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The Journal of Neuroscience, August 1, 1998, 18(15):5746-5765

The Role of the First Postmitotic Cortical Cells in the Development of Thalamocortical Innervation in the Reeler Mouse

Zoltán Molnár¹, Richard Adams¹, André M. Goffinet², and Colin Blakemore¹

¹ University Laboratory of Physiology, Oxford OX1 3PT, United Kingdom, and ² Faculté de Médecine, Département de Physiologie Humaine, Facultés Universitaires Notre-Dame de la Paix, 5000 Namur, Belgium

In the mutant mouse reeler, the tangential distribution of thalamocortical fibers is essentially normal, even though neurons of the cortical plate accumulate below the entire early-born preplate population (). This seems incompatible with the hypothesis that cells of the subplate (the lower component of the preplate in normal mammals) form an axonal scaffold that guides thalamic fibers and act as temporary targets for them (, ).

We used carbocyanine dyes to trace projections in wild-type and reeler mice between embryonic day 13 and postnatal day 3. Preplate formation and early extension of corticofugal fibers to form a topographic array are indistinguishable in the two phenotypes. So too are the emergence of thalamic axons in topographic order through the primitive internal capsule, their meeting with preplate axons, and their distribution over the preplate scaffold. Distinctive differences appear after the cortical plate begins to accumulate below the preplate of reeler, causing the preplate axons to form oblique fascicles, running through the cortical plate. Thalamic axons then pass through the plate within the same fascicles and accumulate in the "superplate" layer for ~2-3 d, before defasciculating and plunging down to terminate deep in the cortical plate, creating the curious "looping" pattern seen in the adult. Thus, thalamocortical innervation in reeler follows the same algorithm of development but in relation to the misplaced population of early-born neurons. Far from challenging the theory that preplate fibers guide thalamic axons, reeler provides strong evidence for it.

Key words: cortex; reeler; development; pioneer axons; preplate; "handshake hypothesis"; thalamus; mouse; subplate; axon guidance; internal capsule

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Copyright © 1998 Society for Neuroscience  0270-6474/98/18155746-20$05.00/0

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