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Differences in action potential propagation speed and axon initial segment plasticity between neurons from Sprague-Dawley rats and C57BL/6 mice

Zhi-Ya Chen Luxin Peng Mengdi Zhao Yu Li Mochizuki Takahiko Louis Tao Peng Zou Yan Zhang

Zhi-Ya Chen, Luxin Peng, Mengdi Zhao, Yu Li, Mochizuki Takahiko, Louis Tao, Peng Zou, Yan Zhang. Differences in action potential propagation speed and axon initial segment plasticity between neurons from Sprague-Dawley rats and C57BL/6 mice. Zoological Research, 2022, 43(4): 615-633. doi: 10.24272/j.issn.2095-8137.2022.121
Citation: Zhi-Ya Chen, Luxin Peng, Mengdi Zhao, Yu Li, Mochizuki Takahiko, Louis Tao, Peng Zou, Yan Zhang. Differences in action potential propagation speed and axon initial segment plasticity between neurons from Sprague-Dawley rats and C57BL/6 mice. Zoological Research, 2022, 43(4): 615-633. doi: 10.24272/j.issn.2095-8137.2022.121

Sprague-Dawley大鼠与C57BL/6小鼠动作电位传播速度和轴突起始节可塑性存在差异

doi: 10.24272/j.issn.2095-8137.2022.121

Differences in action potential propagation speed and axon initial segment plasticity between neurons from Sprague-Dawley rats and C57BL/6 mice

Funds: This work was supported by the National Science and Technology Innovation 2030-Major Program of “Brain Science and Brain-Like Research” (2022ZD0211800), National Natural Science Foundation of China General Research Grant (81971679, 21727806, 31771147) and Major Research Grant (91632305, 32088101), Ministry of Science and Technology (2018YFA0507600, 2017YFA0503600), Qidong-PKU SLS Innovation Fund (2016000663), and Fundamental Research Funds for the Central Universities and National Key R&D Program of China (2020AAA0105200). P.Z. was sponsored by the Bayer Investigator Award
More Information
  • 摘要: 动作电位产生于神经元的轴突起始节(Axon initial segment , AIS),动作电位的爆发与传播,与神经元兴奋性以及神经递质释放密切相关。神经元水平的学习和记忆研究依赖于许多动物模型的使用,尤其是啮齿类动物。该文中,我们利用基于遗传编码电压指示器的电压成像技术,研究动作电位在Sprague-Dawley(SD)大鼠和C57BL/6(C57)小鼠海马神经元中的爆发和传播。我们的实验数据显示,在两种物种的神经元中动作电位都是双向传播的,其中,沿轴突向下传播动作电位与向胞体往回传播动作电位的速度不同,且树突起源和胞体起源的AIS上动作电位的传播有其独特的性质。与大鼠相比,小鼠神经元表现出较高的回传动作电位速度和较低的下传动作电位速度,锚蛋白G (AnkG)在小鼠神经元的AIS上偏向于远端定位,Nav1.2在小鼠神经元AIS上呈现出较长的分布。此外,AIS可塑性发生时,大鼠神经元AIS上AnkG和Nav1.2的位置都向远端偏移,且长度均变短;而小鼠神经元的AIS却呈现出变长的AnkG和向远端定位的Nav1.2。综上,我们的研究结果表明,大鼠和小鼠的海马神经元可能在动作电位传播速度、AIS上AnkG和Nav1.2分布的模式以及AIS可塑性特性等方面都存在差异,对这两个物种的实验结果进行比较时需要要考虑到上述情况。
  • Figure  1.  Well-resolved AP initiation and propagation at AISs via voltage imaging

