Pioneer Neurons and Target Selection in Cerebral Cortical Development

Shatz, CJ; Ghosh, Anirvan; McConnell, Susan K.; Allendoerfer, Karen L.; Friauf, Eckhard; Antonini, Antonella

doi:10.1101/sqb.1990.055.01.046

Cited by 96 publications

(92 citation statements)

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“…Although both of these studies also employed relatively insensitive autoradiographic techniques, Shatz et al (22) are reexamining the development of thalamocortical afferents in cat visual cortex by using DiI and have found both an earlier ingrowth of thalamic afferents than previously reported and a waiting period between the time thalamic fibers arrive at the subplate and their subsequent invasion of the neocortical layers.…”

Section: Discussionmentioning

confidence: 99%

Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat.

Catalano

Robertson

Killackey

1991

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

203

125

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The initial ingrowth of thalamocortical afferents into the presumptive somatosensory cortex was examined in the fetal rat. Thalamic fibers were labeled in fixed brains with the carbocyanine dye 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI). On embryonic day 16, thalamocortical afferents arrive in the neocortex and course tangentially within the intermediate zone immediately underneath the cortical plate. By embryonic day 17, thalamocortical fibers have begun their radial growth into cortex and their arbors span the cell-sparse zone between layer VIb and the bottom of the cortical plate. By the day of birth (embryonic day 21), thalamocortical fibers form a dense plexus within layers VI and V below the dense cortical plate. Our observations indicate that in the rat thalamic afferents arrive in the cortex at a very early age and arborize within the forming cortical layers without an apparent "waiting" period.The mechanisms that control the development and differentiation of the neocortex remain the subject ofintense interest. Recent suggestions (1, 2) that thalamocortical projections play some role in these processes imply that thalamocortical projections make contact with the neocortex at a relatively early stage. However, the available evidence on this point is equivocal. On the one hand, Lund and Mustari (3) have reported that thalamocortical fibers reach the occipital cortex of the rat on embryonic day (E) 18 and then progressively invade the visual cortex on the following days. On the other hand, it has been reported that in the rat somatosensory cortex the thalamocortical fibers accumulate in the white matter below the cortical layers for several days and commence their innervation of the neocortical layers at about the time of birth (4, 5). This observation, as well as those of several other investigators (6,7), has led to the generally held belief that the development of thalamocortical projections is characterized by a "waiting" period. Further, it has been suggested that during this waiting period thalamocortical projections make contact with a transient population of cortical neurons, the subplate, and that these transient interactions play a particularly important role in the development and differentiation of the neocortex (8).We chose to investigate this question further because until recently the methods available to delineate thalamocortical projections were not particularly well-suited for use in the fetal brain. The introduction of carbocyanine dyes, such as 1,1'-dioctadecyl-3,3,3',3'-tetramethylindocarbocyanine perchlorate (DiI), as neuronal tracers in previously fixed tissue (9) overcomes many of the shortcomings of previous methods. Our study focuses on the earliest development of thalamocortical projections to the presumptive somatosensory cortex of the rat (E16 to the day of birth). The later development of these afferents and their adult morphology has been studied (10-12). The available evidence suggests that the somatosensory cortex is one of the first po...

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Section: Discussionmentioning

confidence: 99%

Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat.

Catalano

Robertson

Killackey

1991

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

203

125

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“…Cortical afferents project and synapse on presumptive subplate and early postmitotic presumptive deep-layer neurons (Shatz et al, 1990;De Carlos and O'Leary, 1992); however, in the reeler these neurons are primarily ectopically positioned at the top of the cortex, and thus thalamic axons project superficially (Caviness and Frost, 1983;Molnar and Blakemore, 1992). Neuronal perikarya within superficial reeler cortex survive and maintain projections to the midbrain, but projection neurons in the deep reeler cortex die or retract their axons, perhaps because they fail to capture afferent connections.…”

Section: Discussionmentioning

confidence: 99%

The mouse mutation reeler causes increased adhesion within a subpopulation of early postmitotic cortical neurons

et al. 1995

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Early postmitotic cortical neurons are mostly corticofugal projection neurons that take up positions in deep cortical laminae. Later postmitotic neurons are preferentially localized to superficial cortical laminae. In reeler mutant mice it appears that cortical laminar positions with respect to birthdate are reversed (Caviness, 1982). In a reanalysis of reeler lamination we found that early postmitotic cortical neurons labeled by embryonic day (E) 11–13 injections of a birthdate marker, or by early postnatal day (PND) 2 retrograde labeling through their output projections, appear to take up positions both in the superficial and deep cortex. Neurons born on E11 and E12 are more likely to be situated superficially in the reeler cortex and neurons born on E13 are more likely to be situated in the deep reeler cortex. Many corticofugal projection neurons in the deep (but not superficial) reeler cortex either die or retract their axons before PND 21. We hypothesize that the earliest postmitotic (E11-E12) of the early postmitotic reeler cortical neurons are overly adhesive and act as a barrier to later postmitotic migrating neurons. In vitro cortical aggregation cultures confirmed that early postmitotic (E12) reeler neurons are more adhesive than early postmitotic (E12) wild-type neurons or late postmitotic (E16) reeler or wild-type cortical neurons. We suggest that the moderate wild-type preferential adhesion of early postmitotic cortical neurons to each other helps deep and superficially fated lineages to form cortical laminae.

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“…Within the cortical plate, neuronal cell layering can be divided into the upper marginal zone and the underlying subplate [20]. The cells of the subplate show the characteristics of differentiated neurons and, therefore, can process synaptic information from afferent nerve fibers [21]. Additionally, a projection of the neurons themselves into the cortical plate, the thalamus and the colliculus superior is observed [22].…”

Section: Introductionmentioning

confidence: 99%

Differential Proteomics of the Cerebral Cortex of Juvenile, Adult and Aged Rats: An Ontogenetic Study

Wille¹,

Schumann²,

Kreutzer³

et al. 2017

J Proteomics Bioinform

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Pioneer Neurons and Target Selection in Cerebral Cortical Development

Cited by 96 publications

References 0 publications

Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat.

Early ingrowth of thalamocortical afferents to the neocortex of the prenatal rat.

The mouse mutation reeler causes increased adhesion within a subpopulation of early postmitotic cortical neurons

Differential Proteomics of the Cerebral Cortex of Juvenile, Adult and Aged Rats: An Ontogenetic Study

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