Differential Expression and Cell-Type Specificity of Perineuronal Nets in Hippocampus, Medial Entorhinal Cortex, and Visual Cortex Examined in the Rat and Mouse

Abstract

Perineuronal nets (PNNs) are specialized extracellular matrix (ECM) structures that condense around the soma and proximal dendrites of subpopulations of neurons. Emerging evidence suggests that they are involved in regulating brain plasticity. However, the expression of PNNs varies between and within brain areas. A lack of quantitative studies describing the distribution and cell-specificity of PNNs makes it difficult to reveal the functional roles of PNNs. In the current study, we examine the distribution of PNNs and the identity of PNN-enwrapped neurons in three brain areas with different cognitive functions: the dorsal hippocampus, medial entorhinal cortex (mEC) and primary visual cortex (V1). We compared rats and mice as knowledge from these species are often intermingled. The most abundant expression of PNNs was found in the mEC and V1, while dorsal hippocampus showed strikingly low levels of PNNs, apart from dense expression in the CA2 region. In hippocampus we also found apparent species differences in expression of PNNs. While we confirm that the PNNs enwrap parvalbumin-expressing (PV+) neurons in V1, we found that they mainly colocalize with excitatory CamKII-expressing neurons in CA2. In mEC, we demonstrate that in addition to PV+ cells, the PNNs colocalize with reelin-expressing stellate cells. We also show that the maturation of PNNs in mEC coincides with the formation of grid cell pattern, while PV+ cells, unlike in other cortical areas, are present from early postnatal development. Finally, we demonstrate considerable effects on the number of PSD-95-gephyrin puncta after enzymatic removal of PNNs.

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References 87

1. 1.

   Adams I, Brauer K, Arelin C, Härtig W, Fine A, Mader M, Arendt T, Brückner G (2001 ) Perineuronal nets in the rhesus monkey and human basal forebrain including basal ganglia. Neuroscience 102:285–298.

   Not in our library10.1016/s0306-4522(01)00419-5

2. 2.

   Alcántara S, Ferrer I, Soriano E (1993 ) Postnatal development of parvalbumin and calbindin D28K immunoreactivities in the cerebral cortex of the rat. Anat Embryol (Berl) 188:63–73.

   Not in our library10.1007/bf00191452

3. 3.

   Alpar A, Gartner U, Härtig W, Brückner G (2006 ) Distribution of pyramidal cells associated with perineuronal nets in the neocortex of the rat. Brain Res 1120:13–22.

   Not in our library10.1016/j.brainres.2006.08.069

4. 4.

   Balmer TS, Carels VM, Frisch JL, Nick TA (2009 ) Modulation of perineuronal nets and parvalbumin with developmental song learning. J Neurosci 29:12878–12885.

   Not in our library10.1523/jneurosci.2974-09.2009

5. 5.
   Perineuronal Nets Enhance the Excitability of Fast-Spiking Neurons · 2016

   No notice
6. 6.

   Bartus K, James ND, Bosch KD, Bradbury EJ (2012 ) Chondroitin sulfate proteoglycans: key modulators of spinal cord and brain plasticity. Exp Neurol 235:5–17.

   Not in our library10.1016/j.expneurol.2011.08.008

7. 7.

   Beurdeley M, Spatazza J, Lee HH, Sugiyama S, Bernard C, Di Nardo AA, Hensch TK, Prochiantz A (2012 ) Otx2 binding to perineuronal nets persistently regulates plasticity in the mature visual cortex. J Neurosci 32:9429–9437.

   Not in our library10.1523/jneurosci.0394-12.2012

8. 8.

   Bjerknes TL, Moser EI, Moser MB (2014 ) Representation of geometric borders in the developing rat. Neuron 82:71–78.

   Not in our library10.1016/j.neuron.2014.02.014

9. 9.

   Botcher N, Falck JE, Thomson AM, Mercer A (2014 ) Distribution of interneurons in the CA2 region of the rat hippocampus. Front Neuroanat 8:104.

   Not in our library10.3389/fnana.2014.00104

10. 10.

    Brückner G, Bringmann A, Harthig W, Koppe G, Delpech B, Brauer K (1998 ) Acute and long-lasting changes in extracellular matrix chondroitin-sulfate proteoglycans induced by injection of chondroitinase ABC in the adult rat brain. Exp Brain Res 121:300–310.

