A Novel Functionally Distinct Subtype of Striatal Neuropeptide Y Interneuron

Ibáñez-Sandoval, Osvaldo; Tecuapetla, Fatuel; Ünal, Bengi; Shah, Fulva; Koós, Tibor; Tepper, James M.

doi:10.1523/jneurosci.2628-11.2011

Cited by 130 publications

(205 citation statements)

References 57 publications

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“…3 and 7). Although NPY-NGF interneurons are sparsely distributed in the striatum, considering the reported high-connectivity to SPNs (∼60-87%) (26,55), single NPY-NGF interneurons might possess more powerful inhibition to the striatal network than we expected.…”

Section: Discussionmentioning

confidence: 60%

“…Therefore, dendritic plateau potentials could be sustained despite FS-mediated inhibition. Another interesting finding is the very effective inhibition mediated by GABAergic IPSCs with slow kinetics, presumably mediated by NPY-NGF interneurons (26,55). Dendritic slow GABAergic IPSCs showed the strongest efficacy in dendritic inhibition (Figs.…”

Section: Discussionmentioning

confidence: 91%

“…To model the inhibition generated by the striatal inhibitory microcircuits, we modified the channel kinetics of unitary GABAergic synaptic conductances to mimic different inhibitory inputs ( Fig. 3B) (18,19): (i) FS-mediated perisomatic inhibition (FS GABA), (ii) SPN and LTS interneuron-mediated dendritic inhibition with fast kinetics (fast GABA), and (iii) NPY-expressing neurogilaform (NPY-NGF) interneuron-mediated dendritic inhibition with slow kinetics (slow GABA) (26,39,40). We first monitored the membrane potential perturbations (ΔVm) caused by inhibition with different delay timing (Δt Inh ) on plateau potentials (Fig.…”

Section: Model Predicts a Unique Spatiotemporal Window For Cell-type-mentioning

confidence: 99%

“…GABAergic SPNs receive perisomatic inhibition mediated by parvalbumin (PV)-positive fast-spiking (FS) interneurons (20)(21)(22), as well as dendritically targeted inhibition from somatostatin (SST)-and neuropeptide Y (NPY)-positive lowthreshold spike (LTS) interneurons (23)(24)(25)(26)(27) and dendritically targeted collateral inhibition from neighboring SPNs (22,28,29). How somatic and dendritic inhibition interacts with nonlinear integration of excitatory inputs in the presence of dendritic plateau potentials remains largely unexplored (30,31).…”

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confidence: 99%

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Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Lindroos

et al. 2017

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

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Striatal spiny projection neurons (SPNs) receive convergent excitatory synaptic inputs from the cortex and thalamus. Activation of spatially clustered and temporally synchronized excitatory inputs at the distal dendrites could trigger plateau potentials in SPNs. Such supralinear synaptic integration is crucial for dendritic computation. However, how plateau potentials interact with subsequent excitatory and inhibitory synaptic inputs remains unknown. By combining computational simulation, two-photon imaging, optogenetics, and dualcolor uncaging of glutamate and GABA, we demonstrate that plateau potentials can broaden the spatiotemporal window for integrating excitatory inputs and promote spiking. The temporal window of spiking can be delicately controlled by GABAergic inhibition in a celltype-specific manner. This subtle inhibitory control of plateau potential depends on the location and kinetics of the GABAergic inputs and is achieved by the balance between relief and reestablishment of NMDA receptor Mg 2+ block. These findings represent a mechanism for controlling spatiotemporal synaptic integration in SPNs.O ne of the principal functions of neurons is to integrate excitatory and inhibitory synaptic inputs and transform subthreshold membrane potential fluctuations into suprathreshold spiking activities. Both theoretical and experimental works have proposed that a single neuron can process inputs as a multilayer computational device in which individual dendritic branches function as a computational unit and can generate dendritic spikes or plateau potentials (1-4). In vivo studies have demonstrated that dendritic plateau potentials evoked by coincident inputs can amplify excitatory signals and enhance the capacity of learning and information storage at a specific branch (5-7). However, a majority of the understanding of dendritic computation is based on studies focusing on pyramidal cells of hippocampal and cortical areas. It is relatively less known whether these conclusions apply to the striatal neurons (8).The striatum, the main input nucleus of the basal ganglia, receives convergent glutamatergic inputs from the cortex and thalamus (9-11). The integration of these functionally distinct inputs is critical for fine movement control and action selection (12, 13). The principal neurons in the striatum-spiny projection neurons (SPNs)-display hyperpolarized membrane potentials (∼−80 mV) at rest, often referred to as the "down-state" (14, 15). It is generally believed that coherent cortical inputs can effectively depolarize SPNs and promote membrane potential transitions from a hyperpolarized down-state to a depolarized "up-state" (∼−55 mV), at which point action potentials can be generated (14-16). To achieve this ∼20-to 30-mV state transition, it has been estimated that a large number (hundreds to thousands) of active inputs would be required (14-17). Interestingly, striatal SPNs are capable of producing long-lasting plateau potentials following activation of spatially clustered and temporally synchronized excit...

