Dendritic plateau potentials can process spike sequences across multiple time-scales

Abstract

The brain constantly processes information encoded in temporal sequences of spiking activity. This sequential activity emerges from sensory inputs as well as from the brain's own recurrent connectivity and spans multiple dynamically changing timescales. Decoding the temporal order of spiking activity across these varying timescales is a critical function of the brain, but we do not yet understand its neural implementation. The problem is, that the passive dynamics of neural membrane potentials occur on a short millisecond timescale, whereas many cognitive tasks require the integration of information across much slower behavioral timescales. However, actively generated dendritic plateau potentials do occur on such longer timescales, and their essential role for many aspects of cognition has been firmly established by recent experiments. Here, we build on these discoveries and propose a new model of neural computation that emerges from the interaction of localized plateau potentials across a functionally compartmentalized dendritic tree. We show how this interaction offers a robust solution to the timing invariant detection and processing of sequential spike patterns in single neurons. Stochastic synaptic transmission complements the deterministic all-or-none plateau process and improves information transmission by allowing ensembles of neurons to produce graded responses to continuous combinations of features. We found that networks of such neurons can solve highly complex sequence detection tasks by breaking down long inputs into sequences of shorter, random features that can be classified reliably. These results suggest that active dendritic processes are fundamental to neural computation.