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Research ArticleNew Research, Neuronal Excitability

Phase-Dependent Modulation of Oscillatory Phase and Synchrony by Long-Lasting Depolarizing Inputs in Central Neurons

Satoshi Watanabe and Moritoshi Hirono
eNeuro 5 October 2016, 3 (5) ENEURO.0066-16.2016; DOI: https://doi.org/10.1523/ENEURO.0066-16.2016
Satoshi Watanabe
1Department of Bioengineering and Robotics, Graduate School of Engineering, Tohoku University, Sendai 980-8579, Japan
2Graduate School of Pharmaceutical Sciences, University of Tokyo, Tokyo 113-0033, Japan
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Moritoshi Hirono
3Graduate School of Brain Science, Doshisha University, Kyoto 610-0394, Japan
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  • Figure 1.
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    Figure 1.

    Stimulation of the STN evokes phase-dependent shifting of the LFP oscillation. (A) Schematic of the experiment. The STN was stimulated by a suction electrode. LFP was recorded from the surface of the PC lobe. (B) STN stimulation evokes NO release in the neuropil layer of the PC lobe (shaded area), which rapidly diffuses to the cell mass. The B neurons produce oscillatory activity, and NO is presumed to have uniform effects on B neurons. (C) Voltage imaging of the PC lobe reveals long-lasting depolarization after STN stimulation in the cell mass. The trace shows the fractional change of the fluorescence (negative is upward) from the cell mass. The fluorescence image of the PC lobe is shown on the right. The apical end of the PC lobe is to the bottom left. The cell mass is the area between the blue dotted curves. The red curve shows the region of interest. Two nylon threads fixing the PC lobe (asterisks) are also visible. (D) Response of the LFP oscillation to STN stimulation. The frequency of the LFP oscillation increases after STN stimulation. The LFP peaks after the stimulus shift from the times expected in the absence of the stimulus (dotted vertical lines). The phase–response plot was constructed as shown below. The phase shifts of the three peaks are denoted S1, S2, and S3. The phase of the stimulus is Θ. The relative phase θ of the stimulus is defined so the phase is zero for the unperturbed peak: Embedded Image for the first peak, Embedded Image for the second peak, and Embedded Image for the third peak. Finally, the phase shifts S1, S2, and S3 are plotted against the respective relative phases θ1, θ2, and θ3, as shown on the right. (E) Plot of the phase shift after STN stimulation [SSTN(θ)] in saline. A total of 150 stimuli were applied. The red curve shows the fit with formula (2). (F) Plot of SSTN(θ) in L-NAME. A total of 150 stimuli were applied. The red curve shows the fit with formula (2). (G) Slope of the linear trend [a1 in formula (2)] in saline and L-NAME. The slope was significantly larger in saline than in L-NAME (***p < 0.001, n = 10 for saline and n = 9 for L-NAME). (H) Amplitude of the sinusoidal component [a2 in formula (2)] in saline and L-NAME. The amplitude was significantly greater in saline than in L-NAME (**p < 0.01, n = 10 for saline and n = 9 for L-NAME).

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    Figure 2.

    Uncaging of NO evokes phase-dependent shifting of the LFP. (A) Schematic of the experiment. NO was uncaged in the entire PC lobe by brief UV irradiation. (B) Voltage-clamp recording in a B neuron in the presence of octanol, showing NO uncaging-evoked inward current (holding potential –60 mV). (C) Current-clamp recording in a B neuron in normal saline, showing NO uncaging-evoked slow depolarization and increased frequency of periodic depolarizing events. (D) Plot of the decrease in the interval of periodic depolarizations against the membrane potential at the bottom of the interval in the neuron shown in C. Filled circles are for the intervals before NO uncaging and open circles are for the intervals after NO uncaging. The correlation coefficient was 0.795. (E) Response of LFP oscillation to NO uncaging. (F) Plot of the phase shift following NO uncaging [SNO(θ)]. A total of 60 stimuli were applied. The red curve shows the fit with formula (2). (G) Slope of the linear trend [a1 in formula (2)] in samples stained with caged NO and unstained control samples. The slope was significantly larger in stained samples (NO) than in control samples (***p < 0.001, n = 16 for NO and n = 12 for control). (H) Amplitude of the sinusoidal component [a2 in formula (2)] in stained and unstained control samples. The amplitude was significantly greater in stained samples than in control samples (***p < 0.001, n = 16 for NO and n = 12 for control).

