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Cited by 11Neuroscience and Neuropharmacology ResearchMemory and Neural MechanismsNeurogenesis and neuroplasticity mechanisms

Perineuronal nets labeled by monoclonal antibody VC1.1 ensheath interneurons expressing parvalbumin and calbindin in the rat amygdala

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McDonald, Alexander J., Hamilton, Patricia G., Barnstable, Colin J.·2018·Brain Structure and Function
DOI 10.1007/s00429-017-1542-8PMC PMC5871560
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Abstract

Perineuronal nets (PNNs) are specialized condensations of extracellular matrix that ensheath particular neuronal subpopulations in the brain and spinal cord. PNNs regulate synaptic plasticity, including the encoding of fear memories by the amygdala. The present immunohistochemical investigation studied PNN structure and distribution, as well as the neurochemistry of their ensheathed neurons, in the rat amygdala using monoclonal antibody VC1.1, which recognizes a glucuronic acid 3-sulfate glycan associated with PNNs in the cerebral cortex. VC1.1+ PNNs surrounded the cell bodies and dendrites of a subset of nonpyramidal neurons in cortex-like portions of the amygdala (basolateral amygdalar complex, cortical nuclei, nucleus of the lateral olfactory tract, and amygdalohippocampal region). There was also significant neuropilar VC1.1 immunoreactivity, whose density varied in different amygdalar nuclei. Cell counts in the basolateral nucleus revealed that virtually all neurons ensheathed by VC1.1+ PNNs were parvalbumin-positive (PV+) interneurons, and these VC1.1+/PV+ cells constituted 60% of all PV+ interneurons, including all of the larger PV+ neurons. Approximately 70% of VC1.1+ neurons were calbindin-positive (CB+), and these VC1.1+/CB+ cells constituted about 40% of all CB+ neurons. Colocalization of VC1.1 with Vicia villosa agglutinin (VVA) binding, which stains terminal N-acetylgalactosamines, revealed that VC1.1+ PNNs were largely a subset of VVA+ PNNs. This investigation provides baseline data regarding PNNs in the rat which should be useful for future studies of their function in this species.

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  • All social memory associated regions are highly populated with PNN-surrounded PV neurons.

    “All the social memory associated regions are highly populated with PNN-surrounded PV neurons [46, 66, 130, 131].”

    From The extracellular matrix and perineuronal nets in memory (2022) · cites this paper as [130]

    The Results report that most VC1.1-positive PNN-ensheathed neurons in the rat amygdala were PV-positive, but describe a low density of those neurons in the nuclei examined. The Discussion estimates that they make up about 3.6% of all neurons in the basolateral nucleus. This supports their presence in the amygdala, not the claim that all social-memory-associated regions are highly populated with them. (LLM, conf=0.88)

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Research works printed but not linked: 63

