Saccades are phase-locked to alpha oscillations in the occipital and medial temporal lobe during successful memory encoding

Staudigl, Tobias; Härtl, Elisabeth; Noachtar, Soheyl; Doeller, Christian F.; Jensen, Ole

doi:10.1371/journal.pbio.2003404

Cited by 61 publications

(79 citation statements)

References 35 publications

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“…Beyond responses in theta rhythm, work using intracranial recordings in epileptic cases, as well as magnetoencephalography recordings in healthy participants, revealed that alpha oscillations in occipital, parietal, and temporal regions, including the parahippocampus, showed significantly higher phase‐locking for subsequently remembered, versus forgotten, trials during the time just before a saccade . Work continues to comprehensively outline the broad impact of eye movements on the coordination of distinct bands of neural oscillations within and across brain regions.…”

Section: Neurophysiology and Oscillatory Responsesmentioning

confidence: 99%

The intersection between the oculomotor and hippocampal memory systems: empirical developments and clinical implications

Ryan

Shen

Liu

2019

Annals of the New York Academy of Sciences

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Decades of cognitive neuroscience research has shown that where we look is intimately connected to what we remember. In this article, we review findings from human and nonhuman animals, using behavioral, neuropsychological, neuroimaging, and computational modeling methods, to show that the oculomotor and hippocampal memory systems interact in a reciprocal manner, on a moment‐to‐moment basis, mediated by a vast structural and functional network. Visual exploration serves to efficiently gather information from the environment for the purpose of creating new memories, updating existing memories, and reconstructing the rich, vivid details from memory. Conversely, memory increases the efficiency of visual exploration. We call for models of oculomotor control to consider the influence of the hippocampal memory system on the cognitive control of eye movements, and for models of hippocampal and broader medial temporal lobe function to consider the influence of the oculomotor system on the development and expression of memory. We describe eye movement–based applications for the detection of neurodegeneration and delivery of therapeutic interventions for mental health disorders for which the hippocampus is implicated and memory dysfunctions are at the forefront.

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Section: Neurophysiology and Oscillatory Responsesmentioning

confidence: 99%

The intersection between the oculomotor and hippocampal memory systems: empirical developments and clinical implications

Ryan

Shen

Liu

2019

Annals of the New York Academy of Sciences

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“…Saccades have been shown to modulate LFPs in multiple brain areas, such as PFC (Tremblay et al, 2015) and visual cortex (Ito et al, 2011(Ito et al, , 2013Staudigl et al, 2017) cortices. In V1, both saccades and fixations have been found to elicit PC in the delta/theta and alpha/beta bands (Ito et al, 2011(Ito et al, , 2013.…”

Section: Origin Of Lfp Modulationsmentioning

confidence: 99%

“…The hippocampus is known to play a critical role in associative memory formation and retrieval (Buffalo, ; Eichenbaum, ; Eichenbaum & Cohen, ; Schiller et al, ; Watrous & Ekstrom, ). Previous studies have shown that hippocampal neuronal activity is modulated around eye movement onsets in both human and nonhuman primates (Hoffman et al, ; Jutras, Fries, & Buffalo, ; Ringo, Sobotka, Diltz, & Bunce, ; Sobotka & Ringo, ; Staudigl, Hartl, Noachtar, Doeller, & Jensen, ). This modulation occurs in complete darkness (Sobotka & Ringo, ) or during rapid eye movement sleep (Andrillon, Nir, Cirelli, Tononi, & Fried, ), suggesting that it has an extra‐retinal origin.…”

Section: Introductionmentioning

confidence: 97%

“…Some studies have reported that saccades can “reset” the phase of LFPs in both the hippocampus (Hoffman et al, ; Jutras et al, ; Sobotka & Ringo, ; Staudigl et al, ) and visual cortical areas (Bartlett, Ovaysikia, Logothetis, & Hoffman, ; Burr, Morrone, & Ross, ; Ito, Maldonado, & Grün, ; Ito, Maldonado, Singer, & Grün, ; Rajkai et al, ). Responses of neurons along the visual processing pathways, from the lateral geniculate nucleus to the prefrontal cortex (PFC), are typically suppressed during saccades and enhanced following saccade landing (fixation onset) (Bartlett et al, ; Burr et al, ; Ito et al, , ; Rajkai et al, ; Schroeder, Wilson, Radman, Scharfman, & Lakatos, ).…”

