Long-term potentiation induced by physiologically relevant stimulus patterns

Buzsáki, György; Haas, Helmut L.; Anderson, Edmund G.

doi:10.1016/0006-8993(87)91618-0

Cited by 95 publications

(64 citation statements)

References 18 publications

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“…(Calibration, 0.5 mV, 5 ms.) transmission is not required for AP-LTD. It has been suggested that repetitive high-frequency discharges during TBS resemble SPW-Rs (25). To test other stimulation patterns also resembling spontaneously occurring SPW-Rs (26), the same total number of pulses as used in TBS was delivered antidromically in different patterns, as described in Fig.…”

Section: Facilitation Of Spontaneous Spw-rs Leads To Reduction In Synmentioning

confidence: 99%

Synaptic plasticity by antidromic firing during hippocampal network oscillations

Bukalo

Campanac

Hoffman

et al. 2013

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

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Learning and other cognitive tasks require integrating new experiences into context. In contrast to sensory-evoked synaptic plasticity, comparatively little is known of how synaptic plasticity may be regulated by intrinsic activity in the brain, much of which can involve nonclassical modes of neuronal firing and integration. Coherent high-frequency oscillations of electrical activity in CA1 hippocampal neurons [sharp-wave ripple complexes (SPW-Rs)] functionally couple neurons into transient ensembles. These oscillations occur during slow-wave sleep or at rest. Neurons that participate in SPW-Rs are distinguished from adjacent nonparticipating neurons by firing action potentials that are initiated ectopically in the distal region of axons and propagate antidromically to the cell body. This activity is facilitated by GABA A -mediated depolarization of axons and electrotonic coupling. The possible effects of antidromic firing on synaptic strength are unknown. We find that facilitation of spontaneous SPW-Rs in hippocampal slices by increasing gap-junction coupling or by GABA A -mediated axon depolarization resulted in a reduction of synaptic strength, and electrical stimulation of axons evoked a widespread, long-lasting synaptic depression. Unlike other forms of synaptic plasticity, this synaptic depression is not dependent upon synaptic input or glutamate receptor activation, but rather requires L-type calcium channel activation and functional gap junctions. Synaptic stimulation delivered after antidromic firing, which was otherwise too weak to induce synaptic potentiation, triggered a long-lasting increase in synaptic strength. Rescaling synaptic weights in subsets of neurons firing antidromically during SPW-Rs might contribute to memory consolidation by sharpening specificity of subsequent synaptic input and promoting incorporation of novel information.long-term depression | long-term potentiation | network plasticity | excitability M emory requires more than recording sensory input (1-3).New sensory experience must be incorporated into a cognitive framework, or schema, that preserves temporal sequence and associates the new information together with other relevant aspects of the experience (4). This central processing requires coupling neurons into transiently stable functional assemblies and transferring information between different brain regions (2, 5). The functional coupling of neurons within assemblies is believed to be organized by network oscillations that cover multiple frequency bands and follow distinct mechanisms (6). During slow-wave sleep (SWS) and quiet wakefulness, characterized by decreased sensory and cognitive processing, hippocampal neurons fire in brief periods of high-frequency coherent oscillations (100-300 Hz), termed sharp-wave ripple complexes (SPW-Rs). SPW-Rs coincide with periods of offline replay of neural sequences learned during encoding sensory information (7,8). Disrupting SPW-Rs, and therefore replay, impairs memory retention (9, 10), suggesting that replay of activity sequences...

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Section: Facilitation Of Spontaneous Spw-rs Leads To Reduction In Synmentioning

confidence: 99%

Synaptic plasticity by antidromic firing during hippocampal network oscillations

Bukalo

Campanac

Hoffman

et al. 2013

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

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“…By way of lateral GABAergic inhibition between striatal principal cells (Tunstall et al, 2002;Taverna et al, 2004), this pattern may be sharpened to accentuate activity differences between ensembles. Assuming that ripples, as massive ϳ200 Hz network oscillations, can elicit long-term potentiation (Buzsáki et al, 1987;Staubli and Lynch, 1987), they may not only act as vehicles carrying reactivated information to extra-hippocampal structures, but might also induce long-lasting synaptic changes in glutamatergic inputs to the VS Kombian and Malenka, 1994) or within afferent limbic structures. One of the many elements remaining to be investigated is whether, in rats, the prefrontal and cingulate cortex, midline thalamic nuclei, and basolateral amygdala coreactivate with the hippocampus and VS.…”

