Subthreshold Asynchronous States and Computations in Biophysically Detailed Populations of Neurons

Spikes are metabolically costly to generate and transmit, and spiking rates should be kept to a minimum for efficient coding. How low can the spike rate go? We show that computations and asynchronous states based on excitatory/inhibitory balance can exist without firing any spikes through self-sustaining subthreshold voltage fluctuations in networks of biophysically detailed Hodgkin-Huxley neurons. This novel subthreshold asynchronous state, which we call subthreshold voltage chaos, can be controlled for useful computation and pattern generation, also without firing spikes. Further, we identify candidate ion channels, low-voltage-activated T-Type calcium channels that provide a biophysical mechanism for this type of subthreshold computation. Our work here provides computational evidence for the existence of efficient neural circuits that can compute exclusively with subthreshold voltage dynamics.