Horizontal Interactions in Cat Striate Cortex: I. Anatomical Substrate and Postnatal Development

Luhmann, Heiko J.; Singer, Wolf; Martínez‐Millán, Luis

doi:10.1111/j.1460-9568.1990.tb00426.x

Cited by 103 publications

(75 citation statements)

References 79 publications

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“…This finding is in agreement with previous reports (9,10). The presence of crude orientation columns in neonatal animals (11)(12)(13) and the formation of crude clusters in the absence of normal patterned visual activity suggest that there may be an intrinsic, activityindependent framework designating the presumptive positions of orientation columns (5, 9).…”

Section: Resultssupporting

confidence: 93%

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Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex.

Callaway

Katz

1991

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

180

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Intrinsic horizontal axon collaterals in the striate cortex of adult cats specifically link columns having the same preferred orientation; consequently, retrograde tracer injections result in intrinsic labeling that is sharply clustered. We have previously shown that the normal development of this circuitry involves the emergence of crude clusters from an unclustered pattern during the second postnatal week. Crude clusters are later refined to the adult level of specificity by the selective rearrangement of axonal arbors that initially project to incorrect orientation columns. Here we report that depriving animals of patterned visual experience by binocular lid suture prior to natural eye opening had no discernible effect on the emergence of crude clusters. In contrast, cluster refinement was dramatically affected by binocular deprivation. Injections of retrograde tracers in the striate cortex of animals binocularly deprived for >1 month revealed only crude clusters, indicating that horizontal axon collaterals projecting to incorrect orientation columns were retained well past the age when they normally would have been eliminated. Layer 2/3 pyramidal cells from 6-week-old binocularly deprived animals had abnormal distributions of intrinsic horizontal axon collaterals that mirrored the lack of cluster refinement. The radial clustering of their horizontal collaterals was considerably less precise than normal. These cells, nevertheless, developed many of the features of normal mature arbors, including the distal axonal branches not seen in arbors from younger animals with normal visual experience. Together, these results indicate that axonal rearrangements occurred, but with reduced specificity. Thus, binocular deprivation did not simply arrest the development of this orientation-specific circuit at an immature state but limited the accuracy with which axon collaterals were added or eliminated. We suggest that development of this orientation-specific circuitry, like ocular dominance column segregation, may depend on temporal correlation of activity for regulation of axonal rearrangement. The specificity of rearrangement may be degraded in binocularly deprived cats because they do not experience sharply oriented visual stimuli necessary for concurrent activation of same-orientation columns.Pyramidal neurons in layer 2/3 and layer 5 of adult cat striate cortex have long intrinsic axon collaterals that project horizontally for several millimeters and elaborate clusters offiner terminal branches within isoorientation domains (1-4). Because these connections are reciprocal, clustered horizontal connections can be demonstrated either by intracellular filling of individual neurons (2-4) or by injection ofretrograde tracers into the cortex (1). The latter method results in distinct clusters of retrogradely labeled cells at intervals of roughly 1 mm surrounding the injection site. Clusters of labeled cells are localized to columns having the same orientation specificity as the injection site (1).Injections of retrog...

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Section: Resultssupporting

confidence: 93%

“…Discrepancies related to cluster development in binocularly deprived animals are more easily reconciled. Luhmann et al (10) reported that binocular deprivation had no effect on cluster development during the first 6 postnatal weeks. We, however, observed a lack of refinement of clustered connections in binocularly deprived animals.…”

Section: Resultsmentioning

confidence: 99%

Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex.

Callaway

Katz

1991

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

180

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“…During development, collateral clusters within a cortical layer emerge from an initially diffuse pattern by elimination of collaterals in inappropriate regions and selective growth in appropriate regions (15)(16)(17). There is evidence that this process is under the control of correlated neuronal activity (5,18).…”

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confidence: 99%

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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“…This pruning occurs at a time when visual signals are readily available and appears to be influenced by retinal activity. If visual experience is unrestricted, subpopulations of these pathways are stabilized; if vision is prevented by dark rearing or binocular deprivation, elimination of tangential connections is initially retarded (Callaway and Katz, 1990) but subsequently enhanced so that eventually only a rudimentary network of horizontal connections is maintained (Luhmann et al 1986(Luhmann et al , 1990c.…”

Section: Activity-dependent Selection Of Intracortical Connectionsmentioning

confidence: 99%

“…Developmental studies in the cat have shown that these tangential connections essentially appear postnatally, pass through a phase of exuberant proliferation during which they are particularly numerous and far-reaching, and subsequently become pruned (Price and Blakemore, 1985a,b;Luhmann et al 1990c;Callaway and Katz, 1990). This pruning occurs at a time when visual signals are readily available and appears to be influenced by retinal activity.…”

Section: Activity-dependent Selection Of Intracortical Connectionsmentioning

confidence: 99%

The Formation of Cooperative Cell Assemblies in the Visual Cortex

Singer

1991

Neuronal Cooperativity

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SummaryDuring a critical period of postnatal development of the mammalian visual cortex, synaptic connections are susceptible to use-dependent modifications. Synaptic connections strengthen if pre-and postsynaptic elements are active simultaneously and postsynaptic depolarization is sufficient to allow for the activation of A'-methyl-D-aspartate (NMDA)-receptor-gated conductances. By contrast, synaptic gain decreases if postsynaptic activation exceeds a critical threshold and presynaptic afferents are not capable of activating NMDAreceptor-dependent conductances. These processes lead to selective stabilization of connections between neuronal elements which often exhibit correlated activity and thus modify connectivity according to functional criteria. It is suggested that such experience-dependent selection of circuits serves different purposes at different levels of visual processing. At the input stage to the striate cortex it contributes to optimize the match between the representations of the two eyes. At a later stage of processing it participates in the development of selective connections between cortical columns and thereby serves to establish neuronal representations for frequently occurring constellations of features.Use-dependent changes of synaptic gain can also be induced in the mature visual cortex. These modifications follow the same rules as those occurring during early development and appear to depend on similar molecular mechanisms. However, in the adult the changes of synaptic gain do not seem to be followed by major rearrangements of connectivity. This suggests developmental alterations in mechanisms responsible for growth, removal and stabilization of synaptic connections. Actually, many of the cellular mechanisms thought to be involved in usedependent synaptic plasticity change during development but it is still unclear which of them are responsible for the definitive stabilization of functionally confirmed pathways. Functions requiring use-dependent selection of neuronal connections Fusion and stereopsisHigher mammals and humans, which have frontally positioned eyes with overlapping visual fields, can fuse the images of the two eyes and compute from their differences the distance of objects in space. The basis for this function are J|eurons in the visual cortex which possess two receptive fields, one in each eye,

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Horizontal Interactions in Cat Striate Cortex: I. Anatomical Substrate and Postnatal Development

Cited by 103 publications

References 79 publications

Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex.

Effects of binocular deprivation on the development of clustered horizontal connections in cat striate cortex.

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

The Formation of Cooperative Cell Assemblies in the Visual Cortex

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