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Articles, Behavioral/Systems/Cognitive

An Intersegmental Neuronal Architecture for Spinal Wave Propagation under Deletions

Toni Pérez, Jesus A. Tapia, Claudio R. Mirasso, Jordi García-Ojalvo, Jorge Quevedo, Carlos A. Cuellar and Elias Manjarrez
Journal of Neuroscience 19 August 2009, 29 (33) 10254-10263; https://doi.org/10.1523/JNEUROSCI.1737-09.2009
Toni Pérez
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Jesus A. Tapia
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Claudio R. Mirasso
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Jordi García-Ojalvo
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Jorge Quevedo
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Carlos A. Cuellar
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Elias Manjarrez
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  • Figure 1.
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    Figure 1.

    A, Scheme of the experimental arrangement. B, Recordings of spinal traveling waves and electroneurograms during scratching. The traces illustrate one resetting deletion (d) of the extensor MG motoneuronal activity. The magenta lines illustrate the rostrocaudal propagation of the CDP waves from electrodes 1–8. Flex and Ext indicate the activity of the flexor TA, and extensor, MG nerves, respectively. The arrowheads are spaced at the mean pre-deletion period (average of 5 periods). Intervals on the black horizontal bar were calculated from the hypothesized number of cycles present in the deletion. The interval spanning the deletion d is significantly different from the control (mean pre-deletion period) (p < 0.05). Note the alteration in the phase for the resetting deletion d even after the post-deletion period. Furthermore, note that the deletion interval d is not a multiple integer of the mean pre-deletion period. The recordings show that during the resetting deletion the sinusoidal CDP is abolished. The vertical rectangle shows the end of the resetting phase.

  • Figure 2.
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    Figure 2.

    The same as Figure 1B but for a single non-resetting deletion of the extensor MG motoneuronal activity. The arrowheads are spaced at the mean pre-deletion period (averaged over 5 periods). Intervals on the black horizontal bar were calculated from the hypothesized number of cycles present in the deletion. The interval spanning of the deletion d is not significantly different from the control (mean pre-deletion period) (p > 0.05; ns, statistically nonsignificant) and there was no change in the phase during this deletion.

  • Figure 3.
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    Figure 3.

    A, Absence of sinusoidal CDPs during resetting deletions in the activity of the MG nerve. Bottom, histograms of p values. The p value indicates the statistical significance of the difference between the phase (and cycle periods) before and during the deletion. These values were obtained by the statistical significance of the difference between the phase (and cycle periods) immediately preceding the deletion and the phase (and cycle periods) during deletions. p < 0.05 indicates resetting deletions. B, The same as A but for non-resetting deletions. In this case p > 0.05 indicates a non-resetting deletion. Data obtained from the analysis of 15 cats. The arrows indicate the occurrence of the deletions.

  • Figure 4.
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    Figure 4.

    A, Left plot, averaged cycle period preceding the resetting deletions (black bars) versus the cycle period during the resetting deletion (gray bars). B, Right plot, The same as the left plot, but for non-resetting deletions. B, The same as A, but for the mean phase. C, The same as A, but for the mean amplitude of the sinusoidal CDPs (measured from peak to peak). Error bars indicate the SD for 5 cycles. The numbers in the horizontal axis indicate different scratching episodes. D, Number of deletions versus p value to compare the mean cycle period of the extensor activity preceding the deletion and the cycle period of the hypothetical absence of extensor activity during the deletion (see Materials and Methods).

  • Figure 5.
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    Figure 5.

    A, Schematic representation of the proposed intersegmental CPG network. Eight CPG nodes are assumed to be distributed along the spinal cord in an asymmetric two-layer organization. Each node contains populations of excitatory neurons (gray balls) and populations of inhibitory interneurons (small red balls) synaptically connected (gray and black lines). The light gray arrows within RG and PF layers denote synapses connecting neighboring nodes (motoneuron populations of nodes 2, 3, 5, 6 and 7 are omitted for a better visualization). B, Propagation of the electrical activity along the spinal cord under normal operation (in the absence of induced deletions).

  • Figure 6.
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    Figure 6.

    Example of a resetting deletion. A temporary lack of electrical activity (400 ms) of the eight CPGs (from L4 to S1) and of the extensor motoneurons can be clearly seen. On the contrary, in flexor motoneurons the bursting period increases due to the lack of inhibition induced by the extensor group of the PF layer. Spaced arrowheads indicate the averaged period of the flexor-extensor cycle before the deletion. Note the clear phase shift of the post-deletion rhythm.

  • Figure 7.
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    Figure 7.

    Example of a non-resetting deletion. The electrical activity of the eight CPGs (from L4 to S1) remains unaltered. On the contrary, extensor motoneurons become temporarily silent. In contrast to the resetting deletions during non-resetting deletions flexor motoneurons do not alter their bursting duration. Spaced arrowheads indicate the averaged period of the flexor-extensor cycle before the deletion. Note that there is not a phase shift of the post-deletion rhythm.

Tables

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    Table 1.

    Parameters used in the numerical simulations

    ParameterValue
    gCa4.0 μS/cm2
    gK8.0 μS/cm2
    gL2.0 μS/cm2
    gKca0.25 μS/cm2
    VCa120.0 mV
    VK−84.0 mV
    VL−60.0 ± 0.6 mV
    V11.2 mV
    V218 mV
    W112 mV
    W217.4 mV
    ϕ4.6 s−1
    ε0.0175 s−1
    μ0.015–0.017
    I43.8 μA/cm2
    α0.33 ms−1 mm−1
    β0.2 ms−1
    Es0 mV, −80 mV (excitatory, inhibitory)
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    Table 2.

    Synaptic connectivity values

    ConnectivityValue
    gexc,int0.3 μS/cm2
    gint,exc0.1–0.6 μS/cm2
    g2,42.0 μS/cm2
    g4,flex2.0 μS/cm2
    g3,ext1.75 μS/cm2
    gint,flex1.5 μS/cm2
    gint,ext2.0 μS/cm2
    gexc,exc0.1 μS/cm2
    gCPG–CPG0.1 μS/cm2
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The Journal of Neuroscience: 29 (33)
Journal of Neuroscience
Vol. 29, Issue 33
19 Aug 2009
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An Intersegmental Neuronal Architecture for Spinal Wave Propagation under Deletions
Toni Pérez, Jesus A. Tapia, Claudio R. Mirasso, Jordi García-Ojalvo, Jorge Quevedo, Carlos A. Cuellar, Elias Manjarrez
Journal of Neuroscience 19 August 2009, 29 (33) 10254-10263; DOI: 10.1523/JNEUROSCI.1737-09.2009

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An Intersegmental Neuronal Architecture for Spinal Wave Propagation under Deletions
Toni Pérez, Jesus A. Tapia, Claudio R. Mirasso, Jordi García-Ojalvo, Jorge Quevedo, Carlos A. Cuellar, Elias Manjarrez
Journal of Neuroscience 19 August 2009, 29 (33) 10254-10263; DOI: 10.1523/JNEUROSCI.1737-09.2009
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