Neuronal response impedance mechanism implementing cooperative networks with low firing rates and µs precision.

Realizations of low firing rates in neural networks usually require globally balanced distributions among excitatory and inhibitory links, while feasibility of temporal coding is limited by neuronal millisecond precision. We show that cooperation, governing global network features, emerges through nodal properties, as opposed to link distributions. Using in vitro and in vivo experiments we demonstrate microsecond precision of neuronal response timings under low stimulation frequencies, whereas moderate frequencies result in a chaotic neuronal phase characterized by degraded precision. Above a critical stimulation frequency, which varies among neurons, response failures were found to emerge stochastically such that the neuron functions as a low pass filter, saturating the average inter-spike-interval. This intrinsic neuronal response impedance mechanism leads to cooperation on a network level, such that firing rates are suppressed toward the lowest neuronal critical frequency simultaneously with neuronal microsecond precision. Our findings open up opportunities of controlling global features of network dynamics through few nodes with extreme properties.

Error correction and fast detectors implemented by ultrafast neuronal plasticity.

We experimentally show that the neuron functions as a precise time integrator, where the accumulated changes in neuronal response latencies, under complex and random stimulation patterns, are solely a function of a global quantity, the average time lag between stimulations. In contrast, momentary leaps in the neuronal response latency follow trends of consecutive stimulations, indicating ultrafast neuronal plasticity. On a circuit level, this ultrafast neuronal plasticity phenomenon implements error-correction mechanisms and fast detectors for misplaced stimulations. Additionally, at moderate (high) stimulation rates this phenomenon destabilizes (stabilizes) a periodic neuronal activity disrupted by misplaced stimulations.

Sudden synchrony leaps accompanied by frequency multiplications in neuronal activity.

A classical view of neural coding relies on temporal firing synchrony among functional groups of neurons, however, the underlying mechanism remains an enigma. Here we experimentally demonstrate a mechanism where time-lags among neuronal spiking leap from several tens of milliseconds to nearly zero-lag synchrony. It also allows sudden leaps out of synchrony, hence forming short epochs of synchrony. Our results are based on an experimental procedure where conditioned stimulations were enforced on circuits of neurons embedded within a large-scale network of cortical cells in vitro and are corroborated by simulations of neuronal populations. The underlying biological mechanisms are the unavoidable increase of the neuronal response latency to ongoing stimulations and temporal or spatial summation required to generate evoked spikes. These sudden leaps in and out of synchrony may be accompanied by multiplications of the neuronal firing frequency, hence offering reliable information-bearing indicators which may bridge between the two principal neuronal coding paradigms.