Single neurons are differently involved in stimulus-specific oscillations in cat visual cortex

Abstract

Synchronised oscillatory population events (35–80 Hz; 60–300 ms) can be induced in the visual cortex of cats by specific visual stimulation. The oscillatory events are most prominent in local slow wave field potentials (LFP) and multiple unit spikes (MUA). We investigated how and when single cortical neurons are involved in such oscillatory population events. Simultaneous recordings of single cell spikes, LFP and MUA were made with up to seven microelectrodes. Three states of single cell participation in oscillations were distinguished in spike triggered averages of LFP or MUA from the same electrode: (1) Rhythmic states were characterised by the presence of rhythmicity in single cell spike patterns (35–80 Hz). These rhythms were correlated with LFP and MUA oscillations. (2) Lock-in states lacked rhythmic components in single cell spike patterns, while spikes were phase-coupled with LFP or MUA oscillations. (3) During non-participation states LFP or MUA oscillations were present, but single cell spike trains were neither rhythmic nor phase coupled to these oscillations. Stimulus manipulations (from “optimal” to “suboptimal” for the generation of oscillations) often led to systematic transitions between these states (from rhythmic to lock-in to non-participation). Single cell spike coupling was generally associated with negative peaks in LFP oscillations, irrespective of the cortical separation of single cell and population signals (0–6 mm). Our results suggest that oscillatory cortical population activities are not only supported by local and distant neurons with rhythmic spike patterns, but also by those with irregular patterns in which some spikes occur phase-locked to oscillatory events.