Muscle activity and kinematics show different responses to recurrent laryngeal nerve lesion in mammal swallowing.

Understanding the interactions between neural and musculoskeletal systems is key to identifying mechanisms of functional failure. Mammalian swallowing is a complex, poorly understood motor process. Lesion of the recurrent laryngeal nerve, a sensory and motor nerve of the upper airway, results in airway protection failure (liquid entry into the airway) during swallowing through an unknown mechanism. We examined how muscle and kinematic changes after recurrent laryngeal nerve lesion relate to airway protection in eight infant pigs. We tested two hypotheses: 1) kinematics and muscle function will both change in response to lesion in swallows with and without airway protection failure, and 2) differences in both kinematics and muscle function will predict whether airway protection failure occurs in lesion and intact pigs. We recorded swallowing with high-speed videofluoroscopy and simultaneous electromyography of oropharyngeal muscles pre- and postrecurrent laryngeal nerve lesion. Lesion changed the relationship between airway protection and timing of tongue and hyoid movements. Changes in onset and duration of hyolaryngeal muscles postlesion were less associated with airway protection outcomes. The tongue and hyoid kinematics all predicted airway protection outcomes differently pre- and postlesion. Onset and duration of activity in only one infrahyoid and one suprahyoid muscle showed a change in predictive relationship pre- and postlesion. Kinematics of the tongue and hyoid more directly reflect changes in airway protections pre- and postlesion than muscle activation patterns. Identifying mechanisms of airway protection failure requires specific functional hypotheses that link neural motor outputs to muscle activation to specific movements.NEW & NOTEWORTHY Kinematic and muscle activity patterns of oropharyngeal structures used in swallowing show different patterns of response to lesion of the recurrent laryngeal nerve. Understanding how muscles act on structures to produce behavior is necessary to understand neural control.

Effects of Superior Laryngeal Nerve Lesion on Kinematics of Swallowing and Airway Protection in an Infant Pig Model.

The superior laryngeal nerve provides detailed sensory information from the mucosal surfaces of laryngeal structures superior to the vocal folds, including the valleculae. Injury to this nerve results in airway penetration and aspiration. Furthermore, such injuries might have an impact on the function of multiple structures involved in intraoral transport and swallowing due to connections within the brainstem. We sought to determine the effects of a surgical lesion of the superior laryngeal nerve on kinematics of the tongue, hyoid, and epiglottis during swallowing. We implanted radio-opaque markers into five infant pigs under anesthesia. Then we fed milk mixed with contrast agent to the pigs while they were recorded via video fluoroscopy, before and after a surgery to transect the superior laryngeal nerve. We digitized and rated airway protection in 177 swallows. We found that in most animals, swallow duration was shorter after nerve lesion. The hyoid also traveled a shorter distance after lesion. Frequently, individuals reacted differently to the same nerve lesion. We suggest that these differences are due to individual differences in neurological connections. When comparing hyoid kinematics between swallows with successful or failed airway protection, we found more consistency among individuals. This indicates that protecting the airway requires specific sets of kinematic events to occur, regardless of the neurological differences among individuals.

Specific Vagus Nerve Lesion Have Distinctive Physiologic Mechanisms of Dysphagia.

Swallowing is complex at anatomical, functional, and neurological levels. The connections among these levels are poorly understood, yet they underpin mechanisms of swallowing pathology. The complexity of swallowing physiology means that multiple failure points may exist that lead to the same clinical diagnosis (e.g., aspiration). The superior laryngeal nerve (SLN) and the recurrent laryngeal nerve (RLN) are branches of the vagus that innervate different structures involved in swallowing. Although they have distinct sensory fields, lesion of either nerve is associated clinically with increased aspiration. We tested the hypothesis that despite increased aspiration in both case, oropharyngeal kinematic changes and their relationship to aspiration would be different in RLN and SLN lesioned infant pigs. We compared movements of the tongue and epiglottis in swallows before and after either RLN or SLN lesion. We rated swallows for airway protection. Posterior tongue ratio of safe swallows changed in RLN (p = 0.01) but not SLN lesioned animals. Unsafe swallows post lesion had different posterior tongue ratios in RLN and SLN lesioned animals. Duration of epiglottal inversion shortened after lesion in SLN animals (p = 0.02) but remained unchanged in RLN animals. Thus, although SLN and RLN lesion lead to the same clinical outcome (increased aspiration), the mechanisms of failure of airway protection are different, which suggests that effective therapies may be different with each injury. Understanding the specific pathophysiology of swallowing associated with specific neural insults will help develop targeted, disease appropriate treatments.

