Abstract
The local field potential (LFP) is thought to reflect a temporal reference for neuronal spiking, which may facilitate information coding and orchestrate the communication between neural populations. To explore this proposed role, we recorded the LFP and simultaneously the spike activity of one to three nearby neurons in V1 of anesthetized cats during the presentation of drifting sinusoidal gratings, binary dense noise stimuli, and natural movies. In all stimulus conditions and during spontaneous activity, the average LFP power at frequencies >20 Hz was higher when neurons were spiking versus not spiking. The spikes were weakly but significantly phase locked to all frequencies of the LFP. The average spike phase of the LFP was stable across high and low levels of LFP power, but the strength of phase locking at low frequencies (≤10 Hz) increased with increasing LFP power. In a next step, we studied how strong stimulus responses of single neurons are reflected in the LFP and the LFP–spike relationship. We found that LFP power was slightly increased and phase locking was slightly stronger during strong compared with weak stimulus-locked responses. In summary, the coupling strength between high frequencies of the LFP and spikes was not strongly modulated by LFP power, which is thought to reflect spiking synchrony, nor was it strongly influenced by how strongly the neuron was driven by the stimulus. Furthermore, a comparison between neighboring neurons showed no clustering of preferred LFP phase. We argue that hypotheses on the relevance of phase locking in their current form are inconsistent with our findings.
SIGNIFICANCE STATEMENT The local field potential (LFP) is hypothesized to play a vital role in the efficient communication between neuronal populations, as well as in the efficient coding of information. Underlying these roles is the assumption that spikes can be strongly and reliably locked to certain phases of oscillations in the LFP. Gamma oscillations are thought to be the best candidate mechanism exerting the hypothesized roles of the LFP. They occur most reliably in response to specific artificial stimuli, but are usually very weak in response to natural movies or images. The current study finds that spikes exhibited weak phase locking when the power of gamma oscillations is weak and thus casts doubt on a general relevance of phase locking for neural communication and coding.
