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Static otolithic drive alters presynaptic inhibition in soleus motor pool
Journal of Electromyography and Kinesiology 32 (2017) 37–43
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Static otolithic drive alters presynaptic inhibition in soleus motor pool Apollonia Fox ⇑, David Koceja Indiana University, 1025 E. 7th St, Bloomington, IN 47405, United States
a r t i c l e
i n f o
Article history: Received 18 July 2016 Received in revised form 4 November 2016 Accepted 15 December 2016
Keywords: H-reflex Vestibulospinal Otolith Presynaptic inhibition
a b s t r a c t The vestibular system has both direct and indirect connections to the soleus motor pool via the vestibulospinal and reticulospinal tracts. The exact nature of how this vestibular information is integrated within the spinal cord is largely unknown. The purpose of this study was to identify whether changes in static otolithic drive altered the amount of presynaptic inhibition in the soleus H-reflex pathway. Changes in static otolithic drive were investigated in sixteen healthy participants using a tilt table. Two presynaptic pathways (common peroneal and femoral) to the soleus H-reflex were tested in three weight conditions (supine, non-weight bearing, and weight bearing). The dependent variable was the peak-to-peak amplitude of the soleus H-reflex. Inhibition to the soleus motor pool through the common peroneal nerve pathway differed significantly during weight conditions and tilt. During tilt and non-weight bearing there was greater inhibition of the soleus H-reflex compared to supine, however, this effect was reversed during tilt and weight bearing. Facilitation from the femoral nerve pathway was reduced by tilt compared to supine, but this reduction was unaffected by weight condition. This supports a role of the vestibular system as providing complex, task-dependent presynaptic input to motoneurons in the lower limbs. Published by Elsevier Ltd.
1. Introduction The vestibular system relates the position of the head in space relative to gravity and plays an integral role in maintaining balance and supporting posture (Nashner, 1971). Whereas the semicircular ducts have been implicated in alerting a person to potential falls (Nashner, 1971), the otolithic organs may have an important role for conveying ongoing information about the body with respect to gravity and may be more relevant to postural regulation (Watt, 1981a, 1981b; Greenwood and Hopkins, 1976; Lacour et al., 1978). Otolithic information is transmitted to all levels of the body primarily via the vestibulospinal and reticulospinal tracts (NybergHansen, 1965; Nyberg-Hansen and Mascitti, 1964). The information conveyed by these two tracts is organized reciprocally and is functionally coupled, so that different muscles will receive different, complementary, information from each tract about the position of the head relative to gravity (Orlovsky, 1972; Grillner et al., 1968). Recent research further demonstrates that this coupled, reciprocal patterning of information in the lower limbs is
⇑ Corresponding author at: War Related Illness and Injury Study Center, VA New Jersey Health Care Center, 385 Tremont Avenue, East Orange, NJ 07018, United States. E-mail address: [email protected] (A. Fox). http://dx.doi.org/10.1016/j.jelekin.2016.12.002 1050-6411/Published by Elsevier Ltd.
both muscle and task dependent (Dakin et al., 2013; Bent et al., 2004, 2002). There has been much investigation examining the various factors responsible for appropriate regulation of posture and dynamic maintenance of balance. The picture painted by these studies demonstrates that postural regulation is a task dependent on many factors, from somatosensory inputs (Bove et al., 2006; Inglis et al., 1994; Horak, 2006; Inglis and Macpherson, 1995) and cortical inputs (Barra et al., 2006; Bernard-Demanze et al., 2009; Shinya et al., 2016; Taube et al., 2008), to vestibular inputs (Peterka et al., 2011; Horak, 2009) and each of these factors is relatively weighted in its effect on the postural system (Dichgans and Diener, 1989; Fetter et al., 1990; Horak et al., 1990; Carriot et al., 2015). Vestibular inputs are integrated with and weighted against all of these other inputs for the dynamic modulation of postural responses. Interestingly, however, while these other factors affect long-latency postural responses, vestibular inputs also affect short-latency postural responses like the H-reflex (Kennedy and Inglis, 2001). Vestibular input to short-latency postural responses and the H-reflex have been demonstrated in both dynamic (Greenwood and Hopkins, 1976; Taube et al., 2008; Knikou and Rymer, 2003) environments where a drop or a tilt is initiated and also static environments (Knikou and Rymer, 2003; Aiello et al., 1983) where a tilt is sustained. However, the mechanism of vestibular integration within the spinal networks remains unknown. Several authors have posited that this integration hap-
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pens presynaptically (Kennedy and Inglis, 2001; Knikou and Rymer, 2003; Iles and Pisini, 1992). Gaining insight into these mechanisms could potentially lead to a deeper understanding of how specific vestibular disorders affect postural networks within the spinal cord. The soleus motor pool has long been studied for its relevance to postural regulation. Two well-defined presynaptic pathways to the soleus motor pool include common peroneal nerve conditioning and femoral nerve conditioning. For a full understanding of these pathways, please refer to Hultborn and colleagues (Hultborn et al., 1987a, 1987b; Morin et al., 1984). Based on the anatomy alone, the vestibular system could potentially affect the soleus motor pool presynaptically through the motor neurons directly, Ia afferent fibers, first-order primary afferent depolarization (PAD) interneurons, and/or second-order PAD interneurons (Nyberg-Hansen, 1965; Nyberg-Hansen and Mascitti, 1964). Recognizing the relationship between vestibular and somatosensory inputs, and coupled with the fact that weight-bearing has been shown to down-regulate the soleus Hreflex in humans (Koceja et al., 1993) we also sought to examine how the vestibular system interacts with weight-bearing mechanisms to more fully understand the complexities of vestibular input to spinal networks. The purpose of this study was to examine the role of the vestibular pathways in mediating soleus motoneuron excitability in both a weight-bearing and a non-weightbearing condition. 2. Materials and methods Twenty healthy subjects (14 female) between the ages of 18– 35 years participated in this study. Subjects were excluded for self-report of known neurological disorder, balance disorder, and/ or participation in high levels of physical activity. Prior to participation, all subjects read and signed an Informed Consent Form in accordance with the Declaration of Helsinki and approved by the Human Subjects Committee of Indiana University. Surface EMG was collected after preparing the skin with alcohol, using Ag electrodes (Delsys, Bagnoli 16) configured in a parallel array with 1-cm spacing and their output was pre-amplified with a gain of 1000. The electrodes were placed on the subject’s right leg, parallel to muscle fibers, over the soleus, medial and lateral gastrocnemius, tibialis anterior, and rectus femoris muscles. Signals were monitored, using an online oscilloscope (Tektronix, Model TDS 3012), throughout the experiment to ensure appropriateness of EMG recording. 2.1. H-reflex procedures Percutaneous electrical stimulation was used (GRASS S88D stimulator) to stimulate the appropriate mixed nerve and elicit the H-reflex or the conditioning stimulation. All H-reflex and conditioning stimuli were delivered using a 1 ms square-wave pulse (GRASS, S88stimulator), and monitored online using an oscilloscope (Tektronix, Model TDS 3012), according to standard lab procedures (Hugon, 1973). Briefly, the ideal testing site for the soleus H-reflex was determined by holding the electrode over the popliteal fossa while very slowly increasing the intensity delivered to the subject until the H-reflex appeared on the oscilloscope, in the absence of an M-wave. Once the intensity was high enough to evoke a small H-reflex, the experimenter slightly shifted the position of the electrode within the popliteal fossa to find a location where the largest measureable H-reflex existed at the same intensity of stimulation. Once this optimal location within the popliteal fossa was found, it was marked and the electrode was secured in that position. After the electrode was fully secure, it was doublechecked to be sure that an H-reflex equivalent to the earlier size
