Bidirectional NMDA receptor plasticity controls CA3 output and heterosynaptic metaplasticity
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1 Bidirectional NMDA receptor plasticity controls CA output and heterosynaptic metaplasticity David L. Hunt, Nagore Puente, Pedro Grandes, Pablo E. Castillo a NMDAR EPSC (pa) st 5 nd 5 b NMDAR EPSC (%) n = 8 5 pa ms DCG-IV Supplementary Figure. Stationarity of NMDAR-mediated -CA tramission. a) Average baseline amplitude of NMDAR-EPSCs during the first five minutes ( st 5) and the second five minutes ( nd 5) just before delivering the pairing induction protocol. No significant difference in baseline amplitude between these two segments was observed. b) Time course plot of summary data (8 cells) where no induction protocol was delivered. The mglur/ agonist DCG-IV ( μm) was applied at the end of each experiment. Representative traces from the time points indicated of a single experiment are shown (iet; = p >.). Nature Neuroscience: doi:.8/nn.46
2 NMDAR-EPSC (%) C tet Pre-post (n=9) Pre-post + CPA (n=5) Post-pre (n=8) Post-pre + CPA (n=6) - 5 pa ms 5 pa ms pa ms 5 pa ms Supplementary Figure. tltp and tltd can be induced at more physiological temperatures. The properties of bidirectionality are preserved at -5 C when slices are treated with CPA to deplete calcium from internal stores. Summary data of cells recorded at -5 C for each experimental condition (left); representative traces from single experiments at the time points indicated (right). Nature Neuroscience: doi:.8/nn.46
3 NMDAR-EPSC (%) Long Eva rat Pre post (n=4) Post pre (n=4) - plasticity (%) 5 5 tltpn pa ms pa ms tltdn pre-post (LE) pre-post (W) post-pre (LE) post-pre (W) Supplementary Figure. Bidirectional NMDAR plasticity in Long Eva rat. Summary data for pre-post and post-pre induction protocols (left). Representative traces from single experiments for each condition (right, top); summary data for the average percent plasticity induced relative to baseline for Long Eva and Wistar rats (right, bottom). Nature Neuroscience: doi:.8/nn.46
4 a Pre post b Post pre 5 pa ms pa ms PPF /CV plasticity (%) 5 5 PPF /CV 5 4 plasticity (%) tltpn tltdn Supplementary Figure 4. Burst timing-dependent NMDAR plasticity is unlikely to be expressed presysnaptically. Analysis of paired pulse facilitation (PPF) before () and after () tltpn/tltdn was fully established (- min post-induction). Coistent with these findings, no change in /CV was observed following induction of tltpn or tltdn. ( = p >.5). Nature Neuroscience: doi:.8/nn.46
5 a Third pulse Fourth pulse Fifth pulse mv 5 ms ms mv b spikes/burst spikes/burst (%) Control (n = ) MK 8 (n = ) MK 8 (5 M) MK 8 (5 M) 5 5 DCG IV ( M) DCG IV ( M) Supplementary Figure 5. -NMDARs contribute to mossy fiber-driven output of CA pyramidal neuro. a) Representative experiment showing the effect of NMDAR blockade on -induced action potentials in CA pyramidal neuro. Mossy fibers were activated using 5 stimuli, 5 Hz bursts, and the stimulation inteity was set to elicit spikes after the rd,4 th, and 5 th stimulatio. (top, left) Single trace under control conditio. (top, right) Superimposed traces (n = ) of the last three respoes in the burst before and after bath application of the NMDAR antagonist MK-8. Time course depicting the reduction in spikes per burst due to pharmacological blockade of NMDARs (bottom). b) Summary data showing the reduction of mossy fiber-driven action potentials in the presence of MK-8. Nature Neuroscience: doi:.8/nn.46
6 Peak Off-peak 5 mv ms LY + MPEP EPSP (%) 5 5 Peak Off-peak n = DCG-IV Supplementary Figure 6. -EPSP respoe to group-i mglur antagonism. Co-application of the mglur antagonist LY6785 (5 µm) and the mglur5 antagonist MPEP (4 µm) had no significant effect on basal synaptic tramission (min -5 vs min 5-; peak p =.7, off-peak p =.98; not significant = p >.5). (Top) Representative traces taken at the time points indicated below. (Bottom) Summary data. Synaptic respoes were recorded in current-clamp mode while voltage clamping at -6 mv. MPEP and LY6785 were added to the perfusion solution. Nature Neuroscience: doi:.8/nn.46