    A: Illustration of AIS identification in a neuron after voltage imaging under a microscope. B: Spike-triggered average movie for average AP waveform of each pixel in field of view for the following interpolation. C: Left, cell expressing QuasAr2-mOrange2 was selected and AP train was recorded after current stimulation of the soma, and different regions of interest (ROI) in the neuron in the field-of-view were polygonally outlined in different colors, corresponding to traces in the middle column; Middle, signals of recorded somatic electrophysiological data and corresponding voltage imaging data of selected cells. Injected current (200 pA 10 ms, 4 Hz, shown with gray line) evoked AP trains (electrical signal in soma, gray). Corresponding optical voltage signals were simultaneously recorded with an sCMOS camera in good synchronization (blue: soma; orange: AIS; yellow: axon). Sub-threshold electrical event (failed APs) was well-removed in the traces; Right, average electrical AP trace (black line on top) and optical traces of average AP signals (blue: soma; orange: AIS; yellow: axon) evoked by somatic stimulation (black line on bottom). Average traces were superimposed with single AP trails (gray backward lines). D: Left, superimposed average signals of three ROIs in Supplementary Figure S2B acquired at 484 Hz. Circle markers on solid lines indicate raw optical data points; Right, corresponding 1 000 times upsampled optical signal via a maximum correction-based waveform filter and cubic spline-based interpolation algorithm (interval=2.0658 μs) (Supplementary Figure S4 and Methods). E: According to high spatiotemporal AP initiation and propagation mapping from voltage imaging and interpolation, AIS parameters (e.g., length, distance to soma, and width, left column) and AP propagation details (AP initiation site, bidirectional propagation speed at AIS, soma, axon, and neighbor dendrites, right column). Circles in the right figure represent AP arrival time calculated from original voltage imaging movie. Dashed lines represent AP arrival time from interpolated data.

    Figure  2.  AP speed varied during propagation

    A: Schematic of a neuron, including soma, AIS, and axon. AIS location was defined as distance from the soma to AIS proximal end. AIS length was defined as distance from the proximal end to distal end. AP was initiated at the initiation site (red star) and propagated backward (orange) and forward (green). B: Left, representative image of AIS of DIV12-cultured hippocampal neurons from rat expressing QuasAr2-mOrange2. Fluorescence of mOrange2 (white) and NF-186 (blue) denotes whole cell and AIS, respectively. Red dot denotes AP initiation site (same as map on right side). Arrows denote axon compartments, and corresponding AP propagations are shown in the right chart with different colored lines. Right, slopes of fitted lines are average speed. AP propagation speed on AIS compartments differed after AP initiation (Scale bars: 20 µm). C: Histogram of relative AP initiation site at AIS, mean=48.06%±3.28%, n=32. D: Paired comparison of fpAP speed at AIS/axon (number of pairs=21, mean=1.871±0.39), and paired comparison of fpAP speed/bpAP speed at AIS (number of pairs=29, mean=1.507±0.16). E: Paired comparison of fpAP speed at AIS and axon (number of pairs=21, mean speed at AIS=119.5±18.64 µm/ms, mean speed at axon=73.45±7.76 µm/ms, *: P<0.05). F: Paired comparison of fpAP and bpAP speed at AIS (number of pairs=29, mean bpAP speed=84.99±7.6 µm/ms, mean fpAP speed=112.6±14.2 µm/ms, ns: P>0.05). G: Correlation of AIS location and bpAP speed (n=30, r=−0.224, ns: P>0.05). H: Correlation of AIS length and bpAP speed (n=30, r=−0.334, ns: P>0.05). I: Correlation of AIS location and fpAP speed (n=19, r=−0.603, **: P<0.01). J: Correlation of AIS length and fpAP speed (n=19, r=0.579, **: P<0.01). Error bars represent standard error of the mean (SEM), two-tailed paired t-test was employed in D−F, and linear regression was employed in G−J.

    Figure  3.  fpAP speed was negatively correlated with AIS location and positively correlated with AIS length

