Stimulation in Hippocampal Region CA1 in Behaving Rats Yields Long-Term Potentiation when Delivered to the Peak of Theta and Long-Term Depression when Delivered to the Trough

Hyman, James M.; Wyble, Bradley P.; Goyal, Vikas; Rossi, Christina; Hasselmo, Michael E.

doi:10.1523/jneurosci.23-37-11725.2003

Cited by 339 publications

(317 citation statements)

References 32 publications

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“…Several experiments have now shown that the phase of theta oscillations modulates the induction of synaptic plasticity in the rodent hippocampus (12,14). 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).…”

Section: Discussionmentioning

confidence: 99%

“…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: 87%

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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.

255

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: 99%

mentioning

confidence: 87%

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.

255

231

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“…When imitating such spike train activity using electrical stimulation of hippocampal neurons during Theta, LTP can be easily induced. When stimulating with around five stimuli on the peak of Theta wave, LTP of synaptic transmission can be induced, and when stimulating at the trough of Theta waves, LTD or depotentiation of LTP can be observed (Hölscher et al 1997b;Hyman et al 2003). This mechanism might be the basis for synaptic changes that encode WM information during performance of tasks.…”

Section: How Can Increased Theta Affect Wm?mentioning

confidence: 99%

“…It has been shown that electric stimulation of hippocampal neurons during Theta can affect synaptic transmission significantly. When stimulating hippocampal pathways in synchrony with Theta waves, long-term potentiation (LTP) of synaptic transmission can be induced on the peak of the wave, and long-term depression (LTD) on the trough of the wave (Hölscher et al 1997b;Hyman et al 2003). These mechanisms might be the basis for the synaptic changes that encode WM information during the performance of tasks.…”

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confidence: 99%

Lack of the metabotropic glutamate receptor subtype 7 selectively modulates Theta rhythm and working memory

Hölscher

Schmid²,

Pilz³

et al. 2005

Learn. Mem.

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Metabotropic glutamate receptors (mGluRs) are known to play a role in synaptic plasticity and learning. We have previously shown that mGluR7 deletion in mice produces a selective working memory (WM) impairment, while other types of memory such as reference memory remain unaffected. Since WM has been associated with Theta activity (6-12 Hz) in EEGs, and since EEG abnormalities have been observed in these mice before, we studied the effect of mGluR7 gene ablation on EEG activity in the hippocampus, in particular in the Theta range, during performance of a WM task. In an eight-arm maze with four arms baited, mGluR7 knock-out (KO) and wild-type mice committed the same number of reference memory errors, whereas KOs committed more WM errors. While performing the task, KO mice showed substantially higher Theta amplitudes, and the ratio of Theta to overall EEG power was much increased. No change was seen in the Delta (0-5 Hz), or Gamma (30-40 Hz) EEG bands compared with controls. When recording EEGs during periods of rest in the home cages, no difference was seen between groups. These findings suggest that mGluR7 is important for modulation and control of Theta activity. Since only WM was affected, and only the Theta range of EEG activity was altered, these results show a correlation between Theta rhythm and WM performance, and therefore support the concept that Theta activity in the hippocampus is involved in WM storage.Metabotropic glutamate receptors (mGluRs) are a family of glutamate-sensitive receptors that are coupled to intracellular signal transduction via G-proteins (Pin and Duvoisin 1995). It is known that mGluRs play an important role in the regulation of CNS synaptic plasticity, and also in some processes of memory formation. Pharmacological blockade of mGluR group III receptors (subtypes 4, 6, 7, and 8) has profound effects on the induction of synaptic plasticity (Bashir et al. 1993;Richter-Levin et al. 1994;Hölscher et al. 1997a), synaptic depression (Manahan-Vaughan 2000;Weber et al. 2002), and spatial learning (Hölscher et al. 1996(Hölscher et al. , 1999.In a previous study, we tested the effect of mGluR7 deletion on different forms of learning and memory formation (Hölscher 2003). We showed that mGluR7-deficient (knock-out; KO) mice were not impaired in a non-associative habituation task or in performing reference memory tasks of different complexities (open field, T-maze, four-and eight-arm mazes). However, in tasks that require increased capacity of working memory (WM) performance, mGluR7 KO mice showed clear deficits.WM contains task-related information required to develop plans of action and to guide behavior (Baddeley and Hitch 1974;Olton et al. 1979). In the present paper, we adhere to the definition of WM by Olton et al. (1979), who emphasized the importance of hippocampal activity for supporting WM. How WM is actually encoded and stored in the brain has been under investigation for a long time. The occurrence of oscillations in the EEG of subjects that performed WM tasks had been observed. In pa...

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“…This, according to the model, supports the encoding of new information. Conversely, stimulation at the peak of fissure u leads to depotentiation at the CA3 to CA1 synapses (Huerta and Lisman 1995;Holscher et al 1997;Hyman et al 2003) and to the firing of CA1 pyramidal cells (Skaggs et al 1996;Kamondi et al 1998), thereby relaying information processed in the hippocampus back to the entorhinal cortex. According to the model, the retrieval of already encoded information is favored at the peak of fissure u.…”

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confidence: 99%

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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Stimulation in Hippocampal Region CA1 in Behaving Rats Yields Long-Term Potentiation when Delivered to the Peak of Theta and Long-Term Depression when Delivered to the Trough

Cited by 339 publications

References 32 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

Lack of the metabotropic glutamate receptor subtype 7 selectively modulates Theta rhythm and working memory

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

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