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Research Articles, Behavioral/Cognitive

Left–Right Locomotor Coordination in Human Neonates

Arthur H. Dewolf, Valentina La Scaleia, Adele Fabiano, Francesca Sylos-Labini, Vito Mondi, Simonetta Picone, Ambrogio Di Paolo, Piermichele Paolillo, Yuri Ivanenko and Francesco Lacquaniti
Journal of Neuroscience 24 August 2022, 42 (34) 6566-6580; DOI: https://doi.org/10.1523/JNEUROSCI.0612-22.2022
Arthur H. Dewolf
1Department of Systems Medicine and Center of Space Biomedicine, University of Rome Tor Vergata, 00133 Rome, Italy
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Valentina La Scaleia
2Laboratory of Neuromotor Physiology, Istituto di Ricovero e Cura a Carattere Scientifico Santa Lucia Foundation, 00179 Rome, Italy
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Adele Fabiano
3Neonatology and Neonatal Intensive Care Unit, Casilino Hospital, 00169 Rome, Italy
4Neonatology and Neonatal Intensive Care Unit, Ospedale San Giovanni, 00184 Rome, Italy
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Francesca Sylos-Labini
2Laboratory of Neuromotor Physiology, Istituto di Ricovero e Cura a Carattere Scientifico Santa Lucia Foundation, 00179 Rome, Italy
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Vito Mondi
3Neonatology and Neonatal Intensive Care Unit, Casilino Hospital, 00169 Rome, Italy
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Simonetta Picone
3Neonatology and Neonatal Intensive Care Unit, Casilino Hospital, 00169 Rome, Italy
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Ambrogio Di Paolo
4Neonatology and Neonatal Intensive Care Unit, Ospedale San Giovanni, 00184 Rome, Italy
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Piermichele Paolillo
3Neonatology and Neonatal Intensive Care Unit, Casilino Hospital, 00169 Rome, Italy
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Yuri Ivanenko
2Laboratory of Neuromotor Physiology, Istituto di Ricovero e Cura a Carattere Scientifico Santa Lucia Foundation, 00179 Rome, Italy
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Francesco Lacquaniti
1Department of Systems Medicine and Center of Space Biomedicine, University of Rome Tor Vergata, 00133 Rome, Italy
2Laboratory of Neuromotor Physiology, Istituto di Ricovero e Cura a Carattere Scientifico Santa Lucia Foundation, 00179 Rome, Italy
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  • Figure 1.
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    Figure 1.

    A, Illustration of one neonate performing unilateral stepping with one limb manually blocked in the middle position. B, Examples of raw EMGs and limb kinematics during bilateral and unilateral stepping with the limb blocked in the middle position in two different neonates. VMz, Vertical coordinate of the fifth metatarsal marker. Traces include the transition from bilateral to unilateral stepping or the contrary (vertical line marks transition). Notice that a brief segment of RF activity of the stepping limb of neonate b16 was corrupt and has been replaced by a zero line.

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    Figure 2.

    Kinematics of the stepping limb. A, Thigh, shank, and foot elevation angles of all steps of bilateral and unilateral stepping with the limb blocked in middle position in gray, ensemble-average traces (i.e., average across steps in all neonates) in black. B, Coefficient of correlation and time lag of the cross-correlations between each individual trace and the ensemble-average trace of bilateral stepping. C, Average stride and swing duration; interstride variability; range of motion of the thigh, shank, and foot angles; and the excursion of the fifth metatarso-phalangeal joint in horizontal (x), lateral (y), and vertical (z) direction. Asterisks denote significant differences.

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    Figure 3.

    Recorded bilateral EMG profiles during bilateral and unilateral stepping with the limb blocked in the middle position. A, Examples of raw EMGs of two consecutive steps in four different neonates during bilateral stepping. Note that alternations between left (light gray) and right (dark gray) limb muscles are mostly observed. B, Examples of raw EMGs of two consecutive steps in three different neonates during bilateral stepping. Both alternate and synchronous muscle activation of the stepping limb (light gray) and the blocked limb (blue) are observed. VMz, Vertical coordinate of the fifth metatarsal marker.

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    Figure 4.

