Recent advances in engineering and signal processing have renewed the interest in invasive and surface brain recordings, yet many features of cortical field potentials remain incompletely understood. In the computational study that follows, we show that a model circuit of interneurons, coupled via both GABA A receptor synapses and electrical synapses, reproduces many essential features of the power spectrum of local field potential (LFP) recordings, such as 1/ f power scaling at low frequency (below 10 Hz), power accumulation in the γ-frequency band (30–100 Hz), and a robust α rhythm in the absence of stimulation. The low-frequency 1/ f power scaling depends on strong reciprocal inhibition, whereas the α rhythm is generated by electrical coupling of intrinsically active neurons. As in previous studies, the γ power arises through the amplification of single-neuron spectral properties, owing to the refractory period, by parameters that favor neuronal synchrony, such as delayed inhibition. This study also confirms that both synaptic and voltage-gated membrane currents contribute substantially to the LFP and that high-frequency signals such as action potentials quickly taper off with distance. Given the ubiquity of electrically coupled interneuron circuits in the mammalian brain, they may be major determinants of the recorded potentials.

The ability of individual neurons to modulate the gain of their input-output function is important for information processing in the brain. In a recent study (Mitchell & Silver, 2003), shunting inhibition was found to modulate the gain of cerebellar granule cells subjected to simulated currents through AMPA receptor synapses. Here we investigate the effect on gain modulation resulting from adding the currents mediated by NMDA receptors to a compartmental model of the granule cell. With only AMPA receptors, the changes in gain induced by shunting inhibition decreased gradually with the average firing rate of the afferent mossy fibers. With NMDA receptors present, this decrease was more rapid, therefore narrowing the bandwidth of mossy fiber firing rates available for gain modulation. The deterioration of gain modulation was accompanied by a reduced variability of the input current and saturation of NMDA receptors. However, when the output of the granule cell was plotted as a function of the average input current instead of the input firing frequency, both models showed very similar response curves and comparable gain modulation. We conclude that NMDA receptors do not directly impair gain control by shunting inhibition, but the effective bandwidth decreases as a consequence of the increased total charge transfer.