Specificity in the Development of Vertical Connections in Cat Striate Cortex

Katz, Lawrence C

doi:10.1111/j.1460-9568.1991.tb00805.x

Cited by 48 publications

(40 citation statements)

References 39 publications

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“…The formation of collateral branches was highest on membrane substrates from the target layers and not necessarily on membrane substrates which contained the highest concentration of growth promoters. In vivo, collaterals emerge in the target layers from the main efferent axon after it has grown out of the cortex (21). Sprouting of collateral branches from the primary axon shaft can also occur during the formation of cortical projections to distant targets.…”

Section: Discussionmentioning

confidence: 99%

“…In the developing cat visual cortex in vivo, it has been reported that axonal branches are almost never observed in inappropriate layers (21). There are several possibilities to explain why the branching specificity in the developing rat cortex in vitro is not as sharp as in cat cortex in vivo.…”

Section: Discussionmentioning

confidence: 99%

“…There is evidence that this process is under the control of correlated neuronal activity (5,18). In contrast, the formation of axonal projections between cortical layers is specific from the initial outgrowth; collaterals almost never form in inappropriate cortical layers (19)(20)(21). One mechanism which could explain this high degree of laminar specificity is that molecular surface components expressed in different layers, and recognized by specific axonal populations, control laminar branching specificity.…”

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confidence: 99%

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Membrane-associated molecules regulate the formation of layer-specific cortical circuits

Castellani

Bolz

1997

Proc. Natl. Acad. Sci. U.S.A.

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The columnar organization of the mammalian neocortex is based on radially oriented axon collaterals which precisely link cells from distinct cortical layers. During development, these interlaminar connections are specific from their initial outgrowth: collaterals form only in the target layers and there are no transient axonal collaterals in the nontarget layers. To examine whether positional cues within individual cortical layers regulate the laminar specificity of collateral formation, explants of cells destined for different cortical layers were cultured on membranes prepared from target and nontarget layers. Axonal growth and branching were examined on homogeneous membrane substrates and on alternating stripes of membranes from different layers. Results show that axons branch preferentially on membrane substrates from those layers that they would target in vivo. In addition, when cortical axons were given a choice to grow on membranes from either their target or their nontarget layer, they exhibited a clear preference for the target layers. This indicates that membrane-associated cues confined to individual layers regulate the formation of collaterals of cortical axons and restrict their growth to their target layers. Heat inactivation of membranes from target layers resulted in reduced axonal branching. The same manipulation of membranes from nontarget layers increased axonal branching for one population of cortical neurons. Taken together, these results suggest that membrane-associated molecules confined to individual layers induce and prevent the formation of axon collaterals in distinct populations of cortical neurons. Thus, the expression of layer-specific cues provides important constraints for the remodeling of local circuits during cortical development.A prominent component of the intrinsic circuitry of the neocortex are collateral connections of axons from pyramidal and spiny stellate cells. Within one cortical layer, tangentially oriented collaterals form regular clusters of axonal branches (1-3) and interconnect cells with similar functional specificities (4-6). In the vertical domain, pyramidal neurons have a main axon that projects out of the cortex and makes local connections within some of the 6 cortical layers (7-11) For instance, the axons of pyramidal cells in layers 2͞3 give rise to tangentially oriented collaterals in layers 2͞3 and layer 5 that branch profusely within these layers but do not extend into the adjacent layers 4 or 6 (see Fig. 1 A). On the other hand, many pyramidal cells in layer 6 send their efferent axon back to the thalamus. These axons emit collaterals in layer 6, which ascend to branch in the overlaying layers 4 and 3. As axon collaterals of layer 6 cells traverse layer 5 they make very few branches in this layer. Physiological studies in primary visual cortex revealed that this precise pattern of interlaminar connections generates characteristic response properties of cortical neurons (12)(13)(14).During development, collateral clusters within a cortical layer...

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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Membrane-associated molecules regulate the formation of layer-specific cortical circuits

Castellani

Bolz

1997

Proc. Natl. Acad. Sci. U.S.A.

