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Articles, Cellular/Molecular

Electrical Coupling between Locomotor-Related Excitatory Interneurons in the Mammalian Spinal Cord

Christopher A. Hinckley and Lea Ziskind-Conhaim
Journal of Neuroscience 16 August 2006, 26 (33) 8477-8483; DOI: https://doi.org/10.1523/JNEUROSCI.0395-06.2006
Christopher A. Hinckley
Department of Physiology and Center for Neuroscience, University of Wisconsin Medical School, Madison, Wisconsin 53706
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Lea Ziskind-Conhaim
Department of Physiology and Center for Neuroscience, University of Wisconsin Medical School, Madison, Wisconsin 53706
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    Figure 1.

    Characteristics of Hb9 INs. A, Hb9 INs did not project to the periphery, and they did not express ChAT. Neurons with peripheral axons were retrogradely labeled with rhodamine dextran-amine. Rhodamine-filled somatic (solid arrowhead) and sympathetic (open arrowhead) motoneurons were evident, but rhodamine was absent in GFP+/Hb9 INs (circles). In a different spinal cord, labeling with anti-ChAT antibody was apparent only in the two motoneuron populations. Scale bars, 100 μm. B, Current-clamp recordings from an Hb9 IN (GFP+/Hb9+) and a neighboring GFP−/Hb9− interneuron. Resting membrane potentials in both interneurons were approximately −60 mV. Positive current injection (30 pA/800 ms) evoked a 23 and 13 Hz repetitive firing in Hb9 and GFP− interneurons, respectively. Spike-frequency adaptation characterized the firing in the Hb9 IN. The interspike interval between the last two spikes increased by 67% compared with the first two spikes. Typically, linear I–V relationships were generated in Hb9 INs at potentials more negative than the resting potential, but negative current injections produced hyperpolarization-dependent depolarization sags in the GFP− interneuron. Input resistances were 1.2 and 1.0 GΩ for GFP+/Hb9+ and GFP−/Hb9− interneurons, respectively.

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    Figure 2.

    Bidirectional electrical coupling between Hb9 INs in the hemisected spinal cord of a P3 mouse. A long-duration positive current (30 pA/800 ms, I1) produced a 20 Hz firing in the injected neuron (V1) and synchronous spikelets in the postjunctional neuron (V2). Summation of five to six spikelets reached threshold to generate two action potentials. Negative currents produced hyperpolarizations in both neurons. Similar potential changes were generated when current was injected in neuron 2 (I2), but the spikelets in the coupled interneuron (V1) did not reach action potential threshold. The coupling coefficient was 14.8%.

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    Figure 3.

    Electrical coupling in Hb9 INs was not associated with chemical synaptic transmission. A, Action potential in the prejunctional interneuron (V1) produced a short-latency (∼0.2 ms) inward current in the postjunctional neuron (I2) in a hemisected cord of a P3 mouse. The amplitude of the inward currents did not significantly change at holding potentials ranging from −40 to −80 mV. B, Identical postjunctional inward currents were generated in the absence (black trace) and presence (gray trace) of CNQX (10 μm for 30 min) in coupled Hb9 INs in a P2 mouse. C, In coupled Hb9 INs in the hemicord of a P4 mouse, the inward current was reversibly suppressed by carbenoxolone (100 μm). Recordings were performed after a 25 min exposure to the blocker. The traces in B and C are averages of 10 recordings generated at 0.1 Hz.

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    Figure 4.

    Electrical coupling persisted in juvenile mice. A, Voltage commands of ±50 mV in a prejunctional Hb9 IN (V1) generated currents of approximately −5/+7 pA in the postjunctional neuron (I2) in the spinal cord of a P10 mouse. Similar currents were produced in the first Hb9 IN (I1) in response to voltage commands in neuron 2. The smaller amplitude of the inward than outward currents might reflect differences in input resistance at depolarizing and hyperpolarizing potentials. A junctional conductance of 182 pS was measured in response to a voltage command of −50 mV. B, Histogram showing a wide range of coupling coefficients between electrically coupled Hb9 INs in P1–P4 mice. The mean coupling coefficient was 12.4%.

