The effect of lung volume on the co-ordinated recruitment of scalene and sternomastoid muscles in humans

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1 J Physiol (2007) pp The effect of lung volume on the co-ordinated recruitment of scalene and sternomastoid muscles in humans Anna L. Hudson, Simon C. Gandevia and Jane E. Butler Prince of Wales Medical Research Institute and the University of New South Wales, Sydney 2031, Australia The human scalenes are obligatory inspiratory muscles that have a greater mechanical advantage than sternomastoid, an accessory muscle. This study determined scalene and sternomastoid recruitment during voluntary inspiratory tasks, and whether this activity varied with lung volume, when feedback from the lungs and inspiratory muscles would differ. If afferent feedback has a major role in determining the recruitment of the scalenes and sternomastoid, then at each lung volume, activity would be altered. Intramuscular EMG from scalene and sternomastoid muscles, and oesophageal pressure were recorded while subjects (n = 7) performed inspiratory isovolumetric ramps to maximal inspiratory pressure (MIP) and dynamic inspirations from functional residual capacity (FRC) to total lung capacity (TLC). The static inspiratory ramps were repeated at three lung volumes: FRC, FRC + tidal volume, and TLC. To determine the profile of inspiratory activation, i.e. the initial and ongoing recruitment of the muscles, the root mean square of the EMG was measured throughout the tasks. Scalene was recruited early, and EMG increased with pressure, reaching a plateau at 80% MIP. In contrast, sternomastoid activity began later, but then increased with pressure from 20 to 100% MIP. Similar profiles of activation occurred at all three lung volumes (n.s.). The ratio of sternomastoid to scalene EMG was also the same irrespective of the initial lung volume (n.s.). In dynamic inspirations, scalene and sternomastoid activation had similar stereotypical profiles to the static tasks, but scalene EMG was 15 40% greater (P < 0.05). Sternomastoid activation was the same in both tasks (n.s.). These results suggest that in voluntary tasks, scalene and sternomastoid are recruited in the order of their mechanical advantages, and that alterations in feedback related to changes in lung volume failed to alter their activation. Thus, in humans, the mechanism responsible for the differential activation of these two inspiratory muscles has an element that is preset. (Received 23 May 2007; accepted after revision 7 August 2007; first published online 9 August 2007) Corresponding author S. Gandevia: Prince of Wales Medical Research Institute, Barker Street, Randwick, NSW, 2031, Australia. s.gandevia@unsw.edu.au The human inspiratory muscles in the neck include the scalenes and sternomastoid. These muscles have similar respiratory actions on the chest wall and cause cranial displacement of the sternum and ribcage, but they have different patterns of activity (Campbell, 1970). The scalenes are obligatory muscles of inspiration activated in every breath (Raper et al. 1966; De Troyer & Estenne, 1984; Gandevia et al. 1996), after an average of 7% inspiratory time in multiunit EMG recordings (Saboisky et al. 2007). Sternomastoid is an accessory muscle of inspiration and does not contract during quiet breathing. It is only recruited after 70% of inspiratory capacity when tidal volume is increased by hypercapnia (Campbell, 1955) or volitional hyperpnoea (Raper et al. 1966), or at 35% of maximal inspiratory pressure during a static inspiratory effort at functional residual capacity (Yokoba et al. 2003). Also, in patients with severe chronic obstructive pulmonary disease, intramuscular recordings show strong inspiratory activity in scalenes, but sternomastoid is silent during quiet breathing (De Troyer et al. 1994). De Troyer and colleagues have quantified the action of most human respiratory muscles on the lung (Wilson & De Troyer, 1992; for review see De Troyer et al. 2005). Mechanical advantage, or the change in pleural pressure produced by a muscle per unit muscle mass and unit muscle stress, is assessed by measuring a muscle s fractional length change during passive lung inflation. A muscle with a high mechanical advantage shortens more (per unit of lung volume) than one with a low mechanical advantage. In humans, the mechanical advantage of the scalenes (3.4% l 1 ) is greater than that of sternomastoid (2.0% l 1 ; Legrand et al. 2003). There is a matching of mechanical advantage and inspiratory activity in the intercostal muscles in the DOI: /jphysiol

