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Adult-born dentate granule cells show a critical period of dendritic reorganization and are distinct from developmentally born cells

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Abstract

Adult-born dentate granule cells (abGCs) exhibit a critical developmental phase during function integration. The time window of this phase is debated and whether abGCs become indistinguishable from developmentally born mature granule cells (mGCs) is uncertain. We analyzed complete dendritic reconstructions from abGCs and mGCs using viral labeling. AbGCs from 21–77 days post intrahippocampal injection (dpi) exhibited comparable dendritic arbors, suggesting that structural maturation precedes functional integration. In contrast, significant structural differences were found compared to mGCs: AbGCs had more curved dendrites, more short terminal segments, a different branching pattern, and more proximal terminal branches. Morphological modeling attributed these differences to developmental dendritic pruning and postnatal growth of the dentate gyrus. We further correlated GC morphologies with the responsiveness to unilateral medial perforant path stimulation using the immediate–early gene Arc as a marker of synaptic activation. Only abGCs at 28 and 35 dpi but neither old abGCs nor mGCs responded to stimulation with a remodeling of their dendritic arbor. Summarized, abGCs stay distinct from mGCs and their dendritic arbor can be shaped by afferent activity during a narrow critical time window.

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Acknowledgments

This work was supported by the LOEWE-Program “Neuronal Coordination Research Focus Frankfurt” (NeFF), by the German Science Foundation (CRC 1180), by the Federal Ministry of Education and Research (BMBF, to PJ, No. 01GQ1203A), by a Young Investigators Grant (from the faculty of medicine Goethe-University to PJ), and by a BMBF grant (No. 01GQ1406, Bernstein Award 2013) to HC. MB was further supported by the International Max Planck Research School (IMPRS) for Neural Circuits in Frankfurt. We thank Torsten Felske for help with GC reconstruction. We are indebted to Ute Fertig for technical assistance in preparing and staining of hippocampal slices.

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  1. Institute of Clinical Neuroanatomy, Goethe University, 60528, Frankfurt am Main, Germany

    Marcel Beining, Tassilo Jungenitz, Tijana Radic, Thomas Deller, Peter Jedlicka & Stephan Wolfgang Schwarzacher

  2. Ernst Strüngmann Institute (ESI) for Neuroscience in Cooperation with Max Planck Society, Deutschordenstr. 46, 60528, Frankfurt am Main, Germany

    Marcel Beining & Hermann Cuntz

  3. Frankfurt Institute for Advanced Studies (FIAS), 60438, Frankfurt am Main, Germany

    Marcel Beining & Hermann Cuntz

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  1. Marcel Beining
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Correspondence to Marcel Beining.

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M. Beining, T. Jungenitz are joint-first authors.

H. Cuntz, P. Jedlicka, S. W. Schwarzacher are joint-last authors.

Dendritic morphologies of early- and adult-born dentate granule cells that had been reconstructed for this study are available soon on the widely-used NeuroMorpho data base (Ascoli et al. 2007).

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Beining, M., Jungenitz, T., Radic, T. et al. Adult-born dentate granule cells show a critical period of dendritic reorganization and are distinct from developmentally born cells. Brain Struct Funct 222, 1427–1446 (2017). https://doi.org/10.1007/s00429-016-1285-y

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