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Subthreshold resonance in central neurons Hutcheon, Bruce McCullagh


Electrical signals from the mammalian brain often contain large-amplitude components at characteristic frequencies. What properties of central neuronal networks determine these frequencies? One possibility is that individual neurons are electrically tuned to respond better at some frequencies than others. Such tuning has been called electrical membrane resonance and arises from the interaction of the passive properties of the membrane with time- and voltagedependent membrane currents. In the present work, frequency-domain analyses of neocortical and thalamic neurons were performed to detect resonances at subthreshold potentials. The ionic mechanisms of these resonances and their effect on firing patterns were then examined using a combination of mathematical modeling and experiment. In addition, a novel technique, the reactive current clamp (RCC), was developed for coupling mathematical models of ionic currents to living cells. In approximately 2/3 of neocortical neurons, the hyperpolarization-activated cation current (I[sub]H) caused a 1 to 2 Hertz resonance near the resting potential. Other currents in these neurons attenuated or amplified the resonance in a voltage-dependent manner. Putative inhibitory neurons of the neocortex did not have an In-resonance. The resonance affected neuronal firing patterns. When resonant neocortical neurons were injected with swept-frequency sinusoidal currents, they were most likely to fire action potentials as the input swept through the resonant band; a phenomenon called "frequency-selective firing". In nonresonant neurons, resonance and frequency-selective firing were generated when a model of IH was coupled to the neuron using the RCC. A theoretical analysis based on previously published data showed that a different voltagedependent current, the low-threshold calcium current (I[sub]T), accounts for the 2 to 4 Hz resonance observed in thalamic neurons. In these neurons, spontaneous oscillations of the membrane potential have been observed near the same frequency. It is suggested that spontaneous oscillations arise from resonant mechanisms that are amplified by voltage-dependent currents. In conclusion, subthreshold resonance is an intrinsic property of neurons that may control the frequencies of coordinated activities in neuronal networks. The resonances described here have frequency ranges that are suitable for stabilizing the spindle and delta brain rhythms that arise during sleep in mammals. In the neocortex, this mechanism seems to be limited to excitatory neurons.

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