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Stepping behaviors in chronic spinal cats with one hindlimb deafferented.

Adult cats develop spontaneous airstepping (walking motions without ground contact) 4-6 weeks after spinal transection (Giuliani and Smith, 1985). This unique preparation provides an in vivo model for studying the effects of hindlimb deafferentation on stepping behaviors without rostral input to lumbosacral segments. The primary purpose of this study was to characterize airstepping and, to a lesser extent, bipedal treadmill locomotion in chronic spinal cats after deafferentation. Five cats were spinalized at T12, and EMG electrodes were implanted in selected knee and ankle muscles. After spontaneous airstepping developed, one hindlimb was deafferented extensively. Movements of both hindlimbs were depressed following unilateral deafferentation. By the third week, spontaneous airstepping recovered in the normal hindlimb (N-Limb), but in the deafferented limb (D-Limb) airstepping was not spontaneous during the 3-4 months of testing. By the seventh week, bilateral airstepping was facilitated by tonic exteroceptive simulation (tail-pinch). During bouts of bilateral airstepping, assessed during the third month of deafferentation, D-Limb airstep cycles were characterized by erratic rhythm. Further, cycle periods and extensor burst durations were prolonged, but flexor burst durations were unmodified. In contrast, N-Limb cycles were rhythmic and of normal duration, but extensor burst durations were short and unrelated to cycle periods. Interlimb coordination was markedly unstable, showing only brief periods of alternating steps. When erratic bilateral airstepping was accompanied by micturition, rhythmic and alternate stepping emerged, with normalized intralimb synergies. During hindlimb treadmill locomotion, tested in 2 cats, the N-Limb took weight-bearing steps and followed changes in the belt speed. The D-Limb, however, stepped erratically, making contact on the dorsum of the paw; consistent bouts by bilateral stepping were not obtained. Lumbosacral afference of some type, either from the hindlimb or from regions remote from the limb, such as the bladder, appears to be essential for stabilizing the coupling between hindlimb generators for stable interlimb coordination. Future modeling of interlimb coordination should consider the role of afference.

Animals↗

The effect of frequency on the visual perception of relative phase and phase variability of two oscillating objects.

Relative phase has been studied extensively as a measure of interlimb coordination. Only two relative phases, namely 0 degrees and 180 degrees, are stably produced at the preferred frequency (approximately 1 Hz). When frequency is increased, movement at 180 degrees becomes unstable and relative phase typically switches to 0 degrees, which remains stable at higher frequencies. The current study was designed to investigate the perception of relative phase and of phase variability. Observers viewed two circles moving rhythmically in a computer display. Mean phases varied from 0 degrees to 180 degrees in 30 degrees steps. Phase variability at each mean phase varied from 0 degrees to 5 degrees, 10 degrees, and 15 degrees phase standard deviation (SD). Frequency of oscillation was either 0.75 Hz or 1.25 Hz. One group of ten observers judged mean relative phase. Another group judged phase variability. As predicted, increase in frequency yielded an increase in perceived phase variability at 180 degrees mean phase and other mean phases, but not at 0 degrees mean phase. In contrast, increase in actual phase variability affected judgments of 0 degrees mean phase most strongly. A second control experiment showed that the frequency effects were not produced by changes in display durations or frames per cycle of oscillation. The results are consistent with those in studies of interlimb coordination and indicate that understanding of interlimb coordination requires further investigation of phase perception.

Adolescent↗

Implications of assist-as-needed robotic step training after a complete spinal cord injury on intrinsic strategies of motor learning.

Robotic training paradigms that enforce a fixed kinematic control might be suboptimal for rehabilitative training because they abolish variability, an intrinsic property of neuromuscular control (Jezernik et al., 2003). In the present study we introduce "assist-as-needed" (AAN) robotic training paradigms for rehabilitation of spinal cord injury subjects. To test the efficacy of these robotic control strategies to teach spinal mice to step, we divided 27 adult female Swiss-Webster mice randomly into three groups. Each group was trained robotically by using one of three control strategies: a fixed training trajectory (Fixed group), an AAN training paradigm without interlimb coordination (Band group), and an AAN training paradigm with bilateral hindlimb coordination (Window group). Beginning at 14 d after a complete midthoracic spinal cord transection, the mice were trained daily (10 min/d, 5 d/week) to step on a treadmill 10 min after the administration of quipazine (0.5 mg/kg), a serotonin agonist, for a period of 6 weeks. During weekly performance evaluations, the mice trained with the AAN window paradigm generally showed the highest level of recovery as measured by the number, consistency, and periodicity of steps during the testing sessions. In all three measurements there were no significant differences between the Band and the Fixed training groups. These results indicate that the window training approach, which includes loose alternating interlimb coordination, is more effective than a fixed trajectory paradigm with rigid alternating interlimb coordination or an AAN paradigm without any interlimb constraints in promoting robust postinjury stepping behavior.

