Contribution of spike timing to the neural code: from fast to slow timescales

The publication of Mainen and Sejnowski's 1995 seminal paper strongly renewed interest in how spike timing contributes to the neural code. In the 3 decades since then, considerable experimental and theoretical research has investigated the timescales at which spike timing contributes to the neural code. Here we review theoretical and experimental research of the last 30 years aimed at defining conceptually and measuring operationally these timescales. By a critical review of the literature, we individuate six broad classes of timescales that have been conceptualized and operationalized: the maximal temporal precision of spiking that a neuron can achieve, the encoding time window (the time window containing the information-bearing spike times), the encoding timescale (the coarsest time resolution for measuring spikes without losing information), the maximal discrimination precision timescale (the smallest spike time difference that can be discriminated behaviorally), the encoding-readout intersection timescale (the maximal timing precision at which stimulus information encoded in neural activity is also actually read out to inform behavior), and the information consistency timescale (measuring the stability of information encoding over time). Together, this work has revealed short and long timescales that influence information coding and affect behavior. Short encoding timescales, from milliseconds to tens of milliseconds, are useful for sensory information encoding and perception. Long consistency timescales, ranging from hundreds of milliseconds to seconds, are useful for accumulating evidence and stabilizing decisions.