Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons

Cobb, Stuart; Buhl, Eberhard H.; Halasy, Katalin; Paulsen, Ole; Somogyi, Péter

doi:10.1038/378075a0

Cited by 1,358 publications

(1,016 citation statements)

References 25 publications

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“…As indicated by these and other authors (e.g. Maccaferri et al, 2000;Parra et al, 1998;Cobb et al, 1995), such di¡erences suggest that functionally distinct roles might be played by interneurons.How might we understand this seemingly specialized group of neurons? The dynamical output of a neuron is dictated by incoming synaptic input as well as its morphological structure with its given density and distribution of currents (Mainen and Sejnowski, 1996).…”

supporting

confidence: 59%

supporting

confidence: 59%

“…GABAergic interneurons in the hippocampus exert strong inhibition onto excitatory pyramidal cells via dendritic and somatic synapses. Interneurons have extensive axon arbors and a single interneuron can make contact with over 1000 pyramidal cells so that an individual interneuron can phase-lock the ¢ring of multiple pyramidal cells, by synchronously depressing their activities (Buhl et al, 1994;Cobb et al, 1995;Freund and Buzsa ¤ki, 1996;Csicsvari et al, 1998;Sik et al, 1995). Therefore, individual interneurons capable of producing signals such as bistable tonic ¢ring or bursting (see Sik et al (1995) for in vivo bursting behavior of interneurons), can strongly in£uence the generation of di¡erent rhythmic outputs at the network level.…”

Section: Discussionmentioning

confidence: 99%

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Dynamics and diversity in interneurons: a model exploration with slowly inactivating potassium currents

Saraga¹,

Skinner²

2002

Neuroscience

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supporting

confidence: 59%

supporting

confidence: 59%

Section: Discussionmentioning

confidence: 99%

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Dynamics and diversity in interneurons: a model exploration with slowly inactivating potassium currents

Saraga¹,

Skinner²

2002

Neuroscience

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“…Interneurons are necessary for synchronization of the large principal cell populations 10,47,49 underlying memory consolidation and precise association of distinct external inputs. 8,40 Interestingly, another drug with similar effects on associations, namely morphine, was shown to disrupt the longrange synchronized oscillatory patterns of rodent hippocampal networks.…”

Section: Implications Of Cb1 Receptor Localization For Network Synchrmentioning

confidence: 99%

GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus

et al. 2000

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Abstract-Cannabinoids have been shown to disrupt memory processes in mammals including humans. Although the CB1 neuronal cannabinoid receptor was identified several years ago, neuronal network mechanisms mediating cannabinoid effects are still controversial in animals, and even more obscure in humans. In the present study, the localization of CB1 receptors was investigated at the cellular and subcellular levels in the human hippocampus, using control post mortem and epileptic lobectomy tissue. The latter tissue was also used for [ 3 H]GABA release experiments, testing the predictions of the anatomical data. Detectable expression of CB1 was confined to interneurons, most of which were found to be cholecystokinin-containing basket cells. CB1-positive cell bodies showed immunostaining in their perinuclear cytoplasm, but not in their somadendritic plasmamembrane. CB1-immunoreactive axon terminals densely covered the entire hippocampus, forming symmetrical synapses characteristic of GABAergic boutons. Human temporal lobectomy samples were used in the release experiments, as they were similar to the controls regarding cellular and subcellular distribution of CB1 receptors. We found that the CB1 receptor agonist, WIN 55,212-2, strongly reduced [ 3 H]GABA release, and this effect was fully prevented by the specific CB1 receptor antagonist SR 141716A.This unique expression pattern and the presynaptic modulation of GABA release suggests a conserved role for CB1 receptors in controlling inhibitory networks of the hippocampus that are responsible for the generation and maintenance of fast and slow oscillatory patterns. Therefore, a likely mechanism by which cannabinoids may impair memory and associational processes is an alteration of the fine-tuning of synchronized, rhythmic population events. ᭧ 2000 IBRO. Published by Elsevier Science Ltd. All rights reserved.Key words: CB1 receptor, cholecystokinin, presynaptic, synchronization, memory, release.Most behavioral effects of the active compound of marijuana and hashish are mediated by the CB1 cannabinoid receptor (CB1). 23 Although the impacts of cannabinoid-consumption on human and animal behaviour are well known, 1,3,7,43 the underlying physiological processes and the precise sites of cannabinoid actions in neural networks remain to be identified. The hippocampal formation is one of the brain areas with the highest level of CB1 receptor expression. 18,26,29 In accordance, at the behavioral level, cannabinoids typically interfere with hippocampal functions, i.e. they disrupt memory consolidation and associations both in humans and animals. 3,17 Although several recent experiments attempted to determine the mechanisms of cannabinoid action and the precise cellular and subcellular localization of the CB1 receptor in the rodent and primate hippocampus, the data they provide are inconsistent. 4,20,27,31,34,35,38,44,45 In the rodent hippocampus, a specific class of GABAergic interneurons was shown to express CB1 receptors. 20,27,45 Detailed electron microscopic investigation rev...