2 262 A. L. Hudson and others J Physiol anaesthetized dog (De Troyer et al. 1996b; Legrand et al. 1996; for review see De Troyer et al. 2005), and in humans (De Troyer et al. 2003; Gandevia et al. 2006). This principle of neuromechanical matching (Butler et al. 2007) ensures that intercostal muscles with a high mechanical advantage are active early in inspiration and contract strongly, and those with a low mechanical advantage are active late and contract weakly. In the dog, this pattern of activity is maintained even after muscle afferent feedback is removed by thoracic dorsal rhizotomy or section of the phrenic nerves (De Troyer & Legrand, 1995; De Troyer et al. 1996a; Legrand et al. 1996). However, the role of lung afferents in this neuromechanical matching has not been tested. Human inspiratory muscles in the neck also appear to be recruited according to their mechanical advantage as during quiet breathing there is more activity in scalene, which has a high mechanical advantage, compared to sternomastoid (Legrand et al. 2003). It is not known whether their inspiratory activity is dependent on afferent feedback of lung volume or muscle length, or whether it is controlled by descending drive and recruitment strategies with stereotypical patterns that are preset. In the human medial gastrocnemius, there are changes in motor-unit recruitment depending on muscle length and the relative contribution of this muscle to isometric plantar flexion torque (Kennedy & Cresswell, 2001). This is an example where neural drive is adapted depending on muscle length and task. We have studied scalene and sternomastoid activity during static ramps of inspiratory effort at different lung volumes, and also during dynamic inspirations to high lung volumes. At different lung volumes and muscle lengths, feedback from the lungs and inspiratory muscles will differ. If such feedback has a major role in determining the recruitment of the scalenes and sternomastoid, then their activity will be altered by lung volume. We hypothesized that scalene and sternomastoid activity would be similar despite changes in lung volumes, and we tested it by comparing their activity across a range of volumes. Methods Oesophageal pressure (P oes ) and intramuscular electromyographic activity (EMG) from the right scalene and sternomastoid muscles were recorded (Fig. 1A). Subjects performed inspiratory isovolumetric ( static ) ramps to maximal inspiratory pressure (MIP), at three lung volumes, and voluntary dynamic inspirations from functional residual capacity (FRC) to total lung capacity (TLC). P oes, scalene and sternomastoid EMG were determined at 11 time points across the tasks between A B Figure 1. Experimental set up and analysis of static inspiratory ramps A, subjects were comfortably seated and breathed through a mouthpiece with a solenoid-activated shutter. Electromyographic (EMG) recordings were made with bipolar electrodes inserted into the right scalene and sternomastoid muscles. Oesophageal pressure (P oes ) was recorded. B, representative recordings during a 5 s inspiratory ramp (i.e. static task) at functional residual capacity (FRC). From top to bottom, panels show P oes, and r.m.s. and raw EMG from scalene and sternomastoid. Cursors were placed at baseline and maximal P oes and the corresponding time points were denoted 0% and 100% of the ramp, respectively. P oes, scalene r.m.s. EMG and sternomastoid r.m.s. EMG were then determined at 10% time intervals ( ) to give a profile of muscle activation across the task. Negative pressure is upwards in the pressure trace. Vertical calibration: 500 μv.

