Slow and Fast Inhibition and an H-Current Interact to Create a Theta Rhythm in a Model of CA1 Interneuron Network

• Published in: Journal of neurophysiology 2005-08, Vol.94 (2), p.1509-1518
• Main Authors: Rotstein, Horacio G, Pervouchine, Dmitri D, Acker, Corey D, Gillies, Martin J, White, John A, Buhl, Eberhardt H, Whittington, Miles A, Kopell, Nancy
• Format: Article
• Language: English
• Subjects: Animals; Computer Simulation; Excitatory Amino Acid Antagonists - pharmacology; Hippocampus - cytology; In Vitro Techniques; Interneurons - classification; Interneurons - physiology; Interneurons - radiation effects; Ion Channels - physiology; Membrane Potentials - physiology; Membrane Potentials - radiation effects; Methoxyhydroxyphenylglycol - analogs & derivatives; Methoxyhydroxyphenylglycol - pharmacology; Neural Inhibition - physiology; Neural Inhibition - radiation effects; Neural Networks (Computer); Patch-Clamp Techniques - methods; Periodicity; Quinoxalines - pharmacology; Rats; Rats, Wistar; Synaptic Transmission - physiology; Synaptic Transmission - radiation effects; Theta Rhythm
• ISSN: 0022-3077; 1522-1598
• DOI: 10.1152/jn.00957.2004

1 Department of Mathematics and Statistics and 2 Department of Biomedical Engineering and Center for Biodynamics, Boston University, Boston, Massachusetts; and 3 School of Biomedical Sciences, University of Leeds, Leeds, United Kingdom Submitted 14 September 2004; accepted in final form 27 March 2005 The oriens-lacunosum moleculare (O-LM) subtype of interneuron is a key component in the formation of the theta rhythm (8–12 Hz) in the hippocampus. It is known that the CA1 region of the hippocampus can produce theta rhythms in vitro with all ionotropic excitation blocked, but the mechanisms by which this rhythmicity happens were previously unknown. Here we present a model suggesting that individual O-LM cells, by themselves, are capable of producing a single-cell theta-frequency firing, but coupled O-LM cells are not capable of producing a coherent population theta. By including in the model fast-spiking (FS) interneurons, which give rise to IPSPs that decay faster than those of the O-LM cells, coherent theta rhythms are produced. The inhibition to O-LM cells from the FS cells synchronizes the O-LM cells, but only when the FS cells themselves fire at a theta frequency. Reciprocal connections from the O-LM cells to the FS cells serve to parse the FS cell firing into theta bursts, which can then synchronize the O-LM cells. A component of the model O-LM cell critical to the synchronization mechanism is the hyperpolarization-activated h-current. The model can robustly reproduce relative phases of theta frequency activity in O-LM and FS cells. Address for reprint requests and other correspondence: H. G. Rotstein, Department of Mathematics and Statistics and Center for Biodynamics, Boston University, Boston, MA 02215 (E-mail: horacio{at}math.bu.edu )