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“…Interneurons generate oscillatory activity 1,2 , synchronize the activity of pyramidal cells 3 and set time windows for synaptic integration 4 . A large diversity of interneuronal types is a hallmark of cortical circuits.…”

mentioning

confidence: 99%

Behavior-dependent specialization of identified hippocampal interneurons

et al. 2012

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A large variety of GABAergic interneurons control information processing in hippocampal circuits governing the formation of neuronal representations. Whether distinct hippocampal interneuron types contribute differentially to information-processing during behavior is not known. We employed a novel technique for recording and labeling interneurons and pyramidal cells in drug-free, freely-moving rats. Recorded parvalbumin-expressing basket interneurons innervate somata and proximal pyramidal cell dendrites, whereas nitric-oxide-synthase-and neuropeptide-Y-expressing ivy cells provide synaptic and extrasynaptic dendritic modulation. Basket and ivy cells showed distinct spike timing dynamics, firing at different rates and times during theta and ripple oscillations. Basket but not ivy cells changed their firing rates during movement, sleep and quiet wakefulness, suggesting that basket cells coordinate cell assemblies in a behavioral state-contingent manner, whereas persistently-firing ivy cells might control network excitability and homeostasis. Different interneuron types provide GABA to specific subcellular domains at defined times and rates, thus differentially controlling network activity during behavior.GABAergic interneurons control information processing in cortical circuits as percussionists set the rhythm for a melody, or traffic lights regulate the movement of cars through a city. Interneurons generate oscillatory activity 1, 2 , synchronize the activity of pyramidal cells 3 and set time windows for synaptic integration 4 . A large diversity of interneuronal types is a hallmark of cortical circuits. Different domains of pyramidal cells, such as the soma, axoninitial-segment, proximal or distal dendrites 5 are innervated by distinct types of GABAergic interneuron. They also have distinct inputs and membrane properties 6-10 and show different firing patterns during network oscillations induced in vitro [11][12][13][14] or recorded in anesthetized animals 15 , indicating distinct roles for specific interneuron types. However, research on interneurons in drug-free animals that can freely change their behavior, has so far been limited to recordings from unidentified interneurons because of technical limitations. In the barrel cortex of head-restrained mice, groups of interneurons with distinct membrane dynamics during different behavioral states have been described 16,17 and in the hippocampus unidentified interneurons or interneurons belonging to heterogeneous groups expressing parvalbumin and/or somatostatin have been reported [18][19][20][21] to fire with different firing patterns during network oscillations. But, how do specific types of identified interneurons control the activity of cortical circuits in freely-moving animals? CouldCorrespondence and requests for materials should be addressed to D.L. (damien.lapray@pharm.ox.ac.uk) Results Identification of neurons recorded in freely-moving ratsWe recorded the activity of parvalbumin (PV)-expressing basket, ivy and pyramidal cells in the dorsal CA...

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Synchronization of neuronal activity in hippocampus by individual GABAergic interneurons

Cited by 1,358 publications

References 25 publications

Dynamics and diversity in interneurons: a model exploration with slowly inactivating potassium currents

Dynamics and diversity in interneurons: a model exploration with slowly inactivating potassium currents

GABAergic interneurons are the targets of cannabinoid actions in the human hippocampus

Behavior-dependent specialization of identified hippocampal interneurons

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