Mechanisms of Inhibition within the Telencephalon: “Where the Wild Things Are”

Fishell, Gord; Rudy, Bernardo

doi:10.1146/annurev-neuro-061010-113717

Cited by 219 publications

(241 citation statements)

References 223 publications

(292 reference statements)

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“…Previously, VIPϩ cell loss of function experiments have been performed with either photolytic lesions of a small subset of VIPϩ cells (Fu et al 2014) or tetanus toxin-mediated lesions (Fu et al 2015). It was shown that the gain in the visual response during locomotion (Niell and Stryker 2010) was abolished by lesion of VIPϩ cells.…”

Section: Discussionmentioning

confidence: 99%

“…During visual stimulation, the thalamocortical circuit likely engages VIPϩ cells through a monosynaptic (Fu et al 2015) or polysynaptic excitatory circuit from the thalamus. However, during spontaneous activity or locomotion, top-down (Zhang et al 2014) or cholinergic inputs (Alitto and Dan 2012;Eckenstein et al 1988;Letzkus et al 2011) may be responsible for depolarizing these cells.…”

Section: Discussionmentioning

confidence: 99%

“…Despite the clear connectivity VIPϩ cells maintain in local circuits, it remains unclear how the actions of this small cell population (1-2% of all cortical neurons) could influence the excitability of large groups of pyramidal cells. Previous work has shown that VIPϩ cells in the cortex are active during movement (Fu et al 2014) and sensory processing (Pi et al 2013) and function in gain control (Fu et al 2014;Pi et al 2013) and plasticity (Fu et al 2015). Therefore, their disinhibitory role is thought to function exclusively during specific network states, suggesting a role for VIPϩ cells in particular network processes.…”

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confidence: 99%

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VIP+ interneurons control neocortical activity across brain states

Jackson

Ayzenshtat

Karnani

et al. 2016

Journal of Neurophysiology

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GABAergic interneurons are positioned to powerfully influence the dynamics of neural activity, yet the interneuron-mediated circuit mechanisms that control spontaneous and evoked neocortical activity remains elusive. Vasoactive intestinal peptide (VIPϩ) interneurons are a specialized cell class which synapse specifically on other interneurons, potentially serving to facilitate increases in cortical activity. In this study, using in vivo Ca 2ϩ imaging, we describe the interaction between local network activity and VIPϩ cells and determine their role in modulating neocortical activity in mouse visual cortex. VIPϩ cells were active across brain states including locomotion, nonlocomotion, visual stimulation, and under anesthesia. VIPϩ activity correlated most clearly with the mean level of population activity of nearby excitatory neurons during all brain states, suggesting VIPϩ cells enable high-excitability states in the cortex. The pharmacogenetic blockade of VIPϩ cell output reduced network activity during locomotion, nonlocomotion, anesthesia, and visual stimulation, suggesting VIPϩ cells exert a state-independent facilitation of neural activity in the cortex. Collectively, our findings demonstrate that VIPϩ neurons have a causal role in the generation of high-activity regimes during spontaneous and stimulus evoked neocortical activity.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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VIP+ interneurons control neocortical activity across brain states

Jackson

Ayzenshtat

Karnani

et al. 2016

Journal of Neurophysiology

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“…[2]). The GABAsynthesizing enzyme glutamic acid decarboxylase (GAD) is expressed by all GABAergic interneurons, and the calcium binding proteins calbindin (CB), calretinin (CR), or parvalbumin (PV) [2] are expressed individually or in combination with the neuropeptides somatostatin (SST), neuropeptide Y (NPY), cholecystokinin, and vasoactive intestinal peptide (VIP) [3,4].…”

Section: Introductionmentioning

confidence: 99%

Derivation and Isolation of NKX2.1-Positive Basal Forebrain Progenitors from Human Embryonic Stem Cells

Germain

Banda

Becker

et al. 2013

Stem Cells and Development

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Gamma aminobutyric acid (GABA)-expressing interneurons are the major inhibitory cells of the cerebral cortex and hippocampus. These interneurons originate in the medial ganglionic eminence (MGE) and lateral ganglionic eminence of the ventral forebrain during embryonic development and show reduced survival and function in a variety of neurological disorders, including temporal lobe epilepsy. We and others have proposed that embryonic stem cell (ESC)-derived ventral forebrain progenitors might provide a source of new GABAergic interneurons for cell-based therapies. While human ESCs (hESCs) are readily differentiated in vitro into dorsal telencephalic neural progenitors, standard protocols for generating ventral subtypes of telencephalic progenitors are less effective. We now report efficient derivation of GABAergic progenitors using an established hESC reporter line that expresses green fluorescent protein (GFP) under the control of an endogenous NKX2.1 promoter. GABAergic progenitors were derived from this hESC line by a modified monolayer neural differentiation protocol. Consistent with sonic hedgehog (SHH)-dependent specification of NKX2.1-positive progenitors in the embryonic MGE, we show a dose-dependent increase in the generation of NKX2.1:GFP-positive progenitors after SHH treatment in vitro. Characterization of NKX2.1:GFP-positive cells confirms their identity as MGE-like neural progenitors, based on gene expression profiles and their ability to differentiate into GABAergic interneurons. We are also able to generate highly enriched populations of NKX2.1:GFP-positive progenitors, including cells with telencephalic identity, by fluorescence-activated cell sorting. These hESC-derived ventral forebrain progenitors are suitable candidates for cell-based therapies that aim at replacing dysfunctional or damaged cortical or hippocampal GABAergic interneurons.

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“…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)(29)(30). A putative function of the rich variety of interneurons is temporal organization of principal cell spiking (29)(30)(31)(32). We tested the "localcircuit" hypothesis by comparing the probability of participation and sequential firing of CA1 neurons during theta oscillations, natural spontaneous ripple events, and "synthetic" ripples induced by local optogenetic activation of pyramidal neurons.…”

mentioning

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.

103

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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...

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Mechanisms of Inhibition within the Telencephalon: “Where the Wild Things Are”

Cited by 219 publications

References 223 publications

VIP+ interneurons control neocortical activity across brain states

VIP+ interneurons control neocortical activity across brain states

Derivation and Isolation of NKX2.1-Positive Basal Forebrain Progenitors from Human Embryonic Stem Cells

Local generation of multineuronal spike sequences in the hippocampal CA1 region

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