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Rapid reversal of chondroitin sulfate proteoglycan associated staining in subcompartments of mouse neostriatum during the emergence of behaviour.

Lee H, Leamey CA, Sawatari A - PLoS ONE (2008)

Bottom Line: Remarkably, the PNNs overlap almost exclusively with the neostriatal matrix.This is the first description of a reversal in the distribution of CSPG associated structures, as well as the emergence and maintenance of PNNs in specific subcompartments of the neostriatum.These results suggest diverse roles for CSPGs in the formation of functional corticostriatal and nigrostriatal connectivity within the striosome and matrix compartments of the developing caudate/putamen.

View Article: PubMed Central - PubMed

Affiliation: Discipline of Physiology, School of Medical Sciences and the Bosch Institute, University of Sydney, Sydney, Australia.

ABSTRACT

Background: The neostriatum, the mouse homologue of the primate caudate/putamen, is the input nucleus for the basal ganglia, receiving both cortical and dopaminergic input to each of its sub-compartments, the striosomes and matrix. The coordinated activation of corticostriatal pathways is considered vital for motor and cognitive abilities, yet the mechanisms which underlie the generation of these circuits are unknown. The early and specific targeting of striatal subcompartments by both corticostriatal and nigrostriatal terminals suggests activity-independent mechanisms, such as axon guidance cues, may play a role in this process. Candidates include the chondroitin sulfate proteoglycan (CSPG) family of glycoproteins which have roles not only in axon guidance, but also in the maturation and stability of neural circuits where they are expressed in lattice-like perineuronal nets (PNNs).

Methodology/principal findings: The expression of CSPG-associated structures and PNNs with respect to neostriatal subcompartments has been examined qualitatively and quantitatively using double-labelling for Wisteria floribunda agglutinin (WFA), and the mu-opioid receptor (muOR), a marker for striosomes, at six postnatal ages in mice. We find that at the earliest ages (postnatal day (P)4 and P10), WFA-positive clusters overlap preferentially with the striosome compartment. By P14, these clusters disappear. In contrast, PNNs were first seen at P10 and continued to increase in density and spread throughout the caudate/putamen with maturation. Remarkably, the PNNs overlap almost exclusively with the neostriatal matrix.

Conclusions/significance: This is the first description of a reversal in the distribution of CSPG associated structures, as well as the emergence and maintenance of PNNs in specific subcompartments of the neostriatum. These results suggest diverse roles for CSPGs in the formation of functional corticostriatal and nigrostriatal connectivity within the striosome and matrix compartments of the developing caudate/putamen.

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WFA staining changes in relation to μOR distribution at postnatal day 10.Conventions are the same as for Fig 3. (A–C): Rostral-most section. (D–F): More caudal section. (A, D): WFA distribution. (B, E): μOR distribution. (C, F): merged image. WFA ‘patches’ are mainly confined to the dorsal part of neostriatum, where they still overlap considerably with μOR defined striosomes (arrows). Postnatal day 10 also marks the appearance of punctate labelling which indicate PNN formation in the dorsolateral striatum rostrally (arrowheads; A). More caudally, PNNs are also seen in the lateral striatum and appear more numerous (D). PNNs are mainly confined to the matrix compartment of the neostriatum. Scale bar: 600 μm.
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pone-0003020-g004: WFA staining changes in relation to μOR distribution at postnatal day 10.Conventions are the same as for Fig 3. (A–C): Rostral-most section. (D–F): More caudal section. (A, D): WFA distribution. (B, E): μOR distribution. (C, F): merged image. WFA ‘patches’ are mainly confined to the dorsal part of neostriatum, where they still overlap considerably with μOR defined striosomes (arrows). Postnatal day 10 also marks the appearance of punctate labelling which indicate PNN formation in the dorsolateral striatum rostrally (arrowheads; A). More caudally, PNNs are also seen in the lateral striatum and appear more numerous (D). PNNs are mainly confined to the matrix compartment of the neostriatum. Scale bar: 600 μm.

Mentions: Relatively large amorphous ‘patches’ were observed in the earliest developmental time points examined. These structures were most apparent at P4, where clustered WFA labelling could be observed mainly within the dorsolateral region of rostral neostriatum (Fig 3A, D), although they continued to be expressed through P10 (Fig 4A, D). These WFA-positive patches were no longer detectable by P14 (Fig 5A, D).