7 a c d LTP N (%) spikes ( + pairing) 4 4 whole-cell mv mv cell-attached Fig-7 Fig-8 Sup. Fig- stim OFF stim ON MPEP (+) MPEP (-) heparin (-) heparin (+) r = LTP N tet spikes -LTP (%) b 4 Baseline EPSP amplitude (mv) Figure-7 (n = ) 5 5 stimoff LTP N tet spikes ms r =.59 X5 spikes -LTP summary (%) NMDA only NMDA + MPEP whole-cell whole-cell + MPEP cell-attached cell-attached + MPEP * * stim OFF stim ON MPEP (+) MPEP (-) heparin (-) heparin (+) Supplementary Figure 7. Summary data associated with figures 7, 8 & Sup. Fig-. a) Summary of spikes generated during the + pairing induction for all experimental conditio, no significant differences were observed. b) Summary data of the baseline respoe amplitude for heterosynaptic metaplasticity experiments where individual data points represent respoe amplitudes for and pathways in individual experiments. Bars represent average data for all experiments used in the analysis shown in figures 7 and 8 and supplementary figure respectively. No significant differences were observed between baseline respoes of different conditio for any experimental design. c) (Left) Representative traces for LTP N tet in the whole-cell (top) and cell-attached (bottom) recording configuratio. (Right) Summary data for mean spikes during LTP N tet under different conditio. d) (Left) Correlation plot of LTP N and spikes during LTP N tet, and (Right) -LTP and spikes during LTP N tet. No significant correlatio were observed. e) Summary plot of -LTP generated to illustrate that control conditio [i.e. stim OFF, MPEP(+), and heparin(-)] generate comparable -LTP. ( = p >.5) (* = p <.5). stimon MPEP(-) e Figure-8 (n = 8) MPEP(+) Sup.Fig- (n = 8) heparin(+) heparin(-) * Nature Neuroscience: doi:.8/nn.46
8 KAR plasticity (%) KAR-EPSP (mv) LTP N tet M NBQX 4 5 LTP tet N 8 n = 4 - spikes mv ms 6 4 KAR NMDAR Supplementary Figure 8. LTP N tet does not induce plasticity of KAR-mediated tramission. (Top) Representative experiment demotrating the magnitude of KAR-mediated tramission before and after LTP N tet. KAR-mediated tramission was isolated in the presence of µm GYKI, µm picrotoxin, µm CGP55845 while delivering single pulses at a holding potential -8 mv. Respoes are blocked inthepresenceofµmnbqx.(iet) Representative traces from the time points indicated are shown. (Bottom, left) Summary data from 4 cells indicating that no plasticity of the KAR component is induced by LTP N tet. (Bottom, right) Average spiking output during LTP N tet where no significant difference is observed between conditio. ( = p >.5) Nature Neuroscience: doi:.8/nn.46
9 Peak Off-peak 5 mv ms EPSP (%) pulses ( Hz) 5 M d-apv M GYKI n = 7 M NBQX Supplementary Figure 9. The slow excitatory component of -EPSPs is predominantly mediated by NMDARs. (top) Representative traces taken at the time points indicated below. (bottom) Summary plot of the peak and off-peak amplitudes before and after subsequent bath application of d-apv, GYKI5655 and NBQX, to block NMDARs, AMPARs and KARs, respectively. Synaptic respoes were recorded in current-clamp mode while holding the membrane potential at -6 mv. Pharmacological isolation of the components of excitatory synaptic tramission demotrates that, when recording at the inhibitory reversal potential, the major offpeak component is mediated by NMDAR tramission. Nature Neuroscience: doi:.8/nn.46
