Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm

Pavlides, Constantine; Greenstein, Yoram J.; Grudman, Mark; Winson, Jonathan

doi:10.1016/0006-8993(88)91499-0

Cited by 463 publications

(331 citation statements)

References 13 publications

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“…It has been proposed that theta power increases during successful encoding might reflect the recruitment of cortical regions (Sederberg et al, 2003), where theta oscillations could be induced via hippocampo cortical feedback loops (Klimesch et al, 1996). In this way, human theta oscillations could modulate synaptic plasticity across hippocampus and cortex via a phase dependent mechanism (Crespo Garcia et al, 2010;Osipova et al, 2006;Sederberg et al, 2003) similar to the one demonstrated in the rat hippocampus (Hölscher et al, 1997;Pavlides et al, 1988).…”

Section: Introductionmentioning

confidence: 83%

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

et al. 2016

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a b s t r a c tHuman hippocampal theta oscillations play a key role in accurate spatial coding. Associative encoding involves similar hippocampal networks but, paradoxically, is also characterized by theta power decreases. Here, we inves tigated how theta activity relates to associative encoding of place contexts resulting in accurate navigation. Using MEG, we found that slow theta (2 5 Hz) power negatively correlated with subsequent spatial accuracy for vir tual contextual locations in posterior hippocampus and other cortical structures involved in spatial cognition. A rare opportunity to simultaneously record MEG and intracranial EEG in an epilepsy patient provided crucial in sights: during power decreases, slow theta in right anterior hippocampus and left inferior frontal gyrus phase led the left temporal cortex and predicted spatial accuracy. Our findings indicate that decreased slow theta activ ity reflects local and long range neural mechanisms that encode accurate spatial contexts, and strengthens the view that local suppression of low frequency activity is essential for more efficient processing of detailed information.

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Section: Introductionmentioning

confidence: 83%

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

et al. 2016

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“…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.…”

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.

261

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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“…Interestingly, the increased seizure susceptibility of subcortically denervated hippocampus can be partially suppressed by intrahippocampal grafts of locus coeruleus (Buzsaki et al, 1988). In addition, disinhibition of pyramidal or granule cells via inhibition of GABAergic neurons could be important in long-term potentiation since such potentiation can be preferentially induced when the cells are maximally excited (Larson et al, 1986;Pavlides et al, 1988).…”

Section: Functional Considerationsmentioning

confidence: 99%

GABAergic neurons in the rat hippocampal formation: ultrastructure and synaptic relationships with catecholaminergic terminals

Milner

Bacon

1989

J. Neurosci.

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Numerous studies indicate that gamma-aminobutyric acid (GABA) can either hyperpolarize or depolarize hippocampal pyramidal and granule cells. While the inhibitory action of GABA may occur directly on these cells, the excitatory action may be mediated by interactions of GABAergic neurons with each other or with catecholaminergic afferents. We sought to examine the cellular basis for these interactions and their relative frequency. Thus, the ultrastructural morphology of GABAergic neurons and their relation to terminals exhibiting immunoreactivity for the catecholamine-synthesizing enzyme tyrosine hydroxylase (TH) were examined in the rat hippocampal formation using combined immunoautoradiographic and peroxidase-antiperoxidase labeling methods. By light microscopy, GABAergic perikarya and processes codistributed most noticeably with TH-containing processes in the hilus of the dentate gyrus (DG) and in strata lucidum, radiatum, and lacunosum-moleculare of the CA3 region of the hippocampus. Thus, these regions were examined further by electron microscopy. In the ultrastructural analysis, GABA-like immunoreactivity (GABA-LI) was detected in neuronal perikarya, dendrites, axons, and axon terminals. The GABA-containing perikarya were large, ovoid (20–40 microns in diameter), and contained abundant cytoplasm and an indented nucleus with one nucleolus. Synaptic junctions on the perikarya and dendrites with GABA-LI were both symmetric and asymmetric. Approximately equal numbers of TH-labeled terminals (19% of 133 in DG; 39% of 26 in CA3) and GABA-containing terminals (19% DG, 15% CA3) formed synapses with GABA-labeled perikarya. The remainder of the presynaptic terminals (62% DG, 46% CA3) were unlabeled, i.e., contained unidentified transmitters. Terminals with GABA-LI (0.5–1.6 microns) contained numerous small clear vesicles and from 0 to 2 large dense-core vesicles. The types of associations formed by terminals with GABA-LI were remarkably similar in the DG and hippocampus proper despite differences in intrinsic cell type and function. Terminals with GABA-LI formed associations with unlabeled perikarya and dendrites (24% of 151 in DG, 25% of 75 in CA3) and synapses with GABA-containing perikarya and dendrites (18% DG, 5% CA3). Additionally, GABAergic terminals converged upon the same perikarya or dendrite as a TH-containing terminal (15% DG, 21% CA3) and were in direct apposition to TH-labeled terminals (19% DG, 20% CA3). The remaining GABAergic terminals (24% DG, 28% CA3) were without any apparent synaptic relations. In both the DG and CA3, the junctions formed by GABAergic terminals were symmetric. Terminals showing colocalization of GABA-LI and TH-I were also detected although rarely.(ABSTRACT TRUNCATED AT 400 WORDS)

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Long-term potentiation in the dentate gyrus is induced preferentially on the positive phase of θ-rhythm

Cited by 463 publications

References 13 publications

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

Slow-theta power decreases during item-place encoding predict spatial accuracy of subsequent context recall

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

GABAergic neurons in the rat hippocampal formation: ultrastructure and synaptic relationships with catecholaminergic terminals

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