    A: No significant difference was observed in resting potential of neurons in control group (−64.9±1.2 mV, n=22) and chronic KCl-treated group (−67.5±0.97 mV, n=46), ns: P>0.05. B: KCl treatment (15 mmol/L for 48 h) significantly increased rheobase current (76.18±7.718 pA, n=46) of neurons compared to control group neurons (29.55±3.877 pA, n=22), ***: P<0.001. C: Representative images of cultured wild-type rat hippocampal neurons (DIV12) without treatment (control, upper) and with KCl treatment (15 mmol/L for 48 h, lower). All neurons were transfected in DIV7 with QuasAr2-mOrange2 plasmid. (Left) Selected neurons (white) and their AISs (blue) are indicated by fluorescence of mOrange2 and axonal marker NF-186, respectively; (Right) Corresponding differential interference contrast (DIC) images of neurons in left column (Scale bars: 20 µm). D: Comparison of AIS location (AIS distance to soma). AIS was significantly further from the soma in KCl treatment group (15 mmol/L for 48 h) (14.98±2.30 µm, n=15) compared to control group (6.76±0.85 µm, n=45), ***: P<0.001. E: No significant difference in AIS length was observed between control group (32.51±1.16 µm, n=45) and KCl treatment group (15 mmol/L for 48 h) (30.26±2.40 µm, n=15), ns: P>0.05. F:No significant difference was observed in bpAP speed at AIS of control group neurons (99.46±14.94 µm/ms, n=10) and KCl treatment group neurons (15 mmol/L for 48 h) (83.74±13.89 µm/ms, n=15), ns: P>0.05. G: fpAP speed at AIS in KCl treatment group neurons (15 mmol/L for 48 h) (65.33±9.30 µm/ms, n=10) was lower than that in control group (147.4±26.33 µm/ms, n=7), *: P<0.05. H−K: Correlation between bpAP/fpAP speed and AIS location/length: Correlation between bpAP speed and AIS location (n=15, r=−0.210, ns: P>0.05) (H); Correlation between bpAP speed and AIS length (n=15, r=0.038, ns: P>0.05) (I); Correlation between fpAP speed and AIS location (n=10, r=−0.765, **: P<0.01) (J); Correlation between fpAP speed and AIS length (n=10, r=0.702, *: P<0.05) (K). Error bars represent SEM; two-tailed unpaired t-test was employed in A, B and D−G, and linear regression was employed in H−K.

    Figure  4.  In dendritic AIS neurons, bpAP speed was lower at AISs than at corresponding dendrites

    A: Left, immunofluorescence imaging of hippocampal neurons, white dotted circle and white arrow denote somatic AIS neuron and somatic AIS, respectively; yellow dotted circle and yellow arrow denote neuron with AIS originating from a dendrite (dendritic AIS neuron) and dendritic AIS, respectively (Scale bars: 20 µm). Right, schematic of dendritic AIS neuron. AIS is marked blue, others are yellow. B: Speed ratio of bpAP at corresponding dendrite and AIS. Number of pairs=7, mean=2.444±0.42. C: Paired comparison of bpAP speed at corresponding dendrite and AIS. Speed bpAP at dendrite (yellow dots) was significantly faster than that at AIS (blue dots) (number of pairs=7, **: P<0.01). D: Upper, schematic of multi-compartment dendritic model, depicting all neuronal compartments and injected stimulus in simulation. Soma (20 µm×40 µm) was attached to two dendrites (2 µm×1 000 µm). AIS (1.2 µm×10~70 µm) and axon (1.2 µm×1 000 µm) were attached to one dendrite. Stimulus was a 1 nA current that lasted for 1 ms. Current stimulus was injected into center of soma. Lower, arrival time of AP peaks on segments labeled by black line in dendritic model. Different sections are shown in different colors. Slopes of dashed lines are mean speed in different compartments. E: bpAPs at AIS (red) and dendrite (blue). Inner image shows peaks of APs. F−J: Regulatory effects of each parameter on conduction speed in each component. Each subgraph is modulation of (a) location of axon initiation node (i.e., axon initiation is distance between proximal end of node and soma), (b) length of axon starting node, (c) diameter of axon, (d) diameter of dendrite 2, and (e) axon initiation segment diameter on conduction speed in each compartment. Blue, yellow, green, and red data represent dendritic bpAP speed, AIS bpAP speed, AIS fpAP speed, and axonal fpAP speed, respectively. Error bars represent SEM; two-tailed paired t-test was employed in B, C.

