Effects of postural changes and vestibular lesions on genioglossal muscle activity in conscious cats.

Previous studies in humans showed that genioglossal muscle activity is higher when individuals are supine than when they are upright, and prior experiments in anesthetized or decerebrate animals suggested that vestibular inputs might participate in triggering these alterations in muscle firing. The present study determined the effects of whole body tilts in the pitch (nose-up) plane on genioglossal activity in a conscious feline model and compared these responses with those generated by roll (ear-down) tilts. We also ascertained the effects of a bilateral vestibular neurectomy on the alterations in genioglossal activity elicited by changes in body position. Both pitch and roll body tilts produced modifications in muscle firing that were dependent on the amplitude of the rotation; however, the relative effects of ear-down and nose-up tilts on genioglossal activity were variable from animal to animal. The response variability observed might reflect the fact that genioglossus has a complex organization and participates in a variety of tongue movements; in each animal, electromyographic recordings presumably sampled the firing of different proportions of fibers in the various compartments and subcompartments of the muscle. Furthermore, removal of labyrinthine inputs resulted in alterations in genioglossal responses to postural changes that persisted until recordings were discontinued approximately 1 mo later, demonstrating that the vestibular system participates in regulating the muscle's activity. Peripheral vestibular lesions were subsequently demonstrated to be complete through the postmortem inspection of temporal bone sections or by observing that vestibular nucleus neurons did not respond to rotations in vertical planes.     

The effect of posture on respiratory activity of the abdominal muscles

The purpose of this study was to determine the influence of posture on the expiratory activity of the abdominal muscles. Fifteen young adult men participated in the study. Activities of the external oblique abdominis, internal oblique abdominis, and rectus abdominis muscles were measured electromyographically in various postures. We used a pressure threshold in order to activate the abdominal muscles as these muscles are silent at rest. A spirometer was used to measure the lung volume in various postures. Subjects were placed in the supine, standing, sitting, and sitting-with-elbow-on-the-knee (SEK) positions. Electromyographic activity and mouth pressure were measured during spontaneous breathing and maximal voluntary ventilation under the respiratory load. We observed that the lung volume changed with posture; however, the breathing pattern under respiratory load did not change. During maximal voluntary ventilation, internal oblique abdominis muscle expiratory activity was lower in the SEK position than in any other position, external oblique abdominis muscle inspiratory activity was lower in the supine position than in any other position, and internal oblique abdominis muscle activity was higher in the standing position than in any other position. During spontaneous breathing, external oblique abdominis muscle activity was higher during expiration and inspiration in the SEK position than in any other position. The internal oblique abdominis muscle activity was higher during both inspiration and expiration in the standing position than in any other position. The rectus abdominis muscle activity did not change with changes in posture during both inspiration and expiration. Increase in the external oblique abdominis activity in the SEK position was due to anatomical muscle arrangement that was consistent with the direction of lower rib movement. On the other hand, increase in the internal oblique abdominis activity in the standing position was due to stretching of the abdominal wall by the viscera. We concluded that differences in activity were due to differences in the anatomy of the abdominal muscles and the influence of gravity.     

Effect of hypercapnia and PEEP on expiratory muscle EMG and shortening

The present study examined the effects of hypercapnia and positive end-expiratory pressure (PEEP) on the electromyographic (EMG) activity and tidal length changes of the expiratory muscles in 12 anesthetized, spontaneously breathing dogs. The integrated EMG activity of both abdominal (external oblique, internal oblique, rectus abdominis, and transverse abdominis) and thoracic (triangularis sterni, internal intercostal) expiratory muscles increased linearly with increasing PCO2 and PEEP. However, with both hypercapnia and PEEP, the percent increase in abdominal muscle electrical activity exceeded that of thoracic expiratory muscle activity. Both hypercapnia and PEEP increased the tidal shortening of the external oblique and rectus abdominis muscles. Changes in tidal length correlated closely with simultaneous increases in muscle electrical activity. However, during both hypercapnia and PEEP, length changes of the external oblique were significantly greater than those of the rectus abdominis. We conclude that both progressive hypercapnia and PEEP increase the electrical activity of all expiratory muscles and augment their tidal shortening but produce quantitatively different responses in the several expiratory muscles.     

