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Articles, Systems/Circuits

Sharp Wave Ripples during Visual Exploration in the Primate Hippocampus

Timothy K. Leonard, Jonathan M. Mikkila, Emad N. Eskandar, Jason L. Gerrard, Daniel Kaping, Shaun R. Patel, Thilo Womelsdorf and Kari L. Hoffman
Journal of Neuroscience 4 November 2015, 35 (44) 14771-14782; DOI: https://doi.org/10.1523/JNEUROSCI.0864-15.2015
Timothy K. Leonard
Departments of 1Psychology and
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Jonathan M. Mikkila
Departments of 1Psychology and
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Emad N. Eskandar
2Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114
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Jason L. Gerrard
2Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114
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Daniel Kaping
3Biology, Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada, and
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Shaun R. Patel
2Nayef Al-Rodhan Laboratories, Department of Neurosurgery, Massachusetts General Hospital, Boston, Massachusetts 02114
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Thilo Womelsdorf
3Biology, Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada, and
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Kari L. Hoffman
Departments of 1Psychology and
3Biology, Centre for Vision Research, York University, Toronto, Ontario M3J 1P3, Canada, and
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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.

SIGNIFICANCE STATEMENT 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.

  • change detection
  • macaque
  • natural scenes
  • search
  • sleep
  • theta
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The Journal of Neuroscience: 35 (44)
Journal of Neuroscience
Vol. 35, Issue 44
4 Nov 2015
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Sharp Wave Ripples during Visual Exploration in the Primate Hippocampus
Timothy K. Leonard, Jonathan M. Mikkila, Emad N. Eskandar, Jason L. Gerrard, Daniel Kaping, Shaun R. Patel, Thilo Womelsdorf, Kari L. Hoffman
Journal of Neuroscience 4 November 2015, 35 (44) 14771-14782; DOI: 10.1523/JNEUROSCI.0864-15.2015

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Sharp Wave Ripples during Visual Exploration in the Primate Hippocampus
Timothy K. Leonard, Jonathan M. Mikkila, Emad N. Eskandar, Jason L. Gerrard, Daniel Kaping, Shaun R. Patel, Thilo Womelsdorf, Kari L. Hoffman
Journal of Neuroscience 4 November 2015, 35 (44) 14771-14782; DOI: 10.1523/JNEUROSCI.0864-15.2015
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Keywords

  • change detection
  • macaque
  • natural scenes
  • search
  • sleep
  • theta

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