Perineuronal Nets Enhance the Excitability of Fast-Spiking Neurons

Abstract

Perineuronal nets (PNNs) are specialized complexes of extracellular matrix molecules that surround the somata of fast-spiking neurons throughout the vertebrate brain. PNNs are particularly prevalent throughout the auditory brainstem, which transmits signals with high speed and precision. It is unknown whether PNNs contribute to the fast-spiking ability of the neurons they surround. Whole-cell recordings were made from medial nucleus of the trapezoid body (MNTB) principal neurons in acute brain slices from postnatal day 21 (P21) to P27 mice. PNNs were degraded by incubating slices in chondroitinase ABC (ChABC) and were compared to slices that were treated with a control enzyme (penicillinase). ChABC treatment did not affect the ability of MNTB neurons to fire at up to 1000 Hz when driven by current pulses. However, f – I (frequency–intensity) curves constructed by injecting Gaussian white noise currents superimposed on DC current steps showed that ChABC treatment reduced the gain of spike output. An increase in spike threshold may have contributed to this effect, which is consistent with the observation that spikes in ChABC-treated cells were delayed relative to control-treated cells. In addition, parvalbumin-expressing fast-spiking cortical neurons in >P70 slices that were treated with ChABC also had reduced excitability and gain. The development of PNNs around somata of fast-spiking neurons may be essential for fast and precise sensory transmission and synaptic inhibition in the brain.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 63

1. 1.

   Ashida G, Carr CE (2011 ) Sound localization: Jeffress and beyond. Curr Opin Neurobiol 21:745-751.

   Not in our library10.1016/j.conb.2011.05.008

2. 2.

   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

3. 3.

   Bertolotto A, Manzardo E, Guglielmone R (1996 ) Immunohistochemical mapping of perineuronal nets containing chondroitin unsulfated proteoglycan in the rat central nervous system. Cell Tissue Res 283:283-295.

   Not in our library10.1007/s004410050538

4. 4.

   Blosa M, Sonntag M, Brückner G, Jäger C, Seeger G, Matthews RT, Rübsamen R, Arendt T, Morawski M (2013 ) Unique features of extracellular matrix in the mouse medial nucleus of trapezoid body—implications for physiological functions. Neuroscience 228:215-234.

   Not in our library10.1016/j.neuroscience.2012.10.003

5. 5.

   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 593:4341-4360.

   Not in our library10.1113/jp270849

6. 6.

   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 8:183-200.

   Not in our library10.1002/glia.440080306

7. 7.

   Bryant HL, Segundo JP (1976 ) Spike initiation by transmembrane current: a white-noise analysis. J Physiol 260:279-314.

   Not in our library10.1113/jphysiol.1976.sp011516

8. 8.

   Bukalo O, Schachner M, Dityatev A (2001 ) Modification of extracellular matrix by enzymatic removal of chondroitin sulfate and by lack of tenascin-R differentially affects several forms of synaptic plasticity in the hippocampus. Neuroscience 104:359-369.

   Not in our library10.1016/s0306-4522(01)00082-3

9. 9.

   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

10. 10.

    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

11. 11.

    Celio MR, Spreafico R, De Biasi S, Vitellaro-Zuccarello L (1998 ) Perineuronal nets: past and present. Trends Neurosci 21:510-515.

    Not in our library10.1016/s0166-2236(98)01298-3

12. 12.

    Chattopadhyaya B, Di Cristo G, Higashiyama H, Knott GW, Kuhlman SJ, Welker E, Huang ZJ (2004 ) Experience and activity-dependent maturation of perisomatic GABAergic innervation in primary visual cortex during a postnatal critical period. J Neurosci 24:9598-9611.

    Not in our library10.1523/jneurosci.1851-04.2004

13. 13.

    Dityatev A, Brückner G, Dityateva G, Grosche J, Kleene R, Schachner M (2007 ) Activity-dependent formation and functions of chondroitin sulfate-rich extracellular matrix of perineuronal nets. Dev Neurobiol 67:570-588.

    Not in our library10.1002/dneu.20361

14. 14.

