Dendritic morphology and inhibitory regulation distinguish dentate semilunar granule cells from granule cells through di
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ORIGINAL ARTICLE
Dendritic morphology and inhibitory regulation distinguish dentate semilunar granule cells from granule cells through distinct stages of postnatal development Akshay Gupta1,3 · Archana Proddutur1,3 · Yun‑Juan Chang2 · Vidhatri Raturi1 · Jenieve Guevarra1 · Yash Shah1 · Fatima S. Elgammal1 · Vijayalakshmi Santhakumar1,3 Received: 28 May 2020 / Accepted: 15 October 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020
Abstract Semilunar granule cells (SGCs) have been proposed as a morpho-functionally distinct class of hippocampal dentate projection neurons contributing to feedback inhibition and memory processing in juvenile rats. However, the structural and physiological features that can reliably classify granule cells (GCs) from SGCs through postnatal development remain unresolved. Focusing on postnatal days 11–13, 28–42, and > 120, corresponding with human infancy, adolescence, and adulthood, we examined the somato-dendritic morphology and inhibitory regulation in SGCs and GCs to determine the cell-type specific features. Unsupervised cluster analysis confirmed that morphological features reliably distinguish SGCs from GCs irrespective of animal age. SGCs maintain higher spontaneous inhibitory postsynaptic current (sIPSC) frequency than GCs from infancy through adulthood. Although sIPSC frequency in SGCs was particularly enhanced during adolescence, sIPSC amplitude and cumulative charge transfer declined from infancy to adulthood and were not different between GCs and SGCs. Extrasynaptic GABA current amplitude peaked in adolescence in both cell types and was significantly greater in SGCs than in GCs only during adolescence. Although GC input resistance was higher than in SGCs during infancy and adolescence, input resistance decreased with developmental age in GCs, while it progressively increased in SGCs. Consequently, GCs’ input resistance was significantly lower than SGCs in adults. The data delineate the structural features that can reliably distinguish GCs from SGCs through development. The results reveal developmental differences in passive membrane properties and steady-state inhibition between GCs and SGCs which could confound their use in classifying the cell types. Keywords Inhibition · GABA · Dentate gyrus · Extrasynaptic · Development · Granule cell · Semilunar granule cell
Introduction
Electronic supplementary material The online version of this article (https://doi.org/10.1007/s00429-020-02162-y) contains supplementary material, which is available to authorized users. * Vijayalakshmi Santhakumar vijayas@ucr.edu 1
Department of Pharmacology, Physiology and Neuroscience, Rutgers New Jersey Medical School, Newark, NJ 07103, USA
2
Office of Advance Research Computing, Rutgers New Jersey Medical School, Newark, NJ 07103, USA
3
Department of Molecular, Cell and Systems Biology, University of California, Riverside, CA 92521, USA
The dentate gyrus, the primary gateway for cortical inputs to the hippocampus, plays a unique role in memory processing a
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