3 J Physiol Recruitment of scalene and sternomastoid muscles 263 0% and 100% of time (Fig. 1B). This allowed us to determine the profile of inspiratory activation, i.e. the initial and on-going recruitment of populations of scalene and sternomastoid motor units during isovolumetric ramps and dynamic inspirations. Experimental set-up Data were obtained from seven subjects (aged years, six males) who gave informed consent to the procedures, which conformed to the Declaration of Helsinki, and which had been approved by the Human Research Ethics Committee of the University of New South Wales. Subjects were healthy with no major respiratory or neurological disease. Subjects were seated comfortably with restrictive garments removed and grounded with a large flexible strap on the right shoulder. The locations for insertion of the electrodes were determined by palpation, and for scalenus medius, it was 8 cm superior to the floor of the supraclavicular fossa, and for sternomastoid, it was at the longitudinal midpoint of the muscle. Selective recordings of EMG were made simultaneously with pairs of intramuscular fine-wire electrodes. The electrodes were made from two insulated stainless-steel wires (75 μm diameter) with 2 3 mm of insulation removed and were inserted into each muscle via a 23 gauge needle. The EMG was amplified ( ) and band-pass filtered ( Hz). A catheter was inserted to record P oes (Gaeltec Ltd, UK). It was passed through the nose until the transducer was located in the mid-lower oesophagus. Subjects breathed through a mouth piece connected to a pneumotachometer (Hans Ruldoph Inc., MO, USA) and a solenoid-activated shutter (Honeywell, CT, USA). The signal of airflow was integrated to give volume, and subjects were given visual feedback of lung volume and P oes on a large computer monitor throughout the experiment. All signals were stored on computer via an analog to digital interface for subsequent analysis (Cambridge Electronic Design 1401, Cambridge, UK). EMG was sampled at 5 khz and flow, volume and P oes at 1 khz. Experimental protocol MIP was determined in brief maximal voluntary inspiratory efforts performed against a closed shutter at the three different lung volumes: FRC, FRC + tidal volume (V t ), and near TLC. Volume is expressed relative to the usual end-expiratory level, and therefore this estimate of FRC is considered 0 l. The highest lung volume (near TLC) was 300 ml below TLC. This volume was selected because subjects could not relax their inspiratory muscles completely against the closed shutter at TLC. However, in this study, this volume will be referred to as TLC. Baseline and maximal P oes were calculated from the MIP efforts at each lung volume, and subjects then tracked 5 s ramps of P oes by gradually generating an inspiratory pressure against the closed shutter with visual feedback of P oes. These isovolumetric ramps or static tasks were repeated at three lung volumes: FRC, FRC + V t, and TLC, with three to six repeats at each volume (e.g. Fig. 4). Subjects also performed six dynamic tasks, by inspiring voluntarily from FRC to TLC with the shutter open. The duration of inspiration was 4s. Data analysis Static tasks. Cursors were placed manually at the start (i.e. baseline P oes ) and the end (i.e. maximal P oes ) for each ramp. To determine the profile of inspiratory activation of scalene and sternomastoid throughout the static task, P oes and the root mean square (r.m.s.; time constant, 0.05 s) of the scalene and sternomastoid EMG signals were determined at 11 time points, i.e. at 0%, and 10% time intervals to 100% of the ramp (Fig. 1B). At each time, baseline P oes was subtracted from P oes to give P oes.for comparison between subjects and between lung volumes, P oes was normalized to the brief MIP generated by each subject, at each lung volume (e.g. Fig. 5B). Baseline r.m.s. EMG (near zero at complete relaxation) was subtracted from EMG at each time point, and to allow comparison of scalene and sternomastoid activation across different lung volumes, EMG was normalized to the maximal EMG across all tasks. Therefore, for each muscle, the average maximal EMG during repeated inspiratory ramps at each lung volume was determined, and the maximum value was used for normalization at all time points and volumes. It was not normalized to EMG during the brief maximal inspiratory efforts because the wire electrodes were not inserted until after the MIP was determined. Chest wall recoil pressure (P w ) was measured when subjects relaxed against the closed shutter after inspiration to FRC + V t, or TLC (Agostoni, 1970). Assuming that scalene and sternomastoid activity is representative of all chest wall muscles, some subjects (n = 4) could relax against the shutter (e.g. subject in Fig. 3C). However, others (n = 3) had difficulty relaxing at high lung volumes, and had on-going EMG prior to the onset of the inspiratory ramps. In these subjects, P w was 35% less than those who could relax. The difference in P w ( P w ) between these groups of subjects was 2.1 cmh 2 OatFRC+ V t, and 6.9 cmh 2 O at TLC. This represents a potential error of up to 14%, as MIP at TLC is only 50 cmh 2 O (Agostoni, 1970). Therefore, to calculate the pressure generated by the total respiratory system, and to obtain consistency between all subjects, P w (above) was added to all values of P oes at FRC + V t, and TLC in the three subjects who could not relax.