Animals↗

Development of locomotor mechanisms in the frog.

Tadpoles swim by undulations of the body and tail, whereas frogs locomote by alternate (stepping) and synchronous (frog-kick) movements of the hindlimbs. The development of interlimb coordination was studied by recording the activity of hindlimb motoneurons from the left and right ninth ventral roots of the isolated central nervous system (CNS). Results showed that mechanisms responsible for interlimb coordination of stepping are functional when the hindlimb is still composed of undifferentiated mesenchyme and before the lateral motor column has stabilized (stage III). The early appearance of coordinated activation of hindlimb motoneurons suggests that innervation of appropriate target muscles is not a prerequisite for normal development of circuits that mediate interlimb coordination of stepping. Synchronous activation of left and right hindlimb motoneurons (fictive frog kicks) appeared later in development (stage XIV). Throughout larval development 1:1 frequency coupling between both alternating and synchronous bursts of hindlimb motoneurons and bursts of primary motoneurons (those innervating axial muscles) was found. Recordings of peripheral nerve activity showed that motoneurons innervating antagonistic muscles of the thigh burst in antiphase. This intralimb coordination was present at stage X, a foot paddle stage that was the earliest stage in which the peripheral nerves were successfully dissected. That the neural activity of the isolated nervous system described above indeed underlies coordinated locomotor movements of the hindlimbs was shown by single-frame videotape analysis of hindlimb movements produced by the otherwise isolated CNS. The stepping movements displayed by those preparations were consistent with patterns of electrophysiological burst activity recorded from the ventral roots and peripheral nerves. The ontogenetic sequence in which the different patterns of electrophysiological activity emerged is the same as that of the corresponding behaviors in the intact tadpole. Although there were developmental changes in the reliability with which coordinated activity in the ventral roots and peripheral nerves was observed, each mode of coordination remained qualitatively unchanged from its earliest appearance through metamorphosis. These results show that mechanisms underlying locomotor coordination of the hindlimbs develop very early in larval ontogeny of the frog and can function when isolated from the periphery.

Afferent Pathways↗

Influence of body segment position during in-phase and antiphase hand and foot movements: a kinematic and functional MRI study.

Behavioral studies have provided important insights into the mechanisms governing interlimb coordination. In this study, we combined kinematic and functional magnetic resonance imaging (fMRI) analysis to investigate the brain cortical and subcortical areas involved in interlimb coordination and the influence of direction of movement and of body segment position on the activity of those areas. Fifteen right-handed healthy subjects were studied while performing cyclic in-phase and antiphase hand and foot movements with the dominant, right limbs, with the upper limb positioned either prone or supine, and in front or behind with respect to the trunk. When contrasting antiphase to in-phase movements, fMRI analysis demonstrated an increased recruitment of a widespread sensorimotor network (including regions in the frontal and parietal lobes, bilaterally, the cingulated motor area, the thalami, the visual cortex, and the cerebellum) considered to function in motor, sensory, and multimodal integration processing. When contrasting the anterior to the posterior position of the upper limb with respect to the trunk, we found different recruitment patterns in the frontal and parietal regions as well as the preferential recruitment of the basal ganglia, the insula, and the cerebellum during the first condition and of regions located in the temporal lobes during the second one. Different brain areas are engaged at a different extent during interlimb coordination. In addition to the relative difficulty of the movement, the different cognitive and sensorial loads needed to control and perform the motor act might be responsible for these findings.

Adult↗

Fine motor control in adults with and without chronic hemiparesis: baseline comparison to nondisabled adults and effects of bilateral arm training.