    Not in our library10.1007/s002210050463

11. 11.

    Buetfering C, Allen K, Monyer H (2014 ) Parvalbumin interneurons provide grid cell-driven recurrent inhibition in the medial entorhinal cortex. Nat Neurosci 17:710–718.

    Not in our library10.1038/nn.3696

12. 12.

    Buzsaki G, Moser EI (2013 ) Memory, navigation and theta rhythm in the hippocampal-entorhinal system. Nat Neurosci 16:130–138.

    Not in our library10.1038/nn.3304

13. 13.

    Cabungcal JH, Steullet P, Morishita H, Kraftsik R, Cuenod M, Hensch TK, Do KQ (2013 ) Perineuronal nets protect fast-spiking interneurons against oxidative stress. Proc Natl Acad Sci USA 110:9130–9135.

    Not in our library10.1073/pnas.1300454110

14. 14.

    Carstens KE, Phillips ML, Pozzo-Miller L, Weinberg RJ, Dudek SM (2016 ) Perineuronal nets suppress plasticity of excitatory synapses on CA2 pyramidal neurons. J Neurosci 36:6312–6320.

    Not in our library10.1523/jneurosci.0245-16.2016

15. 15.

    Caruana DA, Alexander GM, Dudek SM (2012 ) New insights into the regulation of synaptic plasticity from an unexpected place: hippocampal area CA2. Learn Mem 19:391–400.

    Not in our library10.1101/lm.025304.111

16. 16.

    Carulli D, Pizzorusso T, Kwok JC, Putignano E, Poli A, Forostyak S, Andrews MR, Deepa SS, Glant TT, Fawcett JW (2010 ) Animals lacking link protein have attenuated perineuronal nets and persistent plasticity. Brain 133:2331–2347.

    Not in our library10.1093/brain/awq145

17. 17.

    Celio MR, Blumcke I (1994 ) Perineuronal nets – a specialized form of extracellular matrix in the adult nervous system. Brain Res Rev 19:128–145.

    Not in our library10.1016/0165-0173(94)90006-x

18. 18.

    Couey JJ, Witoelar A, Zhang SJ, Zheng K, Ye J, Dunn B, Czajkowski R, Moser MB, Moser EI, Roudi Y, Witter MP (2013 ) Recurrent inhibitory circuitry as a mechanism for grid formation. Nat Neurosci 16:318–324.

    Not in our library10.1038/nn.3310

19. 19.

    Dauth S, Grevesse T, Pantazopoulus H, Campbell PH, Maoz BM, Berretta S, Parker KK (2016 ) Extracellular matrix protein expression is brain region dependent. J Comp Neur 524:1309–1336.

    Not in our library10.1002/cne.23965

20. 20.

    Davis M, Efstathiou G, Frenk CS, White SDM (1985 ) The evolution of large-scale structure in a universe dominated by cold dark matter. Astrophys J 292:371–394.

    Not in our library10.1086/163168

21. 21.

    Deepa SS, Carulli D, Galtrey C, Rhodes K, Fukuda J, Mikami T, Sugahara K, Fawcett JW (2006 ) Composition of perineuronal net extracellular matrix in rat brain: a different disaccharide composition for the net-associated proteoglycans. J Biol Chem 281:17789–17800.

    Not in our library10.1074/jbc.m600544200

22. 22.

    de Vivo L, Landi S, Panniello M, Baroncelli L, Chierzi S, Mariotti L, Spolidoro M, Pizzorusso T, Maffei L, Ratto GM (2013 ) Extracellular matrix inhibits structural and functional plasticity of dendritic spines in the adult visual cortex. Nat Commun 4:1484.

    Not in our library10.1038/ncomms2491

23. 23.

    Dick G, Tan CL, Alves JN, Ehlert EM, Miller GM, HsieshWilson LC, Sugahara K, Oosterhof A, van Kuppelvelt TH, Verhaagen J, Fawcett JW, Kwok JC (2013 ) Semaphorin 3A binds to the perineuronal nets via chondroitin sulfate type E motifs in rodent brains. J Biol Chem 288:27384–27395.

