Interneurons of the Dentate–Hilus Border of the Rat Dentate Gyrus: Morphological and Electrophysiological Heterogeneity

Abstract

Interneurons located near the border of the dentate granule cell layer and the hilus were studied in hippocampal slices using whole-cell current clamp and biocytin staining. Because these interneurons exhibit both morphological and electrophysiological diversity, we asked whether passive electrotonic parameters or repetitive firing behavior correlated with axonal distribution. Each interneuron was distinguished by a preferred axonal distribution in the molecular layer or granule cell layer, and four groups could be discerned, the axons of which arborized in (1) the granule cell layer, (2) the inner molecular layer, (3) the outer molecular layer, and (4) diffusely in the molecular layer. In our sample, interneurons with axons arborizing diffusely in the molecular layer were most frequent, and those with axons restricted to the granule cell layer were least frequent. Resting potential, input resistance, time constant, electrotonic length, and spike frequency adaptation (SFA) were not significantly different among the four groups, and the variability in SFA between cells with similar axonal distributions was striking. Clear differences in action potential morphology and afterhyperpolarizations, however, emerged when nonadapting interneurons were compared with those exhibiting SFA. Interneurons exhibiting SFA had characteristically broader spikes, progressive slowing of action potential repolarization during repetitive firing, and slow afterhyperpolarizations that distinguished them from nonadapting interneurons. We propose that the variability in repetitive firing behavior and morphology exhibited by each of these interneurons makes each interneuron unique and may provide a high level of fine tuning of inhibitory control critical to information processing in the dentate.

Synaptic Communication among Hippocampal Interneurons: Properties of Spontaneous IPSCs in Morphologically Identified Cells

“…These results indicate a large heterogeneity of spontaneous GABA A events in a given cell and among interneuron types. Although interneurons are less compact electrotonically than is suggested by their anatomy (Thurbon et al, 1994;Mott et al, 1997), the lower variance of rise times than that of decay time constants in similar amplitude events implies that distinct GABA A receptor kinetics at different synapses may contribute more importantly than electrotonic filtering to determining sIPSC diversity.…”

Distinct Subtypes of Somatostatin-Containing Neocortical Interneurons Revealed in Transgenic Mice

“…Neurochemically, interneurons may express parvalbumin (PV), somatostatin (SOM), cholecystokinin, or calretinin (CR). Unfortunately, classification schemes based on any individual criterion do not correlate with each other in a simple way, and different categories of properties appear at times to vary independently, leading some researchers to conclude that the number of potential GABAergic subtypes is very high (Gupta et al, 2000) or even that each interneuron is unique (Mott et al, 1997;Parra et al, 1998). This lack of consensus on the classification (and the classifiability) of interneurons has greatly hindered progress on deciphering their role in cortical circuitry (Yuste, 2005).…”

Knock-down of synapsin alters cell excitability and action potential waveform by potentiating BK and voltage-gated Ca2+ currents in Helix serotonergic neurons

“…As pointed out before, the increased BK currents and their effect on AHP could be related to the faster spiking rates since deeper AHP facilitates sustained highfrequency firing by limiting the accumulation of Na + and Ca 2+ channel inactivation and by inducing a more rapid channel reactivation following each spike (Mott et al, 1997;Erisir et al, 1999;Faber and Sah, 2003;Fernandez et al, 2005;Shruti et al, 2008;Comunanza et al, 2010;Vandael et al, 2015;Jaffe et al 2011). Paxilline effect on the MFF during the stronger stimulations suggests that the up-regulation of BK channels could in part enable fast spiking by limiting the channel inactivation during repetitive firing.…”