Perineuronal nets in the rhesus monkey and human basal forebrain including basal ganglia
Abstract
Perineuronal nets of extracellular matrix have been shown to characterize the microenvironment of individual neurons and the chemoarchitecture of brain regions such as basal forebrain nuclei. Previous work has also demonstrated that neurons in the human cerebral cortex ensheathed by perineuronal nets rarely undergo cytoskeletal changes in Alzheimer's disease, suggesting a neuroprotective effect of extracellular matrix components. It is not known, however, whether or not perineuronal nets are absent in the microenvironment of the cholinergic basal forebrain neurons that are involved early in the cascade of neurodegeneration in humans. Therefore, the present study was undertaken to examine the distribution patterns of perineuronal nets in the basal forebrain of the higher primates, rhesus monkey and human. Cytochemical staining was performed with the lectin Wisteria floribunda agglutinin and a polyclonal antibody to core proteins of chondroitin sulfate proteoglycans in the perfusion-fixed tissue of rhesus monkeys. In human brains, perineuronal nets were only stained with the immunoreaction for chondroitin sulfate proteoglycans. The results showed similar characteristics in distribution patterns of perineuronal nets in the medial septum, the diagonal band of Broca, the basal nucleus of Meynert (Ch1-Ch4), the lateral septum, the caudate-putamen, and the globus pallidus in both species. Double-labelling revealed that the vast majority of cholinergic neurons, labelled either with antibodies to choline acetyltransferase or the low-affinity neurotrophin receptor p75(NTR), were not ensheathed by perineuronal nets. A small subpopulation of net-associated neurons in close proximity to or intermingled with cholinergic neurons of the Ch1-Ch4 cell groups was found to be immunoreactive for parvalbumin. In the caudate-putamen, a large number of the parvalbumin-positive neurons were surrounded by perineuronal nets, whereas in the external and internal segments of the globus pallidus the coincidence of both markers was nearly complete. The study demonstrates that perineuronal nets of extracellular matrix are associated with different types of non-cholinergic neurons in the primate basal forebrain. The absence of nets around cholinergic basal forebrain neurons may be related to their slow modulatory activity but may also contribute to their susceptibility to degeneration in Alzheimer's disease.
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PNN-bearing neurons are predominantly GABAergic, including but not restricted to those expressing parvalbumin and somatostatin.
“As discussed, these are predominantly represented by GABAergic neurons, including, but not restricted to, those expressing PVB and somatostatin (Adams et al., 2001; Brauer et al., 1993; Bruckner et al., 1993; Hartig et al., 1995; Hartig et al., 2001; Haunso et al., 1999; Morris and Henderson, 2000; Pantazopoulos et al., 2006; Wintergerst et al., 1996) (Pantazopoulos et al., unpublished”
From Losing the sugar coating: Potential impact of perineuronal net abnormalities on interneurons in schizophrenia (2015) · cites this paper as Adams et al., 2001
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Self-citationBrückner, G., Kacza, J., & Grosche, J. (2004) · Journal of Molecular Histology · doi:10.1023/b:hijo.0000023374.22298.50 · Cited by 33 · see citing works
Self-citation
- Authors
- Adams, I., Brauer, K., Arélin, C., Härtig, W., Fine, A., Mäder, M., Arendt, T., & Brückner, G.
- Affiliations
- Leipzig University (DE)
- National Institute for Medical Research (GB)
- University of Göttingen (DE)
- Corresponding author
- Brückner, G
- ORCID
- Arendt, T
- Venue
- Neuroscience
- Publisher
- Elsevier BV
- Published
- 2001-12
- Volume
- 108
- Issue
- 2
- Pages
- 285-298
- ISSN
- 0306-4522 (ISSN-L)
- OpenAlex
- W2023391657
- Cited by
- 48
- References
- 97
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1 · 2023: 1 · 2022: 5 · 2017: 2 · 2016: 2 · 2015: 1 · 2014: 2 · 2013: 2 · 2012: 1
- FWCI
- 0.57
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- GRO (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Proteoglycans and glycosaminoglycans research
- Life Sciences › Neuroscience › Neurology › Neuroinflammation and Neurodegeneration Mechanisms
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- perineuronal nets, extracellular matrix, basal forebrain, basal ganglia, cholinergic neurons, chondroitin sulfate proteoglycans, parvalbumin, choline acetyltransferase, p75 neurotrophin receptor, medial septum, diagonal band of Broca, nucleus basalis of Meynert, caudate-putamen, globus pallidus, rhesus monkeys, human brain, Alzheimer's disease, neurodegeneration
- MeSH terms
- Acetylcholine, Aged, Aged, 80 and over, Animals, Basal Ganglia, Choline O-Acetyltransferase, Cholinergic Fibers, Extracellular Matrix, Female, Globus Pallidus, Humans, Immunohistochemistry, Macaca mulatta, Male, Middle Aged, Neurons, Parvalbumins, Chondroitin Sulfate Proteoglycans, Septal Nuclei, Neostriatum, Neuropil, Basal Nucleus of Meynert, Receptors, N-Acetylglucosamine, Lectins, Plant Lectins
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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
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