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1 Supporting Online Material for Long-Term Potentiation of Neuron-Glia Synapses Mediated by Ca 2+ - Permeable AMPA Receptors Woo-Ping Ge, Xiu-Juan Yang, Zhi-Jun Zhang, Hui-Kun Wang, Wan-Hua Shen, Qiu- Dong Deng, Shumin Duan* *To whom correspondence should be addressed. shumin@ion.ac.cn This PDF file includes: Materials and Methods Figs. S1 to S3 Published 9 June 2006, Science 312, 1533 (2006) DOI: /science

2 Supporting Online Material Slice preparation. Hippocampal slices were prepared as described previously(12). The use and care of animals in this study followed the guideline of the Shanghai Institutes for Biological Sciences Animal Research Advisory Committee. In brief, rats (postnatal 14 ~ 17 days except where noted) were anaesthetized with sodium pentobarbital. After decapitation, hippocampal formation was dissected rapidly and placed in ice-cold oxygenated (95% O 2 and 5% CO 2 ) solution containing (in mm): 119 NaCl, 2.5 KCl, 2.5 CaCl 2, 1.3 MgSO 4, 1 NaH 2 PO 4, 26.2 NaHCO 3 and 11 Glucose. Transverse slices (400 µm thick) were cut with a vibratome and maintained in an incubation chamber for at least 2 hr at 25 o C before recording. During experiments, individual slice was transferred to a submersion-recording chamber and was continuously perfused with the above oxygenated solution (3.0 ml/min) at room temperature (22-25 o C). Slices were visualized with infrared optics using an upright microscope equipped with DIC optics. Electrophysiology. Whole-cell patch recordings were made from glial cells in s. radiatum in the presence of GABA A antagonist bicuculline (10µM) or picrotoxin (50µM). Recording pipettes were routinely filled with a solution containing (in mm): 125 Cs-gluconate, 5 CsCl, 10 HEPES, 8 NaCl, 3 Na 2 ATP, 0.3 Na-GTP, 0.2 EGTA, 10 Na 2 - phosphocreatine, 10 TEA-Cl, 2 BaCl 2 (ph 7.3, mosm). In some experiments 0.1 mm spermine was added to the pipette solution to examine the rectification of SCinduced EPSCs in NG2 cells before and after TBS induction. For K + current recordings and current-clamp recordings, pipette solution contained (in mm): 125 K-gluconate, 15

3 KCl, 10 HEPES, 8 NaCl, 3Na 2 ATP, 0.3 Na-GTP, 10 Na 2 -phosphocreatine, 0.2 EGTA (ph 7.3, mosm). 1 µm TTX was added to the extracellular solution. Extracellular solution for calcium current recording contained (in mm): 89 NaCl, 10 CsCl, 2.5 KCl, 2.5 CaCl 2, 1.3 MgSO 4, 1 NaH 2 PO 4, 20 TEA-Cl, 5 4-Aminopyridine, 1 BaCl 2, 26.2 NaHCO 3 11 Glucose, and TTX. This solution was also used for Na + current recording except that TTX was omitted. In some experiments, current-voltage curves of calcium or sodium channels were examined in the presence of K + channel blockers using a typical protocol (100 ms, 10 mv steps from -70 to +40 mv, preceded by a prepulse conditioning potential of -120 mv for 200ms). The membrane potential was held at 80 mv for NG2 cells and astrocytes and at -70 mv for neurons. Constant current pulses (20 ~ 80 µa, 100 µs, 0.05 or Hz) were applied through extracellular bipolar electrodes placed at SC of CA1 region to induce EPSCs. The same extracellular electrodes were also used for applying TBS to induce LTP. The TBS consists of a train of five bursts of stimuli at 5 Hz with each burst composed of five pulses (100 µs) at 100 Hz, with the same intensity as the test stimulus for evoking EPSCs. The train was repeated twice with a s interval. Field EPSPs were recorded from the dendrites of CA1 pyramidal cells using a glass electrode with a tip less than 1µm filled with extracellular solution (10-20 megohms). The stimulus intensity was set to generate a fepsp with an amplitude that was approximately 30-40% of the maximum response. The same extracellular electrode was also used for applying tetanic stimulations consisting of 100 µs pulses applied at 100 Hz for 1 sec, and repeated twice with a s interval. Data were accepted for analysis only when postsynaptic currents or voltages and

4 the input resistance did not vary beyond 15% of the average values during the control period. Signals filtered at 5 khz using the amplifier circuitry were sampled at 10 khz and analyzed using Clampex 8.2. Immunostaining. Glial cells were filled with 0.1% biocytin (epsilon-n-biotinyl-llysine) or 0.4% lucifer yellow dissolved at in the recording pipette solution. Only one cell was injected with biocytin in each slice. Slices were fixed with 4% paraformaldehyde at room temperature for 3 hr before treated with 0.2% Triton X-100 for 30 min and blocking solution containing 10% BSA for 1 hr. Slices were then stained with anti-gfap antibody (1:1000, polyclonal) and anti-ng2 chondroitin sulfate proteoglycan antibody (1:200, monoclonal.) for 48 hr at 4 o C. Biocytin was visualized with FITC-conjugated streptavidin or Texas-Red streptavidin (1:1000) after washing to remove excess primary antibodies. The slice was imaged with a confocal microscope using a 60X, 1.2 NA water-immersion objectives. Calcium fluorescence imaging. Glial cells were loaded through the recording pipette with Oregon Green 488 BAPTA-1 (OGB-1, 20 µm) or Rhod-2 (200 µm). In some experiment, a control dye FITC (200 µm) was also loaded into the cell to monitor the drift of the recordings. After obtaining the whole-cell configuration, 15 min were allowed for intracellular diffusion of the dyes. Imaging was performed using a two-photon confocal laser scanning microscope LSM 510-MP with a long-range water-immersion objective (40X; 0.8NA). Two-photon fluorescence was excited with a mode-locked Ti:Sapphire laser (76 MHz; nm) pumped by a 5 W diode laser. Fluorescence

