Theta reset produces optimal conditions for long‐term potentiation

McCartney, Holly; Johnson, Andrew D.; Weil, Zachary M.; Givens, Bennet

doi:10.1002/hipo.20019

Cited by 108 publications

(95 citation statements)

References 25 publications

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“…Theta appears to reset its phase during the encoding of new stimuli (33), and it has been argued that this reset provides the basis for enhanced plasticity (13). These findings in rodents support the idea that the phase of theta oscillations provides a temporal separation of encoding and retrieval operations (34).…”

Section: Discussionmentioning

confidence: 55%

“…Recent observations that perception of a stimulus can be influenced by prestimulus brain activity (10,11) raise the additional possibility that the brain state immediately preceding an event could predict later episodic memory. This possibility is supported by findings in rodents that the amplitude of hippocampal theta (3)(4)(5)(6)(7)(8) oscillations, which are held to be important modulators of the induction of synaptic plasticity (12)(13)(14), is associated with enhanced learning in classical conditioning even before stimulus onset (15)(16)(17). Because the medial temporal lobe (MTL) and, in particular, the hippocampus are also critical for episodic memory encoding in humans (18)(19)(20), prestimulus mediotemporal theta states might be linked to effective episodic memory encoding.…”

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confidence: 88%

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Medial temporal theta state before an event predicts episodic encoding success in humans

Guderian

Schott

Richardson‐Klavehn

et al. 2009

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

260

231

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We report a human electrophysiological brain state that predicts successful memory for events before they occur. Using magnetoencephalographic recordings of brain activity during episodic memory encoding, we show that amplitudes of theta oscillations shortly preceding the onsets of words were higher for laterrecalled than for later-forgotten words. Furthermore, single-trial analyses revealed that recall rate in all 24 participants tested increased as a function of increasing prestimulus theta amplitude. This positive correlation was independent of whether participants were preparing for semantic or phonemic stimulus processing, thus likely signifying a memory-related theta state rather than a preparatory task set. Source analysis located this theta state to the medial temporal lobe, a region known to be critical for encoding and recall. These findings provide insight into state-related aspects of memory formation in humans, and open a perspective for improving memory through theta-related brain states.hippocampus ͉ magnetoencephalography ͉ memory ͉ oscillations ͉ prestimulus T he neurocognitive processing that is instantiated by an event determines the longevity and quality of memory for that event. Studies using electrophysiological (1-3) and hemodynamic (4-9) techniques have shown that episodic memory-the ability to recollect an event and its spatiotemporal context-is associated with specific patterns of brain activity during the time the event is originally experienced. Recent observations that perception of a stimulus can be influenced by prestimulus brain activity (10, 11) raise the additional possibility that the brain state immediately preceding an event could predict later episodic memory. This possibility is supported by findings in rodents that the amplitude of hippocampal theta (3-8 Hz) oscillations, which are held to be important modulators of the induction of synaptic plasticity (12)(13)(14), is associated with enhanced learning in classical conditioning even before stimulus onset (15)(16)(17). Because the medial temporal lobe (MTL) and, in particular, the hippocampus are also critical for episodic memory encoding in humans (18)(19)(20), prestimulus mediotemporal theta states might be linked to effective episodic memory encoding.For prestimulus brain activity to qualify as a general encodingrelated state, it should be associated with encoding success independent of preparatory factors related to the cognitive control of particular task demands. A recent event-related potential (ERP) study of episodic memory showed that prestimulus, frontal-negative slow shifts predicted successful encoding of words 250 ms before the onset of word presentation (21). Critically, this prestimulus effect was observed only if the prestimulus task cue required a semantic judgment on the word and not when the task cue required an orthographic judgment (21). Therefore, this prestimulus ERP difference depended on a specific task set and is unlikely to reflect a general encodingrelated state.To examine whether prestimulus the...

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Section: Discussionmentioning

confidence: 55%

mentioning

confidence: 88%

Medial temporal theta state before an event predicts episodic encoding success in humans

Guderian

Schott

Richardson‐Klavehn

et al. 2009

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

260

231

View full text Add to dashboard Cite

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“…The high phase-locking of u-band responses in the Trough group resembles the u reset observed in the dentate gyri of rats performing a working memory task involving both visual and auditory peripheral stimuli (Givens 1996). It has been demonstrated in rats that LTP is preferentially induced if stimulation is timed to occur during the peak of the CA1 u (trough of fissure u) not only when the oscillation occurs spontaneously (Holscher et al 1997) but also when it is evoked and reset by a peripheral stimulus (McCartney et al 2004). Thus, phase-locking or resetting of hippocampal u oscillation to the stimulus onset creates windows of opportunity for enhanced processing of subsequent relevant stimuli.…”

