title: Dendritic inhibition provided by interneuron-specific cells controls the firing rate and timing of the hippocampal feedback inhibitory circuitry.
abstract: In cortical networks, different types of inhibitory interneurons control the activity of glutamatergic principal cells and GABAergic interneurons. Principal neurons represent the major postsynaptic target of most interneurons; however, a population of interneurons that is dedicated to the selective innervation of GABAergic cells exists in the CA1 area of the hippocampus. The physiological properties of these cells and their functional relevance for network computations remain unknown. Here, we used a combination of dual simultaneous patch-clamp recordings and targeted optogenetic stimulation in acute mouse hippocampal slices to examine how one class of interneuron-specific (IS) cells controls the activity of its GABAergic targets. We found that type 3 IS (IS3) cells that coexpress the vasoactive intestinal polypeptide (VIP) and calretinin contact several distinct types of interneurons within the hippocampal CA1 stratum oriens/alveus (O/A), with preferential innervation of oriens-lacunosum moleculare cells (OLMs) through dendritic synapses. In contrast, VIP-positive basket cells provided perisomatic inhibition to CA1 pyramidal neurons with the asynchronous GABA release and were not connected with O/A interneurons. Furthermore, unitary IPSCs recorded at IS3-OLM synapses had a small amplitude and low release probability but summated efficiently during high-frequency firing of IS3 interneurons. Moreover, the synchronous generation of a single spike in several IS cells that converged onto a single OLM controlled the firing rate and timing of OLM interneurons. Therefore, dendritic inhibition originating from IS cells is needed for the flexible activity-dependent recruitment of OLM interneurons for feedback inhibition.
authors.affiliation: Axis of Cellular and Molecular Neuroscience, Institut Universitaire en Santé Mentale de Québec, Department of Biochemistry, Microbiology and Bio-informatics, Université Laval, Québec G1J 2G3, Canada, and Department of Bioengineering, Stanford University, Stanford, California 94305-5444.
authors.forename: Leonid
authors.initials: L
authors.lastname: Tyan
authors.forename: Simon
authors.initials: S
authors.lastname: Chamberland
authors.forename: Elise
authors.initials: E
authors.lastname: Magnin
authors.forename: Olivier
authors.initials: O
authors.lastname: Camiré
authors.forename: Ruggiero
authors.initials: R
authors.lastname: Francavilla
authors.forename: Linda Suzanne
authors.initials: LS
authors.lastname: David
authors.forename: Karl
authors.initials: K
authors.lastname: Deisseroth
authors.forename: Lisa
authors.initials: L
authors.lastname: Topolnik
mesh_terms: D000200:Action Potentials / Q000235:genetics / Q000502:physiology*; D000818:Animals; D000831:Animals, Newborn; D003712:Dendrites / Q000187:drug effects / Q000502:physiology*; D005260:Female; D018756:GABA Antagonists / Q000494:pharmacology; D049452:Green Fluorescent Proteins / Q000235:genetics; D006624:Hippocampus / Q000166:cytology*; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials / Q000187:drug effects / Q000235:genetics; D007395:Interneurons / Q000502:physiology*; D008297:Male; D051379:Mice; D008810:Mice, Inbred C57BL; D008822:Mice, Transgenic; D009415:Nerve Net / Q000187:drug effects / Q000502:physiology*; D009433:Neural Inhibition / Q000187:drug effects / Q000235:genetics / Q000502:physiology*; D011724:Pyridazines / Q000494:pharmacology; D013997:Time Factors; D014660:Vasoactive Intestinal Peptide / Q000235:genetics
chemical_list: D018756:GABA Antagonists; D011724:Pyridazines; C485184:enhanced green fluorescent protein; D049452:Green Fluorescent Proteins; D014660:Vasoactive Intestinal Peptide; C049853:gabazine
keywords: dendrite; hippocampus; inhibition; interneuron; optogenetics; paired recording