OBJECTIVES: To characterize fine motor control through finger tapping in both arms of 10 patients with chronic stroke, to make baseline comparisons with matched controls, and to examine the responsiveness of deficits seen in stroke patients after 6 weeks of bilateral arm-based training. DESIGN: Nonrandomized controlled, cohort before-after trial. SETTING: Research institution. PARTICIPANTS: Ten people from the community with chronic unilateral ischemic stroke and 10 age- and sex-matched healthy controls. Participants with hemiparesis had completed all conventional care and were more than 6 month poststroke. Inclusion criteria were at least 6 months since a unilateral stroke, ability to follow simple instructions and 2-step commands, volitional control of the nonparetic arm, and at least minimal antigravity movement in the shoulder of the paretic arm. INTERVENTIONS: Not applicable. MAIN OUTCOME MEASURES: Measurements included rate and timing consistency of unilateral tapping at a preferred and a maximal rate and the accuracy and stability of interlimb coordination in bilateral simultaneous (inphase) and alternating (antiphase) tapping at a preferred rate. RESULTS: Nonparetic finger control was similar to that of the nondisabled participants except under bilateral conditions, where it was less consistent. A subgroup with residual paretic finger function, had slower and less consistent paretic finger tapping, as well as less accurate and more variable interlimb coordination; however, basic bilateral coupling relationships were preserved. Bilateral arm-based training improved bilateral nonparetic consistency but slowed unilateral preferred tapping. Training also improved paretic fine motor control in 2 of 4 participants with mild stroke severity. The 2 responders, with dominant hemisphere lesions, indicated a possible recovery advantage with bilateral training for such lesions. CONCLUSIONS: In general, nonparetic finger control for tapping was preserved but paretic finger control was compromised. Disruption of nonparetic control of tapping, particularly consistency of tapping, occurred during bilateral tapping tasks but was responsive to 6 weeks of bilateral arm-based training. Despite the apparent lack of training specificity, the generalizable effects of bilateral arm training to fine motor interlimb coordination may reflect central motor control mechanisms for upper-extremity coordination, which may be accessed and may influence the recovery of arm function after stroke.

Chronic Disease↗

Neuromuscular patterns of stereotypic hindlimb behaviors in the first two postnatal months. I. Stepping in normal kittens.

Neuromuscular patterns associated with the development of hindlimb stepping behaviors were studied from birth to postnatal day 60 in normal kittens. Hindlimb muscles were chronically implanted with EMG electrodes at birth to characterize interlimb coordination and intralimb synergies during development of overground and treadmill stepping. Airstepping was also examined but seldom occurred after the second postnatal week. All kittens performed stepping under each condition, including weight-supported stepping, by postnatal day 3. The number of sequential steps on the treadmill and overground increased with age and cycle periods decreased. At onset, stepping behaviors were characterized by adult-like EMG patterns. Interlimb coordination was typified by alternating extensor bursts of similar duration. Extensors at the knee and ankle were coactive during the stance phase, and extensor burst durations were strongly correlated with the cycle periods over a wide range of stepping frequency. Ankle flexor and extensor muscles were reciprocally active during postural tremor, bouts of airstepping, and weight-supported steps on the treadmill and overground. The duration of the reciprocal flexor bust did not vary with cycle period or age. Observations of stepping behaviors and adult-like EMG patterns during initial postnatal development were contingent on optimal testing conditions. Taken together, the data suggest that pattern-generating circuits for regulating interlimb coordination and intralimb muscle synergies are potentially functional prior to the normal ontogenetic onset of locomotion. Perhaps the prolonged postnatal development of locomotion reflects the time required to establish adaptive mechanisms, such as postural control and agility, rather than spinal pattern-generating circuits for locomotion.

Animals↗

Spinal cord coordination of hindlimb movements in the turtle: interlimb temporal relationships during bilateral scratching and swimming.

