Age-dependent and region-specific alteration of parvalbumin neurons and perineuronal nets in the mouse cerebral cortex

Ueno, Hiroshi; Takao, Keizo; Suemitsu, Shunsuke; Murakami, Shinji; Kitamura, Naoya; Wani, Kenta; Okamoto, Masahiro; Aoki, Shozo; Ishihara, Takeshi

doi:10.1016/j.neuint.2017.11.001

Cited by 62 publications

(53 citation statements)

References 49 publications

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“…One limitation of this study was the limited sample size, and it is likely that the abundance of PNNs in the CA1 of adult females would also be significantly lower than adult males with a larger sample size. Both parvalbumin and PNN development are highly region‐specific (Ueno et al, ); however, in most cases PVALB+ neurons increase with age. Our finding that juvenile rats had nearly twice the number of PVALB+ interneurons in the neocortex compared to adults is in sharp contrast to many previous studies, however it is consistent with a prior report in the barrel cortex of mice (Nowicka, Soulsby, Skangiel‐Kramska, & Glazewski, ).…”

Section: Discussionmentioning

confidence: 99%

Age‐dependent sexual dimorphism in hippocampal cornu ammonis‐1 perineuronal net expression in rats

et al. 2019

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Introduction Perineuronal nets (PNNs) are extracellular matrices that encompass parvalbumin‐expressing parvalbumin positive (PVALB+) fast‐spiking inhibitory interneurons where they protect and stabilize afferent synapses. Recent observations that gonadal hormones influence PVALB+ neuron development suggest that PNN regulation may be sexually dimorphic. Sex differences in PNN abundance and complexity have been reported in sexually dimorphic nuclei in zebra finch brains; however, corresponding differences in mammalian brains have not been investigated. Methods In this study we assessed the number of cortical and hippocampal PNNs in juvenile and young adult male and female rats using fluorescent immunohistochemistry for PVALB and the PNN marker Wisteria Floribunda Lectin. Results We report here that PNNs are numerous and well developed in hippocampal cornu ammonis‐1 of adult males but are lower in juvenile and possibly adult females. No significant differences were observed between sexes in cornu ammonis‐3 or adjacent neocortex. There was an observed developmental difference in the neocortex as juveniles had more PVALB+ cells, but fewer PNN+ cells, than adults. Conclusions Because PNNs are integral for several hippocampal‐mediated learning and memory tasks, these observations have potential sex‐dependent translational implications for clinical strategies targeting cognitive dysfunction.

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Section: Discussionmentioning

confidence: 99%

Age‐dependent sexual dimorphism in hippocampal cornu ammonis‐1 perineuronal net expression in rats

et al. 2019

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“…In the case of targeted transduction of PV interneurons, only mCherry+ (DREADD-expressing) or GFP+ (expressing PSAM-GlyR) cells were analyzed ipsilaterally. The region analyzed in V1 was selected using a 20X objective, based on conspicuously low WFA staining in V2 area [ Fig.S1, (Ueno et al, 2018)], as delineated by Paxinos and Franklin (Paxinos and Franklin, 2004). Images were acquired in layers IV-V using a 63X objective, starting medially from the V2/V1 border and progressing laterally into V1 through contiguous acquisition fields.…”

Section: Pnn Density Analysesmentioning

confidence: 99%

Regulation of perineuronal nets in the adult cortex by the electrical activity of parvalbumin interneurons

Devienne

Picaud

Cohen

et al. 2019

Preprint

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Perineuronal net (PNN) accumulation around parvalbumin-expressing (PV) inhibitory interneurons marks the closure of critical periods of high plasticity, whereas PNN removal reinstates juvenile plasticity in the adult cortex. Using targeted chemogenetic in vivo approaches in the adult mouse visual cortex, we found that transient electrical silencing of PV interneurons, directly or through inhibition of local excitatory neurons, induced PNN regression. Conversely, excitation of either neuron types did not reduce the PNN. We also observed that chemogenetically inhibited PV interneurons exhibited reduced PNN compared to their untransduced neighbors, and confirmed that single PV interneurons express multiple genes enabling cell-autonomous control of their own PNN density. Our results indicate that PNNs are dynamically regulated in the adult by PV neurons acting as sensors of their local microcircuit activities. PNN regulation provides individual PV neurons with an activitydependent mechanism to control the local remodeling of adult cortical circuits.