Central nervous system integration of sensorimotor signals in oral and pharyngeal structures: oropharyngeal kinematics response to recurrent laryngeal nerve lesion.

Safe, efficient liquid feeding in infant mammals requires the central coordination of oropharyngeal structures innervated by multiple cranial and spinal nerves. The importance of laryngeal sensation and central sensorimotor integration in this system is poorly understood. Recurrent laryngeal nerve lesion (RLN) results in increased aspiration, though the mechanism for this is unclear. This study aimed to determine the effect of unilateral RLN lesion on the motor coordination of infant liquid feeding. We hypothesized that 1) RLN lesion results in modified swallow kinematics, 2) postlesion oropharyngeal kinematics of unsafe swallows differ from those of safe swallows, and 3) nonswallowing phases of the feeding cycle show changed kinematics postlesion. We implanted radio opaque markers in infant pigs and filmed them pre- and postlesion with high-speed videofluoroscopy. Markers locations were digitized, and swallows were assessed for airway protection. RLN lesion resulted in modified kinematics of the tongue relative to the epiglottis in safe swallows. In lesioned animals, safe swallow kinematics differed from unsafe swallows. Unsafe swallow postlesion kinematics resembled prelesion safe swallows. The movement of the tongue was reduced in oral transport postlesion. Between different regions of the tongue, response to lesion was similar, and relative timing within the tongue was unchanged. RLN lesion has a pervasive effect on infant feeding kinematics, related to the efficiency of airway protection. The timing of tongue and hyolaryngeal kinematics in swallows is a crucial locus for swallow disruption. Laryngeal sensation is essential for the central coordination in feeding of oropharyngeal structures receiving motor inputs from different cranial nerves.

The Physiologic Impact of Unilateral Recurrent Laryngeal Nerve (RLN) Lesion on Infant Oropharyngeal and Esophageal Performance.

Recurrent laryngeal nerve (RLN) injury in neonates, a complication of patent ductus arteriosus corrective surgery, leads to aspiration and swallowing complications. Severity of symptoms and prognosis for recovery are variable. We transected the RLN unilaterally in an infant mammalian animal model to characterize the degree and variability of dysphagia in a controlled experimental setting. We tested the hypotheses that (1) both airway protection and esophageal function would be compromised by lesion, (2) given our design, variability between multiple post-lesion trials would be minimal, and (3) variability among individuals would be minimal. Individuals' swallowing performance was assessed pre- and post-lesion using high speed VFSS. Aspiration was assessed using the Infant Mammalian Penetration-Aspiration Scale (IMPAS). Esophageal function was assessed using two measures devised for this study. Our results indicate that RLN lesion leads to increased frequency of aspiration, and increased esophageal dysfunction, with significant variation in these basic patterns at all levels. On average, aspiration worsened with time post-lesion. Within a single feeding sequence, the distribution of unsafe swallows varied. Individuals changed post-lesion either by increasing average IMPAS score, or by increasing variation in IMPAS score. Unilateral RLN transection resulted in dysphagia with both compromised airway protection and esophageal function. Despite consistent, experimentally controlled injury, significant variation in response to lesion remained. Aspiration following RLN lesion was due to more than unilateral vocal fold paralysis. We suggest that neurological variation underlies this pattern.

Turning the corner in quadrupedal arboreal locomotion: kinetics of changing direction while running in the Siberian chipmunk (Tamias sibiricus).