Section: Ripple Modulation and Off-line Reactivation: A Hypothesismentioning

confidence: 99%

The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples

et al. 2004

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Previously it has been shown that the hippocampus and neocortex can spontaneously reactivate ensemble activity patterns during post-behavioral sleep and rest periods. Here we examined whether such reactivation also occurs in a subcortical structure, the ventral striatum, which receives a direct input from the hippocampal formation and has been implicated in guidance of consummatory and conditioned behaviors. During a reward-searching task on a T-maze, flanked by sleep and rest periods, parallel recordings were made from ventral striatal ensembles while EEG signals were derived from the hippocampus. Statistical measures indicated a significant amount of reactivation in the ventral striatum. In line with hippocampal data, reactivation was especially prominent during postbehavioral slow-wave sleep, but unlike the hippocampus, no decay in pattern recurrence was visible in the ventral striatum across the first 40 min of post-behavioral rest. We next studied the relationship between ensemble firing patterns in ventral striatum and hippocampal ripples-sharp waves, which have been implicated in pattern replay. Firing rates were significantly modulated in close temporal association with hippocampal ripples in 25% of the units, showing a marked transient enhancement in the average response profile. Strikingly, ripple-modulated neurons in ventral striatum showed a clear reactivation, whereas nonmodulated cells did not. These data suggest, first, the occurrence of pattern replay in a subcortical structure implied in the processing and prediction of reward and, second, a functional linkage between ventral striatal reactivation and a specific type of high-frequency population activity associated with hippocampal replay.

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“…Tetanic stimulation, involving three or more episodes of 100 pulses (100 Hz) delivered at 10-min intervals, saturates LTP and last for many hours in mature hippocampal slices in vitro (Huang and Kandel 1994;Frey et al 1995). TBS provides a more natural paradigm, resembling firing patterns of hippocampal pyramidal cells in vivo (Buzsaki et al 1987;Staubli and Lynch 1987;Abraham and Huggett 1997;Nguyen and Kandel 1997;Morgan and Teyler 2001;Buzsaki 2002;Leinekugel et al 2002;Hyman et al 2003;Raymond and Redman 2006;Mohns and Blumberg 2008). TBS, producing maximal LTP, consists of eight trains delivered at 30-s intervals with each train being 10 bursts at 5 Hz of four pulses at 100 Hz (Abraham and Huggett 1997).…”

Section: Ltp As a Model Synaptic Mechanism Contributing To Consolidatmentioning

confidence: 99%

Structural Components of Synaptic Plasticity and Memory Consolidation

Bailey

Kandel

Harris

2015

Cold Spring Harb Perspect Biol

319

259

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Consolidation of implicit memory in the invertebrate Aplysia and explicit memory in the mammalian hippocampus are associated with remodeling and growth of preexisting synapses and the formation of new synapses. Here, we compare and contrast structural components of the synaptic plasticity that underlies these two distinct forms of memory. In both cases, the structural changes involve time-dependent processes. Thus, some modifications are transient and may contribute to early formative stages of long-term memory, whereas others are more stable, longer lasting, and likely to confer persistence to memory storage. In addition, we explore the possibility that trans-synaptic signaling mechanisms governing de novo synapse formation during development can be reused in the adult for the purposes of structural synaptic plasticity and memory storage. Finally, we discuss how these mechanisms set in motion structural rearrangements that prepare a synapse to strengthen the same memory and, perhaps, to allow it to take part in other memories as a basis for understanding how their anatomical representation results in the enhanced expression and storage of memories in the brain.

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Long-term potentiation induced by physiologically relevant stimulus patterns

Cited by 95 publications

References 18 publications

Synaptic plasticity by antidromic firing during hippocampal network oscillations

Synaptic plasticity by antidromic firing during hippocampal network oscillations

The Ventral Striatum in Off-Line Processing: Ensemble Reactivation during Sleep and Modulation by Hippocampal Ripples

Structural Components of Synaptic Plasticity and Memory Consolidation

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