title: Properties and dynamics of inhibitory synaptic communication within the CA3 microcircuits of pyramidal cells and interneurons expressing parvalbumin or cholecystokinin.
abstract: To understand how a network operates, its elements must be identified and characterized, and the interactions of the elements need to be studied in detail. In the present study, we describe quantitatively the connectivity of two classes of inhibitory neurons in the hippocampal CA3 area (parvalbumin-positive and cholecystokinin-positive interneurons), a key region for the generation of behaviourally relevant synchronous activity patterns. We describe how interactions among these inhibitory cells and their local excitatory target neurons evolve over the course of physiological and pathological activity patterns. The results of the present study enable the construction of precise neuronal network models that may help us understand how network dynamics is generated and how it can underlie information processing and pathological conditions in the brain. We show how inhibitory dynamics between parvalbumin-positive basket cells and pyramidal cells could contribute to sharp wave-ripple generation.
  
  
  
  Different hippocampal activity patterns are determined primarily by the interaction of excitatory cells and different types of interneurons. To understand the mechanisms underlying the generation of different network dynamics, the properties of synaptic transmission need to be uncovered. Perisomatic inhibition is critical for the generation of sharp wave-ripples, gamma oscillations and pathological epileptic activities. Therefore, we aimed to quantitatively and systematically characterize the temporal properties of the synaptic transmission between perisomatic inhibitory neurons and pyramidal cells in the CA3 area of mouse hippocampal slices, using action potential patterns recorded during physiological and pathological network states. Parvalbumin-positive (PV+) and cholecystokinin-positive (CCK+) interneurons showed distinct intrinsic physiological features. Interneurons of the same type formed reciprocally connected subnetworks, whereas the connectivity between interneuron classes was sparse. The characteristics of unitary interactions depended on the identity of both synaptic partners, whereas the short-term plasticity of synaptic transmission depended mainly on the presynaptic cell type. PV+ interneurons showed frequency-dependent depression, whereas more complex dynamics characterized the output of CCK+ interneurons. We quantitatively captured the dynamics of transmission at these different types of connection with simple mathematical models, and describe in detail the response to physiological and pathological discharge patterns. Our data suggest that the temporal propeties of PV+ interneuron transmission may contribute to sharp wave-ripple generation. These findings support the view that intrinsic and synaptic features of PV+ cells make them ideally suited for the generation of physiological network oscillations, whereas CCK+ cells implement a more subtle, graded control in the hippocampus.
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.|János Szentágothai, PhD Program of Semmelweis University, Budapest, Hungary.
authors.forename: Z
authors.initials: Z
authors.lastname: Kohus
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.|Péter Pázmány Catholic University, Faculty of Information Technology, Budapest, Hungary.
authors.forename: S
authors.initials: S
authors.lastname: Káli
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.
authors.forename: L
authors.initials: L
authors.lastname: Rovira-Esteban
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.|János Szentágothai, PhD Program of Semmelweis University, Budapest, Hungary.
authors.forename: D
authors.initials: D
authors.lastname: Schlingloff
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.
authors.forename: O
authors.initials: O
authors.lastname: Papp
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.|Péter Pázmány Catholic University, Faculty of Information Technology, Budapest, Hungary.
authors.forename: T F
authors.initials: TF
authors.lastname: Freund
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.
authors.forename: N
authors.initials: N
authors.lastname: Hájos
authors.affiliation: Institute of Experimental Medicine, Hungarian Academy of Sciences, Budapest, Hungary.
authors.forename: A I
authors.initials: AI
authors.lastname: Gulyás
mesh_terms: D000200:Action Potentials / Q000502:physiology; D000818:Animals; D056654:CA3 Region, Hippocampal / Q000502:physiology*; D002766:Cholecystokinin / Q000235:genetics / Q000502:physiology*; D005260:Female; D049452:Green Fluorescent Proteins / Q000235:genetics; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials / Q000502:physiology; D007395:Interneurons / Q000502:physiology*; D008164:Luminescent Proteins / Q000235:genetics; D008297:Male; D008822:Mice, Transgenic; D008959:Models, Neurological; D010320:Parvalbumins / Q000235:genetics / Q000502:physiology*; D011401:Promoter Regions, Genetic; D017966:Pyramidal Cells / Q000166:cytology* / Q000502:physiology*; D009435:Synaptic Transmission / Q000502:physiology*; D000097573:Red Fluorescent Protein
chemical_list: D002766:Cholecystokinin; D049452:Green Fluorescent Proteins; D008164:Luminescent Proteins; D010320:Parvalbumins; D000097573:Red Fluorescent Protein; C485184:enhanced green fluorescent protein