Axial-Appendicular Dynamics and the Integration of Breathing and Gait in Mammal

SYNOPSIS. This paper proposes a biomechanical model for locomotor-respiratorycoupling (LRC) in galloping mammals in which gait and breathingcycles are phase-locked on a 1:1 basis. It also explores someof the physiological and neuromotor implications of LRC. The mechanical coupling of locomotor and respiratory cyclesdepends upon the coordinated, reciprocal oscillations of thecranio-cervical and lumbo-pelvic components of the axial systemand their attendant actions on the intervening thorax via muscularlinkages. Concurrently, accelerational and decelerational forcesimparted to the axial system by the limbs help to drive lungventilation by inducing inertial displacements of a "visceralpiston’ connected to the diaphragm. Several lines of evidence(including cineradiographic data) suggest that an importantfunction of the crural diaphragm is to control the displacementof the visceral piston. The kinematics of LRC indicate thatthe interosseous intercostal muscles must simultaneously operateto assure thoracic stability against locomotor stresses as wellas to promote breathing. The former may be their more essentialrole, however. The characteristic design of the rib cage incursorial mammals (=deep and narrow) appears to maximize theleverage of certain "accessory respiratory muscles" (i.e., sternocleidomastoid,scalenes) while minimizing torsional loading of the thorax duringforelimb support. Physiological implications of LRC include the prediction thatlarge mammals will breathe relatively faster and with relativelysmaller lung volumes when galloping than small species. An additionalprediction, that running mammals could automatically gear lungventilation to speed by simply linking breathing rate to stridefrequency and depth of breath (=tidal volume) to stride length,appears to be supported by experimental data from horses. Finally,the neuromotor basis of LRC probably depends upon the directinteraction of central pattern generators for locomotion andrespiration. This interaction might be modulated, however, byafferent input from thoracic mechanoreceptors, particularlythe intercostal stretch receptors.     

Exercise-induced respiratory muscle fatigue: implications for performance.

It is commonly held that the respiratory system has ample capacity relative to the demand for maximal O(2) and CO(2) transport in healthy humans exercising near sea level. However, this situation may not apply during heavy-intensity, sustained exercise where exercise may encroach on the capacity of the respiratory system. Nerve stimulation techniques have provided objective evidence that the diaphragm and abdominal muscles are susceptible to fatigue with heavy, sustained exercise. The fatigue appears to be due to elevated levels of respiratory muscle work combined with an increased competition for blood flow with limb locomotor muscles. When respiratory muscles are prefatigued using voluntary respiratory maneuvers, time to exhaustion during subsequent exercise is decreased. Partially unloading the respiratory muscles during heavy exercise using low-density gas mixtures or mechanical ventilation can prevent exercise-induced diaphragm fatigue and increase exercise time to exhaustion. Collectively, these findings suggest that respiratory muscle fatigue may be involved in limiting exercise tolerance or that other factors, including alterations in the sensation of dyspnea or mechanical load, may be important. The major consequence of respiratory muscle fatigue is an increased sympathetic vasoconstrictor outflow to working skeletal muscle through a respiratory muscle metaboreflex, thereby reducing limb blood flow and increasing the severity of exercise-induced locomotor muscle fatigue. An increase in limb locomotor muscle fatigue may play a pivotal role in determining exercise tolerance through a direct effect on muscle force output and a feedback effect on effort perception, causing reduced motor output to the working limb muscles.     

The coupled evolution of breathing and locomotion as a game of leapfrog

Because the increase in metabolic rate related to locomotor activity places demands on the cardiorespiratory apparatus, it is not surprising that the evolution of breathing and of locomotion are coupled. As the respiratory faculty becomes more refined, increasingly aerobic life strategies can be explored, and this activity is in turn expedited by a higher-performance respiratory apparatus. This apparent leapfrogging of respiratory and locomotor faculties begins in noncraniate chordates and continues in water-breathing and air-breathing vertebrates. Because both locomotor and cardiorespiratory activities are coordinated in the brain, neurological as well as biochemical coupling is evident. In spite of very different breathing mechanisms in various vertebrate groups, the basic respiratory control mechanisms appear to have been conserved, and respiratory-locomotor coupling is evident in all classes of vertebrates. Hypaxial body wall muscles that were strictly locomotor in fish have respiratory function in amniotes, but some locomotor function remains in all groups.     