Section: Introductionmentioning

confidence: 99%

“…In monkeys and humans, perisaccadic LFP modulations in the hippocampus are time-locked to the onset of eye movements (Andrillon et al, 2015;Hoffman et al, 2013) and linked with memory task performance (Jutras et al, 2013;Staudigl et al, 2017). It has been specifically proposed that the hippocampus may receive a copy of the saccade command (i.e., corollary discharge; Sommer & Wurtz, 2002), which resets the phase of the LFPs to facilitate the processing of sensory information linked to an upcoming fixation target (Meister & Buffalo, 2016).…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2019

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Primates use saccades to gather information about objects and their relative spatial arrangement, a process essential for visual perception and memory. It has been proposed that signals linked to saccades reset the phase of local field potential (LFP) oscillations in the hippocampus, providing a temporal window for visual signals to activate neurons in this region and influence memory formation. We investigated this issue by measuring hippocampal LFPs and spikes in two macaques performing different tasks with unconstrained eye movements. We found that LFP phase clustering (PC) in the alpha/beta (8–16 Hz) frequencies followed foveation onsets, while PC in frequencies lower than 8 Hz followed spontaneous saccades, even on a homogeneous background. Saccades to a solid grey background were not followed by increases in local neuronal firing, whereas saccades toward appearing visual stimuli were. Finally, saccade parameters correlated with LFPs phase and amplitude: saccade direction correlated with delta (≤4 Hz) phase, and saccade amplitude with theta (4–8 Hz) power. Our results suggest that signals linked to saccades reach the hippocampus, producing synchronization of delta/theta LFPs without a general activation of local neurons. Moreover, some visual inputs co‐occurring with saccades produce LFP synchronization in the alpha/beta bands and elevated neuronal firing. Our findings support the hypothesis that saccade‐related signals enact sensory input‐dependent plasticity and therefore memory formation in the primate hippocampus.

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Theta and alpha oscillations in human hippocampus and medial parietal cortex support the formation of location‐based representations

Satish,

Keller,

Raza

et al. 2024

Hippocampus

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Our ability to navigate in a new environment depends on learning new locations. Mental representations of locations are quickly accessible during navigation and allow us to know where we are regardless of our current viewpoint. Recent functional magnetic resonance imaging (fMRI) research using pattern classification has shown that these location‐based representations emerge in the retrosplenial cortex and parahippocampal gyrus, regions theorized to be critically involved in spatial navigation. However, little is currently known about the oscillatory dynamics that support the formation of location‐based representations. We used magnetoencephalogram (MEG) recordings to investigate region‐specific oscillatory activity in a task where participants could form location‐based representations. Participants viewed videos showing that two perceptually distinct scenes (180° apart) belonged to the same location. This “overlap” video allowed participants to bind the two distinct scenes together into a more coherent location‐based representation. Participants also viewed control “non‐overlap” videos where two distinct scenes from two different locations were shown, where no location‐based representation could be formed. In a post‐video behavioral task, participants successfully matched the two viewpoints shown in the overlap videos, but not the non‐overlap videos, indicating they successfully learned the locations in the overlap condition. Comparing oscillatory activity between the overlap and non‐overlap videos, we found greater theta and alpha/beta power during the overlap relative to non‐overlap videos, specifically at time‐points when we expected scene integration to occur. These oscillations localized to regions in the medial parietal cortex (precuneus and retrosplenial cortex) and the medial temporal lobe, including the hippocampus. Therefore, we find that theta and alpha/beta oscillations in the hippocampus and medial parietal cortex are likely involved in the formation of location‐based representations.

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Saccades are phase-locked to alpha oscillations in the occipital and medial temporal lobe during successful memory encoding

Cited by 61 publications

References 35 publications

The intersection between the oculomotor and hippocampal memory systems: empirical developments and clinical implications

The intersection between the oculomotor and hippocampal memory systems: empirical developments and clinical implications

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

Theta and alpha oscillations in human hippocampus and medial parietal cortex support the formation of location‐based representations

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