    Fawcett J (2009 ) Molecular control of brain plasticity and repair. Prog Brain Res 175:501-509.

    Not in our library10.1016/s0079-6123(09)17534-9

15. 15.

    Frankenhaeuser B, Hodgkin AL (1957 ) The action of calcium on the electrical properties of squid axons. J Physiol 137:218-244.

    Not in our library10.1113/jphysiol.1957.sp005808

16. 16.

    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

17. 17.

    Galtrey CM, Asher RA, Nothias F, Fawcett JW (2007 ) Promoting plasticity in the spinal cord with chondroitinase improves functional recovery after peripheral nerve repair. Brain 130:926-939.

    Not in our library10.1093/brain/awl372

18. 18.

    García-Alías G, Barkhuysen S, Buckle M, Fawcett JW (2009 ) Chondroitinase ABC treatment opens a window of opportunity for task-specific rehabilitation. Nat Neurosci 12:1145-1151.

    Not in our library10.1038/nn.2377

19. 19.

    Giger RJ, Hollis ER 2nd, Tuszynski MH (2010 ) Guidance molecules in axon regeneration. Cold Spring Harb Perspect Biol 2:a001867.

    Not in our library10.1101/cshperspect.a001867

20. 20.

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

    Not in our library10.1126/science.1174146

21. 21.

    Harauzov A, Spolidoro M, DiCristo G, De Pasquale R, Cancedda L, Pizzorusso T, Viegi A, Berardi N, Maffei L (2010 ) Reducing intracortical inhibition in the adult visual cortex promotes ocular dominance plasticity. J Neurosci 30:361-371.

    Not in our library10.1523/jneurosci.2233-09.2010

22. 22.

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

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

23. 23.

    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.

    Not in our library10.1016/s0006-8993(99)01784-9

24. 24.

    Härtig W, Singer A, Grosche J, Brauer K, Ottersen OP, Brückner G (2001 ) Perineuronal nets in the rat medial nucleus of the trapezoid body surround neurons immunoreactive for various amino acids, calcium-binding proteins and the potassium channel subunit Kv3.1b. Brain Res 899:123-133.

    Not in our library10.1016/s0006-8993(01)02211-9

25. 25.

    Henze DA, Buzsáki G (2001 ) Action potential threshold of hippocampal pyramidal cells in vivo is increased by recent spiking activity. Neuroscience 105:121-130.

    Not in our library10.1016/s0306-4522(01)00167-1

26. 26.

    Hermann J, Pecka M, von Gersdorff H, Grothe B, Klug A (2007 ) Synaptic transmission at the calyx of Held under in vivo like activity levels. J Neurophysiol 98:807-820.

    Not in our library10.1152/jn.00355.2007

27. 27.

    Hille B (2001 ) Ion channels of excitable membranes, Ed 3 Sunderland, MA: Sinauer Associates.

    Not in our library

28. 28.

    Hrabetová S, Masri D, Tao L, Xiao F, Nicholson C (2009 ) Calcium diffusion enhanced after cleavage of negatively charged components of brain extracellular matrix by chondroitinase ABC. J Physiol 587:4029-4049.

    Not in our library10.1113/jphysiol.2009.170092

29. 29.

    Huang H, Trussell L (2011 ) KCNQ5 channels control resting properties and release probability of a synapse. Nat Neurosci 14:840-847.

    Not in our library10.1038/nn.2830

30. 30.

    Johnston J, Postlethwaite M, Forsythe ID (2009 ) The impact of synaptic conductance on action potential waveform: evoking realistic action potentials with a simulated synaptic conductance. J Neurosci Methods 183:158-164.

    Not in our library10.1016/j.jneumeth.2009.06.025

31. 31.

    Kim J, Renden R, von Gersdorff H (2013 ) Dysmyelination of auditory afferent axons increases the jitter of action potential timing during high-frequency firing. J Neurosci 33:9402-9407.

    Not in our library10.1523/jneurosci.3389-12.2013

32. 32.

    Kirkwood A, Bear MF (1994 ) Hebbian synapses in visual cortex. J Neurosci 14:1634-1645.

    Not in our library10.1523/jneurosci.14-03-01634.1994

33. 33.