  1. Abo T Balch CM 1981 A differentiation antigen of human NK and K cells identified by a monoclonal antibody (HNK-1) J Immunol 127 1024 1029 6790607
  2. Arimatsu Y Naegele JR Barnstable CJ 1987 Molecular markers of neuronal subpopulations in layers 4, 5, and 6 of cat primary visual cortex J Neurosci 7 1250 1263 3553447 PMC6569005
  3. Baker KD Gray AR Richardson R 2017 The development of perineuronal nets around parvalbumin gabaergic neurons in the medial prefrontal cortex and basolateral amygdala of rats Behav Neurosci 131 289 303 28714715
  4. Barnstable CJ Kosaka T Naegele JR Arimatsu Y 1992 Molecular properties of GABAergic local-circuit neurons in the mammalian visual cortex Prog Brain Res 90 503 522 1631310
  5. Berretta S 2012 Extracellular matrix abnormalities in schizophrenia Neuropharmacology 62 1584 1597 21856318 PMC3234338
  6. Bienvenu TC Busti D Magill PJ Ferraguti F Capogna M 2012 Cell-type-specific recruitment of amygdala interneurons to hippocampal theta rhythm and noxious stimuli in vivo Neuron 74 1059 1074 22726836 PMC3391683
  7. Brückner G Grosche J Schmidt S Härtig W Margolis RU Delpech B Seidenbecher CI Czaniera R Schachner M 1999 Postnatal development of perineuronal nets in wild-type mice and in a mutant deficient in tenascin-R J Comp Neurol 428 616 629 11077416
  8. Carulli D Rhodes KE Brown DJ Bonnert TP Pollack SJ Oliver K Strata P Fawcett JW 2006 Composition of perineuronal nets in the adult rat cerebellum and the cellular origin of their components J Comp Neurol 494 559 577 16374793
  9. Celio MR Blümcke I 1994 Perineuronal nets–a specialized form of extracellular matrix in the adult nervous system Brain Res Brain Res Rev 19 128 145 8167657
  10. Celio MR Spreafico R De Biasi S Vitellaro-Zuccarello L 1998 Perineuronal nets: past and present Trends Neurosci 21 510 515 9881847
  11. Condé F Lund JS Jacobowitz DM Baimbridge KG Lewis DA 1994 Local circuit neurons immunoreactive for calretinin, calbindin D-28k or parvalbumin in monkey prefrontal cortex: distribution and morphology J Comp Neurol 341 95 116 8006226
  12. Dauth S Grevesse T Pantazopoulos H Campbell PH Maoz BM Berretta S Parker KK 2016 Extracellular matrix protein expression is brain region dependent J Comp Neurol 524 1309 1336 26780384 PMC7714387
  13. Dityatev A Schachner M 2003 Extracellular matrix molecules and synaptic plasticity Nat Rev Neurosci 4 456 468 12778118
  14. Galtrey CM Fawcett JW 2007 The role of chondroitin sulfate proteoglycans in regeneration and plasticity in the central nervous system Brain Res Rev 54 1 18 17222456
  15. Hancock MB 1986 Two-color immunoperoxidase staining: visualization of anatomic relationships between immunoreactive neural elements Am J Anat 175 343 352 2422916
  16. Härtig W Brückner G Brauer K Schmidt C Bigl V 1995 Allocation of perineuronal nets and parvalbumin-, calbindin-D28k- and glutamic acid decarboxylase-immunoreactivity in the amygdala of the rhesus monkey Brain Res 698 265 269 8581495
  17. Härtig W Derouiche A Welt K Brauer K Grosche J Mäder M Reichenbach A Brückner G 1999 Cortical neurons immunoreactive for the potassium channel Kv3.1b subunit are predominantly surrounded by perineuronal nets presumed as a buffering system for cations Brain Res 842 15 29 10526091
  18. Hensch TK 2005 Critical period plasticity in local cortical circuits Nat Rev Neurosci 6 877 888 16261181
  19. Horii-Hayashi N Sasagawa T Matsunaga W Nishi M 2015 Development and structural variety of the chondroitin sulfate proteoglycans-contained extracellular matrix in the mouse brain Neural Plast 2015 256389 26649203 PMC4663360
  20. Kemppainen S Pitkänen A 2000 Distribution of parvalbumin, calretinin, and calbindin-D(28k) immunoreactivity in the rat amygdaloid complex and colocalization with gamma-aminobutyric acid J Comp Neurol 426 441 467 10992249
  21. Kizuka Y Oka S 2012 Regulated expression and neural functions of human natural killer-1 (HNK-1) carbohydrate Cell Mol Life Sci 69 4135 4147 22669261 PMC11114532
  22. Kosaka T Heizmann CW Barnstable CJ 1989 Monoclonal antibody VC1.1 selectively stains a population of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex Exp Brain Res 78 43 50 2591517
  23. Kosaka T Isogai K Barnstable CJ Heizmann CW 1990 Monoclonal antibody HNK-1 selectively stains a subpopulation of GABAergic neurons containing the calcium-binding protein parvalbumin in the rat cerebral cortex Exp Brain Res 82 566 574 1705516
  24. Lucas EK Jegarl AM Morishita H Clem RL 2016 Multimodal and site-specific plasticity of amygdala parvalbumin interneurons after fear learning Neuron 91 629 643 27427462 PMC4975985
  25. Maeda N 2015 Proteoglycans and neuronal migration in the cerebral cortex during development and disease Front Neurosci 9 98 25852466 PMC4369650
  26. Mascagni F McDonald AJ 2003 Immunohistochemical characterization of cholecystokinin containing neurons in the rat basolateral amygdala Brain Res 976 171 184 12763251
  27. Mascagni F Muly EC Rainnie DG McDonald AJ 2009 Immunohistochemical characterization of parvalbumin-containing interneurons in the monkey basolateral amygdala Neuroscience 158 1541 1550 19059310 PMC2674383
  28. Matthews RT Kelly GM Zerillo CA Gray G Tiemeyer M Hockfield S 2002 Aggrecan glycoforms contribute to the molecular heterogeneity of perineuronal nets J Neurosci 22 7536 7547 12196577 PMC6757962
  29. McDonald AJ Culberson JL 1981 Neurons of the basolateral amygdala: a Golgi study in the opossum (Didelphis virginiana) Am J Anat 162 327 342 7325125
  30. McDonald AJ 1982 Neurons of the lateral and basolateral amygdaloid nuclei: a Golgi study in the rat J Comp Neurol 212 293 312 6185547
  31. McDonald AJ 1992 Cell types and intrinsic connections of the amygdala The amygdala Aggleton JP 67 96 New York Wiley-Liss
  32. McDonald AJ 1997 Calbindin-D28k immunoreactivity in the rat amygdala J Comp Neurol 383 231 244 9182851
  33. McDonald AJ Betette RL 2001 Parvalbumin-containing neurons in the rat basolateral amygdala: morphology and co-localization of calbindin-D(28k) Neuroscience 102 413 425 11166127
