Abstract
Somatostatin-expressing-interneurons (SOMIs) in the dentate gyrus (DG) control formation of granule cell (GC) assemblies during memory acquisition. Hilar-perforant-path-associated interneurons (HIPP cells) have been considered to be synonymous for DG-SOMIs. Deviating from this assumption, we show two functionally contrasting DG-SOMI-types. The classical feedback-inhibitory HIPPs distribute axon fibers in the molecular layer. They are engaged by converging GC-inputs and provide dendritic inhibition to the DG circuitry. In contrast, SOMIs with axon in the hilus, termed hilar interneurons (HILs), provide perisomatic inhibition onto GABAergic cells in the DG and project to the medial septum. Repetitive activation of glutamatergic inputs onto HIPP cells induces long-lasting-depression (LTD) of synaptic transmission but long-term-potentiation (LTP) of synaptic signals in HIL cells. Thus, LTD in HIPPs may assist flow of spatial information from the entorhinal cortex to the DG, whereas LTP in HILs may facilitate the temporal coordination of GCs with activity patterns governed by the medial septum.
Highlights
The dentate gyrus (DG) is situated between the entorhinal cortex and the CA3 area of the hippocampus, forming the first stage of the classical trisynaptic circuit (Andersen et al, 1971; Eichenbaum, 1993; Lisman, 1999)
hilar perforant pathassociated interneuron (HIPP) cells have been considered to be synonymous to DG-somatostatin-expressing dendrite-inhibiting cells (SOMIs) (Freund and Buzsaki, 1996; Mott et al, 1997)
We provide first evidence that DG-SOMIs are diverse and divide at least into two functionally contrasting types on the basis of their morphological characteristics, their intrinsic membrane properties, the nature of their excitatory inputs and postsynaptic target specificity. Their functional embedding into the DG circuitry allows both SOMI types to contribute to the processing of spatial information transmitted by the entorhinal cortex in a highly cell-type-specific manner (Figure 7)
Summary
The DG is situated between the entorhinal cortex and the CA3 area of the hippocampus, forming the first stage of the classical trisynaptic circuit (Andersen et al, 1971; Eichenbaum, 1993; Lisman, 1999). It plays an indispensable role in the formation of new memories and memory associations in various species including humans, nonhuman primates and rodents (Burgess et al, 2002; Leutgeb et al, 2005; Buzsaki and Draguhn, 2004; Bakker et al, 2008) It receives a rich multimodal input from the entorhinal cortex via the perforant path which carries information on various modalities of external cues and translates the rich input stream into sparse segregated (‘orthogonalized’) representations, a process called pattern separation (Marr, 1971; Treves and Rolls, 1994; Leutgeb et al, 2007; Kitamura et al, 2015).
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