Anterior–Posterior Hippocampal Dynamics Support Working Memory Processing

Li, Jin; Cao, Dan; Dimakopoulos, Vasileios; Shi, Weiyang; Yu, Shan; Fan, Lingzhong; Stieglitz, Lennart; Imbach, Lukas L.; Sarnthein, Johannes; Jiang, Tianzi

doi:10.1523/jneurosci.1287-21.2021

Cited by 29 publications

(39 citation statements)

References 52 publications

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“…This interpretation is also consistent with earlier work showing that different patterns of neuronal oscillations modulate feedforward networks during visual perception 51,54 and as well as feedback processing during top-down control and prediction 55 . Consistent with our results, there is also other evidence of neural activity changing direction for specific functional states 25,44,[56][57][58][59][60] , thus suggesting that our results are part of a broader phenomenon.…”

Section: Discussionsupporting

confidence: 92%

The direction and timing of theta and alpha traveling waves modulate human memory processing

Mohan

Zhang

Jacobs

2022

Preprint

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To support a range of behaviors, the brain must flexibly coordinate neural activity across widespread brain regions. One potential mechanism for this coordination is a traveling wave, in which a neural oscillation propagates across the brain while organizing the order and timing of activity across regions (Ermentrout & Kleinfeld, 2001; Muller et al., 2018). Although traveling waves are present across the brain in various species (Lubenov & Siapas, 2009; Zhang et al., 2018; Davis et al., 2020), their potential functional relevance remained unknown. Here, using rare direct human brain recordings, we demonstrate two novel functional roles for traveling waves of theta- and alpha-band (2-13 Hz) oscillations in the cortex. First, traveling waves propagate in different directions during separate cognitive processes. In episodic memory, traveling waves tended to propagate in posterior-to-anterior and anterior-to-posterior directions, respectively, during encoding and retrieval. Second, traveling waves are informative about the timing of behavior, with the phase of ongoing traveling waves indicating when subjects would retrieve memories. Because traveling waves of oscillations correspond to local neuronal spiking, these patterns indicate that rhythmic pulses of activity move across the brain with different directions and timing for separate behaviors. More broadly, our results suggest a fundamental role for traveling waves and oscillations in dynamically coordinating neural connectivity, by flexibly organizing the timing and directionality of network interactions across the cortex to support cognition and behavior.

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Section: Discussionsupporting

confidence: 92%

The direction and timing of theta and alpha traveling waves modulate human memory processing

Mohan

Zhang

Jacobs

2022

Preprint

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“…3(A)), suggesting that both the amygdala and the hippocampus are involved in WM. The elevated activity in low-frequency oscillation in the present study matches the results reported in our previous study in the hippocampus during WM processing (24). We then averaged the spectral power during encoding and maintenance and compared the two spectra.…”

Section: Increased Theta-alpha Power In the Amygdala And Hippocampussupporting

confidence: 89%

Functional Specialization and Coordination in the Amygdala-Hippocampus Circuit Support Working Memory

Cao

Dimakopoulos

et al. 2022

Preprint

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Both the hippocampus and amygdala are involved in working memory (WM) processing. However, it is still an open question how the two structures interact to represent and maintain WM content. Here, we simultaneously recorded intracranial EEG from the amygdala and hippocampus of epilepsy patients while performing a WM task. Using a series of univariate, multivariate, and connectivity analyses, our results revealed a functional specialization of the amygdala-hippocampus circuit: The mnemonic representations in the amygdala were highly distinct but decreased from encoding to maintenance. The hippocampal representations, however, were less specific but remained stable in the absence of stimulus. Furthermore, the amygdala and hippocampus coordinated their activity during WM: The hippocampal representation was reinstated in the amygdala during maintenance, with task induced low-frequency information flow from the hippocampus to the amygdala. Importantly, the functional specificity and coordination were correlated only when they appeared in correct trials. Our study provides new evidence that successful WM processing in humans relies on specialized and coordinated functions within the amygdala-hippocampus circuit.

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“…One study on episodic memory suggests directional information flow to and from hippocampus [40]. Within hippocampus, directional information flow from posterior to anterior hippocampus indicated successful WM maintenance [20]. The frequencies of GC found in the current study were in the [4-8 Hz] theta band, in line with scalp EEG findings during WM tasks [4, 6] and other tasks [29] that activate oscillations in long-range recurrent connections [27, 28].…”

Section: Discussionmentioning

confidence: 99%

“…In cortical brain regions, WM maintenance correlates with sustained neuronal oscillations, most frequently reported in the theta-alpha range (4-12 Hz) [3-7, 9-20] or at even lower frequencies [25, 26]. Also in the hippocampus, WM maintenance was associated with sustained theta-alpha oscillations [15, 19].…”

Section: Introductionmentioning

confidence: 99%

“…Maintaining content in WM requires communication within a widespread network of brain regions. The anatomical basis of WM was shown noninvasively with EEG / MEG [3][4][5][6][7][8][9][10] and invasively with intracranial local field potentials (LFP) [11][12][13][14][15][16][17][18][19][20][21] and single unit recordings [19,[21][22][23][24].…”

Section: Introductionmentioning

confidence: 99%

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Information flows from hippocampus to auditory cortex during replay of verbal working memory items

Dimakopoulos

Stieglitz

Mégevand

et al. 2021

Preprint

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Background: The maintenance of items in working memory (WM) relies on a widespread network of cortical areas and hippocampus where synchronization between electrophysiological recordings reflects functional coupling. We investigated the direction of information between sensory areas and hippocampus during encoding and maintenance of WM items. Methods: Participants (N=15) performed a WM task where a string of letters was presented all at once, thus separating the encoding period from the maintenance period. Participants mentally replayed the letters during maintenance. We recorded sEEG from the hippocampus, scalp EEG and, additionally in 3 participants, temporo-parietal ECoG. Results: When analyzing the information flow to and from auditory cortex by Granger causality, the flow was from ECoG over auditory cortex to hippocampus with a peak in the 12-24 Hz beta range while letters were presented, and this flow was subsequently reversed during maintenance, while letters were maintained in memory. The same pattern appeared to and from hippocampus with ECoG over temporo-parietal cortex. For scalp EEG, the pattern appeared on temporal sites, albeit in the 4-12 Hz theta-alpha range. While the pattern was significantly structured for correct trials, it was unstructured for incorrect trials. Conclusions: The functional interaction between hippocampus and cortex and the reversal of information flow provide a physiological basis for the encoding of memory items and their active replay during maintenance.

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Anterior–Posterior Hippocampal Dynamics Support Working Memory Processing

Cited by 29 publications

References 52 publications

The direction and timing of theta and alpha traveling waves modulate human memory processing

The direction and timing of theta and alpha traveling waves modulate human memory processing

Functional Specialization and Coordination in the Amygdala-Hippocampus Circuit Support Working Memory

Information flows from hippocampus to auditory cortex during replay of verbal working memory items

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