Releasing the peri-neuronal net to patch-clamp neurons in adult CNS

Pflügers Archiv - Tập 448 - Trang 248-258 - 2004
Ezequiel Morales1, Fernando R. Fernandez1, Suzanne Sinclair1, Michael L. Molineux1, W. Hamish Mehaffey1, Ray W. Turner1
1Neuroscience Research Group, University of Calgary, Calgary, Canada

Tóm tắt

The extracellular matrix of adult neural tissue contains chondroitin sulphated proteogylcans that form a dense peri-neuronal net surrounding the cell body and proximal dendrites of many neuronal classes. Development of the peri-neuronal net beyond approximately postnatal day 17 obscures visualization and often access by patch electrodes to neuronal membranes with the result that patch clamp recordings are most readily obtained from early postnatal animals. We describe a technique in which the surface tension of a sucrose-based medium promotes partial dissociation of thin tissue slices from adult tissue. Surface tension spreads the tissue and loosens the peri-neuronal net from neuronal membranes within minutes and in the absence of proteolytic enzymes. Furthermore, the extent of dissociation can be controlled so as to maintain the overall slice structure and allow identification of specific cell classes. Excellent structural preservation of neurons and dendrites can be obtained and full access by patch electrodes made possible for current- or voltage-clamp recordings in tissue well beyond the development of peri-neuronal nets. We demonstrate the feasibility of using this approach through patch recordings from neurons in the brainstem and cerebellum of adult gymnotiform fish and in deep cerebellar nuclei of rats as old as 6 months.

Tài liệu tham khảo

Aizenman, CD, Linden DJ (1999) Regulation of the rebound depolarization and spontaneous firing patterns of deep nuclear neurons in slices of rat cerebellum. J Neurophysiol 82:1697–1709

Baker, GB, Boulton AA, Walz W (eds) (1992) Practical cell culture techniques (Neuromethods series, Vol. 23). Humana Press, Totowa, pp xix, 392

Barres BA, Koroshetz WJ, Chun LL, Corey DP (1990) Ion channel expression by white matter glia: the type-1 astrocyte. Neuron 5:527–544

Beckh S, Noda M, Lubbert H, Numa S (1989) Differential regulation of three sodium channel messenger RNAs in the rat central nervous system during development. EMBO J 8:3611–3616

Berman N, Maler L (1999) Neural architecture of the electrosensory lateral line lobe: adaptations for coincidence detection, a sensory searchlight and frequency-dependent adaptive filtering. J Exp Biol 202:1243–1253

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

Borst JG, Helmchen F, Sakmann B (1995) Pre- and postsynaptic whole-cell recordings in the medial nucleus of the trapezoid body of the rat. J Physiol (Lond) 489:825–840

Brockhaus J, Deitmer JW (2002) Long-lasting modulation of synaptic input to Purkinje neurons by Bergmann glia stimulation in rat brain slices. J Physiol (Lond) 545:581–593

Bruckner G, Brauer K, Hartig 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

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

Bruckner G, Bringmann A, Koppe G, Hartig W, Brauer K (1996) In vivo and in vitro labelling of perineuronal nets in rat brain. Brain Res 720:84–92

Bruckner G, Grosche J (2001) Perineuronal nets show intrinsic patterns of extracellular matrix differentiation in organotypic slice cultures. Exp Brain Res 137:83–93

Bruckner, G, Seeger G, Brauer K, Hartig W, Kacza J, Bigl V (1994) Cortical areas are revealed by distribution patterns of proteoglycan components and parvalbumin in the Mongolian gerbil and rat. Brain Res 658:67–86

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

Colbert CM, Pan E (2002) Ion channel properties underlying axonal action potential initiation in pyramidal neurons. Nat Neurosci 5:533–538

Czubayko U, Sultan F, Thier P, Schwarz C (2001) Two types of neurons in the rat cerebellar nuclei as distinguished by membrane potentials and intracellular fillings. J Neurophysiol 85:2017–2029

Dodt HU, Zieglgansberger W (1998) Visualization of neuronal form and function in brain slices by infrared videomicroscopy. Histochem J 30:141–152

Edwards FA, Konnerth A, Sakmann B, Takahashi T (1989) A thin slice preparation for patch clamp recordings from neurones of the mammalian central nervous system. Pflugers Arch 414:600–612