was still present, yet there was no M-wave present. The same overall procedure was repeated for the common peroneal nerve stimulation, with the electrode placed at the head of the fibula, and the femoral nerve, with the electrode placed in the inguinal crease. Optimal placement of the electrodes was periodically checked throughout the experiment to ensure that there was no movement of the electrodes over the course of the experiment. A soft ankle splint was placed on the subjects’ feet, fixing the angle of the ankle to 90° so that changes in muscle length due to ankle angle did not confound the results. Furthermore, subjects wore a blindfold in all of the conditions, to prevent any visual cues that may have influenced the soleus H-reflex. Finally, the subject was asked to keep their head in a neutral and comfortable position, resting against the tilt table, for the duration of the testing. This head position was visually monitored by the experimenter throughout the testing. All data were recorded on a laboratory computer (Optiplex GX280, Dell Computer Corporation) using custom data acquisition software (AcqKnowledge, version 3.7.3, BioPAC systems Inc.), sampled at 2000 Hz, and stored for offline analysis. Once all electrodes, ankle splint, harness, and blindfold were secured, the subject was asked to lay supine, eyes closed, on the tilt table and M-max of the soleus muscle was determined by slowly increasing the stimulation intensity until the M-wave saturated. Once the M-max value was determined, all further data were obtained by setting the stimulation intensity at an amplitude sufficient to elicit the soleus H-reflex at 15% of M-max. Because the soleus H-reflex was the dependent variable, only M-max of the soleus muscle was obtained. While, theoretically, M-max should be the same across all conditions (McNulty et al., 2012), in our experience M-max has been seen to shift slightly in the same subject over time or in different conditions. This instability has also been documented by others (McNulty et al., 2012). Therefore, Mmax was determined for each subject independently in the three weight conditions (supine, non-weight bearing, and weight bearing) and the H-reflex amplitude for each of the three weight conditions was set at 15% of the M-max for that individual condition. 2.2. Tilt table procedures The clinically-approved tilt table (Tri W-G, model TW6131.HD) moved at a constant slow speed of 4.3°/s (equivalent to 0.01 Hz). During the non-weight bearing condition, a harness assured that as the table angle changed the subject was not supporting any of his/her body weight. During the weight-bearing condition, we estimated that at a tilt of 60° the subject was bearing 86.6% of his/her body weight. 2.3. Experimental procedures There were three different stimulus conditions (soleus H-reflex alone ‘test’, common peroneal nerve conditioning, and femoral nerve conditioning) and three different weight conditions (supine ‘control’, tilted to 60° and non-weight bearing, and tilted to 60° and weight bearing). For all three of the weight conditions, subjects experienced all three of the stimulus conditions, 10 trials for each conditioning stimulus. The test H-reflexes were interleaved with the conditioning stimuli so that prior to one conditioning stimulus there were a minimum of three test H-reflexes at the appropriate stimulation intensity. This is a necessary control due to the nonlinearity of the H-reflex recruitment curve (Crone et al., 1990). The presentation order of stimulus condition and weight condition was counterbalanced across all subjects. All stimuli were presented randomly with an interstimulus interval no shorter than 9 s. Between each of the weight conditions subjects were returned to a supine position and given short breaks. Upon return to the exper-
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iment, all electrodes were rechecked for placement and appropriate response. If the subject needed a break in the middle of a tilted condition, the M-max was rechecked upon returning to the experiment. These breaks were both for subject comfort and so that spinal circuits did not habituate to repeated stimulation. For each of the tilted weight conditions, subjects were brought to a tilted position and then allowed a minute to adjust before testing commenced. In this way, we were confident that the tilt was a measure of static otolithic drive and not due to effects of tilt translation. In order to ensure that our current experimental paradigm was producing the same effect of tilt on the H-reflex as has been demonstrated by others (Knikou and Rymer, 2003; Aiello et al., 1983), we elicited 5 H-reflexes that were conditioned solely by tilt in a subset of subjects. To collect these ‘unconditioned’ H-reflex responses, we set the stimulus intensity to evoke 15% of the Mmax in a supine position and then tilted the subject to 60°, waited a minute, and delivered five stimulations without further adjusting the stimulus intensity. Once these ‘unconditioned’ reflexes were collected, the M-max for the given condition was established and the stimulation intensity was adjusted so that the test H-reflex for the presynaptic conditioning was at 15% of M-max for that condition. 2.4. Conditioning protocols We estimated the amount of presynaptic inhibition (PI) to the soleus Ia fibers in all weight conditions with two independent PI protocols: (1) common peroneal head conditioning and (2) femoral nerve conditioning. In order to evoke PI via the common peroneal nerve conditioning paradigm, an electrical stimulation of the common peroneal nerve at 1.2 times the tibialis anterior motor threshold was elicited 100 ms prior to the soleus H-reflex (Nielsen and Kagamihara, 1993). To evoke PI via the femoral nerve paradigm, an electrical stimulation of the femoral nerve at 1.2 times quadriceps motor threshold was applied 5–7 ms after the soleus H-reflex (Hultborn et al., 1987b). The conditioning stimulus to the femoral nerve was incrementally adjusted in 0.5 ms intervals to assess the initial point of facilitation, rigorously adhering to the methods proposed by Hultborn and colleagues (Hultborn et al., 1987a, 1987b). 2.5. Data analysis Offline, EMG signals were analyzed in Matlab (7.12.0, R2011a student version) using a code written by the author. Signals were segmented into individual trials and bandpass filtered (20– 450 Hz). Background EMG of the soleus muscle was detrended and a root mean square (RMS) value was obtained; for the Hreflex a peak-to-peak value was obtained. Trials were categorized based on the stimulation condition. The soleus background EMG data and the H-reflex (normalized by subject’s M-max for that condition) data for each condition were averaged for statistical analysis.
