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First published online 12 August 2008
doi: 10.1242/jcs.025684

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Gain and fidelity of transmission patterns at cortical excitatory unitary synapses improve spike encoding

¹ State Key Labs for Macrobiomolecules and Brain and Cognitive Sciences, Institute of Biophysics, Chinese Academy of Sciences, Beijing 100101, The People's Republic of China
² Department of Physics, University of Kansas, Lawrence, KS 66049, USA

View larger version (20K): [in this window] [in a new window]   Fig. 1. Unitary synapses in response to presynaptic pair-spikes (50 msecond intervals) express facilitation, depression and parallel patterns. (A) Paired presynaptic spikes (bottom trace) evoke a facilitation pattern of uEPSCs (top trace, R2>R1) at a unitary synapse (W-081200). (B) uEPSC amplitude is larger in R2 than R1 at each unitary synapse (P<0.05, n=12/39). (C) Spikes (bottom trace) evoke a depression pattern of uEPSCs (top trace, R2<R1) at a unitary synapse (W-070800). (D) uEPSC at R1 is larger than at R2 at unitary synapses (P<0.05, n=20/39). (E) Paired-spikes (bottom trace) evoke a parallel pattern of uEPSCs (top trace, R2=R1) at a unitary synapse (W-071203). (F) uEPSC at R2 equals that at R1 at each unitary synapse (P>0.05, n=7/39). In B, D and F, each pair of symbols denotes the averaged R1 and R2 from a unitary synapse. (G) R2-R1 and R1 in all 39 synapses examined are negatively correlated (r2=0.7).

View larger version (28K): [in this window] [in a new window]   Fig. 2. The transmission of presynaptic pair-spikes at unitary synapses that express facilitation, depression or parallel fluctuates among these three patterns in a chaotic manner. (A) The cumulative probability of uEPSCs shows that with a facilitation pattern, R2 () is larger than R1 (). (B) Difference between R2 and R1 (R2–R1) plotted vs time. R2–R1 values fluctuate irregularly around the dotted line (zero). (C) A depression pattern produces uEPSCs with a cumulative probability of R2 () smaller than R1 (). (D) R2-R1 values fluctuate widely around 0. (E) The cumulative probability of uEPSCs for R2 () and R1 () overlaps with a parallel response. (F) R2–R1 values fluctuate around zero irregularly. Data points above dotted line denote synaptic facilitation and those below the line denote depression.

View larger version (39K): [in this window] [in a new window]   Fig. 3. Calcineurin autoinhibitory peptide (CaN-AIP) converts synaptic fluctuation into a depression pattern. The standard solution was filled in the tip of pipettes, and additional 40 µM CaN-AIP was back-filled. (A) R1 and R2–R1 values plotted against time. R1 increases (green symbols). The values of R2–R1 fluctuate across zero (dashed line), and remain below this line 30 minutes after CaN-AIP infusion (pink symbols). uEPSCs were sampled every 10 seconds. (B) Paired uEPSCs were sampled in the initial 4 minutes (control) and 30 minutes after the postsynaptic infusion of CaN-AIP. Correlation between R2–R1 and R1 in this unitary synapse plotted before (blue) and after (red) CaN-AIP infusion. CaN-AIP shifts synaptic fluctuation (blue) toward depression (red). (C) Paired uEPSCs in this unitary synapse are evoked by presynaptic spikes (bottom trace) before (blue) and after (red) CaN-AIP infusion. Calibration bars are 20 mseconds/60 pA for uEPSCs and 50 mV for spikes. (D) Other examples (n=9) showing that CaN-AIP converts synaptic fluctuation (thin lines) into depression (thick lines with same color), in which lines denote the correlation between R2–R1 and R1.

View larger version (34K): [in this window] [in a new window]   Fig. 4. Ca2+-CaM converts synaptic fluctuation into a depression pattern. The standard solution was filled in the tip of pipette, and additional 40/10 µM Ca2+-CaM was back-filled. (A) R1 and R2–R1 are plotted vs time. The infusion of Ca2+-CaM enhances R1 (green symbols) and converts R2-R1 from a fluctuation across dash line initially to below the line 40 minutes after the infusion (pink symbols). uEPSCs were sampled every 10 seconds. (B) Paired uEPSCs were sampled in initial 5 minutes (control) and 50 minutes after postsynaptic Ca2+/CaM infusion. Correlation between R2-R1 and R1 in this unitary synapse is plotted before (blue symbols/line) and after (red) Ca2+/CaM infusion. Dashes line differentiates synaptic facilitation (above) and depression (below). Ca2+/CaM converts synaptic fluctuation (blue) into depression (red below dash line). (C) Paired uEPSCs in this unitary synapse evoked by presynaptic spikes (dark-red trace) before (blue) and after (red) Ca2+/CaM infusion. Calibration bars are 20 ms/160 pA for uEPSCs and 35 mV for spikes. (D) Other examples (n=5) show Ca2+/CaM-induced conversion of the fluctuated pattern (dashed lines) into synaptic depression (solid lines of same color).