Mechanical signatures of transducer gating in the Drosophila ear

Hearing relies on dedicated mechanotransducer channels that convert sound-induced vibrations into electrical signals [1]. Linking this transduction to identified proteins has proven difficult because of the scarcity of native auditory transducers and their tight functional integration into ears [2-4]. We describe an in vivo paradigm for the noninvasive study of auditory transduction. By investigating displacement responses of the Drosophila sound receiver, we identify mechanical signatures that are consistent with a direct mechanotransducer gating in the fly's ear. These signatures include a nonlinear compliance that correlates with electrical nerve responses, shifts with adaptation, and conforms to the gating-spring model of vertebrate auditory transduction. Analyzing this gating compliance in terms of the gating-spring model reveals striking parallels between the transducer mechanisms for hearing in vertebrates and flies. Our findings provide first insights into the mechanical workings of invertebrate mechanotransducer channels and set the stage for using Drosophila to specifically search for, and probe the roles of, auditory transducer components.     

Active auditory mechanics in mosquitoes

In humans and other vertebrates, hearing is improved by active contractile properties of hair cells. Comparable active auditory mechanics is now demonstrated in insects. In mosquitoes, Johnston's organ transduces sound-induced vibrations of the antennal flagellum. A non-muscular 'motor' activity enhances the sensitivity and tuning of the flagellar mechanical response in physiologically intact animals. This motor is capable of driving the flagellum autonomously, amplifying sound-induced vibrations at specific frequencies and intensities. Motor-related electrical activity of Johnston's organ strongly suggests that mosquito hearing is improved by mechanoreceptor motility.     

Time Delay and Long-Range Connection Induced Synchronization Transitions in Newman-Watts Small-World Neuronal Networks

The synchronization transitions in Newman-Watts small-world neuronal networks (SWNNs) induced by time delay and long-range connection (LRC) probability have been investigated by synchronization parameter and space-time plots. Four distinct parameter regions, that is, asynchronous region, transition region, synchronous region, and oscillatory region have been discovered at certain LRC probability as time delay is increased. Interestingly, desynchronization is observed in oscillatory region. More importantly, we consider the spatiotemporal patterns obtained in delayed Newman-Watts SWNNs are the competition results between long-range drivings (LRDs) and neighboring interactions. In addition, for moderate time delay, the synchronization of neuronal network can be enhanced remarkably by increasing LRC probability. Furthermore, lag synchronization has been found between weak synchronization and complete synchronization as LRC probability is a little less than 1.0. Finally, the two necessary conditions, moderate time delay and large numbers of LRCs, are exposed explicitly for synchronization in delayed Newman-Watts SWNNs.     

Locomotor muscle fatigue increases cardiorespiratory responses and reduces performance during intense cycling exercise independently from metabolic stress

Locomotor muscle fatigue, defined as an exercise-induced reduction in maximal voluntary force, occurs during prolonged exercise, but its effects on cardiorespiratory responses and exercise performance are unknown. In this investigation, a significant reduction in locomotor muscle force (-18%, P < 0.05) was isolated from the metabolic stress usually associated with fatiguing exercise using a 100-drop-jumps protocol consisting of one jump every 20 s from a 40-cm-high platform. The effect of this treatment on time to exhaustion during high-intensity constant-power cycling was measured in study 1 (n = 10). In study 2 (n = 14), test duration (871 +/- 280 s) was matched between fatigue and control condition (rest). In study 1, locomotor muscle fatigue caused a significant curtailment in time to exhaustion (636 +/- 278 s) compared with control (750 +/- 281 s) (P = 0.003) and increased cardiac output. Breathing frequency was significantly higher in the fatigue condition in both studies despite similar oxygen consumption and blood lactate accumulation. In study 2, high-intensity cycling did not induce further fatigue to eccentrically-fatigued locomotor muscles. In both studies, there was a significant increase in heart rate in the fatigue condition, and perceived exertion was significantly increased in study 2 compared with control. These results suggest that locomotor muscle fatigue has a significant influence on cardiorespiratory responses and exercise performance during high-intensity cycling independently from metabolic stress. These effects seem to be mediated by the increased central motor command and perception of effort required to exercise with weaker locomotor muscles.     