Fernandez FR, Morales E, Rashid AJ, Dunn RJ, Turner RW (2003) Inactivation of Kv3.3 potassium channels in heterologous expression systems. J Biol Chem 278:40890–40898

Forsythe ID (1994) Direct patch recording from identified presynaptic terminals mediating glutamatergic EPSCs in the rat CNS, in vitro. J Physiol (Lond) 479:381–387

Gabbiani F, Metzner W, Wessel R, Koch C (1996) From stimulus encoding to feature extraction in weakly electric fish. Nature 384:564–567

Gähwiler BH (1988) Organotypic cultures of neural tissue. Trends Neurosci 11:484–489

Gauck V, Jaeger D (2003) The contribution of NMDA and AMPA conductances to the control of spiking in neurons of the deep cerebellar nuclei. J Neurosci 23:8109–8118

Gong B, Rhodes KJ, Bekele-Arcuri Z, Trimmer JS (1999) Type I and type II Na+ channel alpha-subunit polypeptides exhibit distinct spatial and temporal patterning, and association with auxiliary subunits in rat brain. J Comp Neurol 412:342–352

Gray, R, Johnston D (1985) Rectification of single GABA-gated chloride channels in adult hippocampal neurons. J Neurophysiol 54:134–142

Hartig W, Derouiche A, Welt K, Brauer K, Grosche J, Mader M, Reichenbach A, Bruckner 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

Hausen D, Bruckner G, Drlicek M, Hartig W, Brauer K, Bigl V (1996) Pyramidal cells ensheathed by perineuronal nets in human motor and somatosensory cortex. Neuroreport 7:1725–1729

Hirono J, Sato T, Tonoike M, Takebayashi M (1992) Simultaneous recording of [Ca2+]i increases in isolated olfactory receptor neurons retaining their original spatial relationship in intact tissue. J Neurosci Methods 42:185–194

Hockfield S (1990) Proteoglycans in neural development. Semin Dev Biol 1

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

Kay AR, Wong RK (1986) Isolation of neurons suitable for patch-clamping from adult mammalian central nervous systems. J Neurosci Methods 16:227–238

Koppe G, Bruckner G, Brauer K, Hartig W, Bigl V (1997) Developmental patterns of proteoglycan-containing extracellular matrix in perineuronal nets and neuropil of the postnatal rat brain. Cell Tissue Res 288:33–41

Koppe G, Bruckner G, Hartig W, Delpech B, Bigl V (1997) Characterization of proteoglycan-containing perineuronal nets by enzymatic treatments of rat brain sections. Histochem J 29:11–20

Kotecha SA, Eley DW, Turner RW (1997) Tissue printed cells from teleost electrosensory and cerebellar structures. J Comp Neurol 386:277–292

Kotecha SA, Schlichter LC (1999) A Kv1.5 to Kv1.3 switch in endogenous hippocampal microglia and a role in proliferation. J Neurosci 19:10680–10693

Krahe R, Gabbiani F (2004) Burst firing in sensory systems. Nat Rev Neurosci 5:13–23

Lafarga M, Berciano MT, Blanco M (1984) The perineuronal net in the fastigial nucleus of the rat cerebellum. A Golgi and quantitative study. Anat Embryol (Berl) 170:79–85

Lander C, Zhang H, Hockfield S (1998) Neurons produce a neuronal cell surface-associated chondroitin sulfate proteoglycan. J Neurosci 18:174–183

Larkum ME, Kaiser KM, Sakmann B (1999) Calcium electrogenesis in distal apical dendrites of layer 5 pyramidal cells at a critical frequency of back-propagating action potentials. Proc Natl Acad Sci USA 96:14600–14604

Lemon N, Turner RW (2000) Conditional spike backpropagation generates burst discharge in a sensory neuron. J Neurophysiol 89:1519–1530

Mabuchi M, Murakami S, Taguchi T, Ohtsuka A, Murakami T (2001) Purkinje cells in the adult cat cerebellar cortex possess a perineuronal net of proteoglycans. Arch Histol Cytol 64:203–209

Magee JC, Johnston D (1995) Characterization of single voltage-gated Na+ and Ca2+ channels in apical dendrites of rat CA1 pyramidal neurons. J Physiol (Lond) 487:67–90

Maler L (1979) The posterior lateral line lobe of certain gymnotoid fish: quantitative light microscopy. J Comp Neurol 183:323–363