Abdominal muscle use during breathing in unanesthetized dogs

The pattern of abdominal muscle use during breathing in unanesthetized dogs is unknown. Therefore, we have recorded the electromyograms of the rectus abdominis, external oblique, and transversus abdominis in eight conscious animals breathing quietly in the sitting, standing, and prone postures. During quiet breathing in the sitting posture, all animals invariably had a large amount of phasic expiratory activity in the transversus abdominis. In contrast, only four animals showed some expiratory activity in the external oblique, and only one animal had expiratory activity in the rectus abdominis. A similar pattern was observed when the animals were standing or lying prone, although the amount of expiratory activity was less in this posture. Bilateral cervical vagotomy in four animals did not affect the degree of transversus abdominis expiratory activation or the influence of posture. We conclude that in conscious dogs 1) the abdominal muscles play an important role during breathing and make spontaneous quiet expiration a very active process, 2) the transversus abdominis is the primary respiratory muscle of the abdomen, and 3) unlike in anesthetized animals, extrapulmonary receptors play a major role in promoting abdominal expiratory contraction.     

Action of abdominal muscles on rib cage in humans

To assess the actions of the rectus abdominis and external oblique muscles on the rib cage in humans, these two muscles were stimulated with surface electrodes in four normal supine subjects at functional residual capacity. Changes in anteroposterior and transverse rib cage diameters and changes in xiphipubic distance were measured with pairs of magnetometers. Stimulation of rectus abdominis produced a marked decrease in the xiphipubic distance and in the anteroposterior diameter, thus making the rib cage more elliptic. In contrast, stimulation of the external oblique caused a decrease in the transverse diameter, making the rib cage more cylindrical. When both muscles were stimulated simultaneously, the resultant rib cage distortion depended on the relative voltage at which each muscle was stimulated. Electromyogram recordings showed that there was no cross contamination or activity of the diaphragm during the muscle stimulations. Transdiaphragmatic pressure increased with the voltage of stimulation, suggesting passive lengthening of the diaphragm. X-ray studies were performed in two subjects and confirmed the main magnetometer findings. These studies thus confirm that the rib cage in humans is more easily distortable than conventionally thought. The abdominal muscles can distort it in either direction depending on which muscles are contracting.     

Influence of pelvis position on the activation of abdominal and hip flexor muscles

A pelvic position has been sought that optimizes abdominal muscle activation while diminishing hip flexor activation. Thus, the objective of the study was to investigate the effect of pelvic position and the Janda sit-up on trunk muscle activation. Sixteen male volunteers underwent electromyographic (EMG) testing of their abdominal and hip flexor muscles during a supine isometric double straight leg lift (DSLL) with the feet held approximately 5 cm above a board. The second exercise (Janda sit-up) was a sit-up action where participants simultaneously contracted the hamstrings and the abdominal musculature while holding an approximately 45 degrees angle at the knee. Root mean square surface electromyography was calculated for the Janda sit-up and DSLL under 3 pelvic positions: anterior, neutral, and posterior pelvic tilt. The selected muscles were the upper and lower rectus abdominis (URA, LRA), external obliques, lower abdominal stabilizers (LAS), rectus femoris, and biceps femoris. The Janda sit-up position demonstrated the highest URA and LRA activation and the lowest rectus femoris activation. The Janda sit-up and the posterior tilt were significantly greater (p < 0.01 and p < 0.05, respectively) than the anterior tilt for the URA and LRA muscles. Activation levels of the URA and LRA in neutral pelvis were significantly (p < 0.01 and p < 0.05, respectively) less than the Janda sit-up position, but not significantly different from the posterior tilt. No significant differences in EMG activity were found for the external obliques or LAS. No rectus femoris differences were found in the 3 pelvis positions. The results of this study indicate that pelvic position had a significant effect on the activation of selected trunk and hip muscles during isometric exercise, and the activation of the biceps femoris during the Janda sit-up reduced the activation of the rectus femoris while producing high levels of activation of the URA and LRA.     

Lumbar and abdominal muscle activity during walking in subjects with chronic low back pain: Support of the “guarding” hypothesis?