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“…Layer 2/3 Pyramidal Neurons-The development of layer 2/3 pyramidal neurons has previously been described in cats, ferrets, and monkeys (Katz, 1991;Callaway, 1998b;Borrell and Callaway, 2002). Layer 2/3 pyramidal neurons in these studies show a high degree of specificity at all time points, with axons arborizing within layer 2/3 and layer 5 and avoiding layer 4 and layer 6.…”

Section: Development Of Axonal Laminar Specificitymentioning

confidence: 94%

Development of layer-specific axonal arborizations in mouse primary somatosensory cortex

2005

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In the developing neocortex, pyramidal neurons use molecular cues to form axonal arbors selectively in the correct layers. Despite the utility of mice for molecular and genetic studies, little work has been done on the development of layer-specific axonal arborizations of pyramidal neurons in mice. We intracellularly labeled and reconstructed the axons of layer 2/3 and layer 5 pyramidal neurons in slices of primary somatosensory cortex from C57Bl6 mice aged postnatal day 7-21. For all neurons studied, the development of the axonal arborizations in mice follows a pattern similar to that seen in other species; laminar specificity of the earliest axonal branches is similar to that of mature animals. At P7, pyramidal neurons are very simple, having only a main descending axon and few primary branches. Between P7 and P10 there is a large increase in the total number of axonal branches and axons continue to increase in complexity and total length from P10 to P21. Unlike observations in ferrets, cats, and monkeys, two types of layer 2/3 pyramidal neurons are present in both mature and developing mice; cells in superficial layer 2/3 lack axonal arbors in layer 4 while cells close to the layer 4 border have substantial axonal arbors within layer 4. We also describe axonal and dendritic arborization patterns of three pyramidal cell types in layer 5. The axons of tall-tufted layer 5 pyramidal neurons arborize almost exclusively within deep layers while tall-simple and short layer 5 pyramidal neurons also project axons to superficial layers.

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“…An inhibitory mechanism has been suggested for local cortical circuit formation by the observation that collaterals of developing layer 2/3 neurons emerge only in layers 2/3 and 5 from the outset but never appear in layer 4 (Katz, 1991). Likewise, it has also been shown that layer 6 axons bypass layer 5 and arborize specifically in layer 4 in vivo and in vitro (Callaway and Lieber, 1996;Dantzker and Callaway, 1998).…”

Section: Possible Mechanisms For Lamina-specific Branch Formationmentioning

confidence: 99%

Inhibitory Mechanism by Polysialic Acid for Lamina-Specific Branch Formation of Thalamocortical Axons

et al. 2000

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During development, thalamocortical axons form arbors primarily in layer 4 of the neocortex. This lamina-specific branch formation was studied in cultures of rat thalamic explants grown next to chemically fixed cortical slices. After a week in vitro, thalamic axons formed branches specifically in the target layer of fixed cortical slices, regardless of the orientation of the ingrowth. This in vitro system permits a direct assessment of contributions of membrane-associated molecules to thalamic axon branch formation. To this end, the present study uses three enzymatic perturbations: chondroitinase, phosphatidylinositol phospholipase C, or the polysialic acid (PSA)-specific endoneuraminidase (endo N). With endo N pretreatment of cortex, the number of branch points was increased significantly, whereas branch tip length was decreased. In addition, the localization of branch points to the target layer was weakened considerably. These features of branch formation were not altered by the other two enzymatic treatments, except that branch tips were shortened by chondroitinase treatment to the same extent as in endo N treatment. These results suggest that membrane-bound components are involved in lamina-specific branch formation of thalamocortical axons, and in particular that PSA moieties contribute to laminar specificity by inhibiting branch emergence in inappropriate layers.

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Specificity in the Development of Vertical Connections in Cat Striate Cortex

Cited by 48 publications

References 39 publications

Membrane-associated molecules regulate the formation of layer-specific cortical circuits

Membrane-associated molecules regulate the formation of layer-specific cortical circuits

Development of layer-specific axonal arborizations in mouse primary somatosensory cortex

Inhibitory Mechanism by Polysialic Acid for Lamina-Specific Branch Formation of Thalamocortical Axons

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