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In order to ensure that changes in our primary dependent variable were not due to changes in background muscle activity, a separate 3 3 repeated measures ANOVA was conducted on the RMS EMG data, after testing for normality, with an a = 0.05. Finally, to validate that tilt was producing a change in the soleus motor pool, a paired t-test was performed between the unconditioned H-reflex for both weight conditions and the test H-reflex prior to tilt. 3. Results 3.1. Subjects Of the 20 subjects consented, three subjects did not tolerate peripheral nerve stimulation and withdrew from the study. Additionally, one subject was excluded due to an abnormal M-Max causing concerns about subject comfort and safety. Therefore, data from 16 subjects were analyzed and included in this report. Participant ages ranged from 18–32 years (mean 23.0 ± 4.1 years). The range of optimal latency for femoral nerve stimulation in our subjects was between 4–8.5 ms (mean 6.19 ± 1.28 ms). 3.2. Effect of body tilt on soleus H-reflex The ‘unconditioned’ H-reflex response to tilt was evaluated in 13 subjects, in both weight conditions. Paired t-tests demonstrated no significant differences between the unconditioned H-reflex for either weight condition and no significant differences between the test H-reflexes so the results for both conditions were pooled. The pooled mean for the test H-reflex was 14.82% of M-Max (±1.1%) whereas the pooled mean for the unconditioned H-reflex was 41.87% of M-max (±5.5%). Paired t-test showed a significant difference (t (25) = 6.178, p < 0.001) between the unconditioned H-reflex and the supine H-reflex. These results are depicted in Fig. 1. 3.3. Background EMG and unconditioned H-reflex To ensure that the H-reflex measurements were not affected by background soleus muscle activity, we analyzed background EMG data, to reveal no significant differences for any conditions (see Fig. 2). As a result, PI protocols in the different body tilt and weight-bearing conditions were unaffected by changes in background muscle activation between the conditions. 3.4. Determination of PI influence on the soleus motor pool The influence of both the femoral pathway (facilitation) and common peroneal pathway (inhibition) to the soleus motor pool was initially assessed in the supine body position. Stimulation of the common peroneal nerve produced a 60% inhibition to the motor pool whereas the femoral nerve stimulation produced a 31% facilitation to the motor pool. These effects are depicted in Fig. 3.
2.6. Statistical analysis 3.5. H-reflex response to presynaptic conditioning and weight bearing All statistics were computed using SPSS (IBM SPSS Statistics for Windows, version 21.0). The dependent variable was the peak-topeak amplitude of the soleus H-reflex. The overall research design was a 3 3 (stimulus conditioning x weight bearing) repeated measures paradigm. A repeated measures ANOVA was used to compare the dependent variable of the H-reflex amplitude across all conditions with an a = 0.05. Variables were tested for normality and outliers were removed from the analysis (n = 1). When appropriate, post hoc pairwise comparisons with Bonferroni corrections were used.
The omnibus repeated measures ANOVA of the H-reflex revealed a significant stimulus by weight interaction (F(4,60) = 3.479, p = 0.013). Specifically, the change in PI influence from the supine position was examined. For the common peroneal nerve inhibition, there was 15.1% more inhibition from this pathway in the non-body-weight tilt 60° tilt position compared to supine, and 46.7% less inhibition from this pathway in the bodyweight 60° tilt position compared to supine (Fig. 4, left panel). For the femoral pathway, which produced facilitation to the soleus
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Unconditioned H-reflex
*
50%
Percent of M-max
45% 40% 35% 30% 25% 20%
Supine
15%
Tilted
10% 5% 0% Supine
Tilted
Weight Condition Fig. 1. Shows the H-reflex conditioned by tilt alone in both weight-bearing and non-weight bearing conditions.
RMS of background EMG, in mV
Background EMG 0.014 0.012 0.01
Test
0.008
CPN Conditioned
0.006
FEM conditioned
0.004 0.002 0 Supine
NWB
WB
Fig. 2. The background RMS of EMG grand averages (±SEM) for all stimulus and weight conditions.
Fig. 3. The percent change of the H-reflex in the supine condition, for each of the pathways.
motor pool in supine, there was less influence to the soleus motor pool when tilted: there was 2.2% less facilitation in the non-bodyweight 60° tilt position compared to supine, which was nearly
identical (2.6% less facilitation compared to supine) to the bodyweight 60° tilt position (Fig 4, right panel).
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Fig. 4. The percent change of the H-reflex for each presynaptic pathway in each of the tilted weight-bearing conditions.
4. Discussion These results reveal a differential pattern of response for the two PI pathways in different weight conditions. Whereas both presynaptic conditioning paradigms influenced the soleus Hreflex pathway as expected when in the supine position (common peroneal nerve inhibiting the soleus H-reflex and femoral nerve facilitating the soleus H-reflex), this influence was not the same during static tilt at 60°. In all weight-bearing conditions (i.e., supine, tilted weight bearing and tilted non-weight bearing), we saw a significant inhibition of the test H-reflex following common peroneal nerve stimulation. However, this inhibition was different for the non-weight bearing conditions. Whereas the amount of PI in each of the tilted conditions was not significantly different from PI during the supine (control) condition, the amount of PI across the two tilted weight conditions was significantly different; while neither weight nor tilt alone altered the amount of inhibition from the common peroneal nerve pathway to the soleus motor pool, the interaction of these two factors did significantly affect the amount of inhibition to the soleus motor pool within the common peroneal nerve pathway. In contrast to common peroneal nerve stimulation, there was a significant facilitation following femoral nerve stimulation but only in the supine (control) condition. Post-hoc analyses revealed that the femoral nerve stimulation condition was significantly different between the supine and weight bearing condition, with the least amount of facilitation in the weight bearing condition. The loss of this facilitation during the tilted conditions indicates that PI was present, despite femoral nerve stimulation. This would suggest that the PI from second-order PAD interneurons was stronger than the excitation from quadriceps Ia afferent fibers. This could either be due to increased inhibition from the second-order PAD interneuron, or due to reduced facilitation of the quadriceps Ia afferent during tilt. We theorized that changes in the common peroneal nerve pathway without changes in the femoral nerve pathway would likely reflect a greater otolithic influence on first-order PAD interneurons. Conversely, a change in the femoral nerve pathway without changes in the common peroneal pathway would likely reflect a greater otolithic influence on 2nd order PAD interneurons. The current results suggest that the common peroneal nerve pathway is more influenced by changes in otolithic drive than the femoral