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    Figure 3.

    Phase-dependent modification of the spatial synchrony of the LFP by STN stimulation and NO uncaging. (A) Schematic of the experiment of STN stimulation. The LFP was recorded at apical (red) and basal (blue) sites on the PC lobe. (B) An example of the LFP showing modification of synchrony after STN stimulation. In the upper part, the STN was stimulated at a late phase in the LFP interval (Θ = 3.541 rad). Expanded LFP events before (a) and after (b) STN stimulation are shown on the right. STN stimulation decreased the phase lag. In the lower part, the STN was stimulated at an early phase in the LFP interval (Θ = 0.767 rad). STN stimulation increased the phase lag. (C) Schematic of the experiment of NO uncaging. NO was uncaged over the entire PC lobe. (D) An example of the LFP showing modification of synchrony by NO uncaging. In the upper part, NO was uncaged at a late phase in the LFP interval (Θ = 3.164 rad). Expanded LFP events before (a) and after (b) uncaging are shown on the right. NO uncaging decreased the phase lag. In the lower part, NO was uncaged at an early phase in the LFP interval (Θ = 0.302 rad). NO uncaging increased the phase lag. (E) Normalized phase lag after STN stimulation plotted against the phase of STN stimulation in normal saline. A total of 142 stimuli were applied. The average and SEM for the data in each of the bins of a size of 0.1π are shown by the red symbols. (F) Averaged plot of the normalized phase lag after STN stimulation in normal saline (n = 6). (G) Normalized phase lag recorded in L-NAME. A total of 145 stimuli were applied. The average and SEM for the data in each of the bins are shown by the red symbols. (H) Averaged plot of the normalized phase lag after STN stimulation in normal L-NAME (n = 6). (I) Normalized phase lag after NO uncaging. The average and SEM for the data in each of the bins of a size of 0.1π are shown by the red symbols. (J) Averaged plot of the normalized phase lag after NO uncaging (n = 6). (K) The decrease in the normalized phase lag by STN stimulation (average between –0.6π and –0.1π) in normal saline and L-NAME. The decrease was significantly larger in normal saline than in L-NAME (**p < 0.01, n = 10 for saline and n = 9 for L-NAME). (L) The increase in the normalized lag (average between –2.1π and –1.7π) in normal saline and L-NAME. The increase was significantly larger in normal saline than in L-NAME (*p < 0.05, n = 10 for saline and n = 9 for L-NAME). (M) The decrease in the normalized lag (average between –0.6π and –0.1π) by UV illumination in samples stained with caged NO and unstained control samples. The decrease in the phase lag was significantly larger in stained samples than in control samples (*p < 0.05, n = 6 for NO and n = 6 for control). (N) The increase in the normalized lag (average between –2.2π and –1.7π) by UV illumination in stained and unstained control samples. The increase in the phase lag was significantly larger in stained samples than in control samples (**p < 0.01, n = 6 for NO and n = 6 for control).

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    Figure 4.

    Spike phase distribution in NB neurons explains selective release of NO at the timing for synchronization. (A) The phase difference between the apical and basal oscillators leads to either synchronization or desynchronization. In the Limax PC lobe, the apical oscillator is advanced in phase compared to the basal oscillator. With a positive slope in the phase–response plot (a), the phase advance at the apical site is larger than at the basal site, resulting in desynchronization of the oscillation. With a negative slope in the phase–response plot (b), the phase advance at the apical site is smaller than at the basal site, resulting in synchronization. (B) Current-clamp recording in an NB neuron injected with small depolarizing DC current, showing the spontaneous spikes at late phases in the IPSP interval. (C) Spike phase distribution in NB neurons. The spike phases were grouped by the number of spikes that occurred during the cycle. (D) A possible mechanism for phase-dependent release of NO from NB neurons. NB neurons receive olfactory input from the STN, and also periodic inhibitory input from B neurons that is synchronized with the LFP. With an input at an early phase (a), the NB neuron is hyperpolarized and does not release NO (left). With an input at a late phase (b), the NB neuron fires and releases NO (right). This results in NO release only at the late (synchronizing) timing.

