Phase of Firing as a Local Window for Efficient Neuronal Computation: Tonic and Phasic Mechanisms in the Control of Theta Spike Phase

The nature of the neural code remains a central issue of contention in neuroscience. Firing rate based schemes have dominated thinking for most of the past century, but there is a growing acceptance that temporal patterns of neuronal activity have an important role to play, at least in some systems and circumstances. Neuronal oscillations provide a central pillar in the evidence supporting temporal coding, perhaps because temporal codes can ultimately be understood only in the context of population activity and oscillations are at once experimentally accessible and analytically tractable. In the many roles proposed for oscillatory activity, a uniting theme is the control of spike timing, which can broadly be considered on two timescales. On the one hand, fast oscillations may be important in promoting precise synchronization of activity across cells, by providing millisecond windows of enhanced spike probability. Slow oscillations, on the other hand, can provide a broader temporal scaffold, against which other inputs, both tonic and phasic, can determine spike timing on the order of milliseconds to tens of milliseconds. Again, this could be important for synchronization of activity, but equally, could be used to control spike order, for coding, or plasticity purposes, or could be used to desynchronize discrete assemblies, enabling parallel processing. Here, we describe the cellular mechanisms underlying this broader timescale process in the hippocampus, specifically focusing on the effect of tonic and phasic inputs on the control of spike timing in single hippocampal neurons during theta oscillations and the implications for information coding and storage.