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. 2003 Feb 4;100(3):1370-4.
doi: 10.1073/pnas.0337529100. Epub 2003 Jan 13.

Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations

Roger D Traub  1 , Isabel Pais, Andrea Bibbig, Fiona E N LeBeau, Eberhard H Buhl, Sheriar G Hormuzdi, Hannah Monyer, Miles A Whittington
Affiliations

Contrasting roles of axonal (pyramidal cell) and dendritic (interneuron) electrical coupling in the generation of neuronal network oscillations

Roger D Traub et al. Proc Natl Acad Sci U S A. .

Abstract

Electrical coupling between pyramidal cell axons, and between interneuron dendrites, have both been described in the hippocampus. What are the functional roles of the two types of coupling? Interneuron gap junctions enhance synchrony of gamma oscillations (25-70 Hz) in isolated interneuron networks and also in networks containing both interneurons and principal cells, as shown in mice with a knockout of the neuronal (primarily interneuronal) connexin36. We have recently shown that pharmacological gap junction blockade abolishes kainate-induced gamma oscillations in connexin36 knockout mice; without such gap junction blockade, gamma oscillations do occur in the knockout mice, albeit at reduced power compared with wild-type mice. As interneuronal dendritic electrical coupling is almost absent in the knockout mice, these pharmacological data indicate a role of axonal electrical coupling in generating the gamma oscillations. We construct a network model of an experimental gamma oscillation, known to be regulated by both types of electrical coupling. In our model, axonal electrical coupling is required for the gamma oscillation to occur at all; interneuron dendritic gap junctions exert a modulatory effect.

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Figures

Figure 1
Figure 1
Network model of kainate oscillations involves gap junctions between the axons of pyramidal cells (excitatory or “e” cells), gap junctions between dendrites of interneurons (0.525 nS in this case), and chemical synapses. In the latter category are AMPA-receptor-mediated excitation of pyramidal cell and interneuron dendrites, as well as GABAA-receptor-mediated inhibition of pyramidal cells (on axon initial segments, somata, and dendrites; GABAA-receptor-mediated inhibition of interneurons was also included but is not shown in the figure). Typical firing patterns are illustrated for a simulation of kainate-induced γ activity. Randomly occurring spikes in excitatory axons pass across gap junctions to other axons; they also occasionally propagate antidromically to produce a spikelet (*); axonal spikes propagate orthodromically to excite pyramidal cells (E Dendrite, Upper Left) and interneurons (Upper Right). In turn, interneurons inhibit each other and the pyramidal cells. Inhibition in pyramidal cells not only hyperpolarizes the latter but also interferes with the ability of axonal spikes to propagate to other axons, thereby phasically diminishing the gain of the system.
Figure 2
Figure 2
Blockade of chemical synapses in the model uncovers a −200 Hz (ultrafast) population oscillation in pyramidal cells, corresponding to experimental ultrafast oscillations in low [Ca2+]o media (9, 11, 24). The only interaction between pyramidal cells under these model conditions is via axonal gap junctions. Other parameters were as in Fig. 1. (A) Average (inverted) somatic potential of 224 nearby pyramidal cells. (B) Simultaneous trace of pyramidal cell soma (hyperpolarized with 1.0-nA current). Note the numerous spikelets and action potentials with notched rising phases (cf. refs. and 11). (C) Autocorrelation of the signal in A. (D) Power spectrum of 768 ms of data from the signal in A. The spectral peak is at 208 Hz.
Figure 3
Figure 3
Blocking axonal electrical coupling between pyramidal cells abolishes γ oscillations in the model. (A) Simulation with axon gap junctions present (and dendritic gap junctions, 1.05 nS). Signals are the average (inverted) somatic potential of 224 nearby pyramidal cells, the average somatic potential of 28 nearby interneurons, and the somatic potential of a single pyramidal cell (hyperpolarized with −1.0 nA current). (B) The simulation of A was repeated, but with axonal gap junctions blocked. (C) Superimposed power spectra (10–100 Hz) of the local average pyramidal signals from A and B. The power spectrum of A (thin line, axon gap junctions present) reveals a clear peak at 44 Hz. The power spectrum of B (thick line, axon gap junctions blocked) plotted on the same scale shows virtually no γ power.
Figure 4
Figure 4
Dendritic gap junctions, between interneurons, enhance the power of γ oscillations in the model (as shown experimentally; ref. 9). (A) Inverted local average pyramidal cell activity (Upper) and power spectrum (5–100 Hz) of 3.1 s of this activity (Lower) from a simulation with interneuron gap junction conductance 1.05 nS. (B) The same signals, from a simulation with interneuron gap junction conductance 0.00 nS. (C) Scatter plot of data from 24 simulations, each with a different value of interneuron gap junction conductance. The ordinate shows integrated power from 30 to 50 Hz (in power spectra of 3.1 s of local average e-cell activity), expressed relative to the 30- to 50-Hz power when interneuron gap junctions are blocked. The linear regression fit has a positive slope (30% increase in power/nS conductance) with P < 0.0001 and R = 0.81. The slope was also positive with P < 0.002, R = 0.61, when we plotted normalized power from 15 to 60 Hz.
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