nerve pathway, suggesting that the otolithic input is influencing the first-order PAD interneurons to a greater degree than secondorder PAD interneurons. However, it is entirely plausible that there are mechanisms unaccounted for that are also affecting the observed influence on the soleus Ia afferent fibers. For example, it is possible that the spinal pathways carrying otolithic input synapse directly on the alpha motoneurons of these different muscle groups, but if that were the case, it would not seem logical that two independent presynaptic mechanisms would also be involved. It is also possible that the effect seen in this study was due to interactions between these pathways and other mechanisms that also exist within the spinal cord. These other mechanisms include interneurons which convey information from other spinal levels, information from the same spinal level but the contralateral spinal tract, information from somatic receptors (such as the autonomic nervous system), and/or information from other spinal tracts (such as the corticospinal, tectospinal, cerebellospinal, or cerebrospinal tract). The use of a harness to create the non-weight bearing condition may have resulted in somatic signals related to autonomic function (increases in sympathetic output), and/or somatic signals related to pressure of the straps against the body. However, if this were the case it is our expectation that we would see effects in all non-weight bearing conditions. Instead we saw differences in the common peroneal nerve pathway suggesting that non-weight bearing was different from weight-bearing while we saw no difference in the femoral nerve pathway between the non-weight and weight bearing conditions. Therefore, we are interpreting our results to be more related to interactions between otolithic inputs and somatosensory inputs related to changes in weight. We also did not control for the angle of the head against the tilt table, which could have created different effects of cervical involvement, based upon the size and anatomy of the subject, and also theoretically could influence the amount of ‘otolithic load’ each subject experienced. Finally, it is possible that other higher-level processes, such as expectation and or attention, are influencing the results (Ikai et al., 1996). We minimized these factors in this study through counterbalancing the conditions, blindfolding the subjects, asking subjects to maintain a neutral and comfortable head position, utilizing an air cast to limit stretch of the soleus, and repeatedly checking the placement of the electrodes. Our findings of increased spinal excitability in response to otolithic stimulation are consistent with responses seen in other stud-
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ies (Greenwood and Hopkins, 1976; Taube et al., 2008; Knikou and Rymer, 2003; Aiello et al., 1983). Further, our results demonstrated that the measured soleus H-reflex was different for the weight bearing and non-weight bearing conditions in both of the presynaptic pathways examined, with the greatest inhibition in the common fibular pathway during non-weight bearing and the greatest inhibition of the femoral nerve pathway during weightbearing. This finding, especially in the common fibular nerve pathway, appears consistent with the findings of Rudomin et al., 1986 wherein vestibular responses were modified by cutaneous stimulation. Because weight bearing will activate some of these cutaneous receptors, the modulation that we observed seems consistent with this notion. Additionally, our results corroborate previous findings of differential vestibular input depending on muscle and task (Dakin et al., 2013; Bent et al., 2004; Cenciarini and Peterka, 2006). Whereas the current study investigated PI pathways, there are also postsynaptic pathways that likely also receive vestibular input (Iles and Pisini, 1992; Raffensperger and York, 1984; Rossi et al., 1987). Based on these previous studies and the results from our current study, a logical next step would be investigation of postsynaptic pathways within subjects who are weight-bearing and non-weight bearing. Another logical and important future direction would be the investigation of the H-reflex and spinal pathways in subjects with vestibular dysfunction. Ideally, this mechanistic understanding will translate to improved assessment techniques and evidence-based treatment approaches (Herdman, 2013). Conflict of interest The authors have no conflicts of interest. Financial disclosure statement The authors have nothing to disclose. Funding acknowledgement This project was supported by an NIH Training Grant: NIDCD T32 DC000012-34 (David Pisoni). Acknowledgements The authors would like to acknowledge and thank J. Tim Inglis, Koichi Kitano, Rachel Ryder, Najmeh Hoseini, Karen Forrest, Larry Humes, and Jeffrey Alberts for their contributions to the current study. References Aiello, I., Rosati, G., Serra, G., Tugnoli, V., Manca, M., 1983. Static vestibulospinal influences in relation to different body tilts in man. Exp. Neurol. 79, 18–26. Barra, J., Bray, A., Sahni, V., Golding, J.F., Gresty, M.A., 2006. Increasing cognitive load with increasing balance challenge: recipe for catastrophe. Exp. Brain Res. 174, 734–745. Epub 2006/05/25. Bent, L.R., McFadyen, B.J., Inglis, J.T., 2002. Visual-vestibular interactions in postural control during the execution of a dynamic task. Exp. Brain Res. 146, 490–500. Epub 2002/10/02. Bent, L.R., Inglis, J.T., McFadyen, B.J., 2004. When is vestibular information important during walking? J. Neurophysiol. 92, 1269–1275. Bernard-Demanze, L., Dumitrescu, M., Jimeno, P., Borel, L., Lacour, M., 2009. Agerelated changes in posture control are differentially affected by postural and cognitive task complexity. Curr. Aging Sci. 2, 139–149. Epub 2009/12/22. Bove, M., Trompetto, C., Abbruzzese, G., Schieppati, M., 2006. The posture-related interaction between Ia-afferent and descending input on the spinal reflex excitability in humans. Neurosci. Lett. 397, 301–306. Epub 2006/01/24. Carriot, J., Jamali, M., Cullen, K.E., 2015. Rapid adaptation of multisensory integration in vestibular pathways. Front. Syst. Neurosci. 9, 59.
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The effect of different descending systems on flexor and extensor activity during locomotion. Brain Res. 40, 359–371. Epub 1972/05/26. Peterka, R.J., Statler, K.D., Wrisley, D.M., Horak, F.B., 2011. Postural compensation for unilateral vestibular loss. Front. Neurol. 2, 57. Epub 2011/09/17. Raffensperger, M., York, D.H., 1984. Caloric stimulation-induced augmentation of Hreflexes in normal subjects, but not in spinal cord-injured patients. Neurosurgery 14, 562–566. Epub 1984/05/01. Rossi, A., Mazzocchio, R., Scarpini, C., 1987. Evidence for Renshaw cell-motoneuron decoupling during tonic vestibular stimulation in man. Exp. Neurol. 98, 1–12. Epub 1987/10/01.
A. Fox, D. Koceja / Journal of Electromyography and Kinesiology 32 (2017) 37–43 Rudomin, P., Solodkin, M., Jimenez, I., 1986. PAD and PAH response patterns of group Ia- and Ib-fibers to cutaneous and descending inputs in the cat spinal cord. J. Neurophysiol. 56, 987–1006. Epub 1986/10/01. Shinya, M., Kawashima, N., Nakazawa, K., 2016. Temporal, but not directional, prior knowledge shortens muscle reflex latency in response to sudden transition of support surface during walking. Front. Human Neurosci. 10, 29. Taube, W., Leukel, C., Schubert, M., Gruber, M., Rantalainen, T., Gollhofer, A., 2008. Differential modulation of spinal and corticospinal excitability during drop jumps. J. Neurophysiol. 99, 1243–1252. Watt, D.G., 1981a. Effect of vertical linear acceleration on H-reflex in decerebrate cat. II. Sinusoidal stimuli. J. Neurophysiol. 45, 656–666. Epub 1981/04/01. Watt, D.G., 1981b. Effect of vertical linear acceleration on H-reflex in decerebrate cat. I. Transient stimuli. J. Neurophysiol. 45, 644–655. Epub 1981/04/01. Apollonia Fox, PhD. The current clinical approach to assessing vestibular disorders is costly, time-intensive, and uncomfortable for patients. Furthermore, the nuanced assessment does not consistently contribute to the treatment outcomes of patients.
