The neuronal phase code

Recent progress in deciphering the relationship between spiking activity and brain rhythms (including the resonant properties of neurons) has revealed profound modulation of coherence between neurons within local and between distant structures. This modulation of coherence raises the question whether the phase of these oscillations may control spike flow in the brain much faster than slowly adapting synaptic modifications, as earlier thought. For example, the phase of local subthreshold oscillations affects the probability of neurons responding to input from other areas, thus the oscillations are capable of gating the information flow. In turn, the output information flow is then able to pace oscillations in distant targets and synchronize the recipient with the sender area. The other proposed role of oscillations in spike processes is that information can effectively be encoded and transferred in the phase domain, given that ongoing oscillations provide a reliable and accessible reference frame for decoding. The phase of spikes can be decoded by an array of neurons at the receiver side with a repertoire of different oscillation phases. The third role of oscillations is to provide an intrinsic source of temporal segmentation for binding events together that are dispersed in space and time. The fourth role is that the phase relationship between inputs to the neuron is critical to induce synaptic plasticity, such as the case with spike-time dependent plasticity. Switching our mindset from absolute time to phase opens a number of new perspectives for neural coding, some of which nature likely exploited since evolution has been shaping our nervous system.

A number of critical features of an oscillation-based neural coding scheme discovered over the years, including spike phase modulation, the topographic pattern of subthreshold membrane oscillation frequencies, cross-areal field coherence, spike-field coherence, traveling waves, spreading oscillations and spike time dependent plasticity, converge with the discovery of remarkable and robust behavioral regularities, such as firing sequences and phase precession in the hippocampus as well as the profound geometry of grid cell firing in the entorhinal cortex.

While the biological significance of phase coding is arguable, the interpretation of coherence as enabling functional coupling and information transfer between neurons of local or distant areas is undisputed. To facilitate this discussion we welcome studies that shed a light on the intriguing relationship between local field potentials, oscillations, spike-field coherence, spike-phase modulation, the resonant properties of neurons, particularly their behavioral, cognitive and computational aspects.