Conserved properties of dendritic trees in four cortical interneuron subtypes

Kubota, Yoshihiro; Karube, Fuyuki; Nomura, Masaki; Gulledge, Allan T.; Mochizuki, Atsushi; Schertel, Andreas; Kawaguchi, Yasuo

doi:10.1038/srep00089

Cited by 60 publications

(54 citation statements)

References 28 publications

(42 reference statements)

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“…Tissue was then flat-embedded in Epon. Four dendritic segments with identifiable DAB staining were relocated and then further investigated using a combined FIB/SEM (Focused Ion Beam / Scanning Electron Microscope)(Kubota et al, 2011). For EM observation, the Epon block containing the dendritic segments was glued to a stainless-steel sample holder using silver paste to avoid charging the epoxy.…”

Section: Methodsmentioning

confidence: 99%

Inhibitory Synapses Are Repeatedly Assembled and Removed at Persistent Sites In Vivo

Villa

Berry

Subramanian

et al. 2016

Neuron

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180

175

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Summary Older concepts of a hard-wired adult brain have been overturned in recent years by in vivo imaging studies revealing synaptic remodeling, now thought to mediate rearrangements in microcircuit connectivity. Using three-color labeling and spectrally resolved two-photon microscopy, we monitor in parallel the daily structural dynamics (assembly or removal) of excitatory and inhibitory postsynaptic sites on the same neurons in mouse visual cortex in vivo. We find that dynamic inhibitory synapses often disappear and reappear again in the same location. The starkest contrast between excitatory and inhibitory synapse dynamics is on dually innervated spines, where inhibitory synapses frequently recur while excitatory synapses are stable. Monocular deprivation, a model of sensory input-dependent plasticity, shortens inhibitory synapse lifetimes and lengthens intervals to recurrence, resulting in a new dynamic state with reduced inhibitory synaptic presence. Reversible structural dynamics indicates a fundamentally new role for inhibitory synaptic remodeling – flexible, input-specific modulation of stable excitatory connections.

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Section: Methodsmentioning

confidence: 99%

Inhibitory Synapses Are Repeatedly Assembled and Removed at Persistent Sites In Vivo

Villa

Berry

Subramanian

et al. 2016

Neuron

Self Cite

180

175

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“…We also examined the spread of perisomatic inhibition. The fact that signal attenuation is much weaker in the outward direction means that perisomatic inputs (or any signal that reaches the soma) have a more global effect (Kubota et al, 2011, 2015), even in the HCS. In the silent case inhibition completely propagated into all compartments for the PV and CCK cells and it spread reasonably well in the PC and CR cell as well ( Figure 8D ).…”

Section: Resultsmentioning

confidence: 99%

The Effects of Realistic Synaptic Distribution and 3D Geometry on Signal Integration and Extracellular Field Generation of Hippocampal Pyramidal Cells and Inhibitory Neurons

Gulyás

Freund

Káli

2016

Front. Neural Circuits

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In vivo and in vitro multichannel field and somatic intracellular recordings are frequently used to study mechanisms of network pattern generation. When interpreting these data, neurons are often implicitly considered as electrotonically compact cylinders with a homogeneous distribution of excitatory and inhibitory inputs. However, the actual distributions of dendritic length, diameter, and the densities of excitatory and inhibitory input are non-uniform and cell type-specific. We first review quantitative data on the dendritic structure and synaptic input and output distribution of pyramidal cells (PCs) and interneurons in the hippocampal CA1 area. Second, using multicompartmental passive models of four different types of neurons, we quantitatively explore the effect of differences in dendritic structure and synaptic distribution on the errors and biases of voltage clamp measurements of inhibitory and excitatory postsynaptic currents. Finally, using the 3-dimensional distribution of dendrites and synaptic inputs we calculate how different inhibitory and excitatory inputs contribute to the generation of local field potential in the hippocampus. We analyze these effects at different realistic background activity levels as synaptic bombardment influences neuronal conductance and thus the propagation of signals in the dendritic tree. We conclude that, since dendrites are electrotonically long and entangled in 3D, somatic intracellular and field potential recordings miss the majority of dendritic events in some cell types, and thus overemphasize the importance of perisomatic inhibitory inputs and belittle the importance of complex dendritic processing. Modeling results also suggest that PCs and inhibitory neurons probably use different input integration strategies. In PCs, second- and higher-order thin dendrites are relatively well-isolated from each other, which may support branch-specific local processing as suggested by studies of active dendritic integration. In the electrotonically compact parvalbumin- and cholecystokinincontaining interneurons, synaptic events are visible in the whole dendritic arbor, and thus the entire dendritic tree may form a single integrative element. Calretinin-containing interneurons were found to be electrotonically extended, which suggests the possibility of complex dendritic processing in this cell type. Our results also highlight the need for the integration of methods that allow the measurement of dendritic processes into studies of synaptic interactions and dynamics in neural networks.

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“…NGFCs have been described in all layers, but might be more prevalent in supragranular layers and are a major component of L1. The neurogliaform morphology has often been associated with a late-spiking (LS) firing pattern, characterized by a slow ramp depolarization preceding firing and non-adapting spike trains near threshold (Hestrin and Armstrong, 1996; Kawaguchi, 1995; Kubota et al, 2011a; Olah et al, 2009; Tamas et al, 2003). During larger suprathreshold depolarizations, the cells fire adapting spike trains (Kawaguchi and Kubota, 1997; Tamas et al, 2003).…”

Section: Interneuron Diversity In the Neocortexmentioning

confidence: 99%

GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits

Tremblay

Lee

Rudy

2016

Neuron

1,631

1,830

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Cortical networks are composed of glutamatergic excitatory projection neurons and local GABAergic inhibitory interneurons which gate signal flow and sculpt network dynamics. Although they represent a minority of the total neocortical neuronal population, GABAergic interneurons are highly heterogeneous, forming functional classes based on their morphological, electrophysiological and molecular features as well as connectivity and in vivo patterns of activity. Here we review our current understanding of neocortical interneuron diversity and the properties that distinguish among cell types. We then discuss how the involvement of multiple cell types, each with a specific set of cellular properties, plays a crucial role in diversifying and increasing the computational power of a relatively small number of simple circuit motifs forming cortical networks. We illustrate how recent advances in the field have shed light onto the mechanisms by which GABAergic inhibition contributes to network operations.

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Conserved properties of dendritic trees in four cortical interneuron subtypes

Cited by 60 publications

References 28 publications

Inhibitory Synapses Are Repeatedly Assembled and Removed at Persistent Sites In Vivo

Inhibitory Synapses Are Repeatedly Assembled and Removed at Persistent Sites In Vivo

The Effects of Realistic Synaptic Distribution and 3D Geometry on Signal Integration and Extracellular Field Generation of Hippocampal Pyramidal Cells and Inhibitory Neurons

GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits

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