10 a Inhibitory component % Peak Inhibitory component mv Off-peak 5 ms + DCG-IV LTP N tet 5 5 (n =) - b IPSC % Post-pre or Pre-post tet (n=) (n=) - +PTX 5 pa ms Supplementary Figure. Effects of induction tetani on inhibitory tramission. a) Analysis of the -evoked inhibitory component monitored at -6 mv and in the absence of drugs in the bath. Top: Superimposed representative traces of -evoked synaptic respoes before (), 5- min post tetanus () and in the presence of μm DCG-IV. These complex respoes include a fast EPSP (Peak), an inhibitory component ( 5 ms post stim) and a slow component. Bottom: Summary plot showing no significant changes in the magnitude of the inhibitory component before (- to min) and after ( to min) the LTP N -induction tetanus (p >.5). b) Delivering either the pre-post or the post-pre induction protocol elicited a traient depression followed by a modest, but significant long lasting enhancement of inhibitory tramission ( ± %, n = 6 p =.8; paired t-test). Iet: superimposed representative traces before (), 5- min after tetanus () and in the presence of μm picrotoxin(ptx). Nature Neuroscience: doi:.8/nn.46
11 -EPSP (%) + tet pairing mv ms mv ms -EPSP (%) Control (n=9) Heparin (n=7) - mv ms mv ms Supplementary Figure. Attenuation of heterosynaptic plasticity by IP receptor blockade. Intracellular loading of heparin (.5 mg/ml) via the patch pipette robustly decreased -LTP following the + pairing tetanus (same as Fig. 7a) relative to interleaved controls (control; 7 ± 48 % baseline vs. heparin; 7 ± 4 % baseline: p =.57, unpaired t-test). No significant difference in -EPSP amplitude was observed between control and cells loaded with heparin ( = p >.5). Representative traces for each pathway and experimental condition are shown right., summary data is shown left. Nature Neuroscience: doi:.8/nn.46
12 Figure a-e Supplementary,,, 4 f Table. Pharmacological conditio Drug condition µm NBQX, µm picrotoxin, µm CGP55845 (continuous), µm DCG-IV at the end No drugs, µm DCG-IV at the end g µm GYKI, µm picrotoxin, µm CGP55845 (continuous), µm DCG-IV at the end a,b µm NBQX, µm picrotoxin, µm CGP55845, 5 µm LY6785/CPCCOet or 4 µm MPEP (continuous), µm DCG-IV at the end 4a µm NBQX, µm picrotoxin, µm CGP55845 (continuous), 5 µm d-apv (5 min), µm DCG-IV at the end 4b µm NBQX, µm picrotoxin, µm CGP55845, µm Nifedipine (continuous), µm DCG-IV at the end 4c,d µm NBQX, µm picrotoxin, µm CGP55845, µm CPA (continuous), µm DCG-IV at the end 4e µm NBQX, µm picrotoxin, µm CGP55845 (continuous), µm okidaic acid (intracellular), µm DCG-IV at the end 4f µm NBQX, µm picrotoxin, µm CGP55845, 6 µm GDPβs, µm DCG-IV at the end 4g µm NBQX, µm picrotoxin, µm CGP55845 (continuous), 5 µm DIP (intracellular), µm DCG-IV at the end 5a,d No drugs 5b,c 5e,f 4 µm MPEP (continuous) 5 µm LY6785 (continuous) 6 No drugs 7 5 µm MK-8 ( min), µm DCG-IV at the end 8a,b 8c 8d 8e Supplementary 5 Supplementary 6 Supplementary 8 Supplementary 9 Supplementary a Supplementary b Supplementary µm NBQX, µm picrotoxin, µm CGP55845, 4 µm MPEP (continuous) No drugs, µm DCG-IV at the end 4 µm MPEP (continuous), µm DCG-IV at the end 4 µm MPEP (wash-out after LTP N tet), µm DCG-IV at the end 5 µm MK-8 (wash-in), µm DCG-IV at the end 5 µm LY6785, 4 µm MPEP (wash-in), µm DCG-IV at the end μm GYKI 5655, μm picrotoxin, μm CGP55845 (continuous), µm NBQX at the end Wash-in; 5 µm d-apv, µm GYKI 5655, µm NBQX No drugs, µm DCG-IV at the end No drugs, µm picrotoxin at the end.5 mg/ml heparin (intracellular), µm DCG-IV at the end Nature Neuroscience: doi:.8/nn.46
13 Table. Stimulation protocols Tetanus Plasticity induced Protocol Figure Pre-post Pre; subthreshold Post; suprathreshold NMDAR-LTP 5 5 Hz (pre) + ms Hz Hz X a, a, 4d, 5a, 5b, 6a-c, Supplementary,,4a Post-pre Post; suprathreshold Pre; subthreshold NMDAR-LTD Hz (post) - ms 5 5 Hz Hz X b, b, 4a, 4b, 4c, 4e, 5d, 5e, 6d-f Supplementary,,4b + pairing ; subthreshold ; subthreshold -LTP ; 5 Hz 5 Hz ; 5 Hz X 5 Hz 7b-d, 8e, Supplementary LTP N tet ; suprathreshold NMDAR-LTP 5 5 Hz (pre) X 5 Hz 8b-e Supplementary Baseline / post-tetanus acquisition Paired pulse (5 ms Hz Figure a-e a, b 4a-h 8a, 8b pathway: 7b-e, 8e, Supplementary 8 Supplementary,,, 6, 8 Paired pulse (4 ms Hz Supplementary 4 Single Hz 5 pulses ( ms Hz f, g pathway: 7b-d, 8c, Supplementary 9, 5a-f 6a-f Supplementary 5 Nature Neuroscience: doi:.8/nn.46
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