Abstract
ABSTRACTEarly‐born γ‐aminobutyric acid (GABA) neurons (EBGNs) are major components of the hippocampal circuit because at early postnatal stages they form a subpopulation of “hub cells” transiently supporting CA3 network synchronization (Picardo et al. [2011] Neuron 71:695–709). It is therefore essential to determine when these cells acquire the remarkable morphofunctional attributes supporting their network function and whether they develop into a specific subtype of interneuron into adulthood. Inducible genetic fate mapping conveniently allows for the labeling of EBGNs throughout their life. EBGNs were first analyzed during the perinatal week. We observed that EBGNs acquired mature characteristics at the time when the first synapse‐driven synchronous activities appeared in the form of giant depolarizing potentials. The fate of EBGNs was next analyzed in the adult hippocampus by using anatomical characterization. Adult EBGNs included a significant proportion of cells projecting selectively to the septum; in turn, EBGNs were targeted by septal and entorhinal inputs. In addition, most EBGNs were strongly targeted by cholinergic and monoaminergic terminals, suggesting significant subcortical innervation. Finally, we found that some EBGNs located in the septum or the entorhinal cortex also displayed a long‐range projection that we traced to the hippocampus. Therefore, this study shows that the maturation of the morphophysiological properties of EBGNs mirrors the evolution of early network dynamics, suggesting that both phenomena may be causally linked. We propose that a subpopulation of EBGNs forms into adulthood a scaffold of GABAergic projection neurons linking the hippocampus to distant structures. J. Comp. Neurol. 524:2440–2461, 2016. © 2016 Wiley Periodicals, Inc.
Highlights
Cortical g-aminobutyric acid (GABA) neurons play an essential role in coordinating network oscillations during development and adulthood (Freund and Buzsaki, 1996; Klausberger et al, 2004; Bonifazi et al, 2009; Lapray et al, 2012; Royer et al, 2012; Varga et al, 2012)
Given that filopodia were previously designated among the characteristic morphological features of GABA neurons involved in Synchronous plateau assemblies activity (SPAs) (Allene et al, 2012), this could indicate a change in spontaneous firing of early-born GABA neurons (EBGNs) toward the end of the first postnatal week
In agreement with the analysis of immunolabeled EGBNs, we found that some EBGNs displayed spontaneous and evoked firing patterns that indicated their involvement in SPAs until the midweek period, but, toward the end of the postnatal week, EBGNs displayed evoked firing pattern diversity and were all involved in Giant depolarizing potentials (GDPs) (Table 3)
Summary
Cortical g-aminobutyric acid (GABA) neurons play an essential role in coordinating network oscillations during development and adulthood (Freund and Buzsaki, 1996; Klausberger et al, 2004; Bonifazi et al, 2009; Lapray et al, 2012; Royer et al, 2012; Varga et al, 2012). GABA neurons form a diverse population (Freund and Buzsaki, 1996; Cossart et al, 2006; Ascoli et al, 2008; Klausberger and Somogyi, 2008) This diversity is determined partially by developmental programs. Given the potential role of hub neurons in activity-dependent developmental processes and their strong contribution to hippocampal GABAergic connectivity, it is essential to understand how these cells mature from embryonic to adult stages. To this aim, we performed a full morpho-physiological and molecular analysis of early-born GABA neurons (EBGNs) by using a genetic fate mapping strategy. The perinatal period was chosen because it is the time when population coherence emerges in the rodent hippocampus, following a precise sequence as shown in CA1 (Crepel et al, 2007)
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