4 l 264 A. L. Hudson and others J Physiol EMG recordings from sternomastoid could not be analysed in one subject due to movement artefact. In another subject, an adequate recording of scalene EMG could not be made. Therefore, for Fig. 5A and B, P oes (% MIP), scalene EMG and sternomastoid EMG were averaged across six subjects at each lung volume. In Fig. 5C, the ratio of sternomastoid to scalene EMG, data is the average of five subjects with complete data from both muscles. Dynamic tasks. Due to the nature of the task, dynamic tasks (voluntary inspiration to TLC) were analysed in a slightly different way. Cursors were placed at the onset of scalene or sternomastoid activity, and at peak inspired volume (Fig. 2A). Then, for each muscle, lung volume, P oes and EMG were determined at 11 time points, i.e. at zero and 10% time intervals to 100% of time (e.g. vertical dashed line in Fig. 2A). During any dynamic breath, as P oes decreases and lung volume increases, there is a concurrent increase in P w. Therefore, for each subject, volume P w graphs (P w that a subject could generate after relaxation at FRC, FRC + V t, and TLC) were constructed (not shown). Linear regressions determined the P w that a subject could generate at the lung volume at each time point, and P oes was adjusted by the estimated P w to give the pressure generated by the total respiratory system. Volume MIP graphs (MIP that a subject could generate at FRC, FRC + V t, and TLC; Fig. 2B) were also constructed, and linear regressions determined the estimated MIP that each subject could generate at each time point. Voluntary activation of the diaphragm is high during maximal inspiratory efforts across this range of lung volumes (McKenzie et al. 1996). Pressure ( P oes + estimated P w ) was then normalized to the estimated MIP. As in the static tasks, scalene and sternomastoid EMG were normalized to the maximal EMG of the three lung volumes during the static tasks. Pressure (% estimated MIP), scalene, and sternomastoid EMG were averaged across six subjects (see above). Statistics Statistical comparison between the MIP that subjects could generate at different lung volumes was made by analysis of variance (ANOVA) with repeated measures, and post hoc testing using the Student Newman Keul procedure. In A (l) B Figure 2. Analysis of scalene and sternomastoid activation during dynamic tasks A, representative recordings during dynamic tasks, i.e. inspiration from FRC to total lung capacity (TLC) with the shutter open. From top to bottom, panels show lung volume, P oes (negative pressure upwards) and scalene and sternomastoid r.m.s. EMG. Cursors were placed at the onset of scalene or sternomastoid activity (arrows), and at peak inspired volume (continuous vertical line). For analysis, these time points were denoted 0% and 100%, respectively, and then volume, P oes and scalene or sternomastoid EMG values were determined at 10% time intervals. For each time point (e.g. vertical dashed line) and corresponding volume ( x ), the estimated maximal inspiratory pressure (MIP) that each subject could generate at that volume was determined ( y, panel B). Estimated MIP was used to normalize P oes ( z ) at that time interval. B, MIP that each subject ( ) and the group (, mean ± S.E.M, n = 7) could generate at each lung volume. For each subject, MIP was greatest at FRC (0 l), decreased at FRC + tidal volume (V t )( +1l;P < 0.05) and further decreased at TLC ( +2.5 l; P < 0.05). The estimated MIP ( y ) for each lung volume ( x ) was calculated for each subject ( ) for analysis of the dynamic tasks (panel A).