    Not in our library10.1074/jbc.m111.310029

24. 24.

    Dityatev A, Schachner M, Sonderegger P (2010 ) The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat Rev Neurosci 11:735–746.

    Not in our library10.1038/nrn2898

25. 25.

    Donato F, Jacobsen RI, Moser MB, Moser EI (2017 ) Stellate cells drive maturation of the entorhinal-hippocampal circuit. Science 355

    Not in our library10.1126/science.aai8178

26. 26.

    Donato F, Rompani SB, Caroni P (2013 ) Parvalbumin-expressing basket-cell network plasticity induced by experience regulates adult learning. Nature 504:272–276.

    Not in our library10.1038/nature12866

27. 27.

    Dudek SM, Alexander GM, Farris S (2016 ) Rediscovering area CA2: unique properties and functions. Nat Rev Neurosci 17:89–102.

    Not in our library10.1038/nrn.2015.22

28. 28.

    Ebbesen CL, Reifenstein ET, Tang Q, Burgalossi A, Ray S, Schreiber S, Kempter R, Brecht M (2016 ) Cell type-specific differences in spike timing and spike shape in the rat parasubiculum and superficial medial entorhinal cortex. Cell Rep 16:1005–1015.

    Not in our library10.1016/j.celrep.2016.06.057

29. 29.

    Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED (2009 ) Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat Neurosci 12:897–904.

    Not in our library10.1038/nn.2338

30. 30.

    Fujimaru Y, Kosaka T (1996 ) The distribution of two calcium binding proteins, calbindin D-28K and parvalbumin, in the entorhinal cortex of the adult mouse. Neurosci Res 24:329–343.

    Not in our library10.1016/0168-0102(95)01008-4

31. 31.

    Fyhn M, Hafting T, Moser MB, Moser EI (2007 ) Hippocampal remapping and grid cell realignment in the entorhinal cortex. Nature 446:190–194.

    Not in our library10.1038/nature05601

32. 32.

    Giamanco KA, Matthews RT (2012 ) Deconstructing the perineuronal net: cellular contributions and molecular composition of the neuronal extracellular matrix. Neuroscience 218:367–384.

    Not in our library10.1016/j.neuroscience.2012.05.055

33. 33.

    Gogolla N, Caroni P, Luthi A, Herry C (2009 ) Perineuronal nets protect fear memories from erasure. Science 325:1258–1261.

    Not in our library10.1126/science.1174146

34. 34.

    Hafting T, Fyhn M, Molden S, Moser MD, Moser EI (2005 ) Microstructure of a spatial map in the entorhinal cortex. Nature 134:801–806.

    Not in our library10.1038/nature03721

35. 35.

    Happel MFK, Niekisch H, Castiblanco Rivera LL, Ohl FW, Deliano M, Frischknecht R (2014 ) Enhanced cognitive flexibility in reversal learning induced by removal of the extracellular matrix in auditory cortex. Proc Natl Acad Sci USA 111:2800–2805.

    Not in our library10.1073/pnas.1310272111

36. 36.

    Härtig W, Brauer K, Brückner G (1992 ) Wisteria floribunda agglutinin-labelled nets surround parvalbumin-containing neurons. Neuroreport 3:869–872.

    Not in our library10.1097/00001756-199210000-00012

37. 37.

    Hensch TK (2005 ) Critical period plasticity in local cortical circuits. Nat Rev Neurosci 6:877–888.

    Not in our library10.1038/nrn1787

38. 38.

    Hitti FL, Siegelbaum SA (2014 ) The hippocampal CA2 region is essential for social memory. Nature 508:88–92.

    Not in our library10.1038/nature13028

39. 39.

    Hockfield S, McKay RD (1983 ) A surface antigen expressed by a subset of neurons in the vertebrate central nervous system. Proc Natl Acad Sci USA 80:5758–5761.

    Not in our library10.1073/pnas.80.18.5758

40. 40.

    Hockfield S, Kalb RG, Zaremba S, Fryer H (1990 ) Expression of neural proteoglycans correlates with the acquisition of mature neuronal properties in the mammalian brain. Cold Spring Harb Symp Quant Biol 55:505–514.