  • Figure 5.
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    Figure 5.

    Electrical synapses served as low-pass filters. A, Frequency-dependent transmission of sine wave current between Hb9 INs. Left, The coupling coefficient was 13.5% during a 4 Hz sine wave, corresponding to 42% of the steady-state coupling. Right, Mean coupling coefficients as a function of frequency. The coupling coefficient decreased to ∼50% at 3 Hz and 30% at 20 Hz. Coupling coefficients were normalized to steady-state values. Error bars indicate SEs. B, Prejunctional action potentials generated by a prolonged positive current (see Fig. 2) triggered the onset of short-latency postjunctional spikelets. Superimposed are 12 consecutive action potentials and spikelets. Action potential peaks are truncated. Spikelet amplitudes varied from 0.5 to 1.4 mV.

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    Figure 6.

    Episodes of synchronous EPSCs and firing in electrically coupled Hb9 INs. A, Synchronized onset of burst of EPSCs in paired interneurons in a P4 mouse. The burst lasted for >2 s. The coupling coefficient was 26%. B, Coordinated spontaneous firing bursts in electrically coupled Hb9 INs in a P2 mouse. The coupling coefficient was 21%. C, Random firing was synchronized in the same pair of Hb9 INs shown in A. D, Cross-correlogram of action potential firing shown in C demonstrated a significant correlation (∼0.8) of firing within ±1 ms. Although the firing correlation gradually decreased over time, it was significant over a relatively large time scale (±250 ms). The range of +3 × SE is marked by the dashed horizontal line.

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    Figure 7.

    Neurochemically induced coordinated rhythms in electrically coupled Hb9 INs. A, Membrane oscillations in-phase with ventral root bursts (bottom traces) were produced in the presence of NMA (N-methyl-d,l-aspartate; 5 μm), 5-HT (10 μm), and dopamine (50 μm) in a P3 mouse. The electroneurograms were rectified and smoothed using adjacent averaging over 100–200 points (white traces). Exposure to CNQX (10 μm for >30 min) did not suppress the rhythms in the Hb9 IN but eliminated motoneuron bursts. The average cycle period was 6.2 ± 0.3 s (SE; n = 20 cycles), not significantly different from the period recorded in the presence of CNQX (6.4 ± 0.2 s). B, Neurochemically induced membrane oscillations were generated in the presence of TEA (10 mm) and higher Ca2+ concentration (3 mm) in a P4 mouse. The average cycle period was 19.8 ± 0.9 s (n = 20 cycles), and the coefficient of variance was 0.2. Rhythms with similar amplitudes and waveforms were produced, and their onset was synchronized between the coupled interneurons. Marked rhythms (dashed box) were expanded to show these properties (right).

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The Journal of Neuroscience: 26 (33)
Journal of Neuroscience
Vol. 26, Issue 33
16 Aug 2006
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Electrical Coupling between Locomotor-Related Excitatory Interneurons in the Mammalian Spinal Cord
Christopher A. Hinckley, Lea Ziskind-Conhaim
Journal of Neuroscience 16 August 2006, 26 (33) 8477-8483; DOI: 10.1523/JNEUROSCI.0395-06.2006

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Electrical Coupling between Locomotor-Related Excitatory Interneurons in the Mammalian Spinal Cord
Christopher A. Hinckley, Lea Ziskind-Conhaim
Journal of Neuroscience 16 August 2006, 26 (33) 8477-8483; DOI: 10.1523/JNEUROSCI.0395-06.2006
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Keywords

  • electrical coupling
  • gap junction-mediated transmission
  • rhythm coordination
  • locomotor-related interneurons
  • excitatory spinal interneurons
  • mouse spinal cord

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