5 J Physiol Recruitment of scalene and sternomastoid muscles 265 the static tasks, comparison between EMG at the different lung volumes was made by two-way repeated measures ANOVA, with lung volume (FRC, FRC + V t, and TLC) and P oes (0 20%, 20 40%, 40 60%, 60 80% and % MIP) as factors. Contrasts on the volume factor compared FRC with TLC, and their mean with FRC + V t. Contrasts on P oes factor compared each level with the next (i.e. 0 20% MIP with 20 40% MIP, 20 40% MIP with 40 60% MIP, etc.). Scalene and sternomastoid EMG values were averaged in 20% blocks of MIP, on the basis of P oes (% MIP) values at the 11 time points (Fig. 1B). If a subject had a missing value (i.e. no value of P oes in the 20% MIP block) it was replaced with the group mean (Tabachnick & Fidell, 1989). To compare muscle activation during the static and dynamic tasks, a two-way repeated measures ANOVA was used with task (i.e. static verses dynamic) and pressure (0 20% MIP or % estimated MIP, etc., as above) as factors. Contrasts compared task and pressure (as above). For the static task factor, P oes (% MIP), scalene and sternomastoid EMG values during the ramp at FRC were used for comparison to dynamic tasks because all subjects could relax at this volume (see above), and therefore were equally relaxed before the dynamic tasks and static tasks at FRC. Only pressures from 0 to 80% MIP or % estimated MIP (i.e. 4 levels) were compared due to the high number of missing values in the dynamic tasks above 80% estimated MIP. The criterion for statistical significance was taken as P < Data are presented as means ± s.e.m. Results The timing and degree of activity in scalene and sternomastoid differed during voluntary isovolumetric inspiratory ramps (static tasks) to maximal inspiratory pressure (MIP) and dynamic inspirations from functional residual capacity (FRC) to total lung capacity (TLC). To compare activity between static tasks at different lung volumes, and between static and dynamic tasks, inspiratory pressure during the tasks were normalized to MIP. Maximal inspiratory pressure MIP differed between the three test lung volumes (Fig. 2B). For seven subjects, the average MIP decreased from ± 7.6 cmh 2 O (mean ± s.e.m.) at FRC, to 92.7 ± 4.3 cmh 2 OatFRC+ tidal volume (V t ; P < 0.05). It was even smaller at TLC, 56.0 ± 10.5 cmh 2 O(P < 0.05). For each subject, P oes was expressed relative to MIP at that lung volume (Fig. 2B; open circles). Static tasks Inspiratory ramps at three lung volumes for an individual subject are shown in Fig. 3. Despite differences in the pressures produced during the ramps, the profile of scalene and sternomastoid EMG is similar at each lung volume. Scalene was active early in the pressure ramps, often prior to a major change in P oes (e.g. Fig. 3A). In comparison, sternomastoid was recruited later, and in some subjects it was not active until 60% MIP in some ramps (e.g. Fig. 4B, right panel). Recruitment of sternomastoid was delayed equally at all lung volumes despite sternomastoid EMG having been present during the dynamic phase of inspiration to that target volume (Figs 3C and 4B, right panel). A B C Figure 3. Data from a single subject during static inspiratory ramps P oes, r.m.s., and raw EMG from scalene and sternomastoid during inspiratory ramps at different lung volumes for a typical subject. Negative pressure is upwards in the pressure trace. A, during a static task at FRC, the subject generated a MIP of 104 cmh 2 O. Scalene was active early, at the start of the ramp, but sternomastoid recruitment was delayed. B, atfrc+ V t, the subject generated a MIP of 96 cmh 2 O. The recruitment of scalene and sternomastoid is similar to panel A. C, at a high lung volume, TLC, (see Methods), the subject could only generate 54 cmh 2 O. However, scalene and sternomastoid activity remain similar to that at FRC (panel A) and FRC + V t (panel B).