Section: Discussionmentioning

confidence: 77%

Phase matters: responding to and learning about peripheral stimuli depends on hippocampal θ phase at stimulus onset

et al. 2015

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Hippocampal u (3 -12 Hz) oscillations are implicated in learning and memory, but their functional role remains unclear. We studied the effect of the phase of local u oscillation on hippocampal responses to a neutral conditioned stimulus (CS) and subsequent learning of classical trace eyeblink conditioning in adult rabbits. High-amplitude, regular hippocampal u-band responses (that predict good learning) were elicited by the CS when it was timed to commence at the fissure u trough (Trough group). Regardless, learning in this group was not enhanced compared with a yoked control group, possibly due to a ceiling effect. However, when the CS was consistently presented to the peak of u (Peak group), hippocampal u-band responding was less organized and learning was retarded. In well-trained animals, the hippocampal u phase at CS onset no longer affected performance of the learned response, suggesting a time-limited role for hippocampal processing in learning. To our knowledge, this is the first study to demonstrate that timing a peripheral stimulus to a specific phase of the hippocampal u cycle produces robust effects on the synchronization of neural responses and affects learning at the behavioral level. Our results support the notion that the phase of spontaneous hippocampal u oscillation is a means of regulating the processing of information in the brain to a behaviorally relevant degree.

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“…5B), illustrating that the LFP theta-phase resets of the theta-gamma-correlated network also indexed whether attention shifts are successful. A plausible mechanism for such a farreaching consequence of phase-aligned theta activation can be found in recent studies that identified how a cue-induced phase reset effectively gates the outflow of a cortical circuit (35)(36)(37). These studies suggest that the phase reset-gated output of a local circuit can serve as the causal trigger of distant gamma activity phase locked to theta activity.…”

Section: Discussionmentioning

confidence: 99%

“…We thus correlated burst-LFP synchronization of neurons recorded at LFP recording sites that provided theta-phase or gamma-amplitude variations for theta-gamma correlations (SI Result S13). We found that burst synchronization to remote LFP gamma activity varied proportionally with the degree of theta-phase correlation with low-gamma amplitudes (35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46)(47)(48)(49)(50), an effect that was limited to those LFP sites that showed significant theta-gamma correlations (Spearman rank correlation r = 0.2, P = 0.044; Table S2 and SI Result S13). To our knowledge, these findings provide the first quantitative evidence that recording sites with LFP theta phases that engage in longrange gamma correlations also host neurons whose burst firing events synchronize long-range to gamma activity.…”

Section: Theta-gamma Correlation and Its Relation To Synchronization Ofmentioning

confidence: 95%

Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

Voloh

Valiante

Everling

et al. 2015

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

138

129

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Anterior cingulate and lateral prefrontal cortex (ACC/PFC) are believed to coordinate activity to flexibly prioritize the processing of goal-relevant over irrelevant information. This between-area coordination may be realized by common low-frequency excitability changes synchronizing segregated high-frequency activations. We tested this coordination hypothesis by recording in macaque ACC/PFC during the covert utilization of attention cues. We found robust increases of 5-10 Hz (theta) to 35-55 Hz (gamma) phaseamplitude correlation between ACC and PFC during successful attention shifts but not before errors. Cortical sites providing theta phases (i) showed a prominent cue-induced phase reset, (ii) were more likely in ACC than PFC, and (iii) hosted neurons with burst firing events that synchronized to distant gamma activity. These findings suggest that interareal theta-gamma correlations could follow mechanistically from a cue-triggered reactivation of rule memory that synchronizes theta across ACC/PFC.T he anterior cingulate and prefrontal cortex (ACC/PFC) of primates are key structures that ensure the flexible deployment of attention during goal-directed behavior (1, 2). To achieve such flexible control, diverse streams of information need to be taken into account, which are encoded by neuronal populations in anatomically segregated subfields of the ACC/ PFC (3, 4). Information about the expected values of possible attentional targets are prominently encoded in medial prefrontal cortices and ACC, whereas the rules and task goals that structure goal-directed behavior are prominently encoded in the lateral PFC (5, 6). Flexible biasing of attention thus requires the integration of information across anatomically segregated cortical circuits. One candidate means to achieve such interareal integration is by synchronizing local processes in distant brain areas to a common process. A rich set of predominantly rodent studies have documented such interareal neuronal interactions in the form of a phase-amplitude (P-A) correlations between lowfrequency periodic excitability fluctuation and high-frequency gamma-band activity (7-9). It is, however, unknown whether there are reliable cross-frequency P-A interactions between those primate ACC/PFC nodes that underlie flexible attention shifts and, if so, whether P-A correlations are reliably linked to the actual successful deployment of attention (10, 11). We thus set out to test for and characterize P-A interactions during covert control processes by recording local field potential (LFP) activity in macaque ACC/PFC subfields during attentional stimulus selection. ResultsWe recorded LFP activity from 1,104 between-channel pairs of electrodes (344 individual LFP channels) within different subfields in ACC/PFC of two macaques engaged in an attention task (Fig. 1A). In the following, we report results pooled across monkeys and show that individual monkey results were consistent and qualitatively similar in SI Result S1. These recordings were from a dataset that was previously analy...

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Theta reset produces optimal conditions for long‐term potentiation

Cited by 108 publications

References 25 publications

Medial temporal theta state before an event predicts episodic encoding success in humans

Medial temporal theta state before an event predicts episodic encoding success in humans

Phase matters: responding to and learning about peripheral stimuli depends on hippocampal θ phase at stimulus onset

Theta–gamma coordination between anterior cingulate and prefrontal cortex indexes correct attention shifts

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