    Figure  5.  bpAP speed was lower at dendritic AISs than somatic AISs

    A: Speed of bpAP at somatic AISs (pink circles, 99.47±11.35 µm/ms, n=10) was much higher than that at dendritic AISs (light orange circles, 55.65±7.85 µm/ms, n=7), *: P<0.05; at dendritic AISs, bpAP speed showed no difference between untreated group and KCl treatment group (dark orange circles, 73.26±13.35 µm/ms, n=16), ns: P>0.05. B: Speed of fpAP at somatic AISs (pink circles, 137.5±52.43 µm/ms, n=6) was similar than that at dendritic AISs (light orange circles, 91.13±19.42 µm/ms, n=10), ns: P>0.05; at dendritic AISs, fpAP speed showed no difference between untreated group and KCl treatment group (dark orange, KCl treatment group, 66.52±7.78 µm/ms, n=15), ns: P>0.05. C: Immunofluorescence images of AIS length indicated by AnkG, distance between two white arrows represents AIS length (Scale bars: 20 µm). D: Length indicated by AnkG between somatic AISs (30.54±1.14 µm, n=45) and dendritic AISs (32.21±1.51 µm, n=42) was similar, ns: P>0.05. E: Reformed multi-compartment neuronal models and their simplified equivalent cables. Stimulus was a 1 nA current that lasted for 1 ms. Stimulus was injected into one end of the thin cable. In the somatic model (pink), the three cables were 20 µm×50 µm (left), 2 µm×50 µm (middle), and 1.2 µm×500 µm (right). In the dendritic model (orange), the three cables were 20 µm×50 µm (left), 3 µm×50 µm (middle), and 1.2 µm×500 µm (right). Middle cable in dendritic model was thicker than that in the somatic model because the equivalent cable of two dendrites was thicker than one hillock. F: APs in 450–500 µm (AIS) of the model. Solid and dashed lines represent data of somatic and dendritic neuronal models. Peak of the first and last APs are magnified to see peak time. G: Immunofluorescence images of AIS length indicated by Nav1.2, distance between two white arrows represents Nav1.2 length (Scale bars: 20 µm). H: Length indicated by Nav1.2 between somatic AIS (27.98±1.44 µm, n=30) and dendritic AISs (22.65±1.57 µm, n=27) was similar, *: P<0.05. Error bars represent SEM; two-tailed unpaired t-test was employed in A, B, D, H.

    Figure  6.  Mice neurons exhibited higher bpAP speed and lower fpAP speed than rat neurons

    A: Fluorescence images of identical fields of view capturing step of voltage imaging (upper) and AIS identification (lower, after standard immunofluorescence). The highlighted 80 µm×80 µm regions (white lines) in the third column from the left are magnified in right column, showing QuasAr2 (upper, for voltage imaging) and mOrange2/AnkG (lower, for AIS identification), respectively. The co-localized region in QuasAr2 and AnkG was defined as the AIS for AP initiation and propagation analysis (Scale bars: 20 µm). B: Neurons from mice. Paired comparison of bpAP speed at corresponding dendrite and AIS. bpAP speed at dendrite (pink circles) was significantly higher than that at AIS (green circles) (number of pairs=6, *: P<0.05). C: Neurons from mice. bpAP speed at somatic AISs (pink circles, 135.0±14.61 µm/ms, n=6) was much higher than that at dendritic AISs (green circles, 64.24±8.10 µm/ms, n=5), **: P<0.01. D: Neurons from mice. fpAP speed at somatic AISs (pink circles, 77.16±10.27 µm/ms, n=5) was similar to that at dendritic AISs (green circles, 75.18±24.62 µm/ms, n=6), ns: P>0.05. E: In somatic AISs, bpAP speed at AISs in rat neurons (pink circles, 88.22±8.62 µm/ms, n=15) was lower than that in mouse neurons (green circles, 131.3±14.08 µm/ms, n=12), *: P<0.05. F: In somatic AISs, fpAP speed at somatic AISs (pink circles, 141.3±33.57 µm/ms, n=10) was similar to that at dendritic AISs (green circles, 82.92±11.73 µm/ms, n=10), ns: P>0.05. Error bars represent SEM; two-tailed unpaired t-test was employed in B−F.