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    Figure 5.

    Direct electrical stimulation of the PC lobe in the presence of L-NAME evokes phase-dependent shifting of the LFP oscillation, which is equivalent to the PRC. (A) Schematic of the experiment. The apical half of the PC lobe was placed in a suction electrode for stimulation. The LFP was recorded from an electrode placed near the suction electrode. (B) Response of the LFP oscillation to stimulation of the PC lobe. After the stimulation, the LFP phase shifted. (C) Phase shift of the LFP oscillation by electrical stimulation [SE(θ)]. The red curve shows a fit with formula (1). (D) Comparison of the peak phase of –dSNO/dθ and SE(θ). The peak phases were not significantly different between –dSNO/dθ and SE (NS, not significant; n = 16 for NO uncaging and n = 11 for electrical stimulation). (E) Comparison of the ratio of the negative component of –dSNO/dθ and SE (b/a in C). The ratios were not significantly different between –dSNO/dθ and SE (n = 16 for NO uncaging and n = 11 for electrical stimulation). (F) Calculated shift of the peak phase of the phase–response plot, in response to exponentially decaying inputs with different decay time constants. The abscissa is the normalized decay time constant (in units of cycle periods). The ordinate is the shift of the peak phase from that of the PRC (pulse stimuli).

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    Figure 6.

    Phase-dependent shifting of spikes in mouse cerebellar Purkinje cells to step and pulse current injections. (A) Response of Purkinje cell spikes to a current step (100 pA, 100 ms). (B) Response of Purkinje cell spikes to a current pulse (100 pA, 1 ms). A and B are from the same cell. (C) Plot of phase shifting in response to step currents [Sstep(θ)]. The red curve shows a fit with formula (4). The differential of the fitted curve (–dSstep/dθ) is shown below. (D) Plot of phase shifting in response to pulses [Spulse(θ)]. The red curve shows a fit with formula (3). In C and D, step and pulse stimuli (50 pA) were alternately repeated 313 times in the same cell. (E) Comparison of the peak phase of –dSstep/dθ and Spulse(θ). The peak phases were not significantly different between –dSstep/dθ and Spulse(θ) (NS, not significant; n = 8). (F) Comparison of the ratio of the negative component in –dSstep/dθ and Spulse(θ). The ratios were not significantly different between –dSstep/dθ and Spulse(θ) (n = 8).

Tables

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    Table 1.

    Statistical analyses

    LineData structureType of testPower
    avon Mises distributionRayleigh testNA
    bNormal distributionUnpaired t test1.000
    cNormal distributionUnpaired t test0.790
    dvon Mises distributionRayleigh testNA
    eNormal distributionUnpaired t test1.000
    fNormal distributionUnpaired t test0.995
    gNormal distributionUnpaired t test0.928
    hNormal distributionUnpaired t test0.573
    iNormal distributionUnpaired t test0.742
    jNormal distributionUnpaired t test0.990
    kvon Mises distributionRayleigh testNA
    lvon Mises distributionRayleigh testNA
    mvon Mises distributionUnpaired two-sample (Watson–Williams) test0.169
    nNormal distributionUnpaired t test0.158
    ovon Mises distributionRayleigh testNA
    pvon Mises distributionRayleigh testNA
    qvon Mises distributionPaired two-sample test0.720
    rNormal distributionPaired t test0.051
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Phase-Dependent Modulation of Oscillatory Phase and Synchrony by Long-Lasting Depolarizing Inputs in Central Neurons
Satoshi Watanabe, Moritoshi Hirono
eNeuro 5 October 2016, 3 (5) ENEURO.0066-16.2016; DOI: 10.1523/ENEURO.0066-16.2016

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Phase-Dependent Modulation of Oscillatory Phase and Synchrony by Long-Lasting Depolarizing Inputs in Central Neurons
Satoshi Watanabe, Moritoshi Hirono
eNeuro 5 October 2016, 3 (5) ENEURO.0066-16.2016; DOI: 10.1523/ENEURO.0066-16.2016
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Keywords

  • Neural Oscillation
  • Olfactory processing
  • phase–response curve
  • Purkinje cell
  • synchronization

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