Perineuronal nets labeled by monoclonal antibody VC1.1 ensheath interneurons expressing parvalbumin and calbindin in the rat amygdala
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.
KeywordsExtracellular matrix Perineuronal nets Amygdala Calcium-binding proteins Immunohistochemistry
The authors thank Dr. Kenneth G. Baimbridge (University of British Columbia) for his generous donation of the PV and CB polyclonal antisera. This work was supported by NIH Grants R01MH104638 and R01NS19733.
Compliance with ethical standards
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Human and animal rights statement
All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.
Conflict of interest
The authors declare that they have no conflict of interest.
- Blosa M, Sonntag M, Jäger C, Weigel S, Seeger J, Frischknecht R, Seidenbecher CI, Matthews RT, Arendt T, Rübsamen R, Morawski M (2015) The extracellular matrix molecule brevican is an integral component of the machinery mediating fast synaptic transmission at the calyx of Held. J Physiol 593:4341–4360CrossRefPubMedPubMedCentralGoogle Scholar
- Brückner G, Brauer K, Härtig W, Wolff JR, Rickmann MJ, Derouiche A, Delpech B, Girard N, Oertel WH, Reichenbach A (1993) Perineuronal nets provide a polyanionic, glia-associated form of microenvironment around certain neurons in many parts of the rat brain. Glia 8:183–200CrossRefPubMedGoogle Scholar
- Golgi C (1893) Intorno all’origine del quarto nervo cerebrale e una questione isto-fisiologica che a questo argomento si collega. Rendiconti della Reale Accademia dei Lincei (21 maggio) 2:443–450Google Scholar
- 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 842:15–29CrossRefPubMedGoogle Scholar
- McDonald AJ (1992) Cell types and intrinsic connections of the amygdala. In: Aggleton JP (ed) the amygdala. Wiley-Liss, New York, pp 67–96Google Scholar
- Paxinos G, Watson C (1997) The rat brain in stereotaxic coordinates. Academic Press, New YorkGoogle Scholar
- 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 12:3331–33342CrossRefPubMedGoogle Scholar
- Saghatelyan AK, Dityatev A, Schmidt S, Schuster T, Bartsch U, Schachner M (2001) Reduced perisomatic inhibition, increased excitatory transmission, and impaired long-term potentiation in mice deficient for the extracellular matrix glycoprotein tenascin-R. Mol Cell Neurosci 17:226–240CrossRefPubMedGoogle Scholar
- Weber P, Bartsch U, Rasband MN, Czaniera R, Lang Y, Bluethmann H, Margolis RU, Levinson SR, Shrager P, Montag D, Schachner M (1999) Mice deficient for tenascin-R display alterations of the extracellular matrix and decreased axonal conduction velocities in the CNS. J Neurosci 19:4245–4262PubMedGoogle Scholar
- Wegner F, Härtig W, Bringmann A, Grosche J, Wohlfarth K, Zuschratter W, Brückner G (2003) Diffuse perineuronal nets and modified pyramidal cells immunoreactive for glutamate and the GABA(A) receptor alpha1 subunit form a unique entity in rat cerebral cortex. Exp Neurol 184:705–714CrossRefPubMedGoogle Scholar