Arboreal animals frequently change directions during locomotion on tree branches, trunks, or twigs. Linear and rotational impulses required to change direction and rotate the body while running are largely unexplored. We trained Siberian chipmunks (Tamias sibiricus) to run on narrow cylindrical trackways. The first trackway was straight and the second had a 45° bend to the right. A force pole collected substrate reaction forces and torques, and linear and rotational impulses were calculated. When the chipmunks ran and jumped across the bend, they exerted strong impulses to the left, pushing the body to the right. Before the bend the substrate reaction yaw angular impulse rotated the animal to the new heading. After passing over the 45° bend in the trackway, opposing yaw angular impulses were exerted to stop the body's rotation. Rolling angular impulses were mostly similar between straight and turning trials. We conclude that mediolateral forces are more important than craniocaudal forces to change direction in locomotion. Yaw angular impulse is necessary to start and stop the rotation of the body around the center of mass. To avoid rolling during turns, the chipmunks relied on banking rather than exerting rolling torques.

Torque around the center of mass: dynamic stability during quadrupedal arboreal locomotion in the Siberian chipmunk (Tamias sibiricus).

When animals travel on tree branches, avoiding falls is of paramount importance. Animals swiftly running on a narrow branch must rely on movement to create stability rather than on static methods. We examined how Siberian chipmunks (Tamias sibiricus) remain stable while running on a narrow tree branch trackway. We examined the pitch, yaw, and rolling torques around the center of mass, and hypothesized that within a stride, any angular impulse (torque during step time) acting on the center of mass would be canceled out by an equal and opposite angular impulse. Three chipmunks were videotaped while running on a 2cm diameter branch trackway. We digitized the videos to estimate center of mass and center of pressure positions throughout the stride. A short region of the trackway was instrumented to measure components of the substrate reaction force. We found that positive and negative pitch angular impulse was by far the greatest in magnitude. The anterior body was pushed dorsally (upward) when the forelimbs landed simultaneously, and then the body pitched in the opposite direction as both hindlimbs simultaneously made contact. There was no considerable difference between yaw and rolling angular impulses, both of which were small and equal between fore- and hindlimbs. Net angular impulses around all three axes were usually greater than or less than zero (not balanced). We conclude that the chipmunks may balance out the torques acting on the center of mass over the course of two or more strides, rather than one stride as we hypothesized.

The effects of substrate texture on the mechanics of quadrupedal arboreal locomotion in the gray short-tailed opossum (Monodelphis domestica).

Among small mammals, the ability to move on tree trunks, branches, and twigs is nearly ubiquitous. Performance and locomotor mechanics on arboreal substrates may be influenced by variation in the coefficient of friction between the hands/feet of the animal and the surface of the arboreal substrate. To test this, I examined speed, substrate reaction forces, and torque around the long axis of two cylindrical trackways with rough and smooth surfaces in gray short-tailed opossums (Monodelphis domestica). Speed was determined with videography, and forces and torques were measured by an instrumented section of the trackway. The opossums traveled more slowly on the smooth arboreal trackway. There was also significant interaction between limb (forelimbs, hindlimbs) and substrate texture (rough, smooth) in braking, propulsive, and laterally directed impulses. Running on the smooth trackway had the effect of reducing some between-limb (forelimb vs. hindlimb) differences. Stability on the rough trackway was probably maintained by relatively high momentum, but on the smooth trackway, the opossums used static methods (many limbs contacting the substrate, greater muscular effort, lower momentum) to remain stable and avoid toppling. Clearly, momentum and dynamics are often important biomechanical considerations for this generalized mammal. Highly arboreal animals can remain dynamically stable on a wider variety of substrate textures.

Mechanics of generating friction during locomotion on rough and smooth arboreal trackways.

Traveling on arboreal substrates is common among most small mammals living anywhere vegetation grows. Because arboreal supports vary considerably in surface texture, animals must be able to adjust their locomotor biomechanics to remain stable on such supports. I examined how gray short-tailed opossums (Monodelphis domestica), which are generalized marsupials living on or near the ground, adjust to travel on rough and smooth 2 cm-diameter arboreal trackways. Limb contact position was determined via high-speed videography, and substrate reaction force was measured by an instrumented section of each branch trackway. Normal and shear forces were calculated from substrate reaction force and limb contact position around the branch trackways. Normal force is greater in forelimbs, probably because of the forelimb's greater weight support role. Shear force was identical between limb pairs, most likely because of interactions between vertical force, limb placement, mediolateral force, and torque. The opossums adjusted to the smooth trackway mainly by reducing speed, changing footfall patterns and increasing normal force. I predict that arboreal specialists will show less change in performance between rough and smooth arboreal trackways because of their greater ability to grasp or maintain contact with arboreal substrates.

