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

Abstract

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.

Effects of monocular visual deprivation on geniculocortical innervation of area 18 in cat

“…In our earlier study of axons from kittens and normal adult cats, boutons identified at the LM level were a reliable indication of presynaptic sites identified at the EM level (Freund et al, 1985a,b;Friedlander and Martin, 1989). However, it was necessary to make a similar determination for axons in MD cats.…”

“…All quantitative analysis was carried out only on boutons that were fully serially reconstructed as evaluated by collecting full series of sections including the regions with any detectable sign of diameter change in the axon. We have previously demonstrated that boutons visualized at the LM level are sites of synaptic output as seen at the EM level (Freund et al, 1985a,b;Friedlander and Martin, 1989). However, we revalidated this relationship in MD material, and thus we also compared apparent interbouton segments of axon to LM-identified boutons.…”

“…In most cases, no resuturing was required. Control experiments were done on littermates at 5 postnatal weeks (see Friedlander and Martin, 1989) or 1 yr of age. Other normal adult controls were reared in the breeding colony at Oxford University and used as part ofanother study ofgeniculocortical axons (Freund et al, 1985a,b).…”

“…Responses were considered nonlinear if the axon's modulated response had a discernable second harmonic component (see Friedlander, 1986, 1989;Friedlander and Martin, 1989). In cases where the linearity of the cell's response was not clearly identifiable by listening, the cell's response to grating counterphase at several phase positions was collected under computer control.…”

“…The shrinkage factor (6-23%) was incorporated into measurements of bouton spacing and density based on measurements of each individual section analyzed. The arborizations were drawn under oil immersion (40x or 50x objectives), were photographed through the light microscope, had their bouton positions digitized and reconstructed in three-dimensional space, and were reembedded for correlated serial electron microscopy of the individual boutons (see Friedlander and Martin, 1989). A double-blind procedure was used for the sectioning, photography, digitizing, and analysis of the arborizations and individual boutons.…”