Identification of in vitro HSC fate regulators by differential lipid raft clustering

Most hematopoietic stem cells (HSC) in the bone marrow reside in a quiescent state and occasionally enter the cell cycle upon cytokine-induced activation. Although the mechanisms regulating HSC quiescence and activation remain poorly defined, recent studies have revealed a role of lipid raft clustering (LRC) in HSC activation. Here, we tested the hypothesis that changes in lipid raft distribution could serve as an indicator of the quiescent and activated state of HSCs in response to putative niche signals. A semi-automated image analysis tool was developed to map the presence or absence of lipid raft clusters in live HSCs cultured for just one hour in serum-free medium supplemented with stem cell factor (SCF). By screening the ability of 19 protein candidates to alter lipid raft dynamics, we identified six factors that induced either a marked decrease (Wnt5a, Wnt3a and Osteopontin) or increase (IL3, IL6 and VEGF) in LRC. Cell cycle kinetics of single HSCs exposed to these factors revealed a correlation of LRC dynamics and proliferation kinetics: factors that decreased LRC slowed down cell cycle kinetics, while factors that increased LRC led to faster and more synchronous cycling. The possibility of identifying, by LRC analysis at very early time points, whether a stem cell is activated and possibly committed upon exposure to a signaling cue of interest could open up new avenues for large-scale screening efforts.     

Motor cortex excitability does not increase during sustained cycling exercise to volitional exhaustion

The excitability of the motor cortex increases as fatigue develops during sustained single-joint contractions, but there are no previous reports on how corticospinal excitability is affected by sustained locomotor exercise. Here we addressed this issue by measuring spinal and cortical excitability changes during sustained cycling exercise. Vastus lateralis (VL) and rectus femoris (RF) muscle responses to transcranial magnetic stimulation of the motor cortex (motor evoked potentials, MEPs) and electrical stimulation of the descending tracts (cervicomedullary evoked potentials, CMEPs) were recorded every 3 min from nine subjects during 30 min of cycling at 75% of maximum workload (W(max)), and every minute during subsequent exercise at 105% of W(max) until subjective task failure. Responses were also measured during nonfatiguing control bouts at 80% and 110% of W(max) prior to sustained exercise. There were no significant changes in MEPs or CMEPs (P > 0.05) during the sustained cycling exercise. These results suggest that, in contrast to sustained single-joint contractions, sustained cycling exercise does not increase the excitability of motor cortical neurons. The contrasting corticospinal responses to the two modes of exercise may be due to differences in their associated systemic physiological consequences.     

Decreased exercise blood lactate concentrations after respiratory endurance training in humans

For many years, it was believed that ventilation does not limit performance in healthy humans. Recently, however, it has been shown that inspiratory muscles can become fatigued during intense endurance exercise and decrease their exercise performance. Therefore, it is not surprising that respiratory endurance training can prolong intense constant-intensity cycling exercise. To investigate the effects of respiratory endurance training on blood lactate concentration and oxygen consumption (VO2) during exercise and their relationship to performance, 20 healthy, active subjects underwent 30 min of voluntary, isocapnic hyperpnoea 5 days a week, for 4 weeks. Respiratory endurance tests, as well as incremental and constant-intensity exercise tests on a cycle ergometer, were performed before and after the 4-week period. Respiratory endurance increased from 4.6 (SD 2.5) to 29.1 (SD 4.0) min (P < 0.001) and cycling endurance time was prolonged from 20.9 (SD 5.5) to 26.6 (SD 11.8) min (P < 0.01) after respiratory training. The VO2 did not change at any exercise intensity whereas blood lactate concentration was lower at the end of the incremental [10.4 (SD 2.1) vs 8.8 (SD 1.9) mmol x l(-1), P < 0.001] as well as at the end of the endurance exercise [10.4 (SD 3.6) vs 9.6 (SD 2.7) mmol x l(-1), P < 0.01] test after respiratory training. We speculate that the reduction in blood lactate concentration was most likely caused by an improved lactate uptake by the trained respiratory muscles. However, reduced exercise blood lactate concentrations per se are unlikely to explain the improved cycling performance after respiratory endurance training.     

