Interaction between neocortical and hippocampal networks via slow oscillations

Sirota, Anton; Buzsáki, György

doi:10.1017/s1472928807000258

Cited by 230 publications

(237 citation statements)

References 196 publications

(276 reference statements)

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“…1), if infraslow signals are taken to represent the lowfrequency component of the model and δ-band activity is viewed as the higher frequency component. These results represent a departure from rodent hippocampus studies, which associate δ/θ activity with low-frequency signaling, and γ/sharp-wave activity with higher frequency signals (26)(27)(28)(29). We speculate that the differences may be attributable to cross-species effects (16) as well as different signaling processes captured by macro-as opposed to microelectrode recordings (30) (discussed further in Hippocampal Delta, below).…”

Section: Discussionmentioning

confidence: 78%

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Mitra

Snyder

Hacker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

110

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Declarative memory consolidation is hypothesized to require a twostage, reciprocal cortical-hippocampal dialogue. According to this model, higher frequency signals convey information from the cortex to hippocampus during wakefulness, but in the reverse direction during slow-wave sleep (SWS). Conversely, lower-frequency activity propagates from the information "receiver" to the "sender" to coordinate the timing of information transfer. Reversal of sender/ receiver roles across wake and SWS implies that higher-and lower-frequency signaling should reverse direction between the cortex and hippocampus. However, direct evidence of such a reversal has been lacking in humans. Here, we use human resting-state fMRI and electrocorticography to demonstrate that δ-band activity and infraslow activity propagate in opposite directions between the hippocampus and cerebral cortex. Moreover, both δ activity and infraslow activity reverse propagation directions between the hippocampus and cerebral cortex across wake and SWS. These findings provide direct evidence for state-dependent reversals in human cortical-hippocampal communication.D eclarative memories are initially hippocampus-dependent and gradually become hippocampus-independent over time, that is, consolidated (1, 2). It is theorized that a two-stage reciprocal dialogue between the hippocampus and the cerebral cortex underlies memory consolidation (3-5). According to this model, active behavior generates experiential codes in the cortex that are transmitted to the hippocampus, which houses a labile information store. Later, during slow-wave sleep (SWS), recently acquired hippocampal information is reactivated and transmitted to the cerebral cortex, where it is integrated into a more permanent memory store (5, 6). Thus, the hippocampus and cerebral cortex are proposed to exchange roles in sending and receiving information across wake and SWS (5, 6). Importantly, this model does not imply that all signals travel from the "sender" to the "receiver." Instead, the theory proposes that high-frequency activity carries information from the sender to receiver, that is, from the cortex to hippocampus or the hippocampus to cortex, depending on the stage of memory consolidation (wake or SWS, respectively) (4). Conversely, low-frequency activity propagates from the receiver back to the sender to coordinate the transfer of high-frequency information through modulation of the sender's excitability (4, 7-9). Hence, the two-stage reciprocal dialogue model predicts that lower and higher frequency activity between the hippocampus and cortex should propagate in opposite directions across wake and SWS, as illustrated in the schematic in Fig. 1. However, such reversal has not been directly observed in humans.We have recently analyzed temporal lags (delays) in neural signals to study the net propagation of spontaneous activity. In particular, we investigated resting-state fMRI (rs-fMRI) blood oxygen level-dependent (BOLD) signals and demonstrated directed propagation of infraslow activity (<0.1...

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Section: Discussionmentioning

confidence: 78%

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Mitra

Snyder

Hacker

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

110

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“…Buzsaki et al (1988), for example, showed that unilateral lesion of the thalamus did not change power spectrum in the 1-4 Hz band of EEG activity. Nonetheless, a clear mechanistic account from this approach is unlikely because these oscillations reflect a complex system in which cortical and subcortical areas are likely cooperatively involved through reciprocal connections (Steriade and Timofeev, 2003;Sirota and Buzsáki, 2005).…”

Section: Discussionmentioning

confidence: 99%

“…Alternatively, slow waves may represent global or traveling wave-mediated changes in activity that entrain much of the cortex (Massimini et al, 2004). Multichannel EEG recordings have proven useful in addressing these hypotheses and have shown both local patterns of cortical up/down state (Sirota and Buzsáki, 2005) and widespread synchrony (Buzsaki et al, 1988) of cortical slow-wave activity. However, these approaches have been unable to resolve the regional structure and dynamics of these waves because of relatively sparse sampling.…”

Section: Introductionmentioning

confidence: 99%

Mirrored Bilateral Slow-Wave Cortical Activity within Local Circuits Revealed by Fast Bihemispheric Voltage-Sensitive Dye Imaging in Anesthetized and Awake Mice