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In complex disorders this is even more the case. Therefore, my personal career goal is to contribute to a better understanding of how the vestibular system interacts with and influences other systems within the body, as well as how plasticity within each of these systems is affected by vestibular health. I will utilize the tools I have been developing in my multi-disciplinary training over the past eight years across the fields of audiology, motor control, neuroscience, and human physiology, with a goal of helping to improve the clinical assessment and outcomes for dizzy patients. David Koceja, PhD. My research interests focus on the neuromuscular control of human movement. I am currently investigating the role of the spinal reflex system in controlling normal postural sway and recovery from perturbations in elderly subjects. Our mission is to motivate older adults to lead more active lives and enjoy better balance and health. We work in partnership with a number of groups to share the results of this research with elderly citizens in our community and with health and wellness practitioners.
Contents lists available at ScienceDirect
Journal of Electromyography and Kinesiology journal homepage: www.elsevier.com/locate/jelekin
Static otolithic drive alters presynaptic inhibition in soleus motor pool Apollonia Fox ⇑, David Koceja Indiana University, 1025 E. 7th St, Bloomington, IN 47405, United States
a r t i c l e
i n f o
Article history: Received 18 July 2016 Received in revised form 4 November 2016 Accepted 15 December 2016
Keywords: H-reflex Vestibulospinal Otolith Presynaptic inhibition
a b s t r a c t The vestibular system has both direct and indirect connections to the soleus motor pool via the vestibulospinal and reticulospinal tracts. The exact nature of how this vestibular information is integrated within the spinal cord is largely unknown. The purpose of this study was to identify whether changes in static otolithic drive altered the amount of presynaptic inhibition in the soleus H-reflex pathway. Changes in static otolithic drive were investigated in sixteen healthy participants using a tilt table. Two presynaptic pathways (common peroneal and femoral) to the soleus H-reflex were tested in three weight conditions (supine, non-weight bearing, and weight bearing). The dependent variable was the peak-to-peak amplitude of the soleus H-reflex. Inhibition to the soleus motor pool through the common peroneal nerve pathway differed significantly during weight conditions and tilt. During tilt and non-weight bearing there was greater inhibition of the soleus H-reflex compared to supine, however, this effect was reversed during tilt and weight bearing. Facilitation from the femoral nerve pathway was reduced by tilt compared to supine, but this reduction was unaffected by weight condition. This supports a role of the vestibular system as providing complex, task-dependent presynaptic input to motoneurons in the lower limbs. Published by Elsevier Ltd.
1. Introduction The vestibular system relates the position of the head in space relative to gravity and plays an integral role in maintaining balance and supporting posture (Nashner, 1971). Whereas the semicircular ducts have been implicated in alerting a person to potential falls (Nashner, 1971), the otolithic organs may have an important role for conveying ongoing information about the body with respect to gravity and may be more relevant to postural regulation (Watt, 1981a, 1981b; Greenwood and Hopkins, 1976; Lacour et al., 1978). Otolithic information is transmitted to all levels of the body primarily via the vestibulospinal and reticulospinal tracts (NybergHansen, 1965; Nyberg-Hansen and Mascitti, 1964). The information conveyed by these two tracts is organized reciprocally and is functionally coupled, so that different muscles will receive different, complementary, information from each tract about the position of the head relative to gravity (Orlovsky, 1972; Grillner et al., 1968). Recent research further demonstrates that this coupled, reciprocal patterning of information in the lower limbs is
⇑ Corresponding author at: War Related Illness and Injury Study Center, VA New Jersey Health Care Center, 385 Tremont Avenue, East Orange, NJ 07018, United States. E-mail address: [email protected] (A. Fox). http://dx.doi.org/10.1016/j.jelekin.2016.12.002 1050-6411/Published by Elsevier Ltd.
both muscle and task dependent (Dakin et al., 2013; Bent et al., 2004, 2002). There has been much investigation examining the various factors responsible for appropriate regulation of posture and dynamic maintenance of balance. The picture painted by these studies demonstrates that postural regulation is a task dependent on many factors, from somatosensory inputs (Bove et al., 2006; Inglis et al., 1994; Horak, 2006; Inglis and Macpherson, 1995) and cortical inputs (Barra et al., 2006; Bernard-Demanze et al., 2009; Shinya et al., 2016; Taube et al., 2008), to vestibular inputs (Peterka et al., 2011; Horak, 2009) and each of these factors is relatively weighted in its effect on the postural system (Dichgans and Diener, 1989; Fetter et al., 1990; Horak et al., 1990; Carriot et al., 2015). Vestibular inputs are integrated with and weighted against all of these other inputs for the dynamic modulation of postural responses. Interestingly, however, while these other factors affect long-latency postural responses, vestibular inputs also affect short-latency postural responses like the H-reflex (Kennedy and Inglis, 2001). Vestibular input to short-latency postural responses and the H-reflex have been demonstrated in both dynamic (Greenwood and Hopkins, 1976; Taube et al., 2008; Knikou and Rymer, 2003) environments where a drop or a tilt is initiated and also static environments (Knikou and Rymer, 2003; Aiello et al., 1983) where a tilt is sustained. However, the mechanism of vestibular integration within the spinal networks remains unknown. Several authors have posited that this integration hap-
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pens presynaptically (Kennedy and Inglis, 2001; Knikou and Rymer, 2003; Iles and Pisini, 1992). Gaining insight into these mechanisms could potentially lead to a deeper understanding of how specific vestibular disorders affect postural networks within the spinal cord. The soleus motor pool has long been studied for its relevance to postural regulation. Two well-defined presynaptic pathways to the soleus motor pool include common peroneal nerve conditioning and femoral nerve conditioning. For a full understanding of these pathways, please refer to Hultborn and colleagues (Hultborn et al., 1987a, 1987b; Morin et al., 1984). Based on the anatomy alone, the vestibular system could potentially affect the soleus motor pool presynaptically through the motor neurons directly, Ia afferent fibers, first-order primary afferent depolarization (PAD) interneurons, and/or second-order PAD interneurons (Nyberg-Hansen, 1965; Nyberg-Hansen and Mascitti, 1964). Recognizing the relationship between vestibular and somatosensory inputs, and coupled with the fact that weight-bearing has been shown to down-regulate the soleus Hreflex in humans (Koceja et al., 1993) we also sought to examine how the vestibular system interacts with weight-bearing mechanisms to more fully understand the complexities of vestibular input to spinal networks. The purpose of this study was to examine the role of the vestibular pathways in mediating soleus motoneuron excitability in both a weight-bearing and a non-weightbearing condition. 2. Materials and methods Twenty healthy subjects (14 female) between the ages of 18– 35 years participated in this study. Subjects were excluded for self-report of known neurological disorder, balance disorder, and/ or participation in high levels of physical activity. Prior to participation, all subjects read and signed an Informed Consent Form in accordance with the Declaration of Helsinki and approved by the Human Subjects Committee of Indiana University. Surface EMG was collected after preparing the skin with alcohol, using Ag electrodes (Delsys, Bagnoli 16) configured in a parallel array with 1-cm spacing and their output was pre-amplified with a gain of 1000. The electrodes were placed on the subject’s right leg, parallel to muscle fibers, over the soleus, medial and lateral gastrocnemius, tibialis anterior, and rectus femoris muscles. Signals were monitored, using an online oscilloscope (Tektronix, Model TDS 3012), throughout the experiment to ensure appropriateness of EMG recording. 