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“…An excellent example is the primary visual cortex where the developmental increase of PNNs is regulated by visual experience (Beurdeley et al, 2012;Hou et al, 2017). PNNs in mature primary visual cortex mainly surround the soma and proximal dendrites of PV+ interneurons (Celio, 1993;Hartig et al, 1992;Ueno et al, 2018). Mature PNNs are thought to be inhibitory for experience-dependent plasticity, as their increase in developing primary visual cortex correlates with the termination of the critical period and PNN removal in adult primary visual cortex restores plasticity, as measured by ocular dominance plasticity assays (Bavelier et al, 2010;Pizzorusso et al, 2002Pizzorusso et al, , 2006.…”

Section: Discussionmentioning

confidence: 99%

“…Perineuronal nets (PNNs) are specialized extracellular matrix structures that can act as physical barriers or modulators of plasticity, restrict axon regeneration, and form molecular brakes that actively control synaptic maturation and the function of cortical parvalbumin+ (PV+) GABAergic interneurons that drive gamma oscillations (Bartos et al, 2002;Begum and Sng, 2017;Bernard and Prochiantz, 2016;Carstens et al, 2016;Deepa et al, 2002;Dityatev et al, 2007;Donato et al, 2013;Durand et al, 2012;Frischknecht et al, 2009;Gundelfinger et al, 2010;Hartig et al, 1992;Hou et al, 2017;Kalemaki et al, 2018;Kosaka and Heizmann, 1989;Krishnan et al, 2015Krishnan et al, , 2017Nakagawa et al, 1986;Orlando et al, 2012;Pizzorusso et al, 2002Pizzorusso et al, , 2006Sigal et al, 2019;Sugiyama et al, 2009;Suttkus et al, 2012;Ueno et al, 2018;Vo et al, 2013;de Winter et al, 2016;Ye and Miao, 2013). Mature PNNs in the adult cortices are thought to be stable structures, inhibitory to plasticity, and perhaps play roles in long term memory such as "engrams" (Carstens et al, 2016;Gogolla et al, 2009;Thompson et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

Lateralized expression of cortical perineuronal nets during maternal experience is dependent on MECP2

Lau

Layo

Emery

et al. 2019

Preprint

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Cortical neuronal circuits along the sensorimotor pathways are shaped by experience during critical periods of heightened plasticity in early postnatal development. After closure of critical periods, measured histologically by the formation and maintenance of extracellular matrix structures called perineuronal nets (PNNs), the adult mouse brain exhibits restricted plasticity and maturity. Mature PNNs are typically considered to be stable structures that restrict synaptic plasticity on cortical parvalbumin+ GABAergic neurons. Changes in environment (i.e. novel behavioral training) or social contexts (i.e. motherhood) are known to elicit synaptic plasticity in relevant neural circuitry. However, little is known about concomitant changes in the PNNs surrounding the cortical parvalbumin+ GABAergic neurons. Here, we show novel changes in PNN density in the primary somatosensory cortex (SS1) of adult female mice after maternal experience, using systematic microscopy analysis of a whole brain region. On average, PNNs were increased in the right barrel field and decreased in the left forelimb regions. Individual mice had left hemisphere dominance in PNN density. Using adult female mice deficient in methyl-CpG-binding protein 2 (MECP2), an epigenetic regulator involved in regulating experience-dependent plasticity, we found that MECP2 is critical for this precise and dynamic expression of PNN. Adult naïve Mecp2-heterozygous females (Het) had increased PNN density in specific subregions in both hemispheres before maternal experience. The laterality in PNN expression seen in naïve Het was lost after maternal experience, suggesting possible intact mechanisms for plasticity. Together, our results identify subregion and hemisphere-specific alterations in PNN expression in adult females, suggesting extracellular matrix plasticity as a possible neurobiological mechanism for adult behaviors in rodents.

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Age-dependent and region-specific alteration of parvalbumin neurons and perineuronal nets in the mouse cerebral cortex

Cited by 62 publications

References 49 publications

Age‐dependent sexual dimorphism in hippocampal cornu ammonis‐1 perineuronal net expression in rats

Age‐dependent sexual dimorphism in hippocampal cornu ammonis‐1 perineuronal net expression in rats

Regulation of perineuronal nets in the adult cortex by the electrical activity of parvalbumin interneurons

Lateralized expression of cortical perineuronal nets during maternal experience is dependent on MECP2

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