Induction of sharp wave–ripple complexes in vitro and reorganization of hippocampal networks

Behrens, Christoph; Boom, Leander P van den; Hoz, Livia de; Friedman, Alon; Heinemann, Uwe

doi:10.1038/nn1571

Cited by 242 publications

(254 citation statements)

References 45 publications

Supporting

Mentioning

215

Contrasting

Unclassified

Order By: Relevance

“…As basket cells or bistratified cells in the CA1 region of rats (Klausberger et al, 2003(Klausberger et al, , 2004, these interneurons may control the fine tuning of spiking activity by providing a temporal structure relative to which the activity of individual pyramidal cells is coordinated. Such loops have been hypothesized previously to be important for the formation and retrieval of memories across cortical-hippocampal circuits (Buzsáki and Chrobak, 1995;Behrens et al, 2005). Therefore, our present observations could allow for a direct comparison of hippocampal data between rodents and primates, which opens the door to a broad across-species understanding of hippocampal function, including models of memory stabilization (Buzsáki, 1989;Lee and Wilson, 1992;Wilson and McNaughton, 1994).…”

Section: Discussionsupporting

confidence: 56%

“…These ripples originate from the synchronized firing of CA3 cells and spread downstream as spatially coherent oscillations along the CA1-subicular-entorhinal axis (Chrobak and Buzsáki, 1996). This coactivation of hippocampal and neocortical pathways are thought to be crucial for memory consolidation processes, during which memories are gradually translated from short-term hippocampal to longer-term neocortical stores (Buzsáki, 1989;Lee and Wilson, 1992;Wilson and McNaughton, 1994;Behrens et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans

Quyen¹,

Bragin²,

Staba³

et al. 2008

Journal of Neuroscience

149

123

View full text Add to dashboard Cite

High-frequency field ripples occur in the rodent hippocampal formation and are assumed to depend on interneuron type-specific firing patterns, structuring the activity of pyramidal cells. Ripples with similar characteristics are also present in humans, yet their underlying cellular correlates are still unknown. By in vivo recording interneurons and pyramidal cells in the human hippocampal formation, we find that cell type-specific firing patterns and phase-locking on a millisecond timescale can be distinguished during ripples. In particular, pyramidal cells fired preferentially at the highest amplitude of the ripple, but interneurons began to discharge earlier than pyramidal cells. Furthermore, a large fraction of cells were phase-locked to the ripple cycle, but the preferred phase of discharge of interneurons followed the maximum discharge probability of pyramidal neurons. These relationships between human ripples and unit activity are qualitatively similar to that observed in vivo in the rodents, suggesting that their underlying mechanisms are similar.

show abstract

Section: Discussionsupporting

confidence: 56%

Section: Introductionmentioning

confidence: 99%

Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans

Quyen¹,

Bragin²,

Staba³

et al. 2008

Journal of Neuroscience

149

123

View full text Add to dashboard Cite

show abstract

“…Research has established a solid basis for our understanding of how different nerve cells interact, assemble into functional units, and influence behavior and mood (1)(2)(3)(4). High-frequency oscillation of the neuronal membrane potential creates permissive time windows for induction of sensory context-dependent bidirectional plasticity of glutamatergic synaptic transmission (1,5,6), which is a synaptic correlate of discriminative associative memory (6)(7)(8)(9).…”

