Ivy Cells: A Population of Nitric-Oxide-Producing, Slow-Spiking GABAergic Neurons and Their Involvement in Hippocampal Network Activity

Fuentealba, Pablo; Begum, Rahima; Capogna, Marco; Jinno, Shozo; Márton, Lőrinc; Csicsvari, Jozsef; Thomson, Alex M.; Somogyi, Péter; Klausberger, Thomas

doi:10.1016/j.neuron.2008.04.004

Cited by 62 publications

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“…Notably, PV-expressing basket or ivy cells reported here have similar spike timing relative to theta oscillations compared to those recorded under anesthesia 15,25 . This is remarkable considering that the frequency of theta oscillations is twice as high in drug-free compared to anesthetized preparations, and the average firing rates of the neurons are higher in the absence of anesthesia.…”

Section: Discussionmentioning

confidence: 52%

“…We observed that pyramidal cells fire, on average, with similar rates during different behavioral states and they are under constant control via the volume transmission 44 by GABA, NPY and nitric oxide from the dense axonal web of ivy cells. In addition, we observed that ivy cells fire with higher rates when field theta oscillations become faster in frequency and larger in amplitude reflecting increased network activity and synchrony.Notably, PV-expressing basket or ivy cells reported here have similar spike timing relative to theta oscillations compared to those recorded under anesthesia 15,25 . This is remarkable considering that the frequency of theta oscillations is twice as high in drug-free compared to anesthetized preparations, and the average firing rates of the neurons are higher in the absence of anesthesia.…”

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confidence: 52%

“…Ivy cells are the quantitatively most abundant type of GABAergic interneuron in the CA1 area 25 . They provide widespread synaptic and extrasynaptic slow GABAergic input, as well as NPY and nitric oxide to pyramidal cell dendrites and Schaffer collateral/commissural terminals via their exceptionally dense axonal arborizations 25,26 and may mediate the activity-dependent regulation of neurogenesis 43 . The firing patterns identified here, are well suited to control homeostasis in the network.…”

Section: Discussionmentioning

confidence: 99%

“…1 and Table 1; primary antibodies are listed in Supplementary Table 1). Ivy cells 25,26 (n=3) had very fine and dense axons in the stratum-radiatum and stratum-oriens providing synaptic and extrasynaptic GABAergic input to pyramidal cell dendrites. Two out of three cells 27 were immunopositive for neuronal nitric oxide synthase (nNOS), and all tested cells expressed neuropeptide tyrosine (NPY) and a high level of neurokinin 1 receptor (NK1R), as well as the α1 and δ subunits of GABA A receptors in the somato-dendritic membrane ( Fig.…”

Section: Identification Of Neurons Recorded In Freely-moving Ratsmentioning

confidence: 99%

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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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Section: Discussionmentioning

confidence: 52%

mentioning

confidence: 52%

Section: Discussionmentioning

confidence: 99%

Section: Identification Of Neurons Recorded In Freely-moving Ratsmentioning

confidence: 99%

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Behavior-dependent specialization of identified hippocampal interneurons

et al. 2012

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“…Periodic perisomatic inhibition has been held responsible for the generation of the high-frequency components and the phaselocking of neuronal activity [3], but no convincing data are available about the initiation of SWRs, although the SWR state is considered an "off-line" state of the hippocampus [1 2]. To uncover the participation of different types of neurons in SWR generation, several in vivo [28][29][30][31][32][33][34] and in vitro [35][36][37] studies have examined the firing characteristics of identified neuron types (summarized in [38]). Mostly similar relative firing patterns were found for the examined cell types, but there were some contradictory results, which might have arisen from differences between the CA1 and the CA3 area, and most importantly from anaesthetized compared to freely moving animals or in vitro slices.…”

Section: Introductionmentioning

confidence: 99%

Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation

Gulyás

Freund

2015

Current Opinion in Neurobiology

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Laminar and Neurochemical Organization of the Dorsal Cochlear Nucleus of the Human, Monkey, Cat, and Rodents

Baizer

Wong

Paolone

et al. 2014

The Anatomical Record

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The dorsal cochlear nucleus (DCN) is a brainstem structure that receives input from the auditory nerve. Many studies in a diversity of species have shown that the DCN has a laminar organization and identifiable neuron types with predictable synaptic relations to each other. In contrast, studies on the human DCN have found a less distinct laminar organization and fewer cell types, although there has been disagreement among studies in how to characterize laminar organization and which of the cell types identified in other animals are also present in humans. We have reexamined DCN organization in the human using immunohistochemistry to analyze the expression of several proteins that have been useful in delineating the neurochemical organization of other brainstem structures in humans: nonphosphorylated neurofilament protein (NPNFP), nitric oxide synthase (nNOS), and three calcium-binding proteins. The results for humans suggest a laminar organization with only two layers, and the presence of large projection neurons that are enriched in NPNFP. We did not observe evidence in humans of the inhibitory interneurons that have been described in the cat and rodent DCN. To compare humans and other animals directly we used immunohistochemistry to examine the DCN in the macaque monkey, the cat, and three rodents. We found similarities between macaque monkey and human in the expression of NPNFP and nNOS, and unexpected differences among species in the patterns of expression of the calcium-binding proteins.

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Ivy Cells: A Population of Nitric-Oxide-Producing, Slow-Spiking GABAergic Neurons and Their Involvement in Hippocampal Network Activity

Cited by 62 publications

References 0 publications

Behavior-dependent specialization of identified hippocampal interneurons

Behavior-dependent specialization of identified hippocampal interneurons

Generation of physiological and pathological high frequency oscillations: the role of perisomatic inhibition in sharp-wave ripple and interictal spike generation

Laminar and Neurochemical Organization of the Dorsal Cochlear Nucleus of the Human, Monkey, Cat, and Rodents

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