenetic changes in the projections of neocortical neurons , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[31]  R. Coggeshall,et al.  Postnatal development of the rat dorsal funiculus , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[32]  D. Wahlsten,et al.  Axonal guidance during development of the great cerebral commissures: Descriptive and experimental studies, in vivo, on the role of preformed glial pathways , 1982, The Journal of comparative neurology.

[33]  M. Berry,et al.  Ontogeny of interhemispheric evoked potentials in the rat: significance of myelination of the corpus callosum. , 1972, Experimental neurology.

[34]  J. Pachter,et al.  The differential appearance of neurofilament triplet polypeptides in the developing rat optic nerve. , 1984, Developmental biology.

[35]  M. Glicksman,et al.  Differential Expression of the Three Neurofilament Polypeptides a , 1985, Annals of the New York Academy of Sciences.

[36]  P. Reier,et al.  Axonal interactions with connective tissue and glial substrata during optic nerve regeneration in Xenopus larvae and adults. , 1982, The American journal of anatomy.

[37]  M. Willard,et al.  Modulations of neurofilament axonal transport during the development of rabbit retinal ganglion cells , 1983, Cell.

[38]  B. Grafstein,et al.  Postnatal development of the transcallosal evoked response in the cerebral cortex of the cat. , 1963, Journal of neurophysiology.

[39]  G M Innocenti,et al.  Forms and measures of adult and developing human corpus callosum: Is there sexual dimorphism? , 1989, The Journal of comparative neurology.

[40]  D. O'Leary,et al.  The transient corticospinal projection from the occipital cortex during the postnatal development of the rat , 1985, The Journal of comparative neurology.

[41]  R. Lund,et al.  Development of a transient retino-retinal pathway in hooded and albino rats , 1981, Brain Research.

[42]  H. Holländer,et al.  Autoradiographic tracing of developing subcortical projections of the occipital region in fetal rabbits , 1980, The Journal of comparative neurology.

[43]  D. Tolbert,et al.  The transience of cerebrocerebellar projections is due to selective elimination of axon collaterals and not neuronal death. , 1984, Brain research.

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

[45]  C. P. Leblond,et al.  Radioautographic investigation of gliogenesis in the corpus callosum of young rats II. Origin of microglial cells , 1978, The Journal of comparative neurology.

[46]  P. Reier,et al.  Evidence for spontaneous axon degeneration during peripheral nerve maturation. , 1972, The American journal of anatomy.

[47]  R. Lund,et al.  Development of the rat's uncrossed retinotectal pathway and its relation to plasticity studies. , 1979, Science.

[48]  D. O'Leary,et al.  A transient pyramidal tract projection from the visual cortex in the hamster and its removal by selective collateral elimination. , 1986, Brain research.

[49]  S. Clarke,et al.  The organization of immature callosal connections , 1984, The Journal of comparative neurology.

[50]  H. van der Loos,et al.  The time course of the changes in axon number of both oculomotor nerves in normal and unilaterally enucleated Xenopus laevis. , 1986, Brain research.

[51]  Douglas A. Wolfe,et al.  Nonparametric Statistical Methods , 1973 .

[52]  W. Cowan,et al.  Evidence that the early postnatal restriction of the cells of origin of the callosal projection is due to the elimination of axonal collaterals rather than to the death of neurons. , 1981, Brain research.

[53]  G. Innocenti,et al.  Differential expression of neurofilament subunits in the developing corpus callosum. , 1988, Brain research.

[54]  N. K. Wessells,et al.  Veils, mounds, and vesicle aggregates in neurons elongating in vitro. , 1979, Experimental cell research.

[55]  E. Repasky,et al.  Rapid mobility of motile varicosities and inclusions containing alpha- spectrin, actin, and calmodulin in regenerating axons in vitro , 1985, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[56]  B. Droz,et al.  The smooth endoplasmic reticulum: structure and role in the renewal of axonal membrane and synaptic vesicles by fast axonal tranport , 1975, Brain Research.

[57]  M. Karnovsky,et al.  THE ULTRASTRUCTURAL BASIS OF CAPILLARY PERMEABILITY STUDIED WITH PEROXIDASE AS A TRACER , 1967, The Journal of cell biology.

[58]  Sanford L. Palay,et al.  The fine structure of the nervous system: The neurons and supporting cells , 1976 .

[59]  R. Oppenheim,et al.  Cell death of motoneurons in the chick embryo spinal cord. II. A quantitative and qualitative analysis of degenerationin the ventral root, including evidence for axon outgrowth and limb innervation prior to cell death , 1978, The Journal of comparative neurology.

[60]  D. Frost Axonal growth and target selection during development: retinal projections to the ventrobasal complex and other “nonvisual” structures in neonatal Syrian hamsters , 1984, The Journal of comparative neurology.

[61]  A. Spurr A low-viscosity epoxy resin embedding medium for electron microscopy. , 1969, Journal of ultrastructure research.

[62]  H. Killackey,et al.  Ontogenetic change in the distribution of callosal projection neurons in the postcentral gyrus of the fetal rhesus monkey , 1986, The Journal of comparative neurology.

[63]  R. Williams,et al.  Growth cones, dying axons, and developmental fluctuations in the fiber population of the cat's optic nerve , 1986, The Journal of comparative neurology.

[64]  G. Innocenti,et al.  Transitory macrophages in the white matter of the developing visual cortex. II. Development and relations with axonal pathways. , 1983, Brain research.

[65]  E. Hay,et al.  Freeze-fracture studies of the developing cell surface. II. Particle- free membrane blisters on glutaraldehyde-fixed corneal fibroblasts are artefacts , 1978, Journal of Cell Biology.

[66]  G. Innocenti,et al.  Transitory macrophages in the white matter of the developing visual cortex. I. Light and electron microscopic characteristics and distribution. , 1983, Brain research.

[67]  B. Payne,et al.  An exuberant retinocollicular pathway in Siamese kittens: effects of competition and abnormal activity on its maturation. , 1985, Brain research.

[68]  J. Provis,et al.  Human fetal optic nerve: Overproduction and elimination of retinal axons during development , 1985, The Journal of comparative neurology.

[69]  T. Powell,et al.  Centrifugal Fibres to the Retina in the Monkey and Cat , 1965, Nature.

[70]  J. K. Harting,et al.  Transient tectogeniculate projections in neonatal kittens: An autoradiographic study , 1985, The Journal of comparative neurology.

[71]  Colin Blakemore,et al.  Regressive events in the postnatal development of association projections in the visual cortex , 1985, Nature.

[72]  K. Valentino,et al.  The early formation of the corpus callosum: a light and electron microscopic study in foetal and neonatal rats , 1982, Journal of neurocytology.

[73]  P. Rakić,et al.  Overproduction and elimination of retinal axons in the fetal rhesus monkey. , 1983, Science.