Different parts of erector spinae muscle fatigability in subjects with and without low back pain.

BACKGROUND CONTEXT: There is conflicting evidence regarding erector spinae muscle fatigability because previous studies have not considered the thoracic and lumbar components separately. These muscles have very different mechanical responses and, therefore, would be recruited differentially for the chosen task. PURPOSE: The present study was conducted to compare whether fatigability differences exist in the thoracic and lumbar parts of the erector spinae muscles in subjects with and without low back pain (LBP). STUDY DESIGN: This cross-sectional study was conducted in the Motion Analysis Lab at Cleveland State University. PATIENT SAMPLE: The study sample included 40 subjects with LBP and 40 subjects without LBP. OUTCOME MEASURES: The fatigability of the erector spinae muscles was compared based on median frequency of electromyography (EMG) versus time. The level of pain of each subject was also compared using the Oswestry Disability Index. METHODS: Fatigue measurements were evaluated between groups based on the assessed sides as well as the thoracic and lumbar parts of the erector spinae muscles using surface EMG. A modified version of the isometric fatigue test as introduced by Sorensen was used to test the endurance of the erector spinae muscles. RESULTS: There were significant median EMG frequency (F((1, 78))=28.82, p=.001) differences in the thoracic and lumbar parts of the erector spinae muscles between subjects with and without LBP. The thoracic part had a significantly lower median EMG frequency than the lumbar part in subjects with LBP. The thoracic and lumbar parts of the erector spinae muscles had interactions with group (F((1, 78))=47.88, p=.01] and age (F((1, 78))=16.51, p=.01). CONCLUSIONS: The results of this study suggested that subjects with LBP demonstrated higher fatigability of the erector spinae muscles at the thoracic part than at the lumbar part. The increased fatigability of the thoracic part needs to be emphasized in rehabilitation strategies for subjects with LBP. In addition, as age increased, the median frequency of the lumbar part of the erector spinae muscles significantly decreased. Understanding the anatomical and biomechanical characteristics of the erector spinae muscle may enhance clinical outcomes and rehabilitation strategies for subjects with LBP.

Mechanics of torque generation during quadrupedal arboreal locomotion.

Quadrupedal animals moving on arboreal substrates face unique challenges to maintain stability. The torque generated by the limbs around the long axis of a branch during locomotion may clarify how the animals remain stable on arboreal supports. We sought to determine what strategy gray short-tailed opossums (Monodelphis domestica) use to exert torque and avoid toppling. The opossums moved across a branch trackway about half the diameter of their bodies. Part of the trackway was instrumented to measure substrate reaction forces and torque around the long axis of the branch. Kinematic analysis was used to estimate the center of pressure of the manus and pes; from center of pressure and vertical and mediolateral forces, the torque generated by substrate reaction forces versus muscular effort could be determined. Forelimbs generated significantly greater torque than hindlimbs, which is probably explained by the greater weight-bearing role of the forelimbs. Fore- and hindlimbs generated torque in opposite directions because contralateral fore- and hindlimbs typically contacted the branch. Torque generated by muscular effort, however, was often in the same direction in both fore- and hindlimbs. The muscle-generated torque is likely the result of mediolateral movement of the center of mass caused by mediolateral undulation of the torso. These results bear an important implication for the study of arboreal locomotion: center of mass dynamics are at least as important as static positions. M. domestica is a good representative for a primitive mammal, and comparisons with arboreal specialists will shed light on how proficient arboreal locomotion evolved.

Locomotor kinetics on sloped arboreal and terrestrial substrates in a small quadrupedal mammal.