    Not in our library10.1101/sqb.1990.055.01.049

41. 41.

    Hylin MJ, Orsi SA, Moore AN, Dash PK (2013 ) Disruption of the perineuronal net in the hippocampus or medial prefrontal cortex impairs fear conditioning. Learn Mem 20:267–273.

    Not in our library10.1101/lm.030197.112

42. 42.

    Jones MW, McHugh TJ (2011 ) Updating hippocampal representations: CA2 joins the circuit. Trends Neurosci 35:526–535.

    Not in our library10.1016/j.tins.2011.07.007

43. 43.

    Kitamura T, Pignatelli M, Suh J, Kohara K, Yoshiki A, Abe K, Tonegawa S (2014 ) Island cells control temporal association memory. Science 343:896–901.

    Not in our library10.1126/science.1244634

44. 44.

    Kohara K, Pignatelli M, Rivest AJ, Jung HY, Kitamura T, Suh J, Frank D, Kajikawa K, Mise N, Obata Y, Wickersham IR, Tonegawa S (2014 ) Cell type-specific genetic and optogenetic tools reveal hippocampal CA2 circuits. Nat Neurosci 17:269–279.

    Not in our library10.1038/nn.3614

45. 45.

    Kosaka T, Heizmann CW (1989 ) Selective staining of a population of parvalbumin-containing GABAergic neurons in the rat cerebral cortex by lectins with specific affinity for N-terminal acetylgalactosamine. Brain Res 483:158–163.

    Not in our library10.1016/0006-8993(89)90048-6

46. 46.

    Kroppf E, Carmichael JE, Moser MB, Moser EI (2015 ) Speed cells in the medial entorhinal cortex. Nature 523:419–424.

    Not in our library10.1038/nature14622

47. 47.

    Lander C, Kind P, Maleski M, Hockfield S (1997 ) A family of activity-dependent neuronal cell-surface chondroitin sulfate proteoglycans in cat visual cortex. J Neurosci 17:1928–1939.

    Not in our library10.1523/jneurosci.17-06-01928.1997

48. 48.

    Langston RF, Ainge JA, Couey JJ, Canto CB, Bjerknes TL, Witter MP, Moser EI, Moser MB (2010 ) Development of the spatial representation system in the rat. Science 328:1576–1580.

    Not in our library10.1126/science.1188210

49. 49.

    Lendvai D, Morawski M, Negyessy L, Gati G, Jäger C, Baksa G, Glasz T, Attems J, Tanila H, Arendt T, Harkany T, Alpar A (2013 ) Neurochemical mapping of the human hippocampus reveals perisynaptic matrix around functional synapses in Alzheimer’s disease. Acta Neuropathol 125:215–229.

    Not in our library10.1007/s00401-012-1042-0

50. 50.

    Lensjø KK, Lepperød ME, Dick G, Hafting T, Fyhn M (2017 ) Removal of perineuronal nets unlocks juvenile plasticity through mechanisms of decreased inhibition and increased gamma activity. J Neurosci 37:1269–1283.

    Not in our library10.1523/jneurosci.2504-16.2016

51. 51.

    Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004 ) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295–1298.

    Not in our library10.1126/science.1100265

52. 52.
    Perineuronal nets increase inhibitory GABAergic currents during the critical period in rats · 2013

    Not checked
53. 53.

    Mankin EA, Diehl GW, Sparks FT, Leutgeb S, Leutgeb JK (2015 ) Hippocampal CA2 activity patterns change over time to a larger extent than between spatial contexts. Neuron 85:190–201.

    Not in our library10.1016/j.neuron.2014.12.001

54. 54.

    Morawski M, Reinert T, Meyer-Klaucke W, Wagner FE, Tröger W, Reinert A, Jäger C, Brückner G, Arendt T (2015 ) Ion exchanger in the brain: quantitative analysis of perineuronally fixed anionic binding sites suggests diffusion barriers with ion sorting properties. Sci Rep 5:16471.

    Not in our library10.1038/srep16471

55. 55.

    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.

    Not in our library10.1038/srep46024

56. 56.

    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.

    Not in our library10.1155/2016/6021428

57. 57.