6 266 A. L. Hudson and others J Physiol The profile of inspiratory activation, i.e. the initial and on-going recruitment of scalene and sternomastoid from 0 to 100% MIP in repeated inspiratory ramps for an individual subject is shown in Fig. 4. The average activation during inspiratory ramps at FRC, FRC + V t, and TLC for six subjects is shown in Fig. 5. Scalene was active early, with some recruitment at 0% MIP and a continued increase in activity with increasing P oes (P < 0.05), before reaching a plateau at % MIP (P > 0.05). Some subjects could not relax properly at high lung volumes (see Methods); therefore at 0% MIP, the average scalene EMG was elevated at TLC. Sternomastoid EMG did not increase until after an average 20% MIP, but then increased progressively to 100% MIP (P < 0.05). Therefore, while scalene and sternomastoid have different profiles of inspiratory activation, there was no difference for each muscle in activation at different lung volumes. Scalene EMG from 0 to 100% MIP was similar at FRC, FRC + V t, and TLC (P = 0.16), and sternomastoid EMG was also similar during inspiratory ramps at the three test lung volumes (P = 0.43). To study the relationship between the profile of inspiratory activation of the two respiratory muscles, and whether it differed with lung volume, we plotted the ratio of sternomastoid EMG to scalene EMG (Fig. 5C). From 0 to 100% MIP, the ratio of activation was similar during inspiratory ramps at three lung volumes (P = 0.82). Dynamic tasks Figure 6 shows profiles of inspiratory activation of scalene and sternomastoid during dynamic inspirations from FRC to TLC. Activation was consistent between breaths (Fig. 6A), but as in the static tasks, the profile of activation of scalene and sternomastoid differed (Figs 2A and 6). For the group, scalene EMG increased with pressure (% estimated MIP) in dynamic breaths (Fig. 6B, filled circles; P < 0.05). Sternomastoid recruitment was delayed until 20% estimated MIP, but then its activity increased from 20 to 80% estimated MIP (P < 0.05). Figure 6B also compares scalene and sternomastoid EMG during dynamic tasks to EMG during static A B Figure 4. Scalene and sternomastoid activation during inspiratory ramps at different lung volumes in one subject Data from one subject during 6 static inspiratory ramps at each lung volume: FRC, FRC + V t, and TLC. P oes is expressed as a percentage of MIP for each lung volume. Scalene and sternomastoid r.m.s. EMG is expressed as a percentage of maximum EMG across the three lung volumes (see Methods). A, scalene activation from 0 to 100% MIP during inspiratory ramps was consistent within and between lung volumes. B, sternomastoid activity was also similar within and between lung volumes, but the profile of activation is different from that for scalene (panel A). In this subject, sternomastoid was not recruited until after 40% MIP.

