4C Beta Research Articles

Quantitative light and electron microscopic analysis of cytochrome oxidase-rich zones in the striate cortex of the squirrel monkey.

Cytochrome oxidase activity was examined in the striate cortex (area 17) of squirrel monkeys at both the light and ultrastructural levels. Two prominent bands of reactivity were found in 4A and 4C with intermittent puffs of cytochrome oxidase reactivity in laminae 2 and 3. These puffs, spaced 0.5 mm apart, were in register with intermittent concentrations of activity in laminae 4B, 5, and 6. A thin band of reactivity was observed in lamina 1. The upper portion of 4C beta was less reactive than 4C alpha or the lower portion of 4C beta. Reactive neurons included stellate cells in all laminae and pyramidal cells in laminae 2 through 4B, 5, and 6. A row of large reactive pyramidal cells was observed in upper lamina 6. More reactive neurons were found in the puffs (laminae 2 and 3) than were observed in interpuff regions, and the reactive neurons were significantly larger than the nonreactive neurons. Reactive neurons contained two to three times as many reactive mitochondria as did the nonreactive neurons and often had indented nuclei. Based on the number of darkly or highly reactive, moderately reactive and lightly reactive mitochondria, puff regions were significantly different from nonpuff regions; there were approximately two times as many darkly reactive mitochondria in puff regions as compared to a similar nonpuff area. The majority of mitochondria (32% in puff; 44% in nonpuff) were found to reside in the dendritic profiles, which also contained the majority of highly reactive mitochondria. In a separate analysis, the total area of highly reactive mitochondria within puff regions was found to be twice the total area of highly reactive mitochondria in a comparable nonpuff region. An analysis of synapses showed that there were more asymmetrical synapses in both puff and nonpuff regions (55% and 54%, respectively) than symmetrical ones (45% in puff and 46% in nonpuff). There was an increase in mitochondrial reactivity in both asymmetrical and symmetrical synapses in the puff areas; however, the increased reactivity within asymmetrical terminals was significantly greater than that within symmetrical ones. Several somatodendritic synapses were observed and they were all of the symmetrical variety. Axospinous contacts were primarily of the asymmetrical type; however, symmetrical axospinous synapses were observed and were typically seen in association with an asymmetrical synapse. It was concluded that cytochrome oxidase activity is localized primarily within the dendritic profiles in both puff and nonpuff regions.(ABSTRACT TRUNCATED AT 400 WORDS)

Developmental changes in the relationship between type 2 synapses and spiny neurons in the monkey visual cortex.

This study continues an exploration of synaptic development in the primary visual cortex of the monkey (Macaca nemestrina). In a prior study (Mates and Lund, '83a), we observed that type 2 synapses on the cell bodies of spiny stellate neurons of lamina 4C appeared not only to increase in number during early postnatal development but also subsequently decreased during maturation. Using quantitative, stereological electron microscopic methods, we examined the maturation of this synapse population from embryonic day 159 to adult, on spiny stellate neurons of 4C alpha and beta and, for comparison, on pyramidal neurons in upper and lower lamina 6. Tissue was also taken for comparison from two animals reared to 8 weeks of age with binocular eyelid closure from birth. We confirmed that a marked increase and subsequent decrease occurred in this somal type 2 synapse population on both neuron populations. However, due to the infrequency of the smooth dendritic neurons (approximately 5% of the neuron population) giving rise to the type 2 contacts, and due to expansion of the neuropil during maturation increasing intercell distances against constant volume of the type 2 axon arbors, it is concluded that the decrease in type 2 somal synapses may represent a redistribution to dendrites rather than loss from the neuropil. Cells of lamina 4C beta (receiving input from the parvocellular lateral geniculate nucleus-LGN) show a slower initial accumulation of type 2 contacts compared to neurons of lamina 4C alpha (receiving input from magnocellular LGN), or to pyramidal neurons of lamina 6.(ABSTRACT TRUNCATED AT 250 WORDS)

Neuronal composition and development in lamina 4C of monkey striate cortex.

Lamina 4C (Lund, '73) of the monkey, Macaca nemestrina, visual striate cortex occupies a key position as a principal recipient zone of axons from the lateral geniculate nucleus (LGN). Synaptic maturation in lamina 4C is of particular interest since it involves a competitive interaction between thalamic axons for postsynaptic territory: an interaction which is strongly influenced by afferent activity (Hubel et al., '77). As an initial step toward understanding the normal process of synapse maturation in 4C, this study examines Golgi material to define the adult neuron populations of subdivisions 4C alpha (receiving afferents from magnocellular LGN) and 4C beta (receiving afferents from parvocellular LGN). Three groups of spine-bearing neurons are described--one relatively confined to either alpha or beta subdivision, the other two bridging the depth of 4C; four groups of smooth dendritic neurons interact with the spine-bearing population. Electron microscopy of normal and Golgi-impregnated tissue is used to define key features of synapse populations on these neurons. From embryonic day 159 through adulthood the smooth and spiny neurons occur in the same constant proportions in the neuropil (5% smooth, 95% spiny). Changes in the distribution of synapses on the spiny neurons are analyzed qualitatively; type 1 axon terminals (asymmetric apposition--round vesicles) shift from dendritic shafts to spine tips during maturation. Each spine is found to bear a type 1 contact at all ages; these results allow us to conclude that the figures of Boothe et al. ('79) on changes in spine populations during maturation can now be interpreted as changes in type 1 synapse populations. It is shown that type 2 synapses (symmetric appositions--pleomorphic vesicles) arise from axons of the smooth dendritic neurons. These synapses are found to increase in number on the spiny cell somata in early postnatal development, and this is followed by a decrease in number to the adult level.