    Kochlamazashvili G, Henneberger C, Bukalo O, Dvoretskova E, Senkov O, Lievens PM, Westenbroek R, Engel AK, Catterall WA, Rusakov DA, Schachner M, Dityatev A (2010 ) The extracellular matrix molecule hyaluronic acid regulates hippocampal synaptic plasticity by modulating postsynaptic L-type Ca(2+) channels. Neuron 67:116-128.

    Not in our library10.1016/j.neuron.2010.05.030

34. 34.

    Kopp-Scheinpflug C, Tolnai S, Malmierca MS, Rübsamen R (2008 ) The medial nucleus of the trapezoid body: comparative physiology. Neuroscience 154:160-170.

    Not in our library10.1016/j.neuroscience.2008.01.088

35. 35.

    Kuhlman SJ, Lu J, Lazarus MS, Huang ZJ (2010 ) Maturation of GABAergic inhibition promotes strengthening of temporally coherent inputs among convergent pathways. PLoS Comput Biol 6:e1000797.

    Not in our library10.1371/journal.pcbi.1000797

36. 36.

    Kuhlman SJ, Olivas ND, Tring E, Ikrar T, Xu X, Trachtenberg JT (2013 ) A disinhibitory microcircuit initiates critical-period plasticity in the visual cortex. Nature 501:543–546.

    Not in our library10.1038/nature12485

37. 37.

    Massey JM, Hubscher CH, Wagoner MR, Decker JA, Amps J, Silver J, Onifer SM (2006 ) Chondroitinase ABC digestion of the perineuronal net promotes functional collateral sprouting in the cuneate nucleus after cervical spinal cord injury. J Neurosci 26:4406-4414.

    Not in our library10.1523/jneurosci.5467-05.2006

38. 38.

    Mataga N, Mizuguchi Y, Hensch TK (2004 ) Experience-dependent pruning of dendritic spines in visual cortex by tissue plasminogen activator. Neuron 44:1031-1041.

    Not in our library10.1016/j.neuron.2004.11.028

39. 39.

    McGee AW, Yang Y, Fischer QS, Daw NW, Strittmatter SM (2005 ) Experience-driven plasticity of visual cortex limited by myelin and Nogo receptor. Science 309:2222-2226.

    Not in our library10.1126/science.1114362

40. 40.

    Mease RA, Famulare M, Gjorgjieva J, Moody WJ, Fairhall AL (2013 ) Emergence of adaptive computation by single neurons in the developing cortex. J Neurosci 33:12154-12170.

    Not in our library10.1523/jneurosci.3263-12.2013

41. 41.

    Miyata S, Nishimura Y, Hayashi N, Oohira A (2005 ) Construction of perineuronal net-like structure by cortical neurons in culture. Neuroscience 136:95-104.

    Not in our library10.1016/j.neuroscience.2005.07.031

42. 42.

    Morawski M, Reinert T, Brückner G, Wagner FE, Arendt TH, Tröger W (2004 ) The binding of iron to perineuronal nets: a combined nuclear microscopy and Mössbauer study. Hyperfine Interact 159:285-291.

    Not in our library10.1007/s10751-005-9116-1

43. 43.

    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

44. 44.

    Murakami T, Tsubouchi M, Tubouchi Y, Taguchi T, Ohtsuka A (1994 ) The occurrence of neurons with strongly negatively charged surface coats in mammalian, avian, reptilian, amphibian and piscine brains. Acta Med Okayama 48:195-197.

    Not in our library10.18926/amo/31092

45. 45.

    Myers AK, Ray J, Kulesza RJ Jr (2012 ) Neonatal conductive hearing loss disrupts the development of the Cat-315 epitope on perineuronal nets in the rat superior olivary complex. Brain Res 1465:34-47.

    Not in our library10.1016/j.brainres.2012.05.024

46. 46.

    Oertel D (1999 ) The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61:497-519.

    Not in our library10.1146/annurev.physiol.61.1.497

47. 47.

    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

48. 48.

    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 U S A 103:8517-8522.

    Not in our library10.1073/pnas.0602657103

49. 49.

    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

50. 50.