7 J Physiol Recruitment of scalene and sternomastoid muscles 267 inspiratory ramps at FRC. In scalene, the profile of activation was qualitatively similar to the stereotyped activation during the static tasks (Fig. 5A), and EMG continually increases to 80% MIP or % estimated MIP in both tasks. However, there was more scalene activity throughout the dynamic task compared to the static task at FRC (P = 0.04). There was no difference in the profile of activation of sternomastoid in the two tasks (Fig. 6B; P = 0.68). Discussion We have shown that in voluntary tasks, the profile of inspiratory activation of scalene and sternomastoid does not depend on lung volume or feedback from the lungs and inspiratory muscles, and activation is similar during isovolumetric ramps at three lung volumes. The ratio of sternomastoid : scalene EMG is also similar during inspiratory ramps at different lung volumes. The stereotypical activation of scalene and sternomastoid A B Figure 5. The profile of activation of scalene and sternomastoid at different lung volumes Mean ± S.E.M data from six subjects during 5 s inspiratory ramps at FRC ( ), FRC + V t ( ), and TLC ( ). P oes is expressed as a percentage of MIP for each lung volume. Scalene and sternomastoid r.m.s. EMG are expressed as a percentage of maximum EMG across the three lung volumes. A, at all lung volumes, scalene EMG increased with P oes before reaching a plateau at 80% MIP, and a similar profile of activation was observed irrespective of initial lung volume. Scalene EMG is not 0% at 0% MIP because some subjects could not relax fully against the shutter before the ramp, especially near TLC. There was also some recruitment of scalene prior to an increase in P oes (% MIP). B, in contrast to scalene (panel A), sternomastoid recruitment is delayed. At all lung volumes, sternomastoid EMG does not increase until after 20% MIP of the inspiratory ramps. From 20 to 100% MIP, sternomastoid EMG increases similarly at FRC, FRC + V t, and TLC. C, to compare the activity of sternomastoid to that of scalene, the ratio of sternomastoid EMG (panel B) to scalene EMG (panel A) was plotted for each lung volume (mean ± S.E.M.). As subjects could not relax their scalene before the inspiratory task, data at 0% MIP are not shown. There is no difference in sternomastoid: scalene activation during inspiratory ramps at different lung volumes. C

8 268 A. L. Hudson and others J Physiol during static inspiratory tasks was also observed in dynamic inspirations across a wide range of lung volumes. Scalene activity was greater during the dynamic inspirations compared to static ramps at FRC (Fig. 6B; top panel). This may be due to the requirement of the inspiratory muscles to overcome the inertia of the chest wall mass. Based on the force velocity curve, dynamic breaths will also require more neural drive to produce pressure at higher shortening velocities. Despite greater activity in scalene, sternomastoid activity was similar in both tasks (Fig. 6B; bottom panel). This suggests that any changes in afferent feedback as a result of increased scalene EMG in the dynamic tasks did not alter the activation of the accessory muscle, sternomastoid. Differences in lung volume will change feedback from many structures including the lungs, muscles and upper airway. If inspiratory muscle activity depends on feedback of lung volume, inputs from any of the above structures could be responsible. Our data show that A lung volume does not affect the profile of activation in scalene and sternomastoid muscles during voluntary isovolumetric ramps of inspiratory pressure, or greatly affect the activation in dynamic inspirations. Receptors which respond to static changes in lung volume, pressure or muscle length will be activated differentially during static tasks at the different lung volumes, and receptors sensitive to dynamic changes, will be activated during inspiration to TLC (see below). Our results suggest that such behaviour does not alter the overall profile of neural activation of the two muscles. Also, activation does not depend on pressure (or force) as at each lung volume, sternomastoid is recruited at different absolute pressures (e.g. Fig. 3). The pressure at which sternomastoid is recruited at FRC here is similar to that in breaths with an inspiratory resistive load (Adams et al. 1989). The maintained firing of some intrapulmonary slowly adapting stretch receptors, which respond to changes in tension in the airway wall, would differ at the lung B Figure 6. Activity in scalene and sternomastoid during dynamic tasks in a single subject, and comparison with activation in static inspiratory ramps Scalene and sternomastoid EMG are expressed as a percentage of maximum EMG during inspiratory ramps (see Methods). For the dynamic tasks, pressure is expressed as a percentage of estimated MIP (MIP e ; Fig. 2B, ). For the static inspiratory ramps in panel B, EMG and P oes (% MIP) are average values from the ramp at FRC (Fig. 5A). A, scalene and sternomastoid activation during 6 dynamic breaths to TLC for a typical subject. As for static inspiratory ramps (Fig. 4), scalene and sternomastoid activity are consistent in repeated ramps, but different between muscles. Scalene is active early, but sternomastoid recruitment is delayed until 20% MIP e. B, mean ± S.E.M data from 6 subjects during dynamic breaths ( ), compared to the mean ± S.E.M data from the static tasks at FRC ( ), for 0 80 P oes (% MIP or % MIP e ). In scalene, activity is greater during the dynamic tasks compared to static inspiratory tasks (top panel), but there is no difference in the activation of sternomastoid (bottom panel).