Hindlimb interlimb coordination was examined in turtles during symmetrical "same-form" behaviors in which both hindlimbs utilized the same movement strategy ("form") and during asymmetric "mixed-form" behaviors in which the form exhibited by one hindlimb differed from that of its contralateral partner. In spinal turtles, three forms of scratching were examined: rostral, pocket, and caudal. Bilateral symmetrical same-form scratching was studied for each of the forms. Asymmetric mixed-form scratching (rostral scratching of a hindlimb and pocket scratching of the other hindlimb) was also examined. In intact turtles, two forms of swimming were examined: forward swimming and back-paddling. The symmetrical behavior of bilateral forward same-form swimming and the asymmetric behavior of turning mixed-form swimming (forward swimming of 1 hindlimb and back-paddling of the other hindlimb) were studied. For all behaviors examined, most episodes displayed absolute or 1:1 coordination; in this type of coordination, during each movement cycle that began and ended with the onset of ipsilateral hip flexion, there was a single onset of contralateral hip flexion. For most of these episodes there was out-of-phase coordination between hip movements; the onset of contralateral hip flexion occurred near the onset of ipsilateral hip extension midway through the ipsilateral movement cycle. Bilateral caudal/caudal same-form scratching displayed out-of-phase 1:1 coordination during some episodes and in-phase 1:1 coordination during other episodes. During in-phase coordination, the onset of contralateral hip flexion occurred near the onset of ipsilateral hip flexion close to the start of the ipsilateral movement cycle. In a few cases of bilateral same-form scratching there were episodes of relative or 2:1 coordination; in this type of coordination, during each movement cycle of the slowly moving limb that began and ended with ipsilateral hip flexion, there were two distinct occurrences of the onset of contralateral hip flexion. The observation that out-of-phase movements of the hip occurred during symmetrical as well as asymmetric behaviors is consistent with the hypothesis that timing signals related to hip movement play a major role in interlimb phase control. The neural mechanisms responsible for interlimb phase control are not well understood in vertebrates. The present demonstration of bilateral scratching in spinal turtles suggests that this preparation may be suitable for additional experiments to examine mechanisms of vertebrate interlimb phase control.

Animals↗

Coordination of symmetrical and asymmetrical human gait.

Most human gait forms assume symmetrical, alternating patterns of interlimb coordination (e.g., crawling, walking, running). Human galloping is a notable exception. In contrast to extensive information on galloping in animals, little is known about this gait in humans. Therefore, kinematic and topographical analyses of running and galloping were undertaken to investigate the manner in which the lower limbs are uncoupled to produce this asymmetrical gait. Seven adult females were filmed while running and galloping at their preferred speed. Analysis of the gaits revealed differences in the following: (a) preferred speed, (b) coupling between upper- and lower-limb girdles, and (c) point of foot fall (end-point trajectories). In contrast to clear differences in interlimb coordination, intralimb coordination was remarkably similar across gaits, although when galloping was adopted, the rear leg did show more variable change than the front leg.

Journal Article↗

Distinguishing between the effects of frequency and amplitude on interlimb coupling in tapping a 2:3 polyrhythm.

Rhythmic interlimb coordination is characterized by attraction to stable phase and frequency relations. Sudden, unintended transitions between such coordination patterns have been observed in iso- and multifrequency tasks when movement frequency was gradually increased. These transitions have been accounted for by modeling the two limbs as nonlinearly coupled oscillators. The prevailing form of the coupling function is based on time derivatives, but an alternative formulation can be derived by incorporating time delays. These time delays may be related to the neurophysiological delays associated with the use of kinesthetic afferences. The two ways of deriving coupling functions for interlimb coordination allow for different predictions with respect to the effects of movement frequency and amplitude on the strength of interaction between the limbs. In the current experiment, the effects of amplitude and frequency were dissociated experimentally, so as to arrive at an empirically motivated choice between the two ways of formalizing interlimb coupling. Subjects tapped the polyrhythm 2:3 at five different frequencies under three amplitude conditions. Whereas no effects of amplitude were observed, the strength of interaction between the hands decreased with increasing movement frequency. These results support the time-delay version of the model, in which differential (loss of) stability of coordination modes results from differential dependence on movement amplitude, but overall coupling strength is related reciprocally to movement frequency squared. This version of the model was related tentatively to three proposed aspects of interlimb coordination: (1) neurophysiological delays associated with the use of kinesthetic afferences; (2) rate-dependent decrease in pattern stability; and (3) differential entrainment influences of kinesthetic signals.

Adult↗

Intermanual coordination: from behavioural principles to neural-network interactions.

Locomotion in vertebrates and invertebrates has a long history in research as the most prominent example of interlimb coordination. However, the evolution towards upright stance and gait has paved the way for a bewildering variety of functions in which the upper limbs interact with each other in a context-specific manner. The neural basis of these bimanual interactions has been investigated in recent years on different scales, ranging from the single-cell level to the analysis of neuronal assemblies. Although the prevailing viewpoint has been to assign bimanual coordination to a single brain locus, more recent evidence points to a distributed network that governs the processes of neural synchronization and desynchronization that underlie the rich variety of coordinated functions. The distributed nature of this network accounts for disruptions of interlimb coordination across various movement disorders.