It has been hypothesized that changes in trunk muscle activity in chronic low back pain (CLBP) reflect an underlying “guarding” mechanism, which will manifest itself as increased superficial abdominal – and lumbar muscle activity. During a functional task like walking, it may be further provoked at higher walking velocities. The purpose of this cross sectional study was to investigate whether subjects with CLBP show increased co-activation of superficial abdominal – and lumbar muscles during walking on a treadmill, when compared to asymptomatic controls. Sixty-three subjects with CLBP and 33 asymptomatic controls walked on a treadmill at different velocities. Surface electromyography data of the erector spinae, rectus abdominis and obliquus abdominis externus muscles were obtained and averaged per stride. Results show that, compared to asymptomatic controls, subjects with CLBP have increased muscle activity of the erector spinae and rectus abdominis, but not of the obliquus abdominis externus. These differences in trunk muscle activity between groups do not increase with higher walking velocities. In conclusion, the observed increased trunk muscle activity in subjects with CLBP during walking supports the guarding hypothesis.     

Mechanical role of expiratory muscles during breathing in prone anesthetized dogs

The purpose of the present study was to assess the mechanical role of the expiratory muscles during spontaneous breathing in prone animals. The electromyographic (EMG) activity of the triangularis sterni, the rectus abdominis, the external oblique, and the transversus abdominis was studied in 10 dogs light anesthetized with pentobarbital sodium. EMGs were recorded during spontaneous steady-state breathing in supine and prone suspended animals both before and after cervical vagotomy. We also measured the end-expiratory lung volume [functional residual capacity (FRC)] in supine and prone positions to assess the mechanical role of expiratory muscle activation in prone dogs. Spontaneous breathing in the prone posture elicited a significant recruitment of the triangularis sterni, the external oblique, and the transversus abdominis (P less than 0.05). Bilateral cervical vagotomy eliminated the postural activation of the external oblique and the transversus abdominis but not the triangularis sterni. Changes in posture during control and after cervical vagotomy were associated with an increase in FRC. However, changes in FRC, on average, were 132.3 +/- 33.8 (SE) ml larger (P less than 0.01) postvagotomy. We conclude that spontaneous breathing in prone anesthetized dogs is associated with a marked phasic expiratory recruitment of rib cage and abdominal muscles. The present data also indicate that by relaxing at end expiration the expiratory muscles of the abdominal region are directly responsible for generating roughly 40% of the tidal volume.     

Responses of the anterolateral abdominal muscles during cough and expiratory threshold loading in the cat.

The present study was conducted to determine the pattern of activation of the anterolateral abdominal muscles during the cough reflex. Electromyograms (EMGs) of the rectus abdominis, external oblique, internal oblique, transversus abdominis, and parasternal muscles were recorded along with gastric pressure in anesthetized cats. Cough was produced by mechanical stimulation of the lumen of the intrathoracic trachea or larynx. The pattern of EMG activation of these muscles during cough was compared with that during graded expiratory threshold loading (ETL; 1-30 cmH(2)O). ETL elicited differential recruitment of abdominal muscle EMG activity (transversus abdominis > internal oblique > rectus abdominis congruent with external oblique). In contrast, both laryngeal and tracheobronchial cough resulted in simultaneous activation of all four anterolateral abdominal muscles with peak EMG amplitudes 3- to 10-fold greater than those observed during the largest ETL. Gastric pressures during laryngeal and tracheobronchial cough were at least eightfold greater than those produced by the largest ETL. These results suggest that, unlike their behavior during expiratory loading, the anterolateral abdominal muscles act as a unit during cough.     

Consequences of postural changes and removal of vestibular inputs on the movement of air in and out of the lungs of conscious felines.

A variety of experimental approaches in human subjects and animal models established that the vestibular system contributes to regulation of respiration. In cats, the surgical elimination of labyrinthine signals produced changes in the spontaneous activity and posturally related responses of a number of respiratory muscles. However, these effects were complex and sometimes varied between muscle compartments, such that the physiological role of vestibulo-respiratory responses is unclear. The present study determined the functional significance of vestibulo-respiratory influences by examining the consequences of a bilateral labyrinthectomy on breathing rate and the pressure, volume, and flow rate of air exchanged during inspiration and expiration as body orientation with respect to gravity was altered. Data were collected from conscious adult cats acclimated to breathing through a facemask connected to a pneuomotach during 60 degrees head-up pitch and ear-down roll body rotations. Removal of vestibular inputs resulted in a 15% reduction in breathing rate, a 13% decrease in minute ventilation, a 16% decrease in maximal inspiratory airflow rate, and a 14% decrease in the maximal expiratory airflow rate measured when the animals were in the prone position. However, the lesions did not appreciably affect phasic changes in airflow parameters related to alterations in posture. These results suggest that the role of the vestibular system in the control of breathing is to modify baseline respiratory parameters in proportion to the general intensity of ongoing movements, and not to rapidly alter ventilation in accordance with body position.     