2.1. H-reflex procedures Percutaneous electrical stimulation was used (GRASS S88D stimulator) to stimulate the appropriate mixed nerve and elicit the H-reflex or the conditioning stimulation. All H-reflex and conditioning stimuli were delivered using a 1 ms square-wave pulse (GRASS, S88stimulator), and monitored online using an oscilloscope (Tektronix, Model TDS 3012), according to standard lab procedures (Hugon, 1973). Briefly, the ideal testing site for the soleus H-reflex was determined by holding the electrode over the popliteal fossa while very slowly increasing the intensity delivered to the subject until the H-reflex appeared on the oscilloscope, in the absence of an M-wave. Once the intensity was high enough to evoke a small H-reflex, the experimenter slightly shifted the position of the electrode within the popliteal fossa to find a location where the largest measureable H-reflex existed at the same intensity of stimulation. Once this optimal location within the popliteal fossa was found, it was marked and the electrode was secured in that position. After the electrode was fully secure, it was doublechecked to be sure that an H-reflex equivalent to the earlier size
was still present, yet there was no M-wave present. The same overall procedure was repeated for the common peroneal nerve stimulation, with the electrode placed at the head of the fibula, and the femoral nerve, with the electrode placed in the inguinal crease. Optimal placement of the electrodes was periodically checked throughout the experiment to ensure that there was no movement of the electrodes over the course of the experiment. A soft ankle splint was placed on the subjects’ feet, fixing the angle of the ankle to 90° so that changes in muscle length due to ankle angle did not confound the results. Furthermore, subjects wore a blindfold in all of the conditions, to prevent any visual cues that may have influenced the soleus H-reflex. Finally, the subject was asked to keep their head in a neutral and comfortable position, resting against the tilt table, for the duration of the testing. This head position was visually monitored by the experimenter throughout the testing. All data were recorded on a laboratory computer (Optiplex GX280, Dell Computer Corporation) using custom data acquisition software (AcqKnowledge, version 3.7.3, BioPAC systems Inc.), sampled at 2000 Hz, and stored for offline analysis. Once all electrodes, ankle splint, harness, and blindfold were secured, the subject was asked to lay supine, eyes closed, on the tilt table and M-max of the soleus muscle was determined by slowly increasing the stimulation intensity until the M-wave saturated. Once the M-max value was determined, all further data were obtained by setting the stimulation intensity at an amplitude sufficient to elicit the soleus H-reflex at 15% of M-max. Because the soleus H-reflex was the dependent variable, only M-max of the soleus muscle was obtained. While, theoretically, M-max should be the same across all conditions (McNulty et al., 2012), in our experience M-max has been seen to shift slightly in the same subject over time or in different conditions. This instability has also been documented by others (McNulty et al., 2012). Therefore, Mmax was determined for each subject independently in the three weight conditions (supine, non-weight bearing, and weight bearing) and the H-reflex amplitude for each of the three weight conditions was set at 15% of the M-max for that individual condition. 2.2. Tilt table procedures The clinically-approved tilt table (Tri W-G, model TW6131.HD) moved at a constant slow speed of 4.3°/s (equivalent to 0.01 Hz). During the non-weight bearing condition, a harness assured that as the table angle changed the subject was not supporting any of his/her body weight. During the weight-bearing condition, we estimated that at a tilt of 60° the subject was bearing 86.6% of his/her body weight. 2.3. Experimental procedures There were three different stimulus conditions (soleus H-reflex alone ‘test’, common peroneal nerve conditioning, and femoral nerve conditioning) and three different weight conditions (supine ‘control’, tilted to 60° and non-weight bearing, and tilted to 60° and weight bearing). For all three of the weight conditions, subjects experienced all three of the stimulus conditions, 10 trials for each conditioning stimulus. The test H-reflexes were interleaved with the conditioning stimuli so that prior to one conditioning stimulus there were a minimum of three test H-reflexes at the appropriate stimulation intensity. This is a necessary control due to the nonlinearity of the H-reflex recruitment curve (Crone et al., 1990). The presentation order of stimulus condition and weight condition was counterbalanced across all subjects. All stimuli were presented randomly with an interstimulus interval no shorter than 9 s. Between each of the weight conditions subjects were returned to a supine position and given short breaks. Upon return to the exper-
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iment, all electrodes were rechecked for placement and appropriate response. If the subject needed a break in the middle of a tilted condition, the M-max was rechecked upon returning to the experiment. These breaks were both for subject comfort and so that spinal circuits did not habituate to repeated stimulation. For each of the tilted weight conditions, subjects were brought to a tilted position and then allowed a minute to adjust before testing commenced. In this way, we were confident that the tilt was a measure of static otolithic drive and not due to effects of tilt translation. In order to ensure that our current experimental paradigm was producing the same effect of tilt on the H-reflex as has been demonstrated by others (Knikou and Rymer, 2003; Aiello et al., 1983), we elicited 5 H-reflexes that were conditioned solely by tilt in a subset of subjects. To collect these ‘unconditioned’ H-reflex responses, we set the stimulus intensity to evoke 15% of the Mmax in a supine position and then tilted the subject to 60°, waited a minute, and delivered five stimulations without further adjusting the stimulus intensity. Once these ‘unconditioned’ reflexes were collected, the M-max for the given condition was established and the stimulation intensity was adjusted so that the test H-reflex for the presynaptic conditioning was at 15% of M-max for that condition. 2.4. Conditioning protocols We estimated the amount of presynaptic inhibition (PI) to the soleus Ia fibers in all weight conditions with two independent PI protocols: (1) common peroneal head conditioning and (2) femoral nerve conditioning. In order to evoke PI via the common peroneal nerve conditioning paradigm, an electrical stimulation of the common peroneal nerve at 1.2 times the tibialis anterior motor threshold was elicited 100 ms prior to the soleus H-reflex (Nielsen and Kagamihara, 1993). To evoke PI via the femoral nerve paradigm, an electrical stimulation of the femoral nerve at 1.2 times quadriceps motor threshold was applied 5–7 ms after the soleus H-reflex (Hultborn et al., 1987b). The conditioning stimulus to the femoral nerve was incrementally adjusted in 0.5 ms intervals to assess the initial point of facilitation, rigorously adhering to the methods proposed by Hultborn and colleagues (Hultborn et al., 1987a, 1987b). 2.5. Data analysis Offline, EMG signals were analyzed in Matlab (7.12.0, R2011a student version) using a code written by the author. Signals were segmented into individual trials and bandpass filtered (20– 450 Hz). Background EMG of the soleus muscle was detrended and a root mean square (RMS) value was obtained; for the Hreflex a peak-to-peak value was obtained. Trials were categorized based on the stimulation condition. The soleus background EMG data and the H-reflex (normalized by subject’s M-max for that condition) data for each condition were averaged for statistical analysis.