View larger version (52K): [in this window] [in a new window]   Fig. 5. Factors are considered in the quantitative simulation of unitary synaptic inputs. (A) Diagram showing three kinds of unitary synapses that express dominant facilitation, depression and parallel on a single neuron. Red indicates synapses that express facilitation, blue is depression and green in parallel. (B,C) uEPSC1 and EPSC2 fluctuate randomly among fluctuation, depression and parallel in the control, and show a depression with uEPSC1 enhancement uniformly under CaM signal activation. (D) CaN-AIP converts inactive synapses into active ones, which is blocked by 10 µM CNQX (an antagonist of AMPA-glutamate receptor). (E) CaN-AIP enhances the probability of detecting uEPSCs from 0.23±0.05 to 0.81±0.03. (F) Distribution of threshold stimuli, which represents cell excitability, in cortical pyramidal neurons. (G) Correlation between threshold stimuli and difference of resting membrane potential (Vr) vs threshold potentials (Vt) in control (open symbols, r2=0.23) and under conditions of presynaptic neuronal plasticity (filled symbols, r2=0.71, P<0.01). (H) eGFP-expressing fast-spiking neurons from FVB-Tg(GadGFP)45704 Swn/J mice. Image was taken using two-photon microscopy (Olympus FV-1000), which is used to study spike programming.

View larger version (40K): [in this window] [in a new window]   Fig. 6. The quantitative parameters are summated from unitary synaptic inputs under control conditions (open symbols) and upon CaM activation (filled symbols). (A,B) Simulated pulse waves in the control [200 synapses vary among facilitation, depression and parallel in the ratio 12:20:7 (see Fig. 1) and 0.6-1.6 msecond presynaptic inter-input intervals] and upon CaM activation (300 synapses in depression pattern with 0.5-1.0 msecond inter-input intervals). As step two of the simulated waves varies under different conditions and mainly controls the spike programs, we quantified its amplitudes and duration vs inter-input intervals and synapse number. (C) The exponentially decayed correlation between the amplitude and inter-input interval. (D) The linear correlation between the duration and inter-input interval. (E) The amplitude vs the number of synapses. (F) The linear correlation between the pulse duration and the number of synapses.

View larger version (38K): [in this window] [in a new window]   Fig. 7. The influence of the integrated currents from excitatory unitary synapses on spike programming at cortical GABA neurons. The rows from top to bottom are the integrated current pulses, spikes and spike timing; and columns A-C show spike patterns superimposed from 40 traces under three conditions. (A) Spike firing and timing evoked by a pulse similar to that in Fig. 6A (control). (B) Spike firing and timing evoked by a pulse that is simulated so that postsynaptic CaM converts inactive synapses into active ones. Fluctuating synaptic patterns were converted to a uniform pattern with an enhanced uEPSC1. (C) Spike firing and timing evoked by pulses that are simulated when presynaptic inputs are more synchronously activated (*, inter-input intervals changes from 0.6-1.6 to 0.5-1.0 mseconds). Such changes raise the amplitude of the integrated inputs, which improves spike capacity and timing precision.

View larger version (30K): [in this window] [in a new window]   Fig. 8. Influence of the integrated synaptic inputs on spike programming through the refractory periods of sequential spikes. The standard deviation of spike timing (SDST; A) and inter-spike intervals (B) under three conditions: (1) 200 synapses with the fluctuating patterns and 0.6-1.6 msecond inter-input interval (open symbols); (2) 300 synapses with uniform pattern/R1 increase and 0.6-1.6 msecond inter-input interval (gray); and (3) 300 synapses with uniform pattern/R1 increase and 0.5-1.0 msecond inter-input interval (black). SDST vs the number of spikes under the three conditions are statistically different (P1-2<0.001 and P2-3<0.001); and ISI vs the number of spikes under three conditions are significantly different (P1-2<0.001 and P2-3<0.001). Values are means ± s.e.m. (C) The measurement of the influence of input strength on the refractory periods of sequential spikes. Blue traces show weak input strength, and red traces show strong input strength. (D) Linear correlation between the normalized stimulus strength and refractory periods for spike 1 (linear slope, –3.1) and spike 3 (slope, –10.4).

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