Inspiratory and expiratory patterns of the pectoralis major muscle during pulmonary defensive reflexes

Experiments wereconducted to determine the discharge pattern of the pectoralis majormuscle during pulmonary defensive reflexes in anesthetized cats(n = 15). Coughs andexpiration reflexes were elicited by mechanical stimulation of theintrathoracic trachea or larynx. Augmented breaths occurredspontaneously or were evoked by the same mechanical stimuli.Electromyograms (EMGs) were recorded from the diaphragm, rectusabdominis, and pectoralis major muscles. During augmented breaths, thepectoralis major had inspiratory EMG activity similar to that of thediaphragm, but during expiration reflexes the pectoralis major also hadpurely expiratory EMG activity similar to the rectus abdominis. Duringtracheobronchial cough, the pectoralis major had an inspiratory patternsimilar to that of the diaphragm in 10 animals, an expiratory patternsimilar to that of the rectus abdominis in 3 animals, and a biphasicpattern in 2 animals. The pectoralis major was active during both the inspiratory and expiratory phases during laryngeal cough. We conclude that, in contrast to the diaphragm or rectus abdominis muscles, thepectoralis major is active during both inspiratory and expiratory pulmonary defensive reflexes.

     

Effects of bilateral vestibular nucleus lesions on cardiovascular regulation in conscious cats.

The vestibular system participates in cardiovascular regulation during postural changes. In prior studies (Holmes MJ, Cotter LA, Arendt HE, Cas SP, and Yates BJ. Brain Res 938: 62-72, 2002, and Jian BJ, Cotter LA, Emanuel BA, Cass SP, and Yates BJ. J Appl Physiol 86: 1552-1560, 1999), transection of the vestibular nerves resulted in instability in blood pressure during nose-up body tilts, particularly when no visual information reflecting body position in space was available. However, recovery of orthostatic tolerance occurred within 1 wk, presumably because the vestibular nuclei integrate a variety of sensory inputs reflecting body location. The present study tested the hypothesis that lesions of the vestibular nuclei result in persistent cardiovascular deficits during orthostatic challenges. Blood pressure and heart rate were monitored in five conscious cats during nose-up tilts of varying amplitude, both before and after chemical lesions of the vestibular nuclei. Before lesions, blood pressure remained relatively stable during tilts. In all animals, the blood pressure responses to nose-up tilts were altered by damage to the medial and inferior vestibular nuclei; these effects were noted both when animals were tested in the presence and absence of visual feedback. In four of the five animals, the lesions also resulted in augmented heart rate increases from baseline values during 60 degrees nose-up tilts. These effects persisted for longer than 1 wk, but they gradually resolved over time, except in the animal with the worst deficits. These observations suggest that recovery of compensatory cardiovascular responses after loss of vestibular inputs is accomplished at least in part through plastic changes in the vestibular nuclei and the enhancement of the ability of vestibular nucleus neurons to discriminate body position in space by employing nonlabyrinthine signals.     

An electromyographic analysis of the Ab-Slide exercise, abdominal crunch, supine double leg thrust, and side bridge in healthy young adults: implications for rehabilitation professionals

The purpose of this study was to examine the effectiveness of a commercial abdominal machine (Ab-Slide) and three common abdominal strengthening exercises (abdominal crunch, supine double leg thrust, and side bridge) on activating abdominal and minimizing extraneous (nonabdominal) musculature-namely, the rectus femoris muscle. We recruited 10 males and 12 females whose mean (+/- SD) percent body fat was 10.7 +/- 4 and 20.7% +/- 3.2%, respectively. Electromyographic (EMG) data were recorded using surface electrodes for the rectus abdominis, external oblique, internal oblique, and rectus femoris. We recorded peak EMG activity for each muscle during each of the four exercises and normalized the EMG values by maximum muscle contractions (% MVIC). A two-factor repeated-measures analysis of variance assessed differences in normalized EMG activity among the different exercise variations (p < 0.05). Post hoc analyses were performed using the Bonferroni-adjusted alpha to assess between-exercise pair comparisons (p < 0.002). Gender did not affect performance; hence, data were collapsed across gender. We found a muscle x exercise interaction (F9,189 = 5.2, p < 0.001). Post hoc analyses revealed six pairwise differences. The Ab-Slide elicited the greatest EMG activity for the abdominal muscles and the least for the rectus femoris. The supine double leg thrust could be a problem for patients with low-back pathology due to high rectus femoris muscle activity.     