Grey matter volume in early human visual cortex predicts proneness to the sound-induced flash illusion

Visual perception can be modulated by sounds. A drastic example of this is the sound-induced flash illusion: when a single flash is accompanied by two bleeps, it is sometimes perceived in an illusory fashion as two consecutive flashes. However, there are strong individual differences in proneness to this illusion. Some participants experience the illusion on almost every trial, whereas others almost never do. We investigated whether such individual differences in proneness to the sound-induced flash illusion were reflected in structural differences in brain regions whose activity is modulated by the illusion. We found that individual differences in proneness to the illusion were strongly and significantly correlated with local grey matter volume in early retinotopic visual cortex. Participants with smaller early visual cortices were more prone to the illusion. We propose that strength of auditory influences on visual perception is determined by individual differences in recurrent connections, cross-modal attention and/or optimal weighting of sensory channels.     

Legged insects select the optimal locomotor pattern based on the energetic cost

 The gait transition in legged animals has attracted many researchers, and its relation to metabolic cost and mechanical work has been discussed in recent decades. We assumed that the energetic cost during locomotion is given by the sum of positive mechanical work and the heat energy loss that is proportional to the square of joint torque and examined the optimal locomotor pattern based on the energetic cost in a simple dynamical model of a hexapod by computer simulations. The obtained results well agree with characteristics in the locomotor patterns in legged animals; for example, the leg protraction time, step length, and the metabolic cost of transport are almost constant for many velocities, the leg cycling period decreases with velocity, and the energetic cost of locomotion induced by carrying loads linearly increases with mass loaded. This correspondence of the results of calculation to experimental results suggest that the heat energy loss for torque generation is proportional to the square of the torque during locomotion, and that the locomotor pattern in legged animals is highly optimized based on the energetic cost. Received: 22 December 1998 / Accepted: 14 April 2000     

Auditory deprivation modifies biological rhythms in the golden hamster

To assess to what extent auditory sensory deprivation affects biological rhythmicity, sleep/wakefulness cycle and 24 h rhythm in locomotor activity were examined in golden hamsters after bilateral cochlear lesion. An increase in total sleep time as well as a decrease in wakefulness (W) were associated to an augmented number of W episodes, as well as of slow wave sleep (SWS) and paradoxical sleep (PS) episodes in deaf hamsters. The number of episodes of the three behavioural states and the percent duration of W and SWS increased significantly during the light phase of daily photoperiod only. Lower amplitudes of locomotor activity rhythm and a different phase angle as far as light off were found in deaf hamsters kept either under light-dark photoperiod or in constant darkness. Period of locomotor activity remained unchanged after cochlear lesions. The results indicate that auditory deprivation disturbs photic synchronization of rhythms with little effect on the clock timing mechanism itself.     

Local Pain Dynamics during Constant Exhaustive Exercise

The purpose of this study was to delineate the topological dynamics of pain and discomfort during constant exercise performed until volitional exhaustion. Eleven physical education students were tested while cycling and running at a “hard” intensity level (e.g., corresponding to Borg’s RPE (6–20) = 15). During the tests, participants reported their discomfort and pain on a body map every 15s. “Time on task” for each participant was divided into five equal non-overlapping temporal windows within which their ratings were considered for analysis. The analyses revealed that the number of body locations with perceived pain and discomfort increased throughout the five temporal windows until reaching the mean (± SE) values of 4.2 ± 0.7 and 4.1 ± 0.6 in cycling and running, respectively. The dominant locations included the quadriceps and hamstrings during cycling and quadriceps and chest during running. In conclusion, pain seemed to spread throughout the body during constant cycling and running performed up to volitional exhaustion with differences between cycling and running in the upper body but not in the lower body dynamics.     