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Section: Discussionmentioning

confidence: 60%

Section: Discussionmentioning

confidence: 91%

Section: Model Predicts a Unique Spatiotemporal Window For Cell-type-mentioning

confidence: 99%

mentioning

confidence: 99%

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Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Lindroos

et al. 2017

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

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“…Care was taken to distinguish recordings from LTS cells from the neurogliaform interneuron type labeled in the striatum of NPY-GFP mice (Ibáñez-Sandoval et al 2011). LTS cells had ovoid somata and extended, sparsely branched dendritic trees (Fig.…”

Section: Lts Cellsmentioning

confidence: 99%

Cell-type-specific resonances shape the responses of striatal neurons to synaptic input

Beatty

Song

Wilson

2015

Journal of Neurophysiology

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Beatty JA, Song SC, Wilson CJ. Cell-type-specific resonances shape the responses of striatal neurons to synaptic input. J Neurophysiol 113: 688 -700, 2015. First published November 19, 2014 doi:10.1152/jn.00827.2014.-Neurons respond to synaptic inputs in cell-type-specific ways. Each neuron type may thus respond uniquely to shared patterns of synaptic input. We applied statistically identical barrages of artificial synaptic inputs to four striatal cell types to assess differences in their responses to a realistic input pattern. Each interneuron type fired in phase with a specific input-frequency component. The fast-spiking interneuron fired in relation to the gamma-band (and higher) frequencies, the low-threshold spike interneuron to the beta-band frequencies, and the cholinergic neurons to the delta-band frequencies. Low-threshold spiking and cholinergic interneurons showed input impedance resonances at frequencies matching their spiking resonances. Fast-spiking interneurons showed resonance of input impedance but at lower than gamma frequencies. The spiny projection neuron's frequency preference did not have a fixed frequency but instead tracked its own firing rate. Spiny cells showed no input impedance resonance. Striatal interneurons are each tuned to a specific frequency band corresponding to the major frequency components of local field potentials. Their influence in the circuit may fluctuate along with the contribution of that frequency band to the input. In contrast, spiny neurons may tune to any of the frequency bands by a change in firing rate.

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Cell type‐specific distribution of GABA_A receptor subtypes in the mouse dorsal striatum

Boccalaro

Cristiá-Lara

Schwerdel

et al. 2019

J of Comparative Neurology

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The striatum is the main input nucleus of the basal ganglia, mediating motor and cognitive functions. Striatal projection neurons are GABAergic medium spiny neurons (MSN), expressing either the dopamine receptor type 1 (D1‐R MSN) and forming the direct, movement‐promoting pathway, or dopamine receptor type 2 (D2‐R MSN), forming the indirect movement‐suppressing pathway. Locally, activity and synchronization of MSN are modulated by several subtypes of GABAergic and cholinergic interneurons. Overall, GABAergic circuits in the striatum remain poorly characterized, and little is known about the intrastriatal connectivity of interneurons and the distribution of GABAA receptor (GABAAR) subtypes, distinguished by their subunit composition, in striatal synapses. Here, by using immunofluorescence in mouse tissue, we investigated the distribution of GABAARs containing the α1, α2, or α3 subunit in perisomatic synapses of striatal MSN and interneurons, as well as the innervation pattern of D1R‐ and D2R‐MSN soma and axonal initial segment (AIS) by GABAergic and cholinergic interneurons. Our results show that perisomatic GABAergic synapses of D1R‐ and D2R‐MSN contain the GABAAR α1 and/or α2 subunits, but not the α3 subunit; D2R‐MSN have significantly more α1‐GABAARs on their soma than D1R‐MSN. Further, interneurons have few perisomatic synapses containing α2‐GABAARs, whereas α3‐GABAARs (along with the α1‐GABAARs) are abundant in perisomatic synapses of CCK+, NPY+/SOM+, and vAChT+ interneurons. Each MSN and interneuron population analyzed received a distinct pattern of GABAergic and cholinergic innervation, complementing this postsynaptic heterogeneity. In conclusion, intra‐striatal GABAergic circuits are distinguished by cell‐type specific innervation patterns, differential expression and postsynaptic targeting of GABAAR subtypes.

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A Novel Functionally Distinct Subtype of Striatal Neuropeptide Y Interneuron

Cited by 130 publications

References 57 publications

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Cell-type-specific resonances shape the responses of striatal neurons to synaptic input

Cell type‐specific distribution of GABA_A receptor subtypes in the mouse dorsal striatum

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A Novel Functionally Distinct Subtype of Striatal Neuropeptide Y Interneuron

Cited by 130 publications

References 57 publications

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Cell-type–specific inhibition of the dendritic plateau potential in striatal spiny projection neurons

Cell-type-specific resonances shape the responses of striatal neurons to synaptic input

Cell type‐specific distribution of GABAA receptor subtypes in the mouse dorsal striatum

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Cell type‐specific distribution of GABA_A receptor subtypes in the mouse dorsal striatum