Synchronization of neurons during local field potential oscillations in sensorimotor cortex of awake monkeys.

1. The neural activity associated with 20- to 40-Hz oscillations in sensorimotor cortex of awake monkeys was investigated by recording action potentials of single and multiple units. At a given site, activity of many units became synchronized with local field potential (LFP) oscillations. Cycle-triggered histograms (CTHs) of unit spikes aligned on cycles of LFP oscillations indicated that about two thirds of the recorded units (n = 268) were entrained with LFP oscillations. On average, units had the highest probability of spiking 2.7 ms before peak LFP negativity, corresponding to a -27.6 degrees phase shift relative to the negative peak of the LFP. 2. The average relative modulation amplitude (RMA), defined as the ratio of amplitude of oscillatory component of CTH and the baseline multiplied by 100, was 45 +/- 27% (mean +/- SD). The RMAs of single units did not differ significantly from those of multiple units. 3. Phase shifts and RMAs did not vary systematically with the cortical depth of recorded units. 4. Autocorrelation histograms (ACHs) of entrained units exhibited clear 20- to 40-Hz periodicity if they were compiled with spikes that occurred during oscillatory episodes in LFPs. ACHs of spikes outside oscillatory episodes usually did not show periodicity. Global ACHs of all spikes typically showed weak or no evidence of periodic activity. 5. Cross-correlation histograms (CCHs) between pairs of units complied with all spikes, whether they occurred during or outside LFP oscillations, seldom revealed significant features (19 of 134 pairs or 14%). However, CCHs compiled with spikes that occurred during oscillatory episodes (OS-CCHs) had significant features in 67 of 134 pairs recorded ipsilaterally; in these 67 cases, units at both sites showed modulation in CTHs. 6. The latencies of the OS-CCH peaks (taking the medial unit as reference) were normally distributed about a mean of -0.5 +/- 13 ms. Normalized peak height of CCHs (peak/baseline x 100) was, on average, 14.3 +/- 11.2%. Peak latency and normalized peak amplitude did not change significantly with horizontal separation of recorded precentral pairs up to 14 mm. 7. Units in the left and right hemispheres could become synchronized during oscillations. Significant features in OS-CCH were detected in 22 of 42 pairs of units recorded bilaterally. The average peak latency was 0.2 +/- 8.0 ms and the average normalized peak amplitude was 10 +/- 8%. These parameters did not differ significantly from those for ipsilateral OS-CCHs. 8. Oscillations tended to affect both the temporal structure and net rate of unit firing. For each unit, the firing rate was clamped to a narrow range of frequencies during oscillatory episodes. The coefficient of variation (SD/mean) of firing rates was significantly reduced during oscillatory episodes compared with prior rates (P < 0.001, paired t-test). However, the overall mean firing rate of each unit during all oscillatory episodes did not differ from its average rate immediately before the episodes. Thus oscillatory episodes tended to clamp mean firing rates to the cells' average rates outside episodes. 9. The strength of synchronization between units during oscillatory episodes was unrelated to their involvement in the task. For pairs of precentral units recorded ipsilaterally, the probability of occurrence of significant features in the OS-CCH was slightly larger when both units of the pair were task related (33 of 56 pairs or 59%) than when only one unit was task related (20 of 39 pairs or 51%) or neither unit was task related (7 of 16 or 44%). However, these differences were not statistically significant. The magnitude of the correlation peak and the latency to peak were also not significantly different for the three cases. 10. These results suggest that units across wide regions can become transiently synchronized specifically during LFP oscillations, even if their spikes are uncorrelated during nonoscillatory periods.