    A, B, Interlimb coupling during bilateral (A) and unilateral (B) stepping with the blocked limb in middle position. A, B, First line, Polar histograms of center of activity for bilateral stepping versus normalized cycles discretized in 20 sectors; second and third lines, polar histograms of the phase lag between the center of activity of both limbs (ΔCoA) for bilateral stepping versus normalized cycles discretized in 20 sectors; black arrows, progression time, with angle that varies from 0° to 360° corresponding to a 0% and 100% cycle. Bar height denotes the percentage of cycles whose center of activity (or ΔCoA) is located in the corresponding sector. Red arrows, Resultant (circular mean) center of activity (Rayleigh test for nonuniform circular distributions, p < 0.05). The pie chart presents the percentage of steps with alternate or synchronous LG bilateral activation, or with no modulation of LG EMG activity (i.e., where the center of activity of one of the limbs was not identifiable; Rayleigh test, p > 0.05).

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    Figure 5.

    Decomposition of LG envelope time series into their Fourier series components during bilateral stepping (n = 9) and unilateral stepping (n = 13) with the leg blocked in the middle position. A, Examples of bilateral LG envelope during several consecutive steps with similar (top) or different left and right oscillation frequencies (bottom). B, Illustration of the fast Fourier transform analysis and the percentage of neonates with different and similar left and right oscillation frequencies during bilateral and unilateral stepping with leg blocked in the middle position. C, Two examples of the bilateral onset of LG bursts of activation during unilateral stepping with different limb oscillation frequencies. In most cases, there was one burst onset of the blocked limb during each step of the stepping limb (1:1 coordination). In some cases, an episode with two burst onsets of the blocked limb during one step of the stepping limb were observed (2:1 coordination). In other cases, an episode without LG activation of the blocked limb (0:1 coordination) occurred. The pie chart presents the quantification of the different episodes of coordination in unilateral stepping.

  • Figure 6.
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    Figure 6.

    Effect of blocked limb position on stepping limb characteristics. A, Average (across steps in all neonates) stride and swing duration; range of motion of the thigh, shank, and foot angles; and orientation of the thigh, shank, and foot at touch-down and toe-off during unilateral stepping with the limb blocked in the anterior, middle, and posterior positions. B, Average FWHM, CoA, and mean EMG activity across one step of the four stepping limb muscles. Asterisks denote significant differences.

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    Figure 7.

    Effect of blocked limb position on blocked limb characteristics. A, Percentage of steps with alternate or synchronous LG bilateral activation, or with no modulation of LG EMG activity (i.e., where the center of activity of one of the limbs was not identifiable; Rayleigh test, p > 0.05). B, Average FWHM, CoA, and mean EMG activity of the four blocked limb muscles of the alternated (top) or synchronous steps (bottom). Asterisks denote significant differences. C, Schematic illustration of the effect of blocked limb position on muscle activation.

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    Figure 8.

    Top, Illustration of one neonate producing a dorsiflexion of the ankle after the release of the blocked limb in posterior position. Bottom, Examples of raw TA EMGs after the release of the blocked limb in posterior position in six different neonates.

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    Figure 9.

    Loading response of the stepping limb. Knee joint angle, RF and LG EMG envelope of all steps in which an extension of the knee was present during the first half of stance; black, the ensemble-average traces (average across steps in all neonates). The bar plot on the right presents the average knee extension (average across steps in all neonates) during the first 50% of stance.

Tables

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    Table 1.

    Number of steps per neonates

    Number of neonatesNumber of stepsMedian (interquartile range) steps per neonate
    Bilateral stepping373226 (7)
    Unilateral stepping
    Anterior321614 (3)
    Middle432534 (5)
    Posterior301575 (4)
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The Journal of Neuroscience: 42 (34)
Journal of Neuroscience
Vol. 42, Issue 34
24 Aug 2022
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Left–Right Locomotor Coordination in Human Neonates
Arthur H. Dewolf, Valentina La Scaleia, Adele Fabiano, Francesca Sylos-Labini, Vito Mondi, Simonetta Picone, Ambrogio Di Paolo, Piermichele Paolillo, Yuri Ivanenko, Francesco Lacquaniti
Journal of Neuroscience 24 August 2022, 42 (34) 6566-6580; DOI: 10.1523/JNEUROSCI.0612-22.2022

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Left–Right Locomotor Coordination in Human Neonates
Arthur H. Dewolf, Valentina La Scaleia, Adele Fabiano, Francesca Sylos-Labini, Vito Mondi, Simonetta Picone, Ambrogio Di Paolo, Piermichele Paolillo, Yuri Ivanenko, Francesco Lacquaniti
Journal of Neuroscience 24 August 2022, 42 (34) 6566-6580; DOI: 10.1523/JNEUROSCI.0612-22.2022
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Keywords

  • early development
  • human locomotion
  • interlimb coordination
  • neonatal stepping

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