    Pantazopoulos H, Berretta S (2016 ) In sickness and in health: perineuronal nets and synaptic plasticity in psychiatric disorders. Neural Plast 2016:9847696.

    Not in our library10.1155/2016/9847696

58. 58.

    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. Archives of General Psychiatry 67 (2), 155–166.

    Not in our library10.1001/archgenpsychiatry.2009.196

59. 59.

    Pielecka-Fortuna J, Kalogeraki E, Fortuna MG, Löwel S (2015 ) Optimal level activity of matrix metalloproteinases is critical for adult visual plasticity in the healthy and stroke-affected brain. eLife e5:11290.

    Not in our library10.7554/elife.11290

60. 60.

    Pizzorusso T, Medini P, Berardi N, Chierzi S, Fawcett JW, Maffei L (2002 ) Reactivation of ocular dominance plasticity in the adult visual cortex. Science 298:1248–1251.

    Not in our library10.1126/science.1072699

61. 61.

    Pizzorusso T, Medini P, Landi S, Baldini S, Berardi N, Maffei L (2006 ) Structural and functional recovery from early monocular deprivation in adult rats. Proc Natl Acad Sci USA 103:8517–8522.

    Not in our library10.1073/pnas.0602657103

62. 62.

    Ranson A, Cheetham CE, Fox K, Sengpiel F (2012 ) Homeostatic plasticity mechanisms are required for juvenile, but not adult, ocular dominance plasticity. Proc Natl Acad Sci USA 109:1311–1316.

    Not in our library10.1073/pnas.1112204109

63. 63.

    Romberg C, Yang S, Melani R, Andrews MR, Horner AE, Spillantini MG, Bussey TJ, Fawcett JW, Pizzorusso T, Saksida LM (2013 ) Depletion of perineuronal nets enhances recognition memory and long-term depression in the perirhinal cortex. J Neurosci 33:7057–7065.

    Not in our library10.1523/jneurosci.6267-11.2013

64. 64.

    Sadowski M, Wisniewski HM, Jakubowska-Sadowska K, Tarnawski M, Lazarewicz JW, Mossakowski MJ (1999 ) Pattern of neuronal loss in the rat hippocampus following experimental cardiac arrest-induced ischemia. J Neurol Sci 168:13–20.

    Not in our library10.1016/s0022-510x(99)00159-8

65. 65.

    Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser MB, Moser EI (2006 ) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312:758–762.

    Not in our library10.1126/science.1125572

66. 66.

    Sato M, Stryker MP (2008 ) Distinctive features of ocular dominance plasticity. J Neurosci 28:10278–10286.

    Not in our library10.1523/jneurosci.2451-08.2008

67. 67.

    Sawtell NB, Frenkel MY, Philpot BD, Nakazawa K, Tonegawa S, Bear MF (2003 ) NMDA receptor-dependent ocular dominance plasticity in adult visual cortex. Neuron 38:977–985.

    Not in our library10.1016/s0896-6273(03)00323-4

68. 68.

    Seeger G, Brauer K, Härtig W, Brückner G (1994 ) Mapping of perineuronal nets in the rat brain stained by colloidal iron hydroxide histochemistry and lectin cytochemistry. Neuroscience 58:371–388.

    Not in our library10.1016/0306-4522(94)90044-2

69. 69.

    Simons SB, Caruana DA, Zhao M, Dudek SM (2011 ) Caffeine-induced synaptic potentiation in hippocampal CA2 neurons. Nat Neurosci 15:23–25.

    Not in our library10.1038/nn.2962

70. 70.

    Slaker M, Churchill L, Todd RP, Blacktop JM, Zuloaga DG, Raber J, Darling RA, Brown TE, Sorg BA (2015 ) Removal of perineuronal nets in the medial prefrontal cortex impairs the acquisition and reconsolidation of a cocaine-induced conditioned place preference memory. J Neurosci 35:4190–4202.

    Not in our library10.1523/jneurosci.3592-14.2015

71. 71.

    Stensola H, Stensola T, Solstad T, Frøland K, Moser MB, Moser EI (2012 ) The entorhinal grid map discretized. Nature 492:72–78.

    Not in our library10.1038/nature11649

72. 72.

