Rapid Reversal of Chondroitin Sulfate Proteoglycan Associated Staining in Subcompartments of Mouse Neostriatum during the Emergence of Behaviour

Lee, Hyunchul; Leamey, Catherine A.; Sawatari, Atomu

doi:10.1371/journal.pone.0003020

Cited by 19 publications

(39 citation statements)

References 114 publications

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“…Large gaps in their distribution were observed, consistent with their relative avoidance of striosomes [25]. A small effect was detected across the rostrocaudal axis (number/mm 2 , mean ± standard error: rostral (R): 26.897±2.413; middle (Mi): 35.104±0.94; caudal (C): 33.889±3.221; RMANOVA, F (2,4) = 7.992, P = 0.04; Fig.…”

Section: Resultssupporting

confidence: 59%

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Perineuronal Nets Play a Role in Regulating Striatal Function in the Mouse

Lee¹,

Leamey²,

Sawatari

2012

PLoS ONE

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The striatum is the primary input nucleus of the basal ganglia, a collection of nuclei that play important roles in motor control and associative learning. We have previously reported that perineuronal nets (PNNs), aggregations of chondroitin-sulfate proteoglycans (CSPGs), form in the matrix compartment of the mouse striatum during the second postnatal week. This period overlaps with important developmental changes, including the attainment of an adult-like gait. Here, we investigate the identity of the cells encapsulated by PNNs, characterize their topographical distribution and determine their function by assessing the impact of enzymatic digestion of PNNs on two striatum-dependent behaviors: ambulation and goal-directed spatial learning. We show PNNs are more numerous caudally, and that a substantial fraction (41%) of these structures surrounds parvalbumin positive (PV+) interneurons, while approximately 51% of PV+ cells are ensheathed by PNNs. The colocalization of these structures is greatest in dorsal, lateral and caudal regions of the striatum. Bilateral digestion of striatal PNNs led to an increase in both the width and variability of hind limb gait. Intriguingly, this also resulted in an improvement in the acquisition rate of the Morris water maze. Together, these data show that PNNs are associated with specific elements of striatal circuits and play a key role in regulating the function of this important structure in the mouse.

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Section: Resultssupporting

confidence: 59%

“…PNN formation within the postnatal developing striatum coincides with a transition from an immature, predominantly forelimb dependent ‘crawl’ to a more mature gait in mice [25]. This tight temporal relationship suggests that PNNs may play a vital role in consolidating the circuits necessary for the control of adult-like limb movements.…”

Section: Resultsmentioning

confidence: 97%

Perineuronal Nets Play a Role in Regulating Striatal Function in the Mouse

Lee¹,

Leamey²,

Sawatari

2012

PLoS ONE

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“…series showing the pattern of CSPG staining in the striatum at P10 in non-enriched mice. CSPG staining in the striatum is most prominent in diffuse clouds (some highlighted by arrows) which we have previously shown to be associated with striosomes [36]. PNNs, characterised by more punctuate staining, can also be seen in the matrix (arrowheads) but these are present at very low density.…”

Section: Resultsmentioning

confidence: 86%

“…At this stage the density of PNNs is low, but this increases rapidly over the ensuing days [36]. The time course of the appearance of striatal PNNs overlaps with the period when rodent pups begin to walk consistently with all four limbs [29], [31], [51] and with the transition to a more adult-like swimming behaviour [48]–[50].…”

Section: Resultsmentioning

confidence: 93%

Enrichment from Birth Accelerates the Functional and Cellular Development of a Motor Control Area in the Mouse

et al. 2009

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BackgroundThere is strong evidence that sensory experience in early life has a profound influence on the development of sensory circuits. Very little is known, however, about the role of experience in the early development of striatal networks which regulate both motor and cognitive function. To address this, we have investigated the influence of early environmental enrichment on motor development.Methodology/Principal FindingsMice were raised in standard or enriched housing from birth. For animals assessed as adults, half of the mice had their rearing condition reversed at weaning to enable the examination of the effects of pre- versus post-weaning enrichment. We found that exclusively pre-weaning enrichment significantly improved performance on the Morris water maze compared to non-enriched mice. The effects of early enrichment on the emergence of motor programs were assessed by performing behavioural tests at postnatal day 10. Enriched mice traversed a significantly larger region of the test arena in an open-field test and had improved swimming ability compared to non-enriched cohorts. A potential cellular correlate of these changes was investigated using Wisteria-floribunda agglutinin (WFA) staining to mark chondroitin-sulfate proteoglycans (CSPGs). We found that the previously reported transition of CSPG staining from striosome-associated clouds to matrix-associated perineuronal nets (PNNs) is accelerated in enriched mice.Conclusions/SignificanceThis is the first demonstration that the early emergence of exploratory as well as coordinated movement is sensitive to experience. These behavioural changes are correlated with an acceleration of the emergence of striatal PNNs suggesting that they may consolidate the neural circuits underlying these behaviours. Finally, we confirm that pre-weaning experience can lead to life long changes in the learning ability of mice.

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“…, 2005; Chesselet et al. , 2007) and the appearance of perineuronal nets (PNNs) (Lee et al. , 2008).…”

Section: Introductionmentioning

confidence: 99%

Medium spiny neurons of the neostriatal matrix exhibit specific, stereotyped changes in dendritic arborization during a critical developmental period in mice

Lee¹,

Sawatari²

2011

Eur J of Neuroscience

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In mice, the matrix compartment of the striatum (caudate/putamen) undergoes major developmental changes during the second postnatal week, including the establishment of corticostriatal and nigrostriatal afferents, the maturation of parvalbumin-positive interneurons and the appearance of perineuronal nets. It is not known if any of these events influence the dendritic structure of medium spiny neurons, the principal output cells of the striatum. To determine whether any measurable changes in the dendrites of matrix medium spiny neurons occur during this important developmental period, we labeled individual cells at different time points flanking the second postnatal week. These cells exhibit distinct dendritic morphologies from the earliest postnatal time points examined. Furthermore, our data show that the dendritic arbors of these neurons change in length, branch points, diameter and tortuosity, regardless of morphological type. The increase in dendritic length is accompanied by a decrease in the number of branch points that occur in different, but consistent, parts of the dendritic arbor. All of these changes are most pronounced during the second postnatal week, coinciding with a number of developmental events considered important for consolidating circuitry within the striatal matrix. Our results further support the critical importance of this early postnatal period in striatal development.

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Rapid Reversal of Chondroitin Sulfate Proteoglycan Associated Staining in Subcompartments of Mouse Neostriatum during the Emergence of Behaviour

Cited by 19 publications

References 114 publications

Perineuronal Nets Play a Role in Regulating Striatal Function in the Mouse

Perineuronal Nets Play a Role in Regulating Striatal Function in the Mouse

Enrichment from Birth Accelerates the Functional and Cellular Development of a Motor Control Area in the Mouse

Medium spiny neurons of the neostriatal matrix exhibit specific, stereotyped changes in dendritic arborization during a critical developmental period in mice

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