Sleep and Movement Differentiates Actions of Two Types of Somatostatin-Expressing GABAergic Interneuron in Rat Hippocampus

Abstract

SummaryNeuropeptides acting on pre- and postsynaptic receptors are coreleased with GABA by interneurons including bistratified and O-LM cells, both expressing somatostatin but innervating segregated dendritic domains of pyramidal cells. Neuropeptide release requires high-frequency action potentials, but the firing patterns of most peptide/GABA-releasing interneurons during behavior are unknown. We show that behavioral and network states differentiate the activities of bistratified and O-LM cells in freely moving rats. Bistratified cells fire at higher rates during sleep than O-LM cells and, unlike O-LM cells, strongly increase spiking during sharp wave-associated ripples (SWRs). In contrast, O-LM interneurons decrease firing during sleep relative to awake states and are mostly inhibited during SWRs. During movement, both cell types fire cooperatively at the troughs of theta oscillations but with different frequencies. Somatostatin and GABA are differentially released to distinct dendritic zones of CA1 pyramidal cells during sleep and wakefulness to coordinate segregated glutamatergic inputs from entorhinal cortex and CA3.

Dendritic inhibition mediated by O-LM and bistratified interneurons in the hippocampus

“…This phase relationship has also been observed in awake rodents (Varga et al, 2012; Katona et al, 2014). How could a similar phase coupling of O-LM and bistratified cells during theta oscillations influence signal integration on CA1 pyramidal neuron dendrites?…”

Tasks for inhibitory interneurons in intact brain circuits

“…These studies provided information about the spiking relationship of PV+ and SOM+ cells in relation to theta and ripple oscillations (Royer et al , 2012; Stark et al , 2013; Stark et al , 2014), complementing previous juxtacellular studies, mostly performed under anesthesia (reviewed in Klausberger & Somogyi, 2008; but see Varga et al , 2010; Lapray et al , 2012; Viney et al , 2013; Katona et al , 2014 for waking data). Recent data collected in the medial entorhinal cortex indicated that PV+ cells in this region share many properties with PV+ cells identified in the hippocampus (Royer et al , 2012), such as the shape of their spike waveforms, their high firing rate and the low spatial selectivity of their firing fields (Buetfering et al , 2014).…”

“…Studies using single-cell recordings and labeling in freely behaving animals represent complementary approaches towards an exhaustive knowledge of interneuron physiology in the freely behaving animal because they can provide information about the morphology, expression of multiple markers as well as intracellular properties (Isomura et al , 2009; Lapray et al , 2012; Varga et al , 2012; Viney et al , 2013; Katona et al , 2014). Alternatively, refinement of genetic approaches employed to target distinct functional sub-populations of interneurons (Fenno et al , 2014) will allow a more detailed dissection of the circuit elements involved in specific behaviors.…”

CA1 pyramidal cell diversity enabling parallel information processing in the hippocampus

“…Therefore, it will be important determine whether other inhibitory cell types 58–61 are also differentially interconnected with distinct CA1PC subpopulations. For instance, interneurons that innervate dendrites 62–65 or axon initial segments 66–69 may also show preference for CA1PC subgroups to exert subcircuit-selective regulation of input integration and spiking output generation, respectively 66–70 .…”