9 J Physiol Recruitment of scalene and sternomastoid muscles 269 volumes tested here (e.g. Widdicombe, 1954; Davis et al. 1956; Coleridge & Coleridge, 1986; Ho et al. 2001). Intrapulmonary rapidly adapting receptors respond to dynamic changes in inflation (e.g. Coleridge & Coleridge, 1986; Ho et al. 2001), and they would have fired during dynamic inspirations only. Consequently, the feedback from rapidly adapting receptors would differ in dynamic and static contractions. Intramuscular receptors will also be activated differentially at the three lung volumes. At high lung volumes and short muscle length, the background discharge of secondary muscle spindle endings, which respond to static changes in muscle length, will be lower (e.g. Matthews, 1972; Vallbo, 1974). Golgi tendon organs, which signal muscle force (e.g. Houk & Henneman, 1967; Jami, 1992; Gandevia, 1996; Proske & Gregory, 2002) are likely to discharge less at high lung volumes (i.e. short muscle length), as the force-generating capacity of scalene and sternomastoid will be less for the same degree of activation (Farkas & Rochester, 1986). It is difficult to determine the response of primary muscle spindles during static tasks because the balance of drives to α and γ motoneurones of human inspiratory muscles at different lung volumes is not known. However, spindle afferents in limb muscles discharge during slow muscle shortening (e.g. Burke et al. 1978; Al-Falahe et al. 1990; Edin & Vallbo, 1990), so here they will discharge during dynamic inspirations. Their response may be less in dynamic, shortening contractions compared to static tasks when muscle length changes less (Burke et al. 1978). Therefore, primary muscle spindles are likely to respond differently in the dynamic and static tasks. Note also that muscle spindle activity in passive expiratory muscles may also differ at the three lung volumes. Slowly adapting pressure-sensitive receptors in the upper airway may also respond differentially during inspiratory ramps at different lung volumes because the negative pressures developed in the airway will differ (Hwang et al. 1984a, 1984b; Mathew, 1984). In addition, it is likely, but not definitively established, that some skin and joint receptors will discharge differently in the three static and in the dynamic inspiratory tasks. Descending projections to respiratory motoneurones and afferent feedback may differ between voluntary and involuntary conditions. In this study, feedback related to lung volume (irrespective of its origin) failed to alter the voluntary activation of scalene and sternomastoid. This suggests that, wherever the site of integration of the descending projections and afferent pathways, feedback associated with changing lung volume (i.e. not just lung afferents) does not alter the distinct profile of activation of the muscles in this study. Why is there stereotyped activation of scalene and sternomastoid? Respiration requires an efficient, fail-safe system of neural control. Activity in the respiratory muscles during spontaneous breathing, may be driven by a principle of neuromechanical matching to guarantee this efficiency (De Troyer et al. 2005; Butler et al. 2007), as the work done contracting two muscles is minimized if their activity is distributed according to the magnitude of their mechanical advantages (De Troyer et al. 2005). There may also be activation of inspiratory muscles in the neck according to their mechanical advantages as scalene has a high mechanical advantage and is active early in every breath, compared to sternomastoid, which is an accessory inspiratory muscle with a lower mechanical advantage (Legrand et al. 2003). The mechanism responsible for the distribution of inspiratory activity in the canine intercostal muscles does not depend on feedback from the chest wall or diaphragm (De Troyer & Legrand, 1995; De Troyer et al. 1996a; Legrand et al. 1996). In this study, we have shown that feedback related to lung volume (from any source including the lungs) does not affect the profile of activation of the human scalene and sternomastoid muscles in voluntary tasks. This suggests that the mechanism responsible for the activation of inspiratory muscles in humans has an element that is preset, organized either centrally or in the spinal cord. References Adams L, Datta AK & Guz A (1989). 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