Termination of afferent axons in macaque striate cortex

We used horseradish peroxidase (HRP) to orthogradely label afferent axons in macaque striate cortex. Of the 38 axons that we recovered, nine were recorded intracellularly before being filled with HRP. Light microscope and computer reconstructions of filled processes reveal highly stereotyped patterns of arborization and suggest that there are at least five discrete populations of lateral geniculate nucleus (LGN) afferent axon: (1) those to layer 4C beta, which have extremely circumscribed, dense terminal fields (small branches of which occasionally intrude into 4C alpha) but which have not been shown to project to other laminae; (2) afferents to layer 4A, which in some cases send fine ascending collaterals into layer 2-3 and which do not, apparently, send collaterals to other laminae; (3) afferents to layer 1, which are fine, extend over large distances horizontally, and send collaterals to layer 6A; (4) afferents to the lower two-thirds of layer 4C alpha, which have few or no collaterals in layer 6; and (5) afferents to the upper half of layer 4C alpha, which have arborizing collaterals in layer 6B. Of the nine axons that were recorded intracellularly, those with projections to layer 4C beta (two axons) and to layer 1 (one axon) had color-selective properties, whereas those (six axons) which arborized in 4C alpha all had transient, broad band and highly contrast-sensitive receptive fields. These properties are consistent with derivations from somata in the parvocellular and magnocellular divisions of the LGN, respectively. Afferents to 4C alpha were found to cover approximately 6 times as much surface area as afferents to 4C beta. The preterminal trunks of all axons were found to follow tortuous paths through the neuropil--paths that may derive from axon segregation during development. The wide ranging, patchy distributions of single afferents in 4C alpha suggest that individual 4C alpha axons supply more than one ocular dominance stripe. In one case where the terminal arborization of a 4C alpha axon was mapped against the transneuronally determined pattern of ocular dominance, three separate patches of terminal boutons were indeed found to coincide with the bands of one eye.

Ordinal position and afferent input of neurons in monkey striate cortex.

From the extracellular recording of single units in the monkey striate cortex and electrical stimulation at two selected sites in the optic radiations it was possible to estimate 1) the ordinal position of striate neurons (i.e., whether they received a monosynaptic, disynaptic or polysynaptic input from the thalamus) and 2) the nature of the afferent input to these neurons (i.e., whether it came from the magnocellular or parvocellular subdivision of the lateral geniculate nucleus (LGN)). Based on receptive field properties six major classes of striate neuron were identified--three which lacked orientation specificity (the ON-center, the OFF-center, and the ON/OFF or nonoriented (N-0) receptive fields) and three with orientation specific responses (the S, the C, and the B categories of receptive field). Units lacking orientation specificity were concentrated in laminae 4A, 4C beta and 6 while, for the cells with orientation specificity, C cells were found in laminae 4B and 6, B cells in 2/3 and 5, and S cells predominantly in laminae 2/3, 4C alpha, and 5. The results of electrical stimulation indicated that cell-to-cell transmission time in the monkey striate cortex is 1.5 msec, and latency measures showed that cells with a monosynaptic drive from the thalamus were confined to laminae 4 and 6 while disynaptically driven cells were found principally in upper lamina 4 (4A and 4B). No cell class was identified exclusively with a given ordinal position and there were many types of potential first-order neurons. The conduction time from one stimulating electrode to the next in the optic radiation was used to identify the afferent input to each striate neuron. The input to color-coded neurones was found to come exclusively from parvocellular layers while the C cells and two subclasses of the S cell (S2 and S3) were driven predominantly by the magnocellular subdivision. For other cell types (those with ON-center, N-0, and S1 receptive fields) the input came from either type of LGN neuron. The laminar distribution of neurons receiving a direct input from the magnocellular and parvocellular streams is in accord with the results of anatomical studies into the site of termination of the LGN input. The cell types receiving these direct inputs vary in the two streams so that the parvocellular input terminates on cells with ON-center and N-0 receptive fields in lamina 4C beta while the magnocellular input goes to cells with S, ON-center, N-0, and C receptive fields in lamina 4C alpha and the lower part of 4B. Consideration is given to the influence of these results on models for neural processing in monkey striate cortex and a comparison is drawn with the results of similar studies in the cat.