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Development and Structural Variety of the Chondroitin Sulfate Proteoglycans-Contained Extracellular Matrix in the Mouse Brain.

Horii-Hayashi N, Sasagawa T, Matsunaga W, Nishi M - Neural Plast. (2015)

Bottom Line: In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala.Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms.The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634-8521, Japan.

ABSTRACT
Chondroitin sulfate proteoglycans (CSPGs) are major components of the extracellular matrix (ECM) in the brain. In adult mammals, CSPGs form the specialized ECM structure perineuronal nets (PNNs) that surround somata and dendrites of certain types of neurons. PNNs restrict synaptic plasticity and regulate the closure of critical periods. Although previous studies have examined the starting period of PNN formation, focusing on primary sensory cortices, there are no systematic studies at the whole brain level. Here, we examined the starting period of PNN formation in male mice ranging in age from postnatal day 3 to week 11, mainly focusing on several cortical areas, limbic structures, hypothalamus, and brain stem, using lectin histochemistry with Wisteria floribunda agglutinin (WFA). Results showed that early PNN formation was observed in several reticular formations of the brain stem related to the cranial nerves and primary somatosensory cortices. In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala. Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms. The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

No MeSH data available.


WFA-stained ECM in the developing cortex. (a–j) Low- (a–e) and high- (f–j) power images of WFA staining at P3 (a, f), P7 (b, g), P14 (c, h), P21 (d, i), and 5 w (e, j). Rectangular areas in (a) and (b) indicate the magnified areas shown in (f) and (g), respectively. High-power images (g–j) obtained from cortical IV layer of the S1BF. Dotted lines indicate the border between the S1BF and the S1FL. Accumulation of WFA reactivity around particular cell bodies was observed from P7 onward. WFA reactivity clearly surrounding both cell bodies and dendrites was observed from 5 w onward. (k) WFA-labeled serial coronal sections at P7, indicating that PNN-like WFA reactivity was observed in the S1BF, whereas any other regions indicated did not show PNN-like staining. Au1: primary auditory cortex; Cg: cingulate cortex; M1: primary motor cortex; M2: secondary motor cortex; PrL: prelimbic cortex; RSG: retrosplenial granular cortex; S1: primary sensory cortex; S1BF: barrel field of the primary somatosensory cortex; S1FL: forelimb primary somatosensory cortex; V1: primary visual cortex; V2L: lateral area of the secondary visual cortex; V2ML: mediolateral area of the secondary visual cortex; V2MM: mediomedial area of the secondary visual cortex. Scale bars = 500 (a–e), 50 (f–j), and 1000 (k) μm.
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fig1: WFA-stained ECM in the developing cortex. (a–j) Low- (a–e) and high- (f–j) power images of WFA staining at P3 (a, f), P7 (b, g), P14 (c, h), P21 (d, i), and 5 w (e, j). Rectangular areas in (a) and (b) indicate the magnified areas shown in (f) and (g), respectively. High-power images (g–j) obtained from cortical IV layer of the S1BF. Dotted lines indicate the border between the S1BF and the S1FL. Accumulation of WFA reactivity around particular cell bodies was observed from P7 onward. WFA reactivity clearly surrounding both cell bodies and dendrites was observed from 5 w onward. (k) WFA-labeled serial coronal sections at P7, indicating that PNN-like WFA reactivity was observed in the S1BF, whereas any other regions indicated did not show PNN-like staining. Au1: primary auditory cortex; Cg: cingulate cortex; M1: primary motor cortex; M2: secondary motor cortex; PrL: prelimbic cortex; RSG: retrosplenial granular cortex; S1: primary sensory cortex; S1BF: barrel field of the primary somatosensory cortex; S1FL: forelimb primary somatosensory cortex; V1: primary visual cortex; V2L: lateral area of the secondary visual cortex; V2ML: mediolateral area of the secondary visual cortex; V2MM: mediomedial area of the secondary visual cortex. Scale bars = 500 (a–e), 50 (f–j), and 1000 (k) μm.

Mentions: Diffuse WFA reactivity was observed in the ventral layers of the S1BF at P3 (Figures 1(a) and 1(f)), and this observation was similar to a previous report [14]. At P7, WFA reactivity was observed in cortical IV layer (Figure 1(b)) and slightly condensed around particular cell bodies (Figure 1(g)), which were considered immature PNNs. At both P14 (Figures 1(c) and 1(h)) and P21 (Figures 1(d) and 1(i)), PNN-like labeling was observed around cell bodies without a clear dendritic surrounding. The typical PNN shape that is known to surround both cell bodies and dendrites was observed at 5 w (Figures 1(e) and 1(j)) and was almost equal to that seen at 11 w (data not shown). Serial WFA-labeled sections at P7 revealed that PNN-like labeling was observed in the primary somatosensory cortex (S1) and S1BF, whereas it could not be detected in the prelimbic (PrL), primary motor (M1), secondary motor (M2), cingulate (Cg), primary visual (V1), mediolateral (V2ML), and mediomedial (V2MM) areas of the secondary visual, primary auditory (Au1), and retrosplenial granular (RSG) cortices (Figure 1(k)). These results indicated an intercortical difference in the beginning of PNN formation.


Development and Structural Variety of the Chondroitin Sulfate Proteoglycans-Contained Extracellular Matrix in the Mouse Brain.

