Inhibition-Induced Theta Resonance in Cortical Circuits

Stark, Eran; Eichler, Ronny; Roux, Laurent; Fujisawa, Shigeyoshi; Rotstein, Horacio G.; Buzsáki, György

doi:10.1016/j.neuron.2013.09.033

Cited by 307 publications

(369 citation statements)

References 63 publications

(98 reference statements)

Supporting

Mentioning

331

Contrasting

Order By: Relevance

“…Light stimulation (50-to 70-ms light pulses) was applied on every shank separately during spontaneous behavior in the home cage (n = 4 mice) or during urethane anesthesia (n = 6 mice; ref. 49). Offline, spikes were sorted and classified as putatitve PYR or INT using a Gaussian mixture model (49).…”

Section: Methodsmentioning

confidence: 99%

See 1 more Smart Citation

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Stark

Roux

Eichler

et al. 2015

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

Self Cite

103

View full text Add to dashboard Cite

Sequential activity of multineuronal spiking can be observed during theta and high-frequency ripple oscillations in the hippocampal CA1 region and is linked to experience, but the mechanisms underlying such sequences are unknown. We compared multineuronal spiking during theta oscillations, spontaneous ripples, and focal optically induced high-frequency oscillations ("synthetic" ripples) in freely moving mice. Firing rates and rate modulations of individual neurons, and multineuronal sequences of pyramidal cell and interneuron spiking, were correlated during theta oscillations, spontaneous ripples, and synthetic ripples. Interneuron spiking was crucial for sequence consistency. These results suggest that participation of single neurons and their sequential order in population events are not strictly determined by extrinsic inputs but also influenced by local-circuit properties, including synapses between local neurons and single-neuron biophysics.A hypothesized hallmark of cognition is self-organized sequential activation of neuronal assemblies (1). Self-organized neuronal sequences have been observed in several cortical structures (2-5) and neuronal models (6-7). In the hippocampus, sequential activity of place cells (8) may be induced by external landmarks perceived by the animal during spatial navigation (9) and conveyed to CA1 by the upstream CA3 region or layer 3 of the entorhinal cortex (10). Internally generated sequences have been also described in CA1 during theta oscillations in memory tasks (4, 11), raising the possibility that a given neuronal substrate is responsible for generating sequences at multiple time scales. The extensive recurrent excitatory collateral system of the CA3 region has been postulated to be critical in this process (4,7,12,13).The sequential activity of place cells is "replayed" during sharp waves (SPW) in a temporally compressed form compared with rate modulation of place cells (14)(15)(16)(17)(18)(19)(20) and may arise from the CA3 recurrent excitatory networks during immobility and slow wave sleep. The SPW-related convergent depolarization of CA1 neurons gives rise to a local, fast oscillatory event in the CA1 region ("ripple, refs. 8 and 21). Selective elimination of ripples during or after learning impairs memory performance (22-24), suggesting that SPW ripple-related replay assists memory consolidation (12, 13). Although the local origin of the ripple oscillations is well demonstrated (25, 26), it has been tacitly assumed that the ripple-associated, sequentially ordered firing of CA1 neurons is synaptically driven by the upstream CA3 cell assemblies (12, 15), largely because excitatory recurrent collaterals in the CA1 region are sparse (27). However, sequential activity may also emerge by local mechanisms, patterned by the different biophysical properties of CA1 pyramidal cells and their interactions with local interneurons, which discharge at different times during a ripple (28-30). A putative function of the rich variety of interneurons is temporal organization of princip...

show abstract

Section: Methodsmentioning

confidence: 99%

“…49). Offline, spikes were sorted and classified as putatitve PYR or INT using a Gaussian mixture model (49). Spike sequences were detected and compared using a cross-validated template method or an alternate pair-wise method; statistical significance was verified by resampling (permutation test).…”

Section: Methodsmentioning

confidence: 99%

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Stark

Roux

Eichler

et al. 2015

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

Self Cite

103

View full text Add to dashboard Cite

show abstract

“…Optogenetic manipulation of PV + interneuron activity showed that they are necessary and sufficient for the generation of network oscillations in both hippocampus and neocortex. Stimulation of PV + cells at theta frequency induces theta spike resonance in CA1 pyramidal cells (99), and stimulation of PV + cells at gamma frequency leads to gamma oscillations in the local field potential in somatosensory cortex (11)(12). Conversely, suppression of PV + cells reduces gamma oscillations (12).…”