Effects of midline laparotomy on expiratory muscle activation in anesthetized dogs

Abdominal surgery has a marked inhibitory influence on the diaphragm, but its effect on the expiratory muscles is not known. Therefore, we have recorded the electromyograms of the triangularis sterni, abdominal external oblique, and transversus abdominis before and after a midline laparotomy in 10 anesthetized, spontaneously breathing dogs. Measurements were obtained during quiet breathing in the supine posture, during breathing against expiratory threshold loads, during head-up tilting, and during hyperoxic hypercapnia. Expiratory activation of the transversus abdominis in all conditions was considerably reduced after laparotomy. This reduction was real, as no change in the compound muscle action potential during single pulse stimulation was observed. In contrast, expiratory recruitment of either the triangularis sterni or the abdominal external oblique was maintained or increased. We therefore conclude that laparotomy inhibits not only activation of the diaphragm during inspiration but also activation of the transversus abdominis during expiration. Visceral afferents thus affect in concert the two respiratory muscles lining the peritoneum. The present findings also emphasize the important fact that the pattern of activation of a particular abdominal muscle is not necessarily representative of the entire abdominal musculature.     

Transversus abdominis muscle function in humans

We used a high-resolution ultrasound to make electrical recordings from the transversus abdominis muscle in humans. The behavior of this muscle was then compared with that of the external oblique and rectus abdominis in six normal subjects in the seated posture. During voluntary efforts such as expiration from functional residual capacity, speaking, expulsive maneuvers, and isovolume "belly-in" maneuvers, the transversus in general contracted together with the external oblique and the rectus abdominis. In contrast, during hyperoxic hypercapnia, all subjects had phasic expiratory activity in the transversus at ventilations between 10 and 18 l/min, well before activity could be recorded from either the external oblique or the rectus abdominis. Similarly, inspiratory elastic loading evoked transversus expiratory activity in all subjects but external oblique activity in only one subject and rectus abdominis activity in only two subjects. We thus conclude that in humans 1) the transversus abdominis is recruited preferentially to the superficial muscle layer of the abdominal wall during breathing and 2) the threshold for abdominal muscle recruitment during expiration is substantially lower than conventionally thought.     

Effect of head-down tilt on respiratory responses and human inspiratory muscle activity

The effect of a head-down tilt on the responses of the external respiration system and the functional capacity of the diaphragm and parasternal muscles were investigated in 11 healthy subjects. A 30-min head-down tilt posture (−30° relative to the horizontal) significantly increased the inspiratory time, decreased the respiration rate and the inspiratory and expiratory flow rates; and increased the airway resistance compared to these values in the vertical posture. There were no significant changes in tidal volume or minute ventilation. The electromyograms (EMGs) of the diaphragm and parasternal muscles showed that the constant values of tidal volume and minute ventilation during head-down tilt could be provided by an increase in the electric activity of the thoracic inspiratory muscles. It was established that the contribution of the thoracic inspiratory muscles increased, while the diaphragms’ contribution decreased, during patient, spontaneous breathing. The maximal inspiratory effort (Muller’s maneuver) during a head-down tilt evoked the opposite EMG-activity pattern: the contribution of inspiratory thoracic muscles was decreased and the diaphragm EMG activity was increased compared to the vertical posture. These results suggest that coordinated modulations in inspiratory muscle activity make it possible to preserve the functional reserve of human inspiratory muscles during a short-term head-down tilt.     

Posture effects on timing of abdominal muscle activity during stimulated ventilation.

