Postnatal maturation of nonpyramidal neurons in the visual cortex of the cat

Meyer, Gundela; Ferres-Torres, R

doi:10.1002/cne.902280209

Cited by 101 publications

(45 citation statements)

References 41 publications

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“…3). The occurrence of neurons with similar morphologies in Golgi-impregnated preparations from kittens (Meyer and Ferres-Torres, 1984) supports this interpretation. Sea urchin-like cells remind us of multipolar cells reported in the embryonic cortex (Tabata and Nakajima, 2003) and cerebellar granule cells that settle in the inner granular layer (Kawaji et al, 2004).…”

Section: Sea Urchin-like Cellssupporting

confidence: 60%

Cortical GABAergic Interneurons Transiently Assume a Sea Urchin-Like Nonpolarized Shape before Axon Initiation

Yamasaki

Tanaka²,

Yanagawa³

et al. 2010

J. Neurosci.

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Mature neurons polarize by extending an axon and dendrites. In vitro studies of dissociated neurons have demonstrated that axons are initiated from a nonpolarized stage. Dissociated hippocampal neurons form four to five minor neurites shortly after plating but then one of them starts to elongate rapidly to become the future axon, whereas the rest constitutes the dendrites at later stages. However, neuroepithelial cells as well as migrating neurons in vivo are already polarized, raising the possibility that mature neurons inherit the polarities of immature neurons of neuroepithelial or migrating neurons. Here we show that the axon of interneurons in mouse cortical explant emerges from a morphologically nonpolarized shape. The morphological maturation of cortical interneurons labeled by electroporation at an embryonic stage was analyzed by time-lapse imaging during the perinatal stage. In contrast to earlier stages, most interneurons at this stage show sea urchin-like nonpolarized shapes with alternately extending and retracting short processes. Abruptly, one of these processes extends to give rise to an outstandingly long axon-like process. Given that the interneurons exhibit typical polarized shapes during embryonic development, the present results suggest that axon-dendrite polarity develops from a nonpolarized intermediate stage.

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Section: Sea Urchin-like Cellssupporting

confidence: 60%

Cortical GABAergic Interneurons Transiently Assume a Sea Urchin-Like Nonpolarized Shape before Axon Initiation

Yamasaki

Tanaka²,

Yanagawa³

et al. 2010

J. Neurosci.

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“…Spiny cells that are not stellate or pyramidal are occasionally encountered here but, as a group, do not display consistent anatomical or physiological features that might allow them to function as auditory cortical versions of the visual spiny stellates. Our data, combined with anatomical evidence from previous Golgi studies in several species, indicate that the spiny stellate is not the predominant or even a major cell type in any auditory thalamocortical recipient zone studied (McMullen and Glaser, 1982;Meyer and Ferres-Torres, 1984;Winer, 1984;Fitzpatrick and Henson, 1994).…”

Section: Discussionsupporting

confidence: 49%

“…Rose's observation may have foreshadowed observations of fundamental differences between layer 4 in auditory and other sensory cortices. Golgi studies in rabbit (McMullen and Glaser, 1982), cat (Winer, 1984), mustached bat (Fitzpatrick and Henson, 1994), and human (Meyer and Ferres-Torres, 1984;Meyer et al, 1989) showed that spiny stellates are rare in layer 4. In contrast to the symmetric dendritic trees of visual and somatosensory spiny stellates that are confined to layer 4, a great variety occurs in the dendritic arborization patterns of these infrequently encountered cells purported to be spiny stellate homologues.…”

mentioning

confidence: 98%

Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices

Smith

Populin

2001

J of Comparative Neurology

118

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In visual and somatosensory cortices of several species, spiny stellate cells in layer 4 are the first elements in signal processing where thalamic information is integrated and emergent receptive field properties are generated and sent on to more superficial cortical layers. In vivo and in vitro experiments have provided important information about how the anatomy and physiology of these cells and this layer fit into the functional cortical circuitry. No such data exist for the auditory cortex but are requisite if we are to understand whether ideas about information processing in one sensory cortical area can be generalized to another. Accordingly, we used in vitro slices from which to record and labeled cells in the middle layers of the cat auditory and visual cortices to compare basic anatomical and physiological features of cells recovered in similar layers using the same methods. Our results demonstrate a striking difference in a basic characteristic of two primary sensory cortical areas. In the visual cortex, spiny stellate cells predominate, receive short-latency synaptic inputs, and project to supergranular layers. No such spiny stellate population is encountered in the middle layers of the auditory cortex. Spiny cells that are not stellate or pyramidal are occasionally encountered but, as a group, do not display consistent anatomical or physiological features that might allow them to function as auditory cortical versions of the visual spiny stellates. Rather, pyramidal cells in the lower half of layer 3 and layer 4 appear to have assumed this role.

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“…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.…”

mentioning

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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Postnatal maturation of nonpyramidal neurons in the visual cortex of the cat

Cited by 101 publications

References 41 publications

Cortical GABAergic Interneurons Transiently Assume a Sea Urchin-Like Nonpolarized Shape before Axon Initiation

Cortical GABAergic Interneurons Transiently Assume a Sea Urchin-Like Nonpolarized Shape before Axon Initiation

Fundamental differences between the thalamocortical recipient layers of the cat auditory and visual cortices

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

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