Impact Loading and Locomotor-Respiratory Coordination Significantly Influence Breathing Dynamics in Running Humans

Locomotor-respiratory coupling (LRC), phase-locking between breathing and stepping rhythms, occurs in many vertebrates. When quadrupedal mammals gallop, 1∶1 stride per breath coupling is necessitated by pronounced mechanical interactions between locomotion and ventilation. Humans show more flexibility in breathing patterns during locomotion, using LRC ratios of 2∶1, 2.5∶1, 3∶1, or 4∶1 and sometimes no coupling. Previous studies provide conflicting evidence on the mechanical significance of LRC in running humans. Some studies suggest LRC improves breathing efficiency, but others suggest LRC is mechanically insignificant because ‘step-driven flows’ (ventilatory flows attributable to step-induced forces) contribute a negligible fraction of tidal volume. Yet, although step-driven flows are brief, they cause large fluctuations in ventilatory flow. Here we test the hypothesis that running humans use LRC to minimize antagonistic effects of step-driven flows on breathing. We measured locomotor-ventilatory dynamics in 14 subjects running at a self-selected speed (2.6±0.1 ms⁻¹) and compared breathing dynamics in their naturally ‘preferred’ and ‘avoided’ entrainment patterns. Step-driven flows occurred at 1-2X step frequency with peak magnitudes of 0.97±0.45 Ls⁻¹ (mean ±S.D). Step-driven flows varied depending on ventilatory state (high versus low lung volume), suggesting state-dependent changes in compliance and damping of thoraco-abdominal tissues. Subjects naturally preferred LRC patterns that minimized antagonistic interactions and aligned ventilatory transitions with assistive phases of the step. Ventilatory transitions initiated in ‘preferred’ phases within the step cycle occurred 2x faster than those in ‘avoided’ phases. We hypothesize that humans coordinate breathing and locomotion to minimize antagonistic loading of respiratory muscles, reduce work of breathing and minimize rate of fatigue. Future work could address the potential consequences of locomotor-ventilatory interactions for elite endurance athletes and individuals who are overweight or obese, populations in which respiratory muscle fatigue can be limiting.     

Oxygen uptake/heart rate relationship in leg and arm exercise, sitting and standing.

The effect of leg exercise and of arm exercise in sitting and standing body positions on energy output and on some cardiorespiratory parameters was studied in seven male subjects. Oxygen uptake (VO2), heart rate (fH), pulmonary ventilation (VE) and respiratory frequency were measured at rest, in the 7-8th min of submaximal work (300, 600, 900 kpm/min), and at maximal effort. Significantly higher Vo2, fH, and VE in arm cranking than in cycling were found at submaximal work loads above 300 kpm/min. Though the maximal work load in arm exercise was 50-60% of that in cycling, Vo2 in arm work was at maximal effort only 22% lower than in leg exercise while the difference in fH was insignificant. No differences were found in arm work between the results obtained at any work level in sitting and standing body positions. The only postural difference in arm work was a 13% higher work load achieved at maximal effort when standing than when sitting. Differences in fH between arm and leg exercise were much smaller for the same Vo2 than for the same work load and were time dependent. While fH quickly leveled off in leg exercise, fH in arm cranking rose steadily during the first 6 min of work which created the fH differences observed in the 7-8 min of submaximal arm arm and leg exercise. At submaximal work levels a tendency to synchronize the respiratory frequency with the frequency of the rotatory movements was more apparent in arm cranking than in cycling.     

Foot forces during exercise on the International Space Station

Long-duration exposure to microgravity has been shown to have detrimental effects on the human musculoskeletal system. To date, exercise countermeasures have been the primary approach to maintain bone and muscle mass and they have not been successful. Up until 2008, the three exercise countermeasure devices available on the International Space Station (ISS) were the treadmill with vibration isolation and stabilization (TVIS), the cycle ergometer with vibration isolation and stabilization (CEVIS), and the interim resistance exercise device (iRED). This article examines the available envelope of mechanical loads to the lower extremity that these exercise devices can generate based on direct in-shoe force measurements performed on the ISS. Four male crewmembers who flew on long-duration ISS missions participated in this study. In-shoe forces were recorded during activities designed to elicit maximum loads from the various exercise devices. Data from typical exercise sessions on Earth and on-orbit were also available for comparison. Maximum on-orbit single-leg loads from TVIS were 1.77 body weight (BW) while running at 8 mph. The largest single-leg forces during resistance exercise were 0.72 BW during single-leg heel raises and 0.68 BW during double-leg squats. Forces during CEVIS exercise were small, approaching only 0.19 BW at 210 W and 95 RPM. We conclude that the three exercise devices studied were not able to elicit loads comparable to exercise on Earth, with the exception of CEVIS at its maximal setting. The decrements were, on average, 77% for walking, 75% for running, and 65% for squats when each device was at its maximum setting. Future developments must include an improved harness to apply higher gravity replacement loads during locomotor exercise and the provision of greater resistance exercise capability. The present data set provides a benchmark that will enable future researchers to judge whether or not the new generation of exercise countermeasures recently added to the ISS will address the need for greater loading.     