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In order to ensure that changes in our primary dependent variable were not due to changes in background muscle activity, a separate 3 3 repeated measures ANOVA was conducted on the RMS EMG data, after testing for normality, with an a = 0.05. Finally, to validate that tilt was producing a change in the soleus motor pool, a paired t-test was performed between the unconditioned H-reflex for both weight conditions and the test H-reflex prior to tilt. 3. Results 3.1. Subjects Of the 20 subjects consented, three subjects did not tolerate peripheral nerve stimulation and withdrew from the study. Additionally, one subject was excluded due to an abnormal M-Max causing concerns about subject comfort and safety. Therefore, data from 16 subjects were analyzed and included in this report. Participant ages ranged from 18–32 years (mean 23.0 ± 4.1 years). The range of optimal latency for femoral nerve stimulation in our subjects was between 4–8.5 ms (mean 6.19 ± 1.28 ms). 3.2. Effect of body tilt on soleus H-reflex The ‘unconditioned’ H-reflex response to tilt was evaluated in 13 subjects, in both weight conditions. Paired t-tests demonstrated no significant differences between the unconditioned H-reflex for either weight condition and no significant differences between the test H-reflexes so the results for both conditions were pooled. The pooled mean for the test H-reflex was 14.82% of M-Max (±1.1%) whereas the pooled mean for the unconditioned H-reflex was 41.87% of M-max (±5.5%). Paired t-test showed a significant difference (t (25) = 6.178, p < 0.001) between the unconditioned H-reflex and the supine H-reflex. These results are depicted in Fig. 1. 3.3. Background EMG and unconditioned H-reflex To ensure that the H-reflex measurements were not affected by background soleus muscle activity, we analyzed background EMG data, to reveal no significant differences for any conditions (see Fig. 2). As a result, PI protocols in the different body tilt and weight-bearing conditions were unaffected by changes in background muscle activation between the conditions. 3.4. Determination of PI influence on the soleus motor pool The influence of both the femoral pathway (facilitation) and common peroneal pathway (inhibition) to the soleus motor pool was initially assessed in the supine body position. Stimulation of the common peroneal nerve produced a 60% inhibition to the motor pool whereas the femoral nerve stimulation produced a 31% facilitation to the motor pool. These effects are depicted in Fig. 3.
2.6. Statistical analysis 3.5. H-reflex response to presynaptic conditioning and weight bearing All statistics were computed using SPSS (IBM SPSS Statistics for Windows, version 21.0). The dependent variable was the peak-topeak amplitude of the soleus H-reflex. The overall research design was a 3 3 (stimulus conditioning x weight bearing) repeated measures paradigm. A repeated measures ANOVA was used to compare the dependent variable of the H-reflex amplitude across all conditions with an a = 0.05. Variables were tested for normality and outliers were removed from the analysis (n = 1). When appropriate, post hoc pairwise comparisons with Bonferroni corrections were used.
The omnibus repeated measures ANOVA of the H-reflex revealed a significant stimulus by weight interaction (F(4,60) = 3.479, p = 0.013). Specifically, the change in PI influence from the supine position was examined. For the common peroneal nerve inhibition, there was 15.1% more inhibition from this pathway in the non-body-weight tilt 60° tilt position compared to supine, and 46.7% less inhibition from this pathway in the bodyweight 60° tilt position compared to supine (Fig. 4, left panel). For the femoral pathway, which produced facilitation to the soleus
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Unconditioned H-reflex
*
50%
Percent of M-max
45% 40% 35% 30% 25% 20%
Supine
15%
Tilted
10% 5% 0% Supine
Tilted
Weight Condition Fig. 1. Shows the H-reflex conditioned by tilt alone in both weight-bearing and non-weight bearing conditions.
RMS of background EMG, in mV
Background EMG 0.014 0.012 0.01
Test
0.008
CPN Conditioned
0.006
FEM conditioned
0.004 0.002 0 Supine
NWB
WB
Fig. 2. The background RMS of EMG grand averages (±SEM) for all stimulus and weight conditions.
Fig. 3. The percent change of the H-reflex in the supine condition, for each of the pathways.
motor pool in supine, there was less influence to the soleus motor pool when tilted: there was 2.2% less facilitation in the non-bodyweight 60° tilt position compared to supine, which was nearly
identical (2.6% less facilitation compared to supine) to the bodyweight 60° tilt position (Fig 4, right panel).
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Fig. 4. The percent change of the H-reflex for each presynaptic pathway in each of the tilted weight-bearing conditions.
4. Discussion These results reveal a differential pattern of response for the two PI pathways in different weight conditions. Whereas both presynaptic conditioning paradigms influenced the soleus Hreflex pathway as expected when in the supine position (common peroneal nerve inhibiting the soleus H-reflex and femoral nerve facilitating the soleus H-reflex), this influence was not the same during static tilt at 60°. In all weight-bearing conditions (i.e., supine, tilted weight bearing and tilted non-weight bearing), we saw a significant inhibition of the test H-reflex following common peroneal nerve stimulation. However, this inhibition was different for the non-weight bearing conditions. Whereas the amount of PI in each of the tilted conditions was not significantly different from PI during the supine (control) condition, the amount of PI across the two tilted weight conditions was significantly different; while neither weight nor tilt alone altered the amount of inhibition from the common peroneal nerve pathway to the soleus motor pool, the interaction of these two factors did significantly affect the amount of inhibition to the soleus motor pool within the common peroneal nerve pathway. In contrast to common peroneal nerve stimulation, there was a significant facilitation following femoral nerve stimulation but only in the supine (control) condition. Post-hoc analyses revealed that the femoral nerve stimulation condition was significantly different between the supine and weight bearing condition, with the least amount of facilitation in the weight bearing condition. The loss of this facilitation during the tilted conditions indicates that PI was present, despite femoral nerve stimulation. This would suggest that the PI from second-order PAD interneurons was stronger than the excitation from quadriceps Ia afferent fibers. This could either be due to increased inhibition from the second-order PAD interneuron, or due to reduced facilitation of the quadriceps Ia afferent during tilt. We theorized that changes in the common peroneal nerve pathway without changes in the femoral nerve pathway would likely reflect a greater otolithic influence on first-order PAD interneurons. Conversely, a change in the femoral nerve pathway without changes in the common peroneal pathway would likely reflect a greater otolithic influence on 2nd order PAD interneurons. The current results suggest that the common peroneal nerve pathway is more influenced by changes in otolithic drive than the femoral