Horii-Hayashi N, Sasagawa T, Matsunaga W, Nishi M - Neural Plast. (2015)

WFA-stained ECM in the developing cortex. (a–j) Low- (a–e) and high- (f–j) power images of WFA staining at P3 (a, f), P7 (b, g), P14 (c, h), P21 (d, i), and 5 w (e, j). Rectangular areas in (a) and (b) indicate the magnified areas shown in (f) and (g), respectively. High-power images (g–j) obtained from cortical IV layer of the S1BF. Dotted lines indicate the border between the S1BF and the S1FL. Accumulation of WFA reactivity around particular cell bodies was observed from P7 onward. WFA reactivity clearly surrounding both cell bodies and dendrites was observed from 5 w onward. (k) WFA-labeled serial coronal sections at P7, indicating that PNN-like WFA reactivity was observed in the S1BF, whereas any other regions indicated did not show PNN-like staining. Au1: primary auditory cortex; Cg: cingulate cortex; M1: primary motor cortex; M2: secondary motor cortex; PrL: prelimbic cortex; RSG: retrosplenial granular cortex; S1: primary sensory cortex; S1BF: barrel field of the primary somatosensory cortex; S1FL: forelimb primary somatosensory cortex; V1: primary visual cortex; V2L: lateral area of the secondary visual cortex; V2ML: mediolateral area of the secondary visual cortex; V2MM: mediomedial area of the secondary visual cortex. Scale bars = 500 (a–e), 50 (f–j), and 1000 (k) μm.
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fig1: WFA-stained ECM in the developing cortex. (a–j) Low- (a–e) and high- (f–j) power images of WFA staining at P3 (a, f), P7 (b, g), P14 (c, h), P21 (d, i), and 5 w (e, j). Rectangular areas in (a) and (b) indicate the magnified areas shown in (f) and (g), respectively. High-power images (g–j) obtained from cortical IV layer of the S1BF. Dotted lines indicate the border between the S1BF and the S1FL. Accumulation of WFA reactivity around particular cell bodies was observed from P7 onward. WFA reactivity clearly surrounding both cell bodies and dendrites was observed from 5 w onward. (k) WFA-labeled serial coronal sections at P7, indicating that PNN-like WFA reactivity was observed in the S1BF, whereas any other regions indicated did not show PNN-like staining. Au1: primary auditory cortex; Cg: cingulate cortex; M1: primary motor cortex; M2: secondary motor cortex; PrL: prelimbic cortex; RSG: retrosplenial granular cortex; S1: primary sensory cortex; S1BF: barrel field of the primary somatosensory cortex; S1FL: forelimb primary somatosensory cortex; V1: primary visual cortex; V2L: lateral area of the secondary visual cortex; V2ML: mediolateral area of the secondary visual cortex; V2MM: mediomedial area of the secondary visual cortex. Scale bars = 500 (a–e), 50 (f–j), and 1000 (k) μm.
Mentions: Diffuse WFA reactivity was observed in the ventral layers of the S1BF at P3 (Figures 1(a) and 1(f)), and this observation was similar to a previous report [14]. At P7, WFA reactivity was observed in cortical IV layer (Figure 1(b)) and slightly condensed around particular cell bodies (Figure 1(g)), which were considered immature PNNs. At both P14 (Figures 1(c) and 1(h)) and P21 (Figures 1(d) and 1(i)), PNN-like labeling was observed around cell bodies without a clear dendritic surrounding. The typical PNN shape that is known to surround both cell bodies and dendrites was observed at 5 w (Figures 1(e) and 1(j)) and was almost equal to that seen at 11 w (data not shown). Serial WFA-labeled sections at P7 revealed that PNN-like labeling was observed in the primary somatosensory cortex (S1) and S1BF, whereas it could not be detected in the prelimbic (PrL), primary motor (M1), secondary motor (M2), cingulate (Cg), primary visual (V1), mediolateral (V2ML), and mediomedial (V2MM) areas of the secondary visual, primary auditory (Au1), and retrosplenial granular (RSG) cortices (Figure 1(k)). These results indicated an intercortical difference in the beginning of PNN formation.

Bottom Line: In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala.Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms.The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

View Article: PubMed Central - PubMed

Affiliation: Department of Anatomy and Cell Biology, Nara Medical University, 840 Shijo-cho, Kashihara, Nara 634-8521, Japan.

ABSTRACT
Chondroitin sulfate proteoglycans (CSPGs) are major components of the extracellular matrix (ECM) in the brain. In adult mammals, CSPGs form the specialized ECM structure perineuronal nets (PNNs) that surround somata and dendrites of certain types of neurons. PNNs restrict synaptic plasticity and regulate the closure of critical periods. Although previous studies have examined the starting period of PNN formation, focusing on primary sensory cortices, there are no systematic studies at the whole brain level. Here, we examined the starting period of PNN formation in male mice ranging in age from postnatal day 3 to week 11, mainly focusing on several cortical areas, limbic structures, hypothalamus, and brain stem, using lectin histochemistry with Wisteria floribunda agglutinin (WFA). Results showed that early PNN formation was observed in several reticular formations of the brain stem related to the cranial nerves and primary somatosensory cortices. In the limbic system, PNN formation in the hippocampus started earlier than that of the amygdala. Furthermore, in the medial amygdaloid nucleus and some hypothalamic regions, WFA labeling did not show typical PNN-like forms. The present study suggests spatiotemporal differences at the beginning of PNN formation and a structural variety of CSPG-contained ECM in the brain.

No MeSH data available.