Is there a genuine exuberancy of callosal projections in development? A quantitative electron microscopic study in the cat

Koppel, H.; Innocenti, Giorgio M.

doi:10.1016/0304-3940(83)90219-7

Cited by 106 publications

(19 citation statements)

References 26 publications

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“…Aguayo et al (1973) investigating descriptions of the spontaneous loss of axons in normal peripheral nerves (Webster and O'Connell, 1970;Reier and Hughes, 1972), noted 16,000 axons in the cervical sympathetic trunk at birth and only 5760 axons 3 weeks later. A decline of similar magnitude was reported by Koppel and Innocenti (1983): 70% of callosal axons present at birth were eliminated by adulthood. Similarly, there is a significant reduction in the number of corticospinal axons after birth (Reh and Kalil, 1982) and of optic axons in neonates and after birth (Ng and Stone, 1982;Rakic and Riley, 1983;Williams et al, 1983Williams et al, , 1986.…”

Section: Discussionsupporting

confidence: 52%

Postnatal development of the rat dorsal funiculus

Ks¹,

Coggeshall²

1987

J. Neurosci.

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The present study shows that there are approximately 21,000 axons in the neonatal rat dorsal funiculus, as compared to 26,000 in 2-week-old animals. We attribute this increase primarily to arriving corticospinal fibers. In adult animals, however, there are approximately 15,000 axons. This is a decline of 58% from the 2 week level, and the decrease is proportionately similar in the corticospinal area and the dorsal funiculus proper. Thus, axon numbers decline in later postnatal development, and since the decline seems to be well past the time of the histogenetic death of the cells that give rise to these axons, we propose that the loss is not caused by the death of neurons. This is further evidence that a reduction in axon numbers not accompanied by cell death is a widespread phenomenon in mammalian postnatal neural development. We infer that the mechanism of axon loss is a reduction in axon branching and that its function is to sharpen synaptic connections.

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Section: Discussionsupporting

confidence: 52%

Postnatal development of the rat dorsal funiculus

Ks¹,

Coggeshall²

1987

J. Neurosci.

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“…Does a similar process occur at the geniculocortical level or does the Y-innervation of area 18 develop by a retractive process as has been suggested for the geniculocortical innervation of area 17 (LeVay et al 1978) and for a variety of other projections to kitten visual cortex (Innocenti, Fiore & Cemoniti, 1977;Koppel & Innocenti, 1983;Price & Blakemore, 1985)?…”

Section: Introductionmentioning

confidence: 84%

Development of Y‐axon innervation of cortical area 18 in the cat.

Friedlander

Martin

1989

The Journal of Physiology

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SUMMARY1. Geniculocortical Y-axons (n = 38) in the optic radiations of 4-5-week-old kittens (n = 20) and adult cats (n = 18) were studied both physiologically and morphologically. Axons were recorded from intracellularly and subsequently filled ionophoretically with horseradish peroxidase (HRP). The HRP filled the axons' terminal arborizations in visual cortex (particularly well for those innervating area 18). Fourteen axons appeared to be completely filled with HRP (n = 8 in kitten, n = 6 in adult) and served as the basis for the quantitative analysis of the terminal arborizations reported in this study.2. The distribution and correspondence of the axonal boutons to presynaptic elements in cortical layer 4A was analysed at both the light and electron microscope level using computerized three-dimensional analysis and serial section reconstruction, respectively. Compared to adult axons, the boutons of the kitten axons were smaller (x = 0 75 vs. 1-75 ,um length, P < 0-001) and more densely spaced both along individual axon branches (x = 6-60 vs. 11 20 ,sm interbouton interval, P < 0-001) and between neighbouring branches of the same axon (x = 4-7 vs. 6-4 #sm nearest-neighbour distance, P < 0-01).3. Most kitten boutons made a single Gray's type 1 synapse on a cortical neurone, unlike adult boutons which usually contacted two or more postsynaptic targets. Both kitten and adult axons had dendritic spines as their major target. Occasionally, HRP reaction-product was observed in cortical neurones postsynaptic to the labelled geniculocortical axon, which gave some estimate of the number of synaptic contacts between a single geniculocortical axon and target cell (about five).4. The kitten Y-axons innervated the visual cortex in a pattern similar to that of the adult, with the richest terminal branching and bouton density in layer 4A with some additional boutons distributed in layers 3, 4B and 6. The extent of the terminal arborizations primarily in layer 4A (as measured in surface views) of kitten Y-axons in area 18 was significantly less than that of adult Y-axons in area 18 (x = 0.9 mm2 vs. x = 1-2 mm2, P = 0 04).5. We conclude that between 4 and 5 postnatal weeks and 1 year, geniculocortical Y-axons projecting to cortical area 18 undergo four major changes. These include a M. J. FRIEDLANDER AND K. A. C. MARTIN reduction in synaptic bouton density (both in three-dimensional space and along individual branches), a concomitant moderate expansion in the surface area of cortex innervated, an increase in bouton size and an increase in the number of synaptic contacts made by each bouton. A general proportional growth of the individual axons' terminal arborization together with fusion and/or separation of neighbouring boutons is sufficient to explain this development.

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“…In the rat the reported proportions of unmyelinated fibers range from 19% ] to 46.4% [Seggie and Berry, 1972], whereas in the cat these range from zero [Naito et al, 1971] to 85% [Remahl and Hildebrand, 1982]. Note that in one species (cat) even the same group of researchers has documented different proportions of unmyelinated fibers in successive reports: Koppel and Innocenti [1983] reported 43-58% of unmyelinated fibers, whereas Berbel and Innocenti [1988] reported about 74%. Our results fall within the ranges obtained in previous studies (see table 1).…”

Section: Technical Aspectsmentioning

confidence: 93%

Species Differences and Similarities in the Fine Structure of the Mammalian Corpus callosum

Olivares

Montiel²,

Aboitiz³

2001

Brain Behav Evol

142

122

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A cross-species ultrastructural study of the corpus callosum was performed in six domestic species: the rat, the rabbit, the cat, the dog, the horse and the cow. The results indicate cross-species conservatism in callosal fiber composition with a good interspecies relation between fiber number and brain size. Across species, increases in both brain size and callosal area indicate more callosal fibers, although less than expected from the estimated increase in cortical cell number. Within each species, the correlation between fiber number and brain weight tends to disappear, although in most cases a larger callosum implies a larger number of callosal fibers. The median fiber diameter was conservative across species (0.11–0.2 µm), indicating the maintenance of conduction velocity of most callosal fibers regardless of interhemispheric distance. Nevertheless, the maximal fiber diameters tended to be higher in species with larger brains. Therefore, there is a population of coarse-diameter fibers that tend to increase their diameter and conduction velocity with increasing brain size. However, allometric calculations suggest that the associated increase in velocity in these large fibers may not be sufficient to maintain a constant interhemispheric transmission time in different species.

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Is there a genuine exuberancy of callosal projections in development? A quantitative electron microscopic study in the cat

Cited by 106 publications

References 26 publications

Postnatal development of the rat dorsal funiculus

Postnatal development of the rat dorsal funiculus

Development of Y‐axon innervation of cortical area 18 in the cat.

Species Differences and Similarities in the Fine Structure of the Mammalian Corpus callosum

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