In humans during stimulated ventilation, substantial abdominal muscle activity extends into the following inspiration as postexpiratory expiratory activity (PEEA) and commences again during late inspiration as preexpiratory expiratory activity (PREA). We hypothesized that the timing of PEEA and PREA would be changed systematically by posture. Fine-wire electrodes were inserted into the rectus abdominis, external oblique, internal oblique, and transversus abdominis in nine awake subjects. Airflow, end-tidal CO2, and moving average electromyogram (EMG) signals were recorded during resting and CO2-stimulated ventilation in both supine and standing postures. Phasic expiratory EMG activity (tidal EMG) of the four abdominal muscles at any level of CO2 stimulation was greater while standing. Abdominal muscle activities during inspiration, PEEA, and PREA, were observed with CO2 stimulation, both supine and standing. Change in posture had a significant effect on intrabreath timing of expiratory muscle activation at any level of CO2 stimulation. The transversus abdominis showed a significant increase in PEEA and a significant decrease in PREA while subjects were standing; similar changes were seen in the internal oblique. We conclude that changes in posture are associated with significant changes in phasic expiratory activity of the four abdominal muscles, with systematic changes in the timing of abdominal muscle activity during early and late inspiration.     

Electromyographic response of the abdominal musculature to varying abdominal exercises

This study examined the electromyographic (EMG) response of the upper rectus abdominis (URA), lower rectus abdominis (LRA), internal obliques (IOs), external obliques (EOs), and the rectus femoris (RF) during various abdominal exercises (crunch, supine V-up, prone V-up on ball, prone V-up on slide board, prone V-up on TRX, and prone V-up on Power Wheel). The subjects (n = 21) performed an isometric contraction of the abdominal musculature while performing these exercises. Testing revealed no statistically significant differences between any of the exercises with respect to the EOs, the URA, or the LRA. However, when examining the IO muscle, the supine V-up exercise displayed significantly greater muscle activity than did the slide exercise. In addition, EMG activity of the RF during the crunch was significantly less than in any of the other 5 exercises. These results indicate that when performing isometric abdominal exercises, non-equipment-based exercises stressed the abdominal muscles similarly to equipment-based exercises. Based on the findings of the current study, the benefit of training the abdominal musculature in an isometric fashion using commercial equipment could be called into question.     

Changes in intra-abdominal pressure during postural and respiratory activation of the human diaphragm.

In humans, when the stability of the trunk is challenged in a controlled manner by repetitive movement of a limb, activity of the diaphragm becomes tonic but is also modulated at the frequency of limb movement. In addition, the tonic activity is modulated by respiration. This study investigated the mechanical output of these components of diaphragm activity. Recordings were made of costal diaphragm, abdominal, and erector spinae muscle electromyographic activity; intra-abdominal, intrathoracic, and transdiaphragmatic pressures; and motion of the rib cage, abdomen, and arm. During limb movement the diaphragm and transversus abdominis were tonically active with added phasic modulation at the frequencies of both respiration and limb movement. Activity of the other trunk muscles was not modulated by respiration. Intra-abdominal pressure was increased during the period of limb movement in proportion to the reactive forces from the movement. These results show that coactivation of the diaphragm and abdominal muscles causes a sustained increase in intra-abdominal pressure, whereas inspiration and expiration are controlled by opposing activity of the diaphragm and abdominal muscles to vary the shape of the pressurized abdominal cavity.     

Walking slope and heavy backpack loads affect torso muscle activity and kinematics

The independent effects of sloped walking or carrying a heavy backpack on posture and torso muscle activations have been reported. While the combined effects of sloped walking and backpack loads are known to be physically demanding, how back and abdominal muscles adapt to walking on slopes with heavy load is unclear. This study quantified three-dimensional pelvis and torso kinematics and muscle activity from longissimus, iliocostalis, rectus abdominis, and external oblique during walking on 0° and ± 10° degree slopes with and without backpack loads using two different backpack configurations (hip-belt assisted and shoulder-borne). Iliocostalis activity was greater during downhill and uphill compared to level walking, but longissimus was only greater during uphill. Rectus abdominis activity was greater during downhill and uphill compared to level, while external oblique activity decreased as slopes progressed from down to up. Longissimus, but not iliocostalis, activity was reduced during both backpack configurations compared to walking with no pack. Hip-belt assisted load carriage required less rectus abdominis activity compared to using shoulder-borne only backpacks; however, external oblique was not influenced by backpack condition. Our results revealed different responses between iliocostalis and longissimus, and between rectus abdominis and external obliques, suggesting different motor control strategies between anatomical planes.