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The Journal of Neuroscience, February 9, 2005, 25(6):1395-1406; doi:10.1523/JNEUROSCI.4023-04.2005

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Development/Plasticity/Repair
Functional Thalamocortical Synapse Reorganization from Subplate to Layer IV during Postnatal Development in the Reeler-Like Mutant Rat (Shaking Rat Kawasaki)

Shuji Higashi,¹ Kyoji Hioki,² Tohru Kurotani,³ Nicholas Kasim,⁴ and Zoltán Molnár^1,4

¹Division of Neurophysiology, Graduate School, Kyoto Prefectural University of Medicine, Kawaramachi-Hirokoji, Kyoto 602-8566, Japan, ²Central Institute for Experimental Animals, Kawasaki, Kanagawa 213, Japan, ³Department of Visual Neuroscience, Research Institute of Environmental Medicine, Nagoya University, Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan, and ⁴Department of Human Anatomy and Genetics, University of Oxford, Oxford OX1 3QX, United Kingdom

Transient synapse formation between thalamic axons and subplate neurons is thought to be important in thalamocortical targeting. Shaking rat Kawasaki (SRK), having reversed cortical layering similarly observed in reeler mouse, provides an interesting model system to test this idea. The spatial and temporal pattern of excitation was investigated using optical recording with voltage-sensitive dyes in thalamocortical slice preparations from SRK. At postnatal day 0 (P0), a strong optical response was elicited within the superplate of the SRK in the cell layer corresponding to subplate in wild-type (WT) rats. By P3, this response rapidly descended into deep cortical layers comprised of layer IV cells, as identified with 5-bromo-2'-deoxyuridine birthdating at embryonic day 17. During the first 3 postnatal days, both the subplate and cortical plate responses were present, but by P7, the subplate response was abolished. Tracing individual axons in SRK revealed that at P0-P3, a large number of thalamocortical axons reach the superplate, and by P7-P10, the ascending axons develop side branches into the lower or middle cortical layers. Synaptic currents were also demonstrated in WT subplate cells and in SRK superficial cortical cells using whole-cell recording. These currents were elicited monosynaptically, because partial AMPA current blockade did not modify the latencies. These results suggest that the general developmental pattern of synapse formation between thalamic axons and subplate (superplate) neurons in WT and SRK is very similar, and individual thalamic arbors in cortex are considerably remodeled during early postnatal development to find layer IV equivalent neurons.

Key words: reeler; superplate; SRK; thalamocortical slice; subplate; voltage-sensitive dye; optical recording

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Received June 18, 2004; revised December 18, 2004; accepted December 23, 2004.

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