    Figure  7.  Neurons from rats and mice exhibited very different AnkG and Nav1.2 patterns

    A: Immunofluorescence images of AISs in neurons from rats and mice, as indicated by AnkG. Distance between two white arrowheads represents AIS length (Scale bars: 20 µm). B: In somatic AIS neurons in mice (green), AIS position was significantly distal compared to that in rats (pink), while AIS length was similar. Proximal end of AIS in rat neurons (6.44±0.50 µm, n=129) was significantly nearer soma than in mouse neurons (10.28±0.80 µm, n=79), ***: P<0.001. Length of AIS in rat neurons (31.36±0.76 µm, n=129) was similar to that in mouse neurons (30.62±1.15 µm, n=79), ns: P>0.05. Distal end of AIS in rat neurons (37.80±0.94 µm, n=129) was similar to that in mouse neurons (40.9±1.55 µm, n=79), ns: P>0.05. C: Immunofluorescence images of Nav1.2 in neurons from rats and mice. Distance between two white arrowheads represents Nav1.2 length (Scale bars: 20 µm). D: In somatic AIS neurons in mice (green), Nav1.2 length was longer than that in rats (pink), and proximal end location was similar. Proximal end of Nav1.2 in rat neurons (4.45±0.36 µm, n=105) was nearer soma than that in mouse neurons (6.25±0.66 µm, n=57), *: P<0.05. Length of Nav1.2 in rat neurons (27.41±0.76 µm, n=105) was significantly shorter than that in mouse neurons (30.04±1.11 µm, n=57), *: P<0.05. Distal end of Nav1.2 in rat neurons (31.87±0.85 µm, n=105) was significantly more proximal to soma than that in mouse neurons (36.31±1.38 µm, n=57), **: P<0.01. E: Schematic of AnkG and Nav1.2 position in somatic AIS neurons in rats and mice. Rat AnkG, pink filled box; mouse AnkG, green filled box; rat Nav1.2, pink box; mouse Nav1.2, green box. F: In dendritic AISs, bpAP speed at AIS in rat neurons (pink circles, 62.32±10.16 µm/ms, n=8) was comparable to that in mouse neurons (green circles, 68.63±16.14 µm/ms, n=6), ns: P>0.05. G: In dendritic AISs, fpAP speed at somatic AISs (pink circles, 90.30±12.23 µm/ms, n=6) was similar than that at dendritic AISs (green circles, 87.27±18.37 µm/ms, n=6), ns: P>0.05. H: In dendritic AIS neurons in mice (green), AIS location and length were similar to that in rats (pink). Dendritic AIS neurons in rats and mice exhibited similar AIS proximal end (20.82±3.05 µm, n=20; 26.36±1.78 µm, n=22, respectively, ns: P>0.05), AIS length (31.59±2.47 µm, n=20; 33.45±2.35 µm, n=22, respectively, ns: P>0.05), and AIS distal end (52.41±3.57 µm, n=20; 59.81±3.18 µm, n=22, respectively, ns: P>0.05). I: In dendritic AIS neurons in mice (green), Nav1.2 length was similar, while Nav1.2 was significantly distal compared to that in rats (pink). Proximal end of Nav1.2 in rat neurons (13.40±1.43 µm, n=27) was significantly nearer the soma than that in mouse neurons (28.54±2.78 µm, n=11), ***: P<0.001. Length of Nav1.2 in rat neurons (22.65±1.57 µm, n=27) was similar to that in mouse neurons (26.20±3.11 µm, n=11), ns: P>0.05. Distal end of Nav1.2 in rat neurons (36.06±2.26 µm, n=27) was significantly more proximal to soma than that in mouse neurons (54.74±2.54 µm, n=11), ***: P<0.001. J: Schematic of AnkG and Nav1.2 positions in dendritic AIS neurons in rats and mice. Rat AnkG, pink filled box; mouse AnkG, green filled box; rat Nav1.2, pink box; mouse Nav1.2, green box. Error bars represent SEM; two-tailed unpaired t-test was employed in B, D, F−I.