    Schneider CA, Rasband WS, Eliceiri KW (2012 ) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675.

    Not in our library10.1038/nmeth.2089

51. 51.

    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

52. 52.

    Shen Y, Tenney AP, Busch SA, Horn KP, Cuascut FX, Liu K, He Z, Silver J, Flanagan JG (2009 ) PTPsigma is a receptor for chondroitin sulfate proteoglycan, an inhibitor of neural regeneration. Science 326:592-596.

    Not in our library10.1126/science.1178310

53. 53.

    Slee SJ, Higgs MH, Fairhall AL, Spain WJ (2005 ) Two-dimensional time coding in the auditory brainstem. J Neurosci 25:9978-9988.

    Not in our library10.1523/jneurosci.2666-05.2005

54. 54.

    Sonntag M, Blosa M, Schmidt S, Rübsamen R, Morawski M (2015 ) Perineuronal nets in the auditory system. Hear Res 329:21-32.

    Not in our library10.1016/j.heares.2014.12.012

55. 55.

    Srinivasan J, Schachner M, Catterall WA (1998 ) Interaction of voltage-gated sodium channels with the extracellular matrix molecules tenascin-C and tenascin-R. Proc Natl Acad Sci U S A 95:15753-15757.

    Not in our library10.1073/pnas.95.26.15753

56. 56.

    Street SE, Manis PB (2007 ) Action potential timing precision in dorsal cochlear nucleus pyramidal cells. J Neurophysiol 97:4162-4172.

    Not in our library10.1152/jn.00469.2006

57. 57.

    Takesian AE, Hensch TK (2013 ) Balancing plasticity/stability across brain development In: Progress in brain research (Michael M. Merzenich MN, Thomas MVV, eds), pp 3-34. New York: Elsevier.

    Not in our library10.1016/b978-0-444-63327-9.00001-1

58. 58.

    Taschenberger H, von Gersdorff H (2000 ) Fine-tuning an auditory synapse for speed and fidelity: developmental changes in presynaptic waveform, EPSC kinetics, and synaptic plasticity. J Neurosci 20:9162-9173.

    Not in our library10.1523/jneurosci.20-24-09162.2000

59. 59.

    Taschenberger H, Leão RM, Rowland KC, Spirou GA, von Gersdorff H (2002 ) Optimizing synaptic architecture and efficiency for high-frequency transmission. Neuron 36:1127-1143.

    Not in our library10.1016/s0896-6273(02)01137-6

60. 60.

    Trussell LO (1997 ) Cellular mechanisms for preservation of timing in central auditory pathways. Curr Opin Neurobiol 7:487-492.

    Not in our library10.1016/s0959-4388(97)80027-x

61. 61.

    Trussell LO (1999 ) Synaptic mechanisms for coding timing in auditory neurons. Annu Rev Physiol 61:477-496.

    Not in our library10.1146/annurev.physiol.61.1.477

62. 62.

    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.

    Not in our library10.1073/pnas.1310158110

63. 63.

    Vorobyov V, Kwok JC, Fawcett JW, Sengpiel F (2013 ) Effects of digesting chondroitin sulfate proteoglycans on plasticity in cat primary visual cortex. J Neurosci 33:234-243.

    Not in our library10.1523/jneurosci.2283-12.2013

Cited by papers we hold 6

• Microglia as hackers of the matrix: sculpting synapses and the extracellular space · 2021
  No notice
• Impact of Perineuronal Nets on Electrophysiology of Parvalbumin Interneurons, Principal Neurons, and Brain Oscillations: A Review · 2021
  No notice
• Perineuronal nets stabilize the grid cell network · 2021
  No notice
• Perineuronal nets decrease membrane capacitance of peritumoral fast spiking interneurons in a model of epilepsy · 2018
  No notice
• The Perineuronal ‘Safety’ Net? Perineuronal Net Abnormalities in Neurological Disorders · 2018
  No notice
• Differential Expression and Cell-Type Specificity of Perineuronal Nets in Hippocampus, Medial Entorhinal Cortex, and Visual Cortex Examined in the Rat and Mouse · 2017
  No notice

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.