Section: Role Of Pvmentioning

confidence: 99%

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function

Gan

Jónás

2014

Science

1,040

1,001

View full text Add to dashboard Cite

Review summary (print version)Background Fast-spiking, parvalbumin-expressing interneurons (PV + interneurons) play a key role in several functions of the brain. They contribute to feedback and feedforward inhibition, and are critically involved in the generation of network oscillations. A hallmark property of these interneurons is speed. In essence, these cells convert an excitatory input signal into an inhibitory output signal within a millisecond. How these remarkable signaling properties are implemented at the molecular and cellular level has been unclear. Furthermore, how PV + interneurons shape complex network functions has remained an open question. Advances Outlook PV+ interneurons may also play a key role in numerous brain diseases. These include epilepsy, but also complex psychiatric diseases, such as schizophrenia. Thus, PV + interneurons may become important therapeutic targets in the future. However, much needs to be learned about the basic function of these interneurons before clinical neuroscientists will have a chance to successfully use PV + interneurons for therapeutic purposes. 3 Full article (online) AbstractThe success story of fast-spiking, parvalbumin-expressing (PV + ) GABAergic interneurons is amazing. In 1995, the properties of these interneurons were completely unknown. 20 years later, thanks to the massive use of subcellular patchclamp techniques, simultaneous multiple-cell recording, optogenetics, in vivo measurements, and computational approaches, our knowledge about PV + interneurons became more extensive than for several types of pyramidal neurons (Box 1). These findings have implications beyond the "small world" of basic research on GABAergic cells. For example, the results provide a first proof of principle that neuroscientists might be able to close the gaps between molecular, cellular, network, and behavioral level, which represents one of the main challenges at the present time. Furthermore, the results may form the basis for using PV + interneurons as therapeutical targets for brain diseases in the future. However, much needs to be learned about the basic function of these interneurons before clinical neuroscientists will be able to use PV + interneurons for therapeutic purposes.

show abstract

“…In attempts to manipulate the activity of interneurons by selectively knocking out different subunits of glutamatergic and GABAergic receptors in interneurons, alterations in hippocampal theta, gamma, and ripple oscillations have been found [18][19][20][21]. Cell type-specific manipulations based on optogenetics have on the other hand provided in vivo evidence that GABAergic interneurons control oscillatory activity in hippocampal PCs, as shown by changes in theta [22,23] and ripple rhythms [24]. In this study, we made whole-cell recordings on CA1 neurons of a completely isolated hippocampus, in which slow oscillations could be generated intrinsically in hippocampal neurons, to investigate the contribution of GABAergic interneurons to hippocampal generation of neuronal oscillation.…”

Section: Introductionmentioning

confidence: 99%

GABAergic Interneurons are Required for Generation of Slow CA1 Oscillation in Rat Hippocampus

Wang

Liu

et al. 2016

Neurosci. Bull.

View full text Add to dashboard Cite

Neuronal oscillations are fundamental to hippocampal function. It has been shown that GABAergic interneurons make an important contribution to hippocampal oscillations, but the underlying mechanism is not well understood. Here, using whole-cell recording in the complete hippocampal formation isolated from rats at postnatal days 14-18, we showed that GABA A receptormediated activity enhanced the generation of slow CA1 oscillations. In vitro, slow oscillations (0.5-1.5 Hz) were generated in CA1 neurons, and they consisted primarily of excitatory rather than inhibitory membrane-potential changes. These oscillations were greatly reduced by blocking GABA A receptor-mediated activity with bicuculline and were enhanced by increasing such activity with midazolam, suggesting that interneurons are required for oscillation generation. Consistently, CA1 fast-spiking interneurons were found to generate action potentials usually preceding those in CA1 pyramidal cells. These findings indicate a GABA A receptor-based mechanism for the generation of the slow CA1 oscillation in the hippocampus.

show abstract

Inhibition-Induced Theta Resonance in Cortical Circuits

Cited by 307 publications

References 63 publications

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function

GABAergic Interneurons are Required for Generation of Slow CA1 Oscillation in Rat Hippocampus

Contact Info

Product

Resources

About

Inhibition-Induced Theta Resonance in Cortical Circuits

Cited by 307 publications

References 63 publications

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Local generation of multineuronal spike sequences in the hippocampal CA1 region

Fast-spiking, parvalbumin + GABAergic interneurons: From cellular design to microcircuit function

GABAergic Interneurons are Required for Generation of Slow CA1 Oscillation in Rat Hippocampus

Contact Info

Product

Resources

About

Fast-spiking, parvalbumin ⁺ GABAergic interneurons: From cellular design to microcircuit function