    Figure  8.  AnkG and Nav1.2 length/location were differentially altered during AIS plasticity in somatic AIS neurons

    A: Immunofluorescence images of AIS (upper) and Nav1.2 (under) in neurons from control rats (left) and 3 h 20 mmol/L glucose-treated rats (right). White arrowheads represent proximal and distal ends of AIS/Nav1.2 (Scale bars: 10 µm). B: Immunofluorescence images of AIS (upper) and Nav1.2 (under) in neurons from control mice (left) and 3 h 20 mmol/L glucose-treated mice (right). White arrowheads represent proximal and distal ends of AIS/Nav1.2 (Scale bars: 10 µm). C: In somatic AIS neurons in rats, compared with control group (gray), AIS location showed significant distal shift and shorter length in 3 h 20 mmol/L glucose-treated group (pink). Left, proximal end of AIS in 20 mmol/L glucose-treated group (9.85±0.59 µm, n=109) was significantly further from soma than that in control group (6.47±0.41 µm, n=126), ***: P<0.001. Middle, AIS length in 20 mmol/L glucose-treated group (28.21±0.89 µm, n=109) was significantly shorter than that in control group (31.98±0.74 µm, n=126), **: P<0.01. Right, distal end of AIS in 20 mmol/L glucose-treated group (38.05±1.14 µm, n=109) was similar to that in control group (38.45±0.84 µm, n=126), ns: P>0.05. D: In somatic AIS neurons in rats, compared with control group (gray), Nav1.2 location showed significant distal shift and shorter length in 3 h 20 mmol/L glucose-treated group (green). Left, proximal end of Nav1.2 in 20 mmol/L glucose-treated group (7.54±0.42 µm, n=150) was significantly further from soma than that in control group (4.41±0.34 µm, n=114), ***: P<0.001. Middle, Nav1.2 length in 20 mmol/L glucose-treated group (24.42±0.66 µm, n=150) was significantly shorter than that in control group (27.37±0.70 µm, n=114), **: P<0.01. Right, distal end of Nav1.2 in 20 mmol/L glucose-treated group (31.96±0.81 µm, n=150) was similar to that in control group (31.77±0.84 µm, n=114), ns: P>0.05. E: Schematic of AnkG and Nav1.2 position in rats. AnkG, pink filled box, Nav1.2, green filled box. F: In somatic AIS neurons in mice, compared with control group (gray), AIS length was longer in 3 h 20 mmol/L glucose-treated group (pink), while AIS location was similar. Left, proximal end of AIS in 20 mmol/L glucose-treated group (9.93±0.69 µm, n=81) was similar to that in control group (10.14±0.34 µm, n=77), ns: P>0.05. Middle, AIS length in 20 mmol/L glucose-treated group (35.84±1.30 µm, n=81) was significantly longer than that in control group (30.21±1.09 µm, n=77), **: P<0.01. Right, distal end of AIS in 20 mmol/L glucose-treated group (45.77±1.46 µm, n=81) showed significant distal shift compared with control group (40.34±1.24 µm, n=77), **: P<0.01. G: In somatic AIS neurons in mice, compared with control group (gray), Nav1.2 location showed significant distal shift in 3 h 20 mmol/L glucose-treated group (green), while Nav1.2 length was similar. Left, proximal end of Nav1.2 in 20 mmol/L glucose-treated group (9.66±0.83 µm, n=57) was significantly further from soma than that in control group (6.18±0.48 µm, n=30), ***: P<0.001. Middle, Nav1.2 length in 20 mmol/L glucose-treated group (26.91±1.30 µm, n=57) was similar to that in control group (28.61±1.14 µm, n=30), ns: P>0.05. Right, distal end of Nav1.2 in 20 mmol/L glucose-treated group (36.57±1.52 µm, n=57) was similar to that in control group (34.79±1.24 µm, n=30), ns: P>0.05. H: Schematic of AnkG and Nav1.2 position in mice. AnkG, pink box, Nav1.2, green box. Error bars represent SEM; two-tailed unpaired t-test was employed in C, D, F, G.

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  • 收稿日期:  2022-05-16
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