Animals↗

Adaptations in interlimb and intralimb coordination to asymmetrical loading in human walking.

The purpose of this study was to examine both the intralimb (within a limb) and interlimb (between the right and left limbs) adaptations that occur in response to a unilaterally applied leg load as subjects walked at their preferred walking speed. It was hypothesized that this adaptation would alter interlimb coordination while intralimb coordination remained invariant. Subjects (n = 12) were required to walk on a treadmill at preferred walking speed. Bilateral 3-D kinematic data were collected while a load placed on the leg was increased. Gait adaptations to leg-loading were assessed through changes in coordination patterns between specific limb couplings. Continuous relative phase (CRP) was used to evaluate changes in limb coordination under each experimental load condition compared to a no load baseline condition. Both changes in magnitude of CRP (root-mean-square (RMS) analysis) as well as temporal changes in CRP across the stride cycle (cross-correlation) were assessed. Cross-Correlation values changed with load for all interlimb couplings assessed suggesting alterations in interlimb coordination across the stride cycle. CRP cross-correlation values were close to 1.0 in all the intralimb couplings examined, showing a relative invariance in intralimb coordination. Coordination changes in RMS were also observed for the interlimb couplings. RMS changes were also observed in the intralimb couplings on the loaded side. It appears that gait adaptations to a unilaterally applied leg load appear both at the intralimb and interlimb level. However, the majority of changes did appear at the interlimb level, where CRP as assessed through both cross-correlation and RMS measures changed. This study supports previous results that suggested a tighter coupling exists at the intralimb level, leaving the majority of gait adaptations to occur at the interlimb level. The observed adaptation in differences between interlimb and intralimb coordination may provide insight into gait adaptations in pathological gait.

Adult↗

Bimanual coordination dynamics in poststroke hemiparetics.

Poststroke hemiparetic individuals (n = 9) and a control group (n = 9) completed a frequency-scaled circle-drawing task in unimanual and bimanual conditions. Measures of intralimb spatial and temporal task accuracy and interlimb coordination parameters were analyzed. Significant reductions in task performance were seen in both limbs of the patients and controls with the introduction of bimanual movement. Spatial performance parameters suggested that the 2 groups focused on different hands during bimanual conditions. In the controls, interlimb coordination variables indicated predictable hand dominance effects, whereas in the patient group, dominance was influenced by the side of impairment and prior handedness of the individual. Therefore, in this particular bimanual task, performance improvements in the hemiplegic side could not be elicited. Intrinsic coupling asymmetries between the hands can be altered by unilateral motor deficits.

Adult↗

Functional recovery in hemiplegic cerebral palsy: ipsilateral electromyographic responses to focal transcranial magnetic stimulation.

The patterns of functional recovery after unilateral cerebral damage occurring in the prenatal to infantile periods were studied in nine patients with hemiplegic cerebral palsy. Motor evoked potentials (MEPs) recorded from the small hand muscles were investigated using focal transcranial magnetic stimulation (TMS). The MEPs findings could be separated into three subtypes based on the features of ipsilateral MEPs elicited by TMS over the unaffected motor cortex. Bilateral MEPs of similar latency were obtained in three patients. These patients each having a congenital lesion invariably exhibited mirror movements and severe hemiparesis. Meanwhile, ipsilateral MEPs with markedly prolonged latency were demonstrated in two other patients, who exhibited synergistic associated movements and severe hemiparesis caused by an acquired lesion. In the remaining four patients, who showed mild hemiparesis without such abnormal interlimb coordinations, there were no ipsilateral MEPs. Thus, we suggest that TMS is useful for confirming the electrophysiological findings relevant to functional recovery in hemiplegic cerebral palsy underlying such abnormal interlimb coordinations. Specifically, bilateral MEPs of similar latency were considered consistent with compensatory mirror movements originating from bilateral motor representation in the unaffected motor cortex.

Adolescent↗

Bimanual coordination between isometric contractions and rhythmic movements: an asymmetric coupling.