5 signals of nm and nm were collected for FITC and Rhod-2 fluorescence respectively with a sampling rate of frame/1 2 s. Relative changes in fluorescence were calculated and normalized against the base line by F/F, where F is the fluorescence intensity before stimulation and F is the change in fluorescence during stimulation. Calcium elevation in NG2 cells was evoked by local application of glutamate (500 µm) via a microtube (tip diameter of 50 µm) and positioned at 500 µm from the dye-filled NG2 cells, in the presence of TTX (5 µm), bicuculline (50 µm), APV (250 µm), nifedipine (50 µm), and CTZ (100µM). In some experiments, SC stimulation-induced Ca 2+ elevation in NG2 cells was examined by line scanning along the process of interest (total length, µm). A line was scanned for 1.2 ms, and five lines were averaged offline, resulting in a temporal resolution of 6 ms. Data were presented as means±s.e.m. and statistical differences were determined by Student s t test. Fig. S1. Distinct properties of two types of glial cells. (A) Immunostaining with antibodies against the astrocyte marker GFAP (red, left and right panels) and the NG2 cell marker NG2 (green, middle and right panels). (B) Example micrograph showing that the cell exhibiting electrophysiological properties of NG2 cells was loaded with biocytin (red, left and right panels) through recording pipette and confirmed as NG2 - immunopositive (green, middle and right panels). (C) Example micrograph showing that the cell exhibiting electrophysiological properties of astrocytes was loaded with biocytin (red, left and right panels) and confirmed as GFAP-immunopositive (green, middle and

6 right panels). Note the biocytin staining in surrounding astrocytes. Arrows in (B) indicate the microvessel that is also NG2-immunopositive. Arrowheads in (B) and (C) indicate cells that were loaded with biocytin. (D) Superimposed membrane potential changes in NG2 cell (top), astrocyte (middle), and pyramidal neuron (bottom) in responses to a series of current injections (100 ms in duration with an interval of 15 sec) from a holding potential of -80, -80, and -70 mv respectively. In NG2 cells only a single small spike-like depolarizing transient (arrow) could be evoked upon each depolarizing current injection. (E) Rapid reversible blockage of EPSCs in NG2 cell by ionotropic glutamate receptor antagonist Kyn (0.5mM) applied during the period indicated by the bar. Insets above: sample EPSC traces before, during and after washout of Kyn. Fig. S2. SC stimulation-induced transient Ca 2+ elevation detected by line scan imaging. (A) Fluorescence photomicrograph showing Rhod-2 and FITC-loaded NG2 cell in a P13 slice. (B) Example sequential line scans through the center of two fluorescence puncta indicated by the white arrow and numbers in (A). The arrow at the top of the panel marked the time when SC stimulation applied. (C) A plot of F/F amplitude in response to a train of SC stimulation (5 pulses, 25Hz) as shown in (B). Note transient increase in the fluorescence intensity of Rhod-2 (red), but not FITC (green) signal after SC stimulation. Black trace at the bottom, simultaneous whole-cell patch recording from the same imaged cell. Numbers (1, 2) associated with each scanning line in (B) and (C) correspond to the imaged pucnta indicated in (A). Fig. S3. Comparing efficiency of TBS and tetanic stimulation in LTP induction. (A) Example EPSCs recorded in a NG2 cell during TBS (upper panel) and tetanic stimulation

7 (lower panel) of SC. Red and black arrows mark EPSCs and stimulation artifacts respectively. (B) Summary data from NG2 cell recordings as shown in (A). Data are normalized by the averaged first 5 EPSCs in each recording. Every 5 consecutive EPSCs are averaged into one data point. (C) Summary data showing the time course of EPSCs at SC-NG2 synapses before and after TBS (filled red circles, n = 21) or tetanic stimulation (open black circles, n = 6). Data are normalized as in Fig.3. (D) Summary data showing the time course of field EPSCs recorded at CA1 region before and after TBS (filled red circles, n = 5) or tetanic stimulation (open black circles, n = 10).

8 A GFAP+ NG2+ Merge 20um B Biocytin NG2+ Merge 20um C Biocytin GFAP+ Merge 20um D NG2 cell Astrocyte Neuron EPSC Ampl. (pa) 20mV 10ms E Kyn 30pA 10ms Time (min) Ge et al. Fig. S1

9 A 2 1 5um B Rhod-2 FITC Merge C F/F Current 50% F/F 0.2 s 150pA Ge et al. Fig. S2

10 A TBS Tetanic 50pA 10ms B Norm. EPSC Ampl Tetanic TBS Time (ms) C Norm. EPSC Ampl Tetanic TBS D Norm. fepsp Ampl Tetanic TBS Time (min) Time (min) Ge et al. Fig. S3

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