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Research Article
Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain
S. Sponberg, R. J. Full
Journal of Experimental Biology 2008 211: 433-446; doi: 10.1242/jeb.012385
S. Sponberg
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R. J. Full
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Figures

  • Fig. 1.
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    Fig. 1.

    Cockroaches (B. discoidalis) were run over a rough terrain (A) with a Gaussian distribution of surface heights (B) up to three times the hip height of the animal (C). The cockroach experienced repeated random perturbation while negotiating the terrain. Offsetting the terrain from the entry and exit tracks resulted in very large (4–6 times hip height) perturbations to the first and last steps on the terrain. The level surface of all blocks was 1 cm×1 cm.

  • Fig. 2.
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    Fig. 2.

    Muscle action potentials during running over flat versus rough terrain. (A) Recordings of the muscle action potentials (MAPs) activating the ventral femoral extensor (179) in the hind left leg of a cockroach running on flat (black trace) and rough terrain (blue trace). Each cluster of spikes occurs during a single stance phase. Changes in neural stimulation would necessitate neural feedback in the control of locomotion over the rough terrain. (B) Four measures of the activation burst describe the degree of stimulation (number of spikes) and the relevant timing parameters (interspike interval, interburst interval and burst phase).

  • Fig. 3.
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    Fig. 3.

    Kinematic perturbations of cockroaches running on flat versus rough terrain. While locomoting on rough terrain (blue traces), cockroaches encountered perturbations in pitch (A), roll (B) and yaw (C) away from typical patterns found during flat, unperturbed running (black traces). Due to small misalignment of the cross introducing a constant offset, roll traces are normalized around a baseline of zero. Yaw was also normalized to zero to represent deviation from the straight-line path between beginning and ending points during a single trial.

  • Fig. 4.
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    Fig. 4.

    Histograms of the proportion of steps that contained one through seven action potentials. (A) The distributions are statistically indistinguishable between flat (black) and rough (blue) terrain running, indicating that this parameter (spike number) was not modified by typical rough terrain perturbations. Neural modulation of spike number was evident during the large ascending perturbation at the start of the rough terrain (B) and during the final large descending step (C).

  • Fig. 5.
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    Fig. 5.

    Distribution of interspike intervals (ISIs) between all spikes within a burst compared between flat (A) and rough (B) terrain running. Neither the individual animal nor the order of the spiking event in the step (time between first and second spike vs time between second and third spike) significantly affected the distribution. Running speed did correlate with ISI and was corrected for in the normalized ISI values (C,D). No significant differences between terrain type were present in normalized ISI distributions.

  • Table 1.

    Duty factors and gait statistics for flat and rough terrain running

    Duty factorP-values for Flat vs Rough terrain (t-tests)
    Leg*Flat terrainRough terrainDuty factorStance initiation phaseSwing initiation phase
    FL0.51±0.010.54±0.020.4540.4090.079
    FR0.53±0.010.54±0.020.9740.1120.318
    ML0.60±0.010.61±0.020.6020.4560.346
    MR0.58±0.010.58±0.020.9040.4870.998
    HL0.50±0.010.52±0.030.130N/A†0.130
    HR0.50±0.010.50±0.030.4370.3480.056
    • Values are means ± s.e.m.

    • ↵* FL, front left; FR, front right; ML, middle left; MR, middle right; HL, hind left; HR, hind right

    • ↵† Since hind left leg stance initiation defines a phase of zero there can be no comparison

  • Table 2.

    Individual leg gait phase for flat and rough terrain running

    Flat terrain Rough terrain
    LegStance onset phaseSwing onset phase*Stance onset phaseSwing onset phase*
    FL–0.09±0.010.40±0.01–0.07±0.020.48±0.04
    FR0.40±0.010.90±0.010.45±0.030.94±0.04
    ML0.42±0.011.02±0.010.45±0.021.04±0.02
    MR–0.07±0.010.51±0.01–0.06±0.020.51±0.02
    HL0†0.51±0.010†0.54±0.02
    HR0.49±0.011.02±0.010.51±0.021.06±0.02
    • Values are means ± s.e.m.; FL, front left; FR, front right; ML, middle left; MR, middle right; HL, hind left; HR, hind right

    • ↵* Swing onset phase=stance termination phase

    • ↵† Hind left leg stance onset was defined as the reference phase of 0

  • Fig. 6.
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    Fig. 6.