    Sugiyama S, Di Nardo AA, Aizawa S, Matsuo I, Volovitch M, Prochiantz A, Hensch TK (2008 ) Experience-dependent transfer of Otx2 homeoprotein into the visual cortex activates postnatal plasticity. Cell 134:508–520.

    Not in our library10.1016/j.cell.2008.05.054

73. 73.

    Sun C, Kitamura T, Yamamoto J, Martin J, Pignatelli M, Kitch LJ, Schnitzer MJ, Tonegawa S (2015 ) Distinct speed dependence of entorhinal island and ocean cells, including respective grid cells. Proc Natl Acad Sci USA 112:9466–9471.

    Not in our library10.1073/pnas.1511668112

74. 74.

    Tagawa Y, Kanold PO, Majdan M, Shatz CJ (2005 ) Multiple periods of ocular dominance plasticity in mouse visual cortex. Nat Neurosci 8:380–388.

    Not in our library10.1038/nn1410

75. 75.

    Tang Q, Burgalossi A, Ebbesen CL, Ray S, Naumann R, Schmidt H, Brecht M (2014 ) Pyramidal and stellate cell specificity of grid and border representations in layer 2 of medial entorhinal cortex. Neuron 84:1191–1197.

    Not in our library10.1016/j.neuron.2014.11.009

76. 76.

    Tsien RY (2013 ) Very long-term memories may be stored in the pattern of holes in the perineuronal net. Proc Natl Acad Sci USA 110:12456–12461.

    Not in our library10.1073/pnas.1310158110

77. 77.

    Wandell BA, Smirnakis SM (2009 ) Plasticity and stability of visual field maps in adult primary visual cortex. Nat Rev Neurosci 10:873–884.

    Not in our library10.1038/nrn2741

78. 78.

    Wang BS, Sarnaik R, Cang J (2010 ) Critical period plasticity matches binocular orientation preference in the visual cortex. Neuron 65:246–256.

    Not in our library10.1016/j.neuron.2010.01.002

79. 79.

    Wegner F, Härtig W, Bringmann A, Grosche J, Woglfarth 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 184:705–714.

    Not in our library10.1016/s0014-4886(03)00313-3

80. 80.

    Wills TJ, Cacucci F, Burgess N, O’Keefe J (2010 ) Development of the hippocampal cognitive map in preweanling rats. Science 328:1573–1576.

    Not in our library10.1126/science.1188224

81. 81.

    Witter M (2007 ) The perforant path: projections from the entorhinal cortex to the dentate gyrus. Prog Brain Res 163:43–61.

    Not in our library10.1016/s0079-6123(07)63003-9

82. 82.

    Wouterlood FG, Härtig W, Brückner G, Witter MP (1995 ) Parvalbumin-immunoreactive neurons in the entorhinal cortex of the rat: localization, morphology, connectivity and ultrastructure. J Neurocytol 24:135–153.

    Not in our library10.1007/bf01181556

83. 83.

    Yamada J, Jinno S (2013 ) Spatio-temporal differences in perineuronal net expression in the mouse hippocampus, with reference to parvalbumin. Neuroscience 253:368–379.

    Not in our library10.1016/j.neuroscience.2013.08.061

84. 84.

    Yamada J, Ohgomori T, Jinno S (2015 ) Perineuronal nets affect parvalbumin expression in GABAergic neurons of the mouse hippocampus. Eur J Neurosci 41:368–379.

    Not in our library10.1111/ejn.12792

85. 85.

    Yamada J, Jinno S (2016 ) Molecular heterogeneity of aggrecan-based perineuronal nets around five subclasses of parvalbumin-expressing neurons in the mouse hippocampus. J Comp Neur 525:1234-1249.

    Not in our library10.1111/ejn.12792

86. 86.

    Ye Q, Miao Q (2013 ) Experience-dependent development of perineuronal nets and chondroitin sulfate proteoglycan receptors in mouse visual cortex. Matrix Biol 32:352–363.

    Not in our library10.1016/j.matbio.2013.04.001

87. 87.

    Zao M, Choi YS, Obrietan K, Dudek SM (2007 ) Synaptic plasticity (and the lack thereof) in hippocampal CA2 neurons. J Neurosci 27:12025–12032.

    Not in our library10.1523/jneurosci.4094-07.2007

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