  34. McDonald AJ Mascagni F 2001 Colocalization of calcium-binding proteins and GABA in neurons of the rat basolateral amygdala Neuroscience 105 681 693 11516833
  35. McDonald AJ Mascagni F 2002 Immunohistochemical characterization of somatostatin containing interneurons in the rat basolateral amygdala Brain Res 943 237 244 12101046
  36. McDonald AJ Mascagni F Mania I Rainnie DG 2005 Evidence for a perisomatic innervation of parvalbumin-containing interneurons by individual pyramidal cells in the basolateral amygdala Brain Res 1035 32 40 15713274
  37. McDonald AJ Mascagni F 2006 Differential expression of Kv3.1b and Kv3.2 potassium channel subunits in interneurons of the basolateral amygdala Neuroscience 138 537 547 16413129
  38. Morikawa S Ikegaya Y Narita M Tamura H 2017 Activation of perineuronal net-expressing excitatory neurons during associative memory encoding and retrieval Sci Rep 7 46024 28378772 PMC5380958
  39. Mueller AL Davis A Sovich S Carlson SS Robinson FR 2016 Distribution of n-acetylgalactosamine-positive perineuronal nets in the macaque brain: Anatomy and Implications Neural Plast 2016 6021428 26881119 PMC4735937
  40. Naegele JR Katz LC 1990 Cell surface molecules containing N-acetylgalactosamine are associated with basket cells and neurogliaform cells in cat visual cortex J Neurosci 10 540 557 2303859 PMC6570148
  41. Naegele JR Barnstable CJ 1991 A carbohydrate epitope defined by monoclonal antibody VC1.1 is found on N-CAM and other cell adhesion molecules Brain Res 559 118 129 1723642
  42. Pantazopoulos H Woo TU Lim MP Lange N Berretta S 2010 Extracellular matrix-glial abnormalities in the amygdala and entorhinal cortex of subjects diagnosed with schizophrenia Arch Gen Psychiatry 67 155 166 20124115 PMC4208310
  43. Pantazopoulos H Markota M Jaquet F Ghosh D Wallin A Santos A Caterson B Berretta S 2015 Aggrecan and chondroitin-6-sulfate abnormalities in schizophrenia and bipolar disorder: a postmortem study on the amygdala Transl Psychiatry 5 e496 25603412 PMC4312825
  44. Pantazopoulos H Berretta S 2016 In Sickness and in Health: Perineuronal Nets and Synaptic Plasticity in Psychiatric Disorders Neural Plast 2016 9847696 26839720 PMC4709762
  45. Pape HC Narayanan RT Smid J Stork O Seidenbecher T 2005 Theta activity in neurons and networks of the amygdala related to long-term fear memory Hippocampus 15 874 880 16158424
  46. Paxinos G Watson C 1997 The rat brain in stereotaxic coordinates Academic Press New York 1997 6110810
  47. Rainnie DG Mania I Mascagni F McDonald AJ 2006 Physiological and morphological characterization of parvalbumin-containing interneurons of the rat basolateral amygdala J Comp Neurol 498 142 161 16856165
  48. Ren JQ Heizmann CW Kosaka T 1994 Regional difference in the distribution of parvalbumin-containing neurons immunoreactive for monoclonal antibody HNK-1 in the mouse cerebral cortex Neurosci Lett 166 221 225 8177503
  49. Saghatelyan AK Gorissen S Albert M Hertlein B Schachner M Dityatev A 2000 The extracellular matrix molecule tenascin-R and its HNK-1 carbohydrate modulate perisomatic inhibition and long-term potentiation in the CA1 region of the hippocampus Eur J Neurosci 12 3331 33342 10998116
  50. Smith PD Coulson-Thomas VJ Foscarin S Kwok JC Fawcett JW 2015 “GAG-ing with the neuron”: The role of glycosaminoglycan patterning in the central nervous system Exp Neurol 274 Pt B 100 114 26277685
  51. Trouche S Sasaki JM Tu T Reijmers LG 2013 Fear extinction causes target-specific remodeling of perisomatic inhibitory synapses Neuron 80 1054 1065 24183705 PMC3840076
  52. Tsien RY 2013 Very long-term memories may be stored in the pattern of holes in the perineuronal net Proc Natl Acad Sci U S A 110 12456 12461 23832785 PMC3725115
  53. Umemori J Winkel F Castrén E Karpova NN 2015 Distinct effects of perinatal exposure to fluoxetine or methylmercury on parvalbumin and perineuronal nets, the markers of critical periods in brain development Int J Dev Neurosci 44 55 64 25997908
  54. Vereczki VK Veres JM Müller K Nagy GA Rácz B Barsy B Hájos N 2016 Synaptic organization of perisomatic GABAergic inputs onto the principal cells of the mouse basolateral amygdala Front Neuroanat 10 20 27013983 PMC4779893
  55. Veres JM Nagy GA Hájos N 2017 Perisomatic GABAergic synapses of basket cells effectively control principal neuron activity in amygdala networks Elife 2017 1 6 6 pii e20721 PMC5218536 28060701
  56. Viapiano MS Matthews RT 2006 From barriers to bridges: chondroitin sulfate proteoglycans in neuropathology Trends Mol Med 12 488 496 16962376
  57. Wolff SB Gründemann J Tovote P Krabbe S Jacobson GA Müller C Herry C Ehrlich I Friedrich RW Letzkus JJ Lüthi A 2014 Amygdala interneuron subtypes control fear learning through disinhibition Nature 509 453 458 24814341
  58. Woodruff AR Sah P 2007 Networks of parvalbumin-positive interneurons in the basolateral amygdala J Neurosci 27 553 563 17234587 PMC6672782
  59. Woodson W Farb CR Ledoux JE 2000 Afferents from the auditory thalamus synapse on inhibitory interneurons in the lateral nucleus of the amygdala Synapse 38 124 137 11018786
  60. Xue YX Xue LF Liu JF He J Deng JH Sun SC Han HB Luo YX Xu LZ Wu P Lu L 2014 Depletion of perineuronal nets in the amygdala to enhance the erasure of drug memories J Neurosci 34 6647 6658 24806690 PMC6608143
  61. Yamada J Jinno S 2015 Subclass-specific formation of perineuronal nets around parvalbumin-expressing GABAergic neurons in Ammon’s horn of the mouse hippocampus J Comp Neurol 523 790 804 25420705
  62. Yamamoto M Marshall P Hemmendinger LM Boyer AB Caviness VS Jr 1988 Distribution of glucuronic acid-and-sulfate-containing glycoproteins in the central nervous system of the adult mouse Neurosci Res 5 273 298 2453818
  63. Zaremba S Naegele JR Barnstable CJ Hockfield S 1990 Neuronal subsets express multiple high-molecular-weight cell-surface glycoconjugates defined by monoclonal antibodies Cat-301 and VC1.1 J Neurosci 10 2985 2995 2204685 PMC6570258