Interactions between rhythmically moving limbs typically result in attraction to a limited number of coordination modes, which are distinguished in terms of their stability. In addition, the stability of coordination typically decreases with elevations in movement frequency. To gain more insight into the neurophysiological mechanisms underlying these stability characteristics, the effects of phasic voluntary muscle activation onto the movement pattern of the contralateral limb as well as onto the stability of interlimb coordination were examined. This was done in circumstances in which a minimal degree of movement-elicited afferent information was available to mediate the coupling influences. The task involved rhythmic application of isometric torque by one hand, while the other hand was moving rhythmically with unconstrained amplitude. The effects of two levels of applied torque, two coordination patterns (inphase and antiphase), and two movement frequencies were determined, both at the behavioural level (movement kinematics and kinetics) and the neuromuscular level (EMG). The isometric applications of torque clearly influenced the muscle-activation profile and movement pattern of the other limb, affecting both temporal variability and amplitude. Surprisingly, there were no differences between the two coordination patterns or between the tempo conditions. As such, the results did not conform to the Haken-Kelso-Bunz model for rhythmic movement coordination. These data suggest that the archetypal differences in stability of rhythmic bimanual coordination are contingent upon a correspondence between the limbs in terms of their respective tasks. This interpretation is elaborated in terms of the role of sensory feedback and the functional specificity of motor unit recruitment in rhythmic interlimb coordination.

Adult↗

Walking of cats on a grid: performance of locomotor task in spinal intact and hemisected cats.

We have investigated interlimb coordination during walking by observing locomotion of cats on a grid. Control cats made no error in forelimb placement on the grid, and landed their hindlimbs on the rung where each ipsilateral forelimb left moments earlier. This suggests that locomotor command signals were modified by grid information including its size and direction and affected the pattern generators of both forelimbs and hindlimbs. Hemisected cats, made both at high cervical and lower thoracic, showed deteriorated placement of the hindlimbs suggesting that interlimb coordination is carried out mainly by descending pathways from the brainstem such as ventrolateral fasciculus and dorsolateral fasciculus. Interlimb reflex pathways may play a limited role.

Animals↗

Interaction between central programs and afferent input in the control of posture and locomotion.

Two basic aspects of the neuronal control of bipedal stance and gait have been discussed, namely the interlimb coordination and the antigravity function of leg extensors. During stance and gait both legs act in a cooperative manner as each limb affects the strength of muscle activation and the time-space behaviour of the other. There are indications that interlimb coordination is mediated by spinal interneuronal circuits, which are themselves under supraspinal (e.g. cerebral and cerebellar) control. Proprioceptive reflexes involved in the maintenance of body equilibrium depend on the presence of contract forces opposing gravity. Extensor load receptors are thought to signal changes of the projection of body's centre of mass with respect to the feet. According to recent observations in the spinal cat, this afferent input probably arises from Golgi tendon organs and represents a newly discovered function of these receptors in the regulation of stance and gait.

Adaptation, Physiological↗

Ankle restraint modifies motility at E12 in chick embryos.

The chick's relationship to its environment changes dramatically over 21 days of embryonic development. At early ages embryos are buoyant; their posture and movements are relatively unconstrained. As embryos grow and fluid level in ovo decreases, movements are increasingly constrained by gravitational forces and reactive forces due to body contact with the shell wall. The issue of how age-related changes in the constraints on movement in ovo may affect embryonic motility is addressed in this paper. Our long-term goal is to determine whether experience imposed by these conditions contributes to development of posthatching motor behaviors. Because previous work indicated that parameters of motility can be modified by a reduction in buoyancy at embryonic day (E) 9, we sought to determine whether a restraint localized to a single joint could also alter either the episodic distribution of activity or the spatiotemporal patterns of limb movement at either E9 or E12. Thus a restraint was applied to the right ankle of embryos prepared for kinematic recordings. Video and kinematic analyses indicated that the restraint had minimal effect at E9, but significantly modified several motility parameters in both the wing and leg at E12. Ankle restraint decreased episode duration. Restraint also decreased most joint excursion parameters, including excursion range, cycles per sequence, and excursion velocity. Restraint increased cycle period duration and signal frequency content under 1.0 Hz. Parameters of intralimb and interlimb coordination exhibited small mixed effects. Results provide support for the hypothesis that environmental conditions contribute to features of embryonic motility. Further, significant modifications of wing excursions in ankle restrained embryos suggest that sensory feedback arising from mechanical perturbations of leg movements may entrain rostral spinal circuits for preservation of interlimb coordination at E12. Potential mechanisms and implications are discussed.

Animals↗