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15. COMPUTERIZED DYNAMIC POSTUROGRAPHY: METHODOLOGY AND INTERPRETATIONS 395
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Appendix 15–A
Table 15–A1. Normal Subject Posture-Evoked Response Latencies*
Reference Number of Subjects Short Latency Medium Latency Long Latency
2 10 42.9 ± 3.3 86.6 ± 6.4 128.6 ± 10.1
8 50 43.5 ± 4.2 89.5 ± 10.0 125.3 ± 17.8
21t 26 34 ± 3 86 ± 6 114 ± 16
t and :j: 74 30.0 ± 4.6 73.3 ± 11.2 104.2 ± 17.0
* All studies used 50-deg/s 4-degree toes-up rotations.In these studies, time was determined by the actual platform movement
onset rather than the movement command, reducing latencies by 10 to 15 ms.
Source:
Data provided to NeuroCom International, Inc. by Chris Diener, Universitat Essen, Germany.
Table 15–A2. Mean (+1.67 SO) Latency Scores as Functions of Translation Size, Direction,
Subject Age
and
Population Latency Scores (ms)
20–59 Years
Movement
Medium back 156 (182) 160 (187) 168 (200)
Large back 137 (168) 148 (171) 155 (178)
Medium forward 164 (194) 164 (184) 170 (196)
Large forward 153 (167) 155 (173) 159 (177)
Table 15–A3. Mean (±2 SD) Active Force Strengths as Functions of Translation Direction, Size, and Subject Age*
Movement
Small back 03.4 ± (1.4) 04.1 ± (4.6) 04.2 ± (4.5)
Medium back 07.1 ± (5.8) 07.8 ± (5.5) 07.9 ± (7.0)
Large back 08.7 ± (5.2) 09.9 ± (5.5) 10.4 ± (7.4)
(n = 58)
Population Strength Scores
20–59 Years
(n = 29)
60–69 Years
(n = 54)
60–69 Years
(n = 54)
70–79 Years
(n = 28)
70–79 Years
(n = 28)
Small forward 03.6 ± (3.9) 05.1 ± (4.5) 05.2 ± (4.2)
Medium forward 08.4 ± (4.9) 09.0 ± (5.0) 08.6 ± (4.2)
Large forward 10.0 ± (5.7) 10.1 ± (5.3) 09.7 ± (6.0)
*All values are in units of angular momentum normalized for differences in body mass.
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Table 15–A4. Mean (+1.67 SO) Sway Energy Scores as Functions of Toes-Up and Toes-Down Trial Numbers and Subject Age*
Population Adaptation Scores
20–59 Years
Motion
Toes up
1 85 (160) 76 (125) 75 (132)
2 67 (109) 68 (97) 74 (118)
3 62 (99) 62 (91) 74 (103)
4 54 (76) 59 (81) 72 (111)
5 53 (75) 60 (83) 66 (91)
Toes down
1 76 (134) 75 (120) 72 (113)
2 45 (66) 59 (88) 66 (112)
3 40 (58) 52 (81) 61 (95)
4 37 (54) 49 (77) 60 (99)
5 36 (50) 49 (76) 60 (99)
*All values are in units of sway energy normalized for differences in body mass.
(n = 64)
60–69 Years
(n = 54)
70–79 Years
(n = 28)
Table 15–A5. Mean (Fifth Percentile) Equilibrium Scores as Functions of Age and Sensory Test Condition
Population Equilibrium Scores
20–59 Years
Condition
1 94 (90) 94 (90) 89 (70)
2 92 (85) 91 (86) 86 (63)
3 Average 91 (86) 89 (80) 88 (82)
4 Average 82 (70) 85 (77) 78 (69)
5 Average 69 (52) 65 (51) 61 (45)
6 Average 67 (48) 65 (49) 53 (27)
Composite 798 (704) 776 (676) 729 (638)
(n = 112)
60–69 Years
(n = 54)
70–79 Years
(n = 28)
15. COMPUTERIZED DYNAMIC POSTUROGRAPHY: METHODOLOGY AND INTERPRETATIONS 397
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Table 15–A6. Mean(±2 SO) COG Alignment Scores as Functions of Sensory Test Conditions and Age*
Population Alignment Scores
20–59 Years
Condition
Initial dynamic
1 0.2 ± (2.0) −0.3 ± (1.9) −0.2 ± (1.9)
2 0.3 ± (1.6) −0.1 ± (2.0) 0.0 ± (1.7)
3 0.3 ± (1.6) 0.0 ± (2.1) −0.2 ± (1.7)
4 0.3 ± (1.6) −0.1 ± (2.1) −0.1 ± (1.7)
5 0.7 ± (1.8) 0.1 ± (2.2) 0.2 ± (2.2)
6 0.8 ± (1.9) 0.4 ± (2.3) 0.3 ± (1.7)
*All values are in units of degrees from the center position.
(n = 77)
0.3 ± (1.8) −0.1 ± (2.0) 0.0 ± (1.8)
60–69 