Extracellular Molecular Markers and Soma Size of Inhibitory Neurons: Evidence for Four Subtypes of GABAergic Cells in the Inferior Colliculus

Beebe, Nichole L.; Young, Jesse W.; Mellott, Jeffrey G.; Schofield, Brett R.

doi:10.1523/jneurosci.0217-16.2016

Cited by 58 publications

(93 citation statements)

References 50 publications

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“…Although the expression of PNN and its association with specific cell types have been well characterized in rodent visual and somatosensory cortex (Pizzorusso et al, 2002; McRae et al, 2007; Liu et al, 2013; Takesian and Hensch, 2013) and subcortical auditory areas (Beebe et al, 2016), the expression patterns in A1 are only beginning to be described (reviewed in Sonntag et al, 2015). The relationship between PV and PNN expression in A1 has not been previously characterized.…”

Section: Discussionmentioning

confidence: 99%

Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice

Brewton

Kokash

Jimenez

et al. 2016

Front. Aging Neurosci.

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Age-related changes in inhibitory neurotransmission in sensory cortex may underlie deficits in sensory function. Perineuronal nets (PNNs) are extracellular matrix components that ensheath some inhibitory neurons, particularly parvalbumin positive (PV+) interneurons. PNNs may protect PV+ cells from oxidative stress and help establish their rapid spiking properties. Although PNN expression has been well characterized during development, possible changes in aging sensory cortex have not been investigated. Here we tested the hypothesis that PNN+, PV+ and PV/PNN co-localized cell densities decline with age in the primary auditory cortex (A1). This hypothesis was tested using immunohistochemistry in two strains of mice (C57BL/6 and CBA/CaJ) with different susceptibility to age-related hearing loss and at three different age ranges (1–3, 6–8 and 14–24 months old). We report that PNN+ and PV/PNN co-localized cell densities decline significantly with age in A1 in both mouse strains. In the PNN+ cells that remain in the old group, the intensity of PNN staining is reduced in the C57 strain, but not the CBA strain. PV+ cell density also declines only in the C57, but not the CBA, mouse suggesting a potential exacerbation of age-effects by hearing loss in the PV/PNN system. Taken together, these data suggest that PNN deterioration may be a key component of altered inhibition in the aging sensory cortex, that may lead to altered synaptic function, susceptibility to oxidative stress and processing deficits.

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Section: Discussionmentioning

confidence: 99%

Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice

Brewton

Kokash

Jimenez

et al. 2016

Front. Aging Neurosci.

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“…IC GABAergic neurons can be classified into four types using the presence/absence of VGLUT2+ axosomatic rings and perineuronal nets (Beebe et al . ), and in the study, the authors found that the majority of GABAergic neurons without axosomatic rings (i.e. SG cells) are not covered with perineuronal nets, whereas most LG neurons were covered with perineuronal nets, suggesting a difference in plastic ability between SG and LG cells.…”

Section: Discussionmentioning

confidence: 79%

“…; Beebe et al . ). Recently, Goyer and colleagues () found a subgroup of GLU cells which express VIP, have a less‐flat dendritic field, and show a gradient of intrinsic membrane properties inside the ICC.…”

Section: Discussionmentioning

confidence: 97%

Different coding strategy of sound information between GABAergic and glutamatergic neurons in the auditory midbrain

Ito

2020

The Journal of Physiology

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Key points In the central nucleus of the inferior colliculus (ICC), which acts as the hub of the auditory pathways, how the sound is coded by distinct cell types is largely unknown. Large GABAergic cells are tuned broadly to pure tones and respond more strongly to frequency‐modulated sweeps than small GABAergic and glutamatergic (GLU) cells. Neurons, especially GLU cells, which share sharpness of tuning and sweep sensitivity, were spatially clustered inside the ICC. The difference in responsiveness between cell types was partially explained by the morphology of dendritic trees and the spatial distributions of excitatory and inhibitory inputs. The results suggest that each ICC cell type has a particular sound‐encoding strategy, which is partially determined by the morphological characteristics and location of cells, and contributes information coding in higher centres in different ways. Abstract The rules governing the encoding of sound information in the higher auditory centres are largely unknown. In the central nucleus of the inferior colliculus (ICC), which acts as the hub of the auditory pathways, the presence of functional maps other than tonotopicity has been suggested but not established, due to significant heterogeneity in the response properties of single microdomains. Since each ICC cell type has distinct neuronal circuitry, each cell type might encode sound information differently. Here, juxtacellular recording from rat ICC of both sexes revealed that large GABAergic (LG), small GABAergic (SG) and glutamatergic (GLU) cells encode sound information differently. LG cells are broadly tuned and respond more strongly to frequency‐modulated sweeps than SG and GLU cells. At a population level, responsiveness to sweeps is location dependent: the responsiveness to sweeps is shared in local clusters of GLU cells, whereas that to directional selectivity of sweeps is shared in local clusters of LG cells. The difference in responsiveness between cell types was partially explained by the morphology of dendritic trees and the spatial distributions of excitatory and inhibitory inputs. LG neurons had a dense local axonal plexus with projection fibres to multiple distant targets, whereas GLU projection neurons mainly aimed at a single, distant target and had less dense local collaterals. These results suggest that each ICC cell type has a particular sound‐encoding strategy, which is partially determined by the morphological characteristics and location of the cell, and the different cell types contribute information coding in higher centres in different ways.