Section: Introductionmentioning

confidence: 99%

Changes in neural network homeostasis trigger neuropsychiatric symptoms

Winkelmann¹,

Maggio²,

Eller³

et al. 2014

J. Clin. Invest.

Self Cite

117

View full text Add to dashboard Cite

The mechanisms that regulate the strength of synaptic transmission and intrinsic neuronal excitability are well characterized; however, the mechanisms that promote disease-causing neural network dysfunction are poorly defined. We generated mice with targeted neuron type-specific expression of a gain-of-function variant of the neurotransmitter receptor for glycine (GlyR) that is found in hippocampectomies from patients with temporal lobe epilepsy. In this mouse model, targeted expression of gain-of-function GlyR in terminals of glutamatergic cells or in parvalbumin-positive interneurons persistently altered neural network excitability. The increased network excitability associated with gain-of-function GlyR expression in glutamatergic neurons resulted in recurrent epileptiform discharge, which provoked cognitive dysfunction and memory deficits without affecting bidirectional synaptic plasticity. In contrast, decreased network excitability due to gain-of-function GlyR expression in parvalbumin-positive interneurons resulted in an anxiety phenotype, but did not affect cognitive performance or discriminative associative memory. Our animal model unveils neuron type-specific effects on cognition, formation of discriminative associative memory, and emotional behavior in vivo. Furthermore, our data identify a presynaptic disease-causing molecular mechanism that impairs homeostatic regulation of neural network excitability and triggers neuropsychiatric symptoms. IntroductionResearch has established a solid basis for our understanding of how different nerve cells interact, assemble into functional units, and influence behavior and mood (1-4). High-frequency oscillation of the neuronal membrane potential creates permissive time windows for induction of sensory context-dependent bidirectional plasticity of glutamatergic synaptic transmission (1, 5, 6), which is a synaptic correlate of discriminative associative memory (6-9). Thus, temporal precision of neuronal inputs relative to the actual membrane potential is an important determinant of information coding and memory formation (5, 10-12). GABAergic synaptic transmission is equally relevant for cognitive function, because GABAergic interneurons regulate neuronal excitability and provide a spatiotemporal control framework for the timing of synaptic glutamatergic transmission. Fast-spiking (parvalbumin-positive) interneurons, for example, regulate hippocampal neural network oscillation in cognitively relevant high-gamma frequency ranges (13,14). In conjunction with other interneuron types, they form a precision clockwork without which cortical operations are not possible (15,16). Thus, spatiotemporal coordination of glutamatergic and GABAergic synaptic transmission is essential for sensory processing and cognitive performance.

show abstract

“…SW-Rs are complex network oscillations that apparently require the balanced contribution of glutamatergic excitation and GABAergic inhibition (25,36,37). Thus, cannabinoid-induced SW-R suppression may depend on modulations of the release of both glutamate and GABA.…”

Section: Discussionmentioning

confidence: 99%

“…Experiments were performed with the approval of the animal experiment ethics committee at the University of Tokyo (approval number [19][20][21][22][23][24][25][26][27][28][29][30][31][32][33][34][35] according to the University of Tokyo guidelines for the care and use of laboratory animals.…”

Section: Animal Ethicsmentioning

confidence: 99%

Cannabinoid Receptor Activation Disrupts the Internal Structure of Hippocampal Sharp Wave–Ripple Complexes

Sun

Norimoto²,

Pu³

et al. 2012

J Pharmacol Sci

View full text Add to dashboard Cite

Abstract. Cannabinoid agonists impair hippocampus-dependent learning and memory. Using mouse hippocampal slice preparations, we examined the effect of anandamide, an endogenous cannabinoid, on sharp wave-ripple (SW-R) complexes, which are believed to mediate memory consolidation during slow-wave sleep or behavioral immobility. Anandamide reduced the frequency of SW-Rs recorded from the CA3 region, and this effect was abolished by AM251, a cannabinoid CB1-receptor antagonist. We further addressed the action of anandamide using a functional multineuron calcium imaging technique. Anandamide reduced the firing rate of hippocampal neurons as well as disrupted the temporal coordination of their firings during SW-R.

show abstract

Induction of sharp wave–ripple complexes in vitro and reorganization of hippocampal networks

Cited by 242 publications

References 45 publications

Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans

Cell Type-Specific Firing during Ripple Oscillations in the Hippocampal Formation of Humans

Changes in neural network homeostasis trigger neuropsychiatric symptoms

Cannabinoid Receptor Activation Disrupts the Internal Structure of Hippocampal Sharp Wave–Ripple Complexes

Contact Info

Product

Resources

About