Mohajerani¹,

McVea²,

Fingas³

et al. 2010

J. Neurosci.

253

280

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Spontaneous slow-wave oscillations of neuronal membrane potential occur about once every second in the rodent cortex and may serve to shape the efficacy of evoked neuronal responses and consolidate memory during sleep. However, whether these oscillations reflect the entrainment of all cortical regions via propagating waves or whether they exhibit regional and temporal heterogeneity that reflects processing in local cortical circuits is unknown. Using voltage-sensitive dye (VSD) imaging within an adult C57BL/6J mouse crossmidline large craniotomy preparation, we recorded this depolarizing activity across most of both cortical hemispheres simultaneously in both anesthetized and quiet awake animals. Spontaneous oscillations in the VSD signal were highly synchronized between hemispheres, and acallosal I/LnJ mice indicated that synchrony depended on the corpus callosum. In both anesthetized and awake mice (recovered from anesthesia), the oscillations were not necessarily global changes in activity state but were made up of complex local patterns characterized by multiple discrete peaks that were unevenly distributed across cortex. Although the local patterns of depolarizing activity were complex and changed over tens of milliseconds, they were faithfully mirrored in both hemispheres in mice with an intact corpus callosum, to perhaps ensure parallel modification of related circuits in both hemispheres. We conclude that within global rhythms of spontaneous activity are complex events that reflect orchestrated processing within local cortical circuits.

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“…The conflict arises because A and B are known to belong together as a pair, but now B is also being paired with C. Introduction of this conflicting information is thought to reactivate the previously learned pair (A-B) as well. Resolution of this conflict has been shown to involve an increase in connectivity between the hippocampus and the vmPFC (van Kesteren, Fernández, Norris, & Hermans, 2010;Zeithamova, Dominick, & Preston, 2012), with activity in the vmPFC phase locked to hippocampal theta oscillations that are prominent both in waking activity and during rapid eye movement (REM) sleep (Sirota & Buzsáki, 2005). Furthermore, the degree of activation of the vmPFC and hippocampus during this conflict predicts the successful formation of indirect, relational associations (A-C), which resolves the conflict by incorporating how B is related to A and C and defining the relationship between all three components (van Kesteren et al, 2010;Zeithamova et al, 2012).…”

Section: Direct Associative Memories and Relational Memory Formationmentioning

confidence: 99%

The differential effects of emotional salience on direct associative and relational memory during a nap

Alger

Payne

2016

Cogn Affect Behav Neurosci

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Relational memories are formed from shared components between directly learned memory associations, flexibly linking learned information to better inform future judgments. Sleep has been found to facilitate both direct associative and relational memories. However, the impact of incorporating emotionally salient information into learned material and the interaction of emotional salience and sleep in facilitating both types of memory is unknown. Participants encoded two sets of picture pairs, with either emotionally negative or neutral objects paired with neutral faces. The same objects were present in both sets, paired with two different faces across the sets. Baseline memory for these directly paired associates was tested immediately after encoding, followed by either a 90-min nap opportunity or wakefulness. Five hours after learning, a surprise test assessed relational memory, the indirect association between two faces paired with the same object during encoding, followed by a retest of direct associative memory. Overall, negative information was remembered better than neutral for directly learned pairs. A nap facilitated both preservation of direct associative memories and formation of relational memories, compared to remaining awake. Interestingly, however, this sleep benefit was observed specifically for neutral directly paired associates, while both neutral and negative relational associations benefitted from a nap. Finally, REM sleep played opposing roles in neutral direct and relational associative memory formation, with more REM sleep leading to forgetting of direct associations but promoting relational associations, suggesting that, while not benefitting memory consolidation for directly learned details, REM sleep may foster the memory reorganization needed for relational memory.Keywords Emotion . Associative memory . Naps . Sleep . Inference . Relational memory In our encounters with the everyday stream of information, we do not encode and store all individual experiences in a veridical fashion. Rather, new information is integrated with old, and overlapping details are consolidated into schemata, or networks linked by common features of related memories, to flexibly form novel relationships (Eichenbaum, 2004;Eichenbaum & Cohen, 2001). We use these new representations derived from related memories to adaptively make inferential judgments about future experiences. However, our everyday experiences are not devoid of emotion. Emotional salience, defined by the valence (negative to positive) and arousal (calming to arousing) of an experience, is a biologically adaptive cue that can influence how an event is remembered and possibly how it is integrated in memory. In addition to the influence of emotion, sleep during the consolidation and integration period of a new memory may impact its fate. This experiment investigates the separate and interacting contributions of emotional salience and sleep to the consolidation of direct associative and relational memories, the indirect associations between two...

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Interaction between neocortical and hippocampal networks via slow oscillations

Cited by 230 publications

References 196 publications

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Human cortical–hippocampal dialogue in wake and slow-wave sleep

Mirrored Bilateral Slow-Wave Cortical Activity within Local Circuits Revealed by Fast Bihemispheric Voltage-Sensitive Dye Imaging in Anesthetized and Awake Mice

The differential effects of emotional salience on direct associative and relational memory during a nap

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