Small animals must be capable of moving on a wide variety of surfaces; thus, examining the mechanics of locomotion on a wide variety of substrates is necessary to understand how the animal can utilize its habitat. Therefore, locomotor kinetics are examined on arboreal and terrestrial sloped substrates in the marsupial Monodelphis domestica (gray short-tailed opossum). Substrate reaction forces were measured as opossums moved across four trackways: 30 degrees upslope and 30 degrees downslope trackways, which were flat ("terrestrial") or cylindrical ("arboreal"). Regardless of substrate slope, medial limb forces were measured on arboreal trackways and usually lateral limb forces on terrestrial trackways. Otherwise the general patterns of vertical and craniocaudal forces and impulses were similar between same-sloped terrestrial and arboreal trackways. Some significant modifications to these gross patterns occurred: on the arboreal upslope trackway, hindlimbs supported more body weight than on the terrestrial uphill, possibly because hindlimbs were more stably positioned on the upslope arboreal trackway than forelimbs. Furthermore, the difference between fore- and hindlimbs with respect to craniocaudal impulses was less on the arboreal sloped trackways. In conclusion, kinetic patterns can usually be explained by body weight support roles and by the placement of the limbs on the arboreal trackway.

Locomotor kinetics and kinematics on inclines and declines in the gray short-tailed opossum Monodelphis domestica.

Small terrestrial animals continually encounter sloped substrates when moving about their habitat; therefore, it is important to understand the mechanics and kinematics of locomotion on non-horizontal substrates as well as on level terrain. To this end, we trained gray short-tailed opossums (Monodelphis domestica) to move along level, 30 degrees inclined, and 30 degrees declined trackways instrumented with a force platform. Vertical, craniocaudal and mediolateral impulses, peak vertical forces, and required coefficient of friction (mu(req)) of individual limbs were calculated. Two high speed video cameras were used to simultaneously capture whole limb craniocaudal and mediolateral angles at limb touchdown, midstance and lift-off. Patterns on the level terrain were typical for non-primate quadrupeds: the forelimbs supported the majority of the body weight, forelimbs were net braking and hindlimbs net propulsive, and both limb pairs exerted small laterally directed impulses. M. domestica moved more slowly on sloped substrates in comparison to level locomotion, and exhibited a greater mu(req). On inclines, both limb pairs were more protracted at touchdown and more retracted at lift-off, fore- and hindlimbs had equal roles in body weight support, forelimbs exerted greater propulsive impulse than hindlimbs, and mu(req) was greater in the forelimbs than in hindlimbs. On declines, only the forelimbs were more protracted at touchdown; forelimbs supported the great majority of body weight while they generated nearly all of the braking impulse and, despite the disparity in fore- vs hindlimb function on the decline, mu(req) was not significantly different between limbs. These differences on the inclined and declined surfaces most likely result from (1) the location of the opossums' center of mass, which is closer to the forelimbs than to the hindlimbs, and (2) the greater functional range of the forelimbs versus the hindlimbs.

The biodynamics of arboreal locomotion: the effects of substrate diameter on locomotor kinetics in the gray short-tailed opossum (Monodelphis domestica).

Effects of substrate diameter on locomotor biodynamics were studied in the gray short-tailed opossum (Monodelphis domestica). Two horizontal substrates were used: a flat 'terrestrial' trackway with a force platform integrated into the surface and a cylindrical 'arboreal' trackway (20.3 mm diameter) with a force-transducer instrumented region. On both terrestrial and arboreal substrates, fore limbs exhibited higher vertical impulse and peak vertical force than hind limbs. Although vertical limb impulses were lower on the terrestrial substrate than on the arboreal support, this was probably due to speed effects because the opossums refused to move as quickly on the arboreal trackway. Vertical impulse decreased significantly faster with speed on the arboreal substrate because most of these trials were relatively slow, and stance duration decreased with speed more rapidly at these lower speeds. While braking and propulsive roles were more segregated between limbs on the terrestrial trackway, fore limbs were dominant both in braking and in propulsion on the arboreal trackway. Both fore and hind limbs exerted equivalently strong, medially directed limb forces on the arboreal trackway and laterally directed limb forces on the terrestrial trackway. We propose that the modifications in substrate reaction force on the arboreal trackway are due to the differential placement of the limbs about the dorsolateral aspect of the branch. Specifically, the pes typically made contact with the branch lower and more laterally than the manus, which may explain the significantly lower required coefficient of friction in the fore limbs relative to the hind limbs.