The effects of rhythmic sensory cues on the temporal dynamics of human gait

Walking is a complex, rhythmic task performed by the locomotor system. However, natural gait rhythms can be influenced by metronomic auditory stimuli, a phenomenon of particular interest in neurological rehabilitation. In this paper, we examined the effects of aural, visual and tactile rhythmic cues on the temporal dynamics associated with human gait. Data were collected from fifteen healthy adults in two sessions. Each session consisted of five 15-minute trials. In the first trial of each session, participants walked at their preferred walking speed. In subsequent trials, participants were asked to walk to a metronomic beat, provided through visually, aurally, tactile or all three cues (simultaneously and in sync), the pace of which was set to the preferred walking speed of the first trial. Using the collected data, we extracted several parameters including: gait speed, mean stride interval, stride interval variability, scaling exponent and maximum Lyapunov exponent. The extracted parameters showed that rhythmic sensory cues affect the temporal dynamics of human gait. The auditory rhythmic cue had the greatest influence on the gait parameters, while the visual cue had no statistically significant effect on the scaling exponent. These results demonstrate that visual rhythmic cues could be considered as an alternative cueing modality in rehabilitation without concern of adversely altering the statistical persistence of walking.     

Spontaneous Group Synchronization of Movements and Respiratory Rhythms

We tested whether pre-assigned arm movements performed in a group setting spontaneously synchronized and whether synchronization extended to heart and respiratory rhythms. We monitored arm movements, respiration and electrocardiogram at rest and during spontaneous, music and metronome-associated arm-swinging. No directions were given on whether or how the arm swinging were to be synchronized between participants or with the external cues. Synchronization within 3 groups of 10 participants studied collectively was compared with pseudo-synchronization of 3 groups of 10 participants that underwent an identical protocol but in an individual setting. Motor synchronization was found to be higher in the collective groups than in the individuals for the metronome-associated condition. On a repetition of the protocol on the following day, motor synchronization in the collective groups extended to the spontaneous, un-cued condition. Breathing was also more synchronized in the collective groups than in the individuals, particularly at rest and in the music-associated condition. Group synchronization occurs without explicit instructions, and involves both movements and respiratory control rhythms.     

Aging,Spatial Disparity,and the Sound-Induced Flash Illusion

The present study examined age-related differences in multisensory integration and the effect of spatial disparity on the sound-induced flash illusion—-an illusion used in previous research to assess age-related differences in multisensory integration. Prior to participation in the study, both younger and older participants demonstrated their ability to detect 1–2 visual flashes and 1–2 auditory beep presented unimodally. After passing the pre-test, participants were then presented 1–2 flashes paired with 0–2 beeps that originated from one of five speakers positioned equidistantly 100cm from the participant. One speaker was positioned directly below the screen, two speakers were positioned 50cm to the left and right from the center of the screen, and two more speakers positioned to the left and right 100cm from the center of the screen. Participants were told to report the number of flashes presented and to ignore the beeps. Both age groups showed a significant effect of the beeps on the perceived number of flashes. However, neither younger nor older individuals showed any significant effect of spatial disparity on the sound-induced flash illusion. The presence of a congruent number of beeps increased accuracy for both older and younger individuals. Reaction time data was also analyzed. As expected, older individuals showed significantly longer reaction times when compared to younger individuals. In addition, both older and younger individuals showed a significant increase in reaction time for fusion trials, where two flashes and one beep are perceived as a single flash, as compared to congruent single flash trials. This increase in reaction time was not found for fission trials, where one flash and two beeps were perceived as two flashes. This suggests that processing may differ for the two forms for fission as compared to fusion illusions.