nerve pathway, suggesting that the otolithic input is influencing the first-order PAD interneurons to a greater degree than secondorder PAD interneurons. However, it is entirely plausible that there are mechanisms unaccounted for that are also affecting the observed influence on the soleus Ia afferent fibers. For example, it is possible that the spinal pathways carrying otolithic input synapse directly on the alpha motoneurons of these different muscle groups, but if that were the case, it would not seem logical that two independent presynaptic mechanisms would also be involved. It is also possible that the effect seen in this study was due to interactions between these pathways and other mechanisms that also exist within the spinal cord. These other mechanisms include interneurons which convey information from other spinal levels, information from the same spinal level but the contralateral spinal tract, information from somatic receptors (such as the autonomic nervous system), and/or information from other spinal tracts (such as the corticospinal, tectospinal, cerebellospinal, or cerebrospinal tract). The use of a harness to create the non-weight bearing condition may have resulted in somatic signals related to autonomic function (increases in sympathetic output), and/or somatic signals related to pressure of the straps against the body. However, if this were the case it is our expectation that we would see effects in all non-weight bearing conditions. Instead we saw differences in the common peroneal nerve pathway suggesting that non-weight bearing was different from weight-bearing while we saw no difference in the femoral nerve pathway between the non-weight and weight bearing conditions. Therefore, we are interpreting our results to be more related to interactions between otolithic inputs and somatosensory inputs related to changes in weight. We also did not control for the angle of the head against the tilt table, which could have created different effects of cervical involvement, based upon the size and anatomy of the subject, and also theoretically could influence the amount of ‘otolithic load’ each subject experienced. Finally, it is possible that other higher-level processes, such as expectation and or attention, are influencing the results (Ikai et al., 1996). We minimized these factors in this study through counterbalancing the conditions, blindfolding the subjects, asking subjects to maintain a neutral and comfortable head position, utilizing an air cast to limit stretch of the soleus, and repeatedly checking the placement of the electrodes. Our findings of increased spinal excitability in response to otolithic stimulation are consistent with responses seen in other stud-
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ies (Greenwood and Hopkins, 1976; Taube et al., 2008; Knikou and Rymer, 2003; Aiello et al., 1983). Further, our results demonstrated that the measured soleus H-reflex was different for the weight bearing and non-weight bearing conditions in both of the presynaptic pathways examined, with the greatest inhibition in the common fibular pathway during non-weight bearing and the greatest inhibition of the femoral nerve pathway during weightbearing. This finding, especially in the common fibular nerve pathway, appears consistent with the findings of Rudomin et al., 1986 wherein vestibular responses were modified by cutaneous stimulation. Because weight bearing will activate some of these cutaneous receptors, the modulation that we observed seems consistent with this notion. Additionally, our results corroborate previous findings of differential vestibular input depending on muscle and task (Dakin et al., 2013; Bent et al., 2004; Cenciarini and Peterka, 2006). Whereas the current study investigated PI pathways, there are also postsynaptic pathways that likely also receive vestibular input (Iles and Pisini, 1992; Raffensperger and York, 1984; Rossi et al., 1987). Based on these previous studies and the results from our current study, a logical next step would be investigation of postsynaptic pathways within subjects who are weight-bearing and non-weight bearing. Another logical and important future direction would be the investigation of the H-reflex and spinal pathways in subjects with vestibular dysfunction. Ideally, this mechanistic understanding will translate to improved assessment techniques and evidence-based treatment approaches (Herdman, 2013). Conflict of interest The authors have no conflicts of interest. Financial disclosure statement The authors have nothing to disclose. Funding acknowledgement This project was supported by an NIH Training Grant: NIDCD T32 DC000012-34 (David Pisoni). Acknowledgements The authors would like to acknowledge and thank J. Tim Inglis, Koichi Kitano, Rachel Ryder, Najmeh Hoseini, Karen Forrest, Larry Humes, and Jeffrey Alberts for their contributions to the current study. References Aiello, I., Rosati, G., Serra, G., Tugnoli, V., Manca, M., 1983. Static vestibulospinal influences in relation to different body tilts in man. Exp. Neurol. 79, 18–26. Barra, J., Bray, A., Sahni, V., Golding, J.F., Gresty, M.A., 2006. Increasing cognitive load with increasing balance challenge: recipe for catastrophe. Exp. Brain Res. 174, 734–745. Epub 2006/05/25. Bent, L.R., McFadyen, B.J., Inglis, J.T., 2002. Visual-vestibular interactions in postural control during the execution of a dynamic task. Exp. Brain Res. 146, 490–500. Epub 2002/10/02. Bent, L.R., Inglis, J.T., McFadyen, B.J., 2004. When is vestibular information important during walking? J. Neurophysiol. 92, 1269–1275. Bernard-Demanze, L., Dumitrescu, M., Jimeno, P., Borel, L., Lacour, M., 2009. Agerelated changes in posture control are differentially affected by postural and cognitive task complexity. Curr. Aging Sci. 2, 139–149. Epub 2009/12/22. Bove, M., Trompetto, C., Abbruzzese, G., Schieppati, M., 2006. The posture-related interaction between Ia-afferent and descending input on the spinal reflex excitability in humans. Neurosci. Lett. 397, 301–306. Epub 2006/01/24. Carriot, J., Jamali, M., Cullen, K.E., 2015. Rapid adaptation of multisensory integration in vestibular pathways. Front. Syst. Neurosci. 9, 59.
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A. Fox, D. Koceja / Journal of Electromyography and Kinesiology 32 (2017) 37–43 Rudomin, P., Solodkin, M., Jimenez, I., 1986. PAD and PAH response patterns of group Ia- and Ib-fibers to cutaneous and descending inputs in the cat spinal cord. J. Neurophysiol. 56, 987–1006. Epub 1986/10/01. Shinya, M., Kawashima, N., Nakazawa, K., 2016. Temporal, but not directional, prior knowledge shortens muscle reflex latency in response to sudden transition of support surface during walking. Front. Human Neurosci. 10, 29. Taube, W., Leukel, C., Schubert, M., Gruber, M., Rantalainen, T., Gollhofer, A., 2008. Differential modulation of spinal and corticospinal excitability during drop jumps. J. Neurophysiol. 99, 1243–1252. Watt, D.G., 1981a. Effect of vertical linear acceleration on H-reflex in decerebrate cat. II. Sinusoidal stimuli. J. Neurophysiol. 45, 656–666. Epub 1981/04/01. Watt, D.G., 1981b. Effect of vertical linear acceleration on H-reflex in decerebrate cat. I. Transient stimuli. J. Neurophysiol. 45, 644–655. Epub 1981/04/01. Apollonia Fox, PhD. The current clinical approach to assessing vestibular disorders is costly, time-intensive, and uncomfortable for patients. Furthermore, the nuanced assessment does not consistently contribute to the treatment outcomes of patients.
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In complex disorders this is even more the case. Therefore, my personal career goal is to contribute to a better understanding of how the vestibular system interacts with and influences other systems within the body, as well as how plasticity within each of these systems is affected by vestibular health. I will utilize the tools I have been developing in my multi-disciplinary training over the past eight years across the fields of audiology, motor control, neuroscience, and human physiology, with a goal of helping to improve the clinical assessment and outcomes for dizzy patients. David Koceja, PhD. My research interests focus on the neuromuscular control of human movement. I am currently investigating the role of the spinal reflex system in controlling normal postural sway and recovery from perturbations in elderly subjects. Our mission is to motivate older adults to lead more active lives and enjoy better balance and health. We work in partnership with a number of groups to share the results of this research with elderly citizens in our community and with health and wellness practitioners.