Sharp Wave Ripples during Visual Exploration in the Primate Hippocampus

Abstract

Hippocampal sharp-wave ripples (SWRs) are highly synchronous oscillatory field potentials that are thought to facilitate memory consolidation. SWRs typically occur during quiescent states, when neural activity reflecting recent experience is replayed. In rodents, SWRs also occur during brief locomotor pauses in maze exploration, where they appear to support learning during experience. In this study, we detected SWRs that occurred during quiescent states, but also during goal-directed visual exploration in nonhuman primates (Macaca mulatta). The exploratory SWRs showed peak frequency bands similar to those of quiescent SWRs, and both types were inhibited at the onset of their respective behavioral epochs. In apparent contrast to rodent SWRs, these exploratory SWRs occurred during active periods of exploration, e.g., while animals searched for a target object in a scene. SWRs were associated with smaller saccades and longer fixations. Also, when they coincided with target-object fixations during search, detection was more likely than when these events were decoupled. Although we observed high gamma-band field potentials of similar frequency to SWRs, only the SWRs accompanied greater spiking synchrony in neural populations. These results reveal that SWRs are not limited to off-line states as conventionally defined; rather, they occur during active and informative performance windows. The exploratory SWR in primates is an infrequent occurrence associated with active, attentive performance, which may indicate a new, extended role of SWRs during exploration in primates.

Rhythms of the hippocampal network

“…Moreover, hippocampal ripples are coupled with neocortical spindles in human epilepsy patients 103,173 , as they are in rats 102,108 . In monkey hippocampus, sharp wave-ripples that appear very similar to their counterparts in rodents also occur during inactive and active states 174,175 . Finally, separate slow and fast gamma rhythms may occur in primates, as in rodents.…”

Modulation of local field potentials and neuronal activity in primate hippocampus during saccades

“…Secondly, the magnitude of myogenic artifacts is modulated across ipsiversive and contraversive saccades, whereas our data do not show a correlation between LFP magnitude and saccade direction. Thirdly, in primates hippocampal LFP polarity reverses along the mediolateral axis (Hoffman et al, ), and possibly not across cellular laminae (Leonard et al, ) as is the case in rodents, a trend found across simultaneously recorded electrode pairs spanning the mediolateral axis (Figure S4). Lastly, regarding possible thalamic contamination, where neurons encode efference copy signals for saccades (Sommer & Wurtz, ), as far as we know these cells do not encode saccade amplitudes in their firing rate.…”

Hippocampal gamma‐slow oscillation coupling in macaques during sedation and sleep

“…SWRs are biased to occur during neocortical UP states (Battaglia et al, ; Molle et al, ), which may facilitate both remote replay of HIPP spiking sequences in the neocortex and, ultimately, memory consolidation (Ji and Wilson, ). In primates and humans, the ripple oscillation has a lower frequency range (∼80–130 Hz) than in rodents (Bragin, Engel, Wilson, Fried., & Buzsaki, ; Clemens et al, ; Leonard et al, ; Ramirez‐Villegas, Logothetis, & Besserve, ; Skaggs et al, ). This mechanism could, therefore, explain the fast gamma‐SO coupling we observed in SWS.…”