Noisy Juxtacellular Stimulation In Vivo Leads to Reliable Spiking and Reveals High-Frequency Coding in Single Neurons.

Single cells in the motor and somatosensory cortex of rats were stimulated in vivo with broadband fluctuating currents applied juxtacellularly. Unlike the DC current steps used previously, fluctuating stimulation currents reliably evoked spike trains with precise timing of individual spikes. Fluctuating currents resulted in strong cellular responses at stimulation frequencies beyond the inverse membrane time constant and the mean firing rate of the neuron. Neuronal firing was associated with high rates of information transmission, even for the high-frequency components of the stimulus. Such response characteristics were also revealed in additional experiments with sinusoidal juxtacellular stimulation. For selected cells, we could reproduce these statistics with compartmental models of varying complexity. We also developed a method to generate Gaussian stimuli that evoke spike trains with prescribed spike times (under the constraint of a certain rate and coefficient of variation) and exemplify its ability to achieve precise and reliable spiking in cortical neurons in vivo. Our results demonstrate a novel method for precise control of spike timing by juxtacellular stimulation, confirm and extend earlier conclusions from ex vivo work about the capacity of cortical neurons to generate precise discharges, and contribute to the understanding of the biophysics of information transfer of single neurons in vivo at high frequencies.