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Gap junction networks can generate both ripple‐like and fast ripple‐like oscillations
Author(s) -
Simon Anna,
Traub Roger D.,
Vladimirov Nikita,
Jenkins Alistair,
Nicholson Claire,
Whittaker Roger G.,
Schofield Ian,
Clowry Gavin J.,
Cunningham Mark O.,
Whittington Miles A.
Publication year - 2014
Publication title -
european journal of neuroscience
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.346
H-Index - 206
eISSN - 1460-9568
pISSN - 0953-816X
DOI - 10.1111/ejn.12386
Subject(s) - gap junction , axon , neuroscience , ripple , pyramidal cell , coupling (piping) , antidromic , physics , connexin , population , biophysics , electrophysiology , chemistry , biology , materials science , intracellular , microbiology and biotechnology , hippocampus , demography , quantum mechanics , voltage , sociology , metallurgy
Fast ripples ( FR s) are network oscillations, defined variously as having frequencies of > 150 to > 250 Hz, with a controversial mechanism. FR s appear to indicate a propensity of cortical tissue to originate seizures. Here, we demonstrate field oscillations, at up to 400 Hz, in spontaneously epileptic human cortical tissue in vitro , and present a network model that could explain FR s themselves, and their relation to ‘ordinary’ (slower) ripples. We performed network simulations with model pyramidal neurons, having axons electrically coupled. Ripples (< 250 Hz) were favored when conduction of action potentials, axon to axon, was reliable. Whereas ripple population activity was periodic, firing of individual axons varied in relative phase. A switch from ripples to FR s took place when an ectopic spike occurred in a cell coupled to another cell, itself multiply coupled to others. Propagation could then start in one direction only, a condition suitable for re‐entry. The resulting oscillations were > 250 Hz, were sustained or interrupted, and had little jitter in the firing of individual axons. The form of model FR was similar to spontaneously occurring FR s in excised human epileptic tissue. In vitro , FR s were suppressed by a gap junction blocker. Our data suggest that a given network can produce ripples, FR s, or both, via gap junctions, and that FR s are favored by clusters of axonal gap junctions. If axonal gap junctions indeed occur in epileptic tissue, and are mediated by connexin 26 (recently shown to mediate coupling between immature neocortical pyramidal cells), then this prediction is testable.