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“…GABAergic IC neurons were shown to be classified based on their cell body size (Ito et al, ; Beebe et al, ). We therefore measured the perimeter of two types of GABAergic neurons in young adult mice: PV + /NOS − /GAD67 + neurons (DC, n = 74 cells; LC, n = 79 cells; ICC, n = 78 cells) and PV + /NOS + /GAD67 + neurons (DC, n = 13 cells; LC, n = 15 cells; ICC, n = 75 cells).…”

Section: Resultsmentioning

confidence: 99%

“…6A): PV 1 /NOS 2 / GAD67 1 neurons, PV 1 /NOS 1 /GAD67 1 neurons, PV 1 / NOS 2 /GAD67 2 neurons, and PV 2 /NOS 1 /GAD67 2 neurons. In all three subdivisions of the IC, the largest population was PV 2 /NOS 1 /GAD67 2 neurons ( GABAergic IC neurons were shown to be classified based on their cell body size (Ito et al, 2009;Beebe et al, 2016). We therefore measured the perimeter of two types of GABAergic neurons in young adult mice: PV 1 /NOS 2 /GAD67 1 neurons (DC, n 5 74 cells; LC, n 5 79 cells; ICC, n 5 78 cells) and PV 1 /NOS 1 / GAD67 1 neurons (DC, n 5 13 cells; LC, n 5 15 cells; ICC, n 5 75 cells).…”

Section: Comparisons Of the Four Types Of Ic Neurons Defined By Pv Nmentioning

confidence: 99%

Late postnatal shifts of parvalbumin and nitric oxide synthase expression within the GABAergic and glutamatergic phenotypes of inferior colliculus neurons

Fujimoto

Konno

Watanabe

et al. 2016

J of Comparative Neurology

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The inferior colliculus (IC) is partitioned into three subdivisions: the dorsal and lateral cortices (DC and LC) and the central nucleus (ICC), and serves as an integration center of auditory information. Recent studies indicate that a certain population of IC neurons may represent the non-GABAergic phenotype, while they express well-established cortical/hippocampal GABAergic neuron markers. In this study we used the optical disector to investigate the phenotype of IC neurons expressing parvalbumin (PV) and/or nitric oxide synthase (NOS) in C57BL/6J mice during the late postnatal period. Four major types of IC neurons were defined by the presence (+) or absence (-) of PV, NOS, and glutamic acid decarboxylase 67 (GAD67): PV /NOS /GAD67 , PV /NOS /GAD67 , PV /NOS /GAD67 , and PV /NOS /GAD67 . Fluorescent in situ hybridization for vesicular glutamate transporter 2 mRNA indicated that almost all GAD67 IC neurons represented the glutamatergic phenotype. The numerical densities (NDs) of total GAD67 IC neurons remained unchanged in all subdivisions. The NDs of PV /NOS /GAD67 neurons and PV /NOS /GAD67 neurons were reduced with age in the ICC, while they remained unchanged in the DC and LC. By contrast, the NDs of PV /NOS /GAD67 neurons and PV /NOS /GAD67 neurons were increased with age in the ICC, although there were no changes in the DC and LC. The cell body size of GAD67 IC neurons did not vary according to the expression of PV with or without NOS. The present findings indicate that the expression of PV and NOS may shift with age within the GABAergic and glutamatergic phenotypes of IC neurons during the late postnatal period. J. Comp. Neurol. 525:868-884, 2017. © 2016 Wiley Periodicals, Inc.

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Extracellular Molecular Markers and Soma Size of Inhibitory Neurons: Evidence for Four Subtypes of GABAergic Cells in the Inferior Colliculus

Cited by 58 publications

References 50 publications

Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice

Age-Related Deterioration of Perineuronal Nets in the Primary Auditory Cortex of Mice

Different coding strategy of sound information between GABAergic and glutamatergic neurons in the auditory midbrain

Late postnatal shifts of parvalbumin and nitric oxide synthase expression within the GABAergic and glutamatergic phenotypes of inferior colliculus neurons

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