title: 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.
  
  
  CONCLUSIONS
  Sharp-wave ripples (SWRs) are high-frequency oscillations that generate highly synchronized activity in neural populations. Their prevalence in sleep and quiet wakefulness, and the memory deficits that result from their interruption, suggest that SWRs contribute to memory consolidation during rest. Here, we report that SWRs from the monkey hippocampus occur not only during behavioral inactivity but also during successful visual exploration. SWRs were associated with attentive, focal search and appeared to enhance perception of locations viewed around the time of their occurrence. SWRs occurring in rest are noteworthy for their relation to heightened neural population activity, temporally precise and widespread synchronization, and memory consolidation; therefore, the SWRs reported here may have a similar effect on neural populations, even as experiences unfold.
authors.affiliation: Departments of Psychology and.
authors.forename: Timothy K
authors.initials: TK
authors.lastname: Leonard
authors.affiliation: Departments of Psychology and.
authors.forename: Jonathan M
authors.initials: JM
authors.lastname: Mikkila
authors.affiliation: Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114.
authors.forename: Emad N
authors.initials: EN
authors.lastname: Eskandar
authors.affiliation: Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114.
authors.forename: Jason L
authors.identifier: http://orcid.org/0000-0001-6971-1407
authors.initials: JL
authors.lastname: Gerrard
authors.affiliation: Biology, Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada, and.
authors.forename: Daniel
authors.initials: D
authors.lastname: Kaping
authors.affiliation: Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114.
authors.forename: Shaun R
authors.initials: SR
authors.lastname: Patel
authors.affiliation: Biology, Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada, and.
authors.forename: Thilo
authors.identifier: http://orcid.org/0000-0001-6921-4187
authors.initials: T
authors.lastname: Womelsdorf
authors.affiliation: Departments of Psychology and Biology, Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada, and khoffman@yorku.ca.
authors.forename: Kari L
authors.identifier: http://orcid.org/0000-0003-0560-8157
authors.initials: KL
authors.lastname: Hoffman
mesh_terms: D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D058256:Brain Waves / Q000502:physiology*; D005133:Eye Movements / Q000502:physiology*; D005260:Female; D006624:Hippocampus / Q000502:physiology*; D008253:Macaca mulatta; D008297:Male; D010775:Photic Stimulation / Q000379:methods*; D014796:Visual Perception / Q000502:physiology*
keywords: change detection; macaque; natural scenes; search; sleep; theta