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Authors
McDonald, A. J., Hamilton, P. G., & Barnstable, C. J.
Affiliations
  • University of South Carolina (US)
  • Pennsylvania State University (US)
Corresponding author
McDonald, Alexander J.
ORCID
Venue
Brain Structure and Function
Publisher
Springer Science and Business Media LLC
Published
2017-11-01
Volume
223
Issue
3
Pages
1133-1148
ISSN
  • 1863-2653 (ISSN-L)
  • 1863-2661
DOI
10.1007/s00429-017-1542-8
PMC
PMC5871560
OpenAlex
W2765888286
Cited by
11
References
16
Citations by year
2026: 2 · 2024: 2 · 2023: 1 · 2022: 1 · 2021: 1 · 2020: 3 · 2018: 1
FWCI
0.54
Type
journal article
Language
en
Open access
Licence
Locations
  • Brain Structure and Function (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
National Institutes of Health (R01MH104638, R01NS19733)
Topics
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
Keywords
perineuronal nets, parvalbumin, calbindin, amygdala, interneurons, extracellular matrix, basolateral amygdala, fear memory, synaptic plasticity, N-acetylgalactosamine
MeSH terms
Acetylgalactosamine, Amygdala, Animals, Antibodies, Monoclonal, Antibody Specificity, Extracellular Matrix, Glucuronates, Interneurons, Male, Parvalbumins, Rats, Sprague-Dawley, CD57 Antigens, Conotoxins, Rats, Calbindins, S100 Calcium Binding Protein G

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