Maler L, Sas EK, Rogers J (1981) The cytology of the posterior lateral line lobe of high-frequency weakly electric fish (Gymnotidae): dendritic differentiation and synaptic specificity in a simple cortex. J Comp Neurol 195:87–139

Margrie TW, Brecht M, Sakmann B (2002) In vivo, low-resistance, whole-cell recordings from neurons in the anaesthetized and awake mammalian brain. Pflugers Arch 444:491–498

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

Milev P, Maurel P, Chiba A, Mevissen M, Popp S, Yamaguchi Y, Margolis RK, Margolis RU (1998) Differential regulation of expression of hyaluronan-binding proteoglycans in developing brain: aggrecan, versican, neurocan, and brevican. Biochem Biophys Res Commun 247:207–212

Morris NP, Henderson Z (2000) Perineuronal nets ensheath fast spiking, parvalbumin-immunoreactive neurons in the medial septum/diagonal band complex. Eur J Neurosci 12:828–838

Murakami T, Su WD, Ohtsuka A, Abe K, Ninomiya Y (1999) Perineuronal nets of proteoglycans in the adult mouse brain are digested by collagenase. Arch Histol Cytol 62:199–204

Noonan L, Doiron B, Laing C, Longtin A, Turner RW (2003) A dynamic dendritic refractory period regulates burst discharge in the electrosensory lobe of weakly electric fish. J Neurosci 23:1524–1534

Prescott SA, De Koninck Y (2002) Four cell types with distinctive membrane properties and morphologies in lamina I of the spinal dorsal horn of the adult rat. J Physiol (Lond) 539:817–836

Raman IM, Gustafson AE, Padgett D (2000) Ionic currents and spontaneous firing in neurons isolated from the cerebellar nuclei. J Neurosci 20:9004–9016

Rashid AJ, Dunn RJ, Turner RW (2001) A prominent soma-dendritic distribution of Kv3.3 K+ channels in electrosensory and cerebellar neurons. J Comp Neurol 441:234–247

Rashid AJ, Morales E, Turner RW, Dunn RW (2001) The contribution of dendritic Kv3 K+ channels to burst threshold in a sensory neuron. J Neurosci 21:125–135

Rose GJ, Fortune ES (1996) New techniques for making whole-cell recordings from CNS neurons in vivo. Neurosci Res 26:89–94

Sas E, Maler L (1987) The organization of afferent input to the caudal lobe of the cerebellum of the gymnotid fish Apteronotus leptorhynchus. Anat Embryol (Berl) 177:55–79

Schoniger S, Wehming S, Gonzalez C, Schobitz K, Rodriguez E, Oksche A, Yulis CR, Nurnberger F (2001) The dispersed cell culture as model for functional studies of the subcommissural organ: preparation and characterization of the culture system. J Neurosci Methods 107:47–61

Severson CA, Wang W, Pieribone VA, Dohle CI, Richerson GB (2003) Midbrain serotonergic neurons are central pH chemoreceptors. Nat Neurosci 6:1139–1140

Spruston N, Schiller Y, Stuart G, Sakmann B (1995) Activity-dependent action potential invasion and calcium influx into hippocampal CA1 dendrites [see comments]. Science 268:297–300

Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173–182

Stuart G, Spruston N, Sakmann B, Hausser M (1997) Action potential initiation and backpropagation in neurons of the mammalian CNS. Trends Neurosci 20:125–131

Tanaka M, Maeda N, Noda M, Marunouchi T (2003) A chondroitin sulfate proteoglycan PTPzeta/RPTPbeta regulates the morphogenesis of Purkinje cell dendrites in the developing cerebellum. J Neurosci 23:2804–2814

Turner RW, Borg LL, Syed NI (1995) A technique for the primary dissociation of neurons from restricted regions of the vertebrate CNS. J Neurosci Methods 56:57–70

Turner RW, Plant JR, Maler L (1996) Oscillatory and burst discharge across electrosensory topographic maps. J Neurophysiol 76:2364–2382

Victorov IV, Lyjin AA, Aleksandrova OP (2001) A modified roller method for organotypic brain cultures: free-floating slices of postnatal rat hippocampus. Brain Res Brain Res Protoc 7:30–37

Yamaguchi Y (2000) Lecticans: organizers of the brain extracellular matrix. Cell Mol Life Sci 57:276–289

Thông tin
Thông tin xuất bản

Pflügers Archiv

Tập 448

248-258

Thông tin tác giả