    Distributions of the interburst interval (IBI) of the MAP burst (A) and the phase of the MAP burst (B) compared between flat and rough terrain running. As with ISI values, IBI values correlated with running speed and were speed normalized (A, right panels). Phase is defined relative to stance initiation events of the hind left leg. No significant differences between terrain type were present in normalized IBI or phase distributions.

  • Fig. 7.
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    Fig. 7.

    Large perturbation mis-steps. A small number of rough terrain steps included a leg that failed to contact the substrate during stance. Here, the hind left leg (three pink points in image 1) swings through a trough formed by several particularly high obstacles (A). Normal activation of muscle 179 occurs even though contact is absent (B); however, there is a subsequent increase in stride period in the following step (B,C), indicating a stride-to-stride change in the clock-like activation of 179. This change requires neural feedback. Stride period returns to the original time within two strides of the mis-step following kinematic recovery from the perturbation. Histograms in C are normalized with respect to the baseline stride period taken 2 steps before the perturbation.

  • Fig. 8.
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    Fig. 8.

    Proportion of steps demonstrating follow-the-leader gait. Histograms report the proportion of steps during rough terrain running in which pairs of ipsilateral legs (FL—ML, ML—HL, etc.) use the same 1 cm×1 cm block on two sequential steps. This indicator of follow-the-leader (FTL) stepping occurs in less than a third of steps despite the relatively large target area. Middle/front leg pairs use the same blocks more often than do hind/middle leg pairs. FL, front left; FR, front right; ML, middle left; MR, middle right; HL, hind left; HR, hind right.

  • Fig. 9.
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    Fig. 9.

    Follow-the-leader (FTL) foot placements. FTL deviation plotted for each of the four pairs of legs (A). In each plot the origin was defined as the point of anterior leg placement with positive axes pointed anteriorly and to the right side of the animal. Points in quadrant I therefore represent a stance position in front of and to the right of where the anterior leg had foot placement. Flat terrain steps are in black, rough terrain in blue. In both cases, footfalls were significantly skewed away from the origin, indicating lack of FTL stepping. The distance of the deviations are represented as histograms for flat (top) and rough (bottom) terrain running (B). Deviation distance is the Euclidean distance to the origin for each point from the four plots in A, pooled across all pairs of legs. The peaks of the distributions are shifted from zero (perfect FTL stepping) and the means are above both the strict (3 mm) and minimal (5 mm) FTL deviation criteria.

  • Fig. 10.
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    Fig. 10.

    Stance or swing duration as a function of speed. Stance and swing duration decrease as a function of speed until mid-speed (Full and Tu, 1990). No change in duration is observed at high speeds. Animals ran at the mid-speed range in the present study. Most previous studies of cockroach locomotor control, other than escape response elicitation, have been conducted at speeds less than 1/6 the maximal speed. aPresent study; b(Watson and Ritzmann, 1998a); c(Watson and Ritzmann, 1998b); d(Ridgel and Ritzmann, 2005); e(Tryba and Ritzmann, 2000a; Tryba and Ritzmann, 2000b); f(Watson et al., 2002a; Watson et al., 2002b).

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Research Article
Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain
S. Sponberg, R. J. Full
Journal of Experimental Biology 2008 211: 433-446; doi: 10.1242/jeb.012385
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Research Article
Neuromechanical response of musculo-skeletal structures in cockroaches during rapid running on rough terrain
S. Sponberg, R. J. Full
Journal of Experimental Biology 2008 211: 433-446; doi: 10.1242/jeb.012385

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