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

Abstract

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...

Development of Individual Axon Arbors in a Thalamocortical Circuit Necessary for Song Learning in Zebra Finches

“…We found large-scale pruning of the branches of these axons over the course of vocal learning, unlike axon arbors that have been described in other developing systems (Crepel et al, 1976(Crepel et al, , 1980Lichtman, 1977;Smolen and Raisman, 1979;Changeux, 1980, 1981;Johnson and Purves, 1981;Shatz, 1984, 1986;Rubin, 1985;Young and Rubel, 1986;Callaway and Katz, 1991;Agmon et al, 1993;Antonini and Stryker, 1993;Catalano et al, 1996;Gan and Lichtman, 1998). Additionally, the dramatic changes in overall volume of the DLM terminal field within lMAN could be explained by changes in spatial extent and degree of overlap between individual DLM axon arbors.…”

“…For example, adult patterns of connec- tivity within developing sensory systems emerge as a result of extensive elaboration of axonal branches within restricted regions of postsynaptic targets. This increase in the number of axonal branches is accompanied by the elimination of a relatively small number of branches within "inappropriate" areas Shatz, 1984, 1986;Young and Rubel, 1986;Callaway and Katz, 1991;Agmon et al, 1993;Antonini and Stryker, 1993;Catalano et al, 1996;Snider et al, 1999). Thus, nascent axon arbors tend to be simple in shape and restricted in extent, and initial axonal connections can be extremely specific (Crowley and Katz, 1999).…”

Altered Intrinsic Neuronal Interactions in the Visual Cortex of the Blind

“…In congenital blindness, normal sensory experience is absent during development, and, as a result, brain areas that mainly subserve visual functions in sighted individuals undergo dramatic plastic changes in blind individuals. The visual cortex of blind individuals is smaller in terms of surface area and volume (Noppeney et al, 2005;Bridge et al, 2009;Park et al, 2009), but is increased in thickness (Bridge et al, 2009;Jiang et al, 2009;Park et al, 2009), which is consistent with disturbances in synaptic pruning and the elimination of exuberant neonatal connectivity that would normally establish the specificity of visual cortical organization based on sensory experience (Singer and Tretter, 1976;Movshon and Van Sluyters, 1981;Huttenlocher et al, 1982;Callaway and Katz, 1991). Strikingly, a wealth of studies has consistently demonstrated an altered functional role for occipital areas of blind individuals.…”

“…1976; Movshon and Van Sluyters, 1981;Huttenlocher et al, 1982;Callaway and Katz, 1991;Katz and Shatz, 1996). Indeed, a distinguishing feature of neuronal activity in visual cortex is the spread of fast-traveling waves along horizontal connections (Sato et al, 2012), which may underlie integration of information across large areas of cortex.…”

A neural network model for the development of simple and complex cell receptive fields within cortical maps of orientation and ocular dominance

“…These connections spread evenly across large regions of the cortex shortly after birth, gradually coalesce, and eventually form the clustered patterns seen in the adult (Callaway and Katz, 1990). In accord with the need for correlated visual input to drive the final development of long-range connections, it has been shown that binocular deprivation leads to poor segregation of these developing connections (Callaway and Katz, 1991). In the model, as orientation tuning gets initiated due to prenatal amplification and smoothing of initial random biases in geniculocortical connections, activitydependent processes could lead to initial clustering of long-range connections, and correlations present in the visual environment could subsequently produce long-range correlations in the map of complex cells, which could in turn drive associative learning of the adult pattern of long-range connections (Callaway and Katz, 1990).…”