Theta- and gamma-band oscillatory uncoupling in the macaque hippocampus

ABSTRACT Nested hippocampal oscillations in the rodent give rise to temporal dynamics that may underlie learning, memory, and decision making. Although theta/gamma coupling in rodent CA1 occurs during exploration, in contrast to sharp-wave ripples that emerge in quiescence, it is less clear that these oscillatory regimes extend to primates. We, therefore, sought to identify correspondences in frequency bands, nesting, and behavioral coupling taken from the macaque hippocampus. We found that, in contrast to rodent oscillations, theta and gamma frequency bands in macaque CA1 were segregated by behavioral states. Beta2/gamma (15-70 Hz) had greater power during visual search while the theta band (3-10 Hz; peak ∼8 Hz) dominated during quiescence. Moreover, theta band amplitude was strongest when beta2/slow gamma (20-35 Hz) amplitude was weakest, occurring instead concomitant with higher frequencies (60-150 Hz). Spike-field coherence was most frequently seen in these three bands, (3-10 Hz, 20-35 Hz, and 60-150 Hz); however, the theta-band coherence was largely due to spurious coupling during sharp-wave ripples. Accordingly, no intrinsic theta spiking rhythmicity was apparent. These results support a role for beta2/slow gamma modulation in CA1 during active exploration in the primate that is decoupled from theta oscillations. The apparent difference to the rodent oscillatory canon calls for a shift in focus of frequency when considering the primate hippocampus.