Rapid reversal of chondroitin sulfate proteoglycan associated staining in subcompartments of mouse neostriatum during the emergence of behaviour.

Lee H, Leamey CA, Sawatari A - PLoS ONE (2008)

WFA staining changes in relation to μOR distribution at postnatal day 10.Conventions are the same as for Fig 3. (A–C): Rostral-most section. (D–F): More caudal section. (A, D): WFA distribution. (B, E): μOR distribution. (C, F): merged image. WFA ‘patches’ are mainly confined to the dorsal part of neostriatum, where they still overlap considerably with μOR defined striosomes (arrows). Postnatal day 10 also marks the appearance of punctate labelling which indicate PNN formation in the dorsolateral striatum rostrally (arrowheads; A). More caudally, PNNs are also seen in the lateral striatum and appear more numerous (D). PNNs are mainly confined to the matrix compartment of the neostriatum. Scale bar: 600 μm.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2500190&req=5

pone-0003020-g004: WFA staining changes in relation to μOR distribution at postnatal day 10.Conventions are the same as for Fig 3. (A–C): Rostral-most section. (D–F): More caudal section. (A, D): WFA distribution. (B, E): μOR distribution. (C, F): merged image. WFA ‘patches’ are mainly confined to the dorsal part of neostriatum, where they still overlap considerably with μOR defined striosomes (arrows). Postnatal day 10 also marks the appearance of punctate labelling which indicate PNN formation in the dorsolateral striatum rostrally (arrowheads; A). More caudally, PNNs are also seen in the lateral striatum and appear more numerous (D). PNNs are mainly confined to the matrix compartment of the neostriatum. Scale bar: 600 μm.
Mentions: Relatively large amorphous ‘patches’ were observed in the earliest developmental time points examined. These structures were most apparent at P4, where clustered WFA labelling could be observed mainly within the dorsolateral region of rostral neostriatum (Fig 3A, D), although they continued to be expressed through P10 (Fig 4A, D). These WFA-positive patches were no longer detectable by P14 (Fig 5A, D).

Bottom Line: Remarkably, the PNNs overlap almost exclusively with the neostriatal matrix.This is the first description of a reversal in the distribution of CSPG associated structures, as well as the emergence and maintenance of PNNs in specific subcompartments of the neostriatum.These results suggest diverse roles for CSPGs in the formation of functional corticostriatal and nigrostriatal connectivity within the striosome and matrix compartments of the developing caudate/putamen.

View Article: PubMed Central - PubMed

Affiliation: Discipline of Physiology, School of Medical Sciences and the Bosch Institute, University of Sydney, Sydney, Australia.

ABSTRACT

Background: The neostriatum, the mouse homologue of the primate caudate/putamen, is the input nucleus for the basal ganglia, receiving both cortical and dopaminergic input to each of its sub-compartments, the striosomes and matrix. The coordinated activation of corticostriatal pathways is considered vital for motor and cognitive abilities, yet the mechanisms which underlie the generation of these circuits are unknown. The early and specific targeting of striatal subcompartments by both corticostriatal and nigrostriatal terminals suggests activity-independent mechanisms, such as axon guidance cues, may play a role in this process. Candidates include the chondroitin sulfate proteoglycan (CSPG) family of glycoproteins which have roles not only in axon guidance, but also in the maturation and stability of neural circuits where they are expressed in lattice-like perineuronal nets (PNNs).

Methodology/principal findings: The expression of CSPG-associated structures and PNNs with respect to neostriatal subcompartments has been examined qualitatively and quantitatively using double-labelling for Wisteria floribunda agglutinin (WFA), and the mu-opioid receptor (muOR), a marker for striosomes, at six postnatal ages in mice. We find that at the earliest ages (postnatal day (P)4 and P10), WFA-positive clusters overlap preferentially with the striosome compartment. By P14, these clusters disappear. In contrast, PNNs were first seen at P10 and continued to increase in density and spread throughout the caudate/putamen with maturation. Remarkably, the PNNs overlap almost exclusively with the neostriatal matrix.

Conclusions/significance: This is the first description of a reversal in the distribution of CSPG associated structures, as well as the emergence and maintenance of PNNs in specific subcompartments of the neostriatum. These results suggest diverse roles for CSPGs in the formation of functional corticostriatal and nigrostriatal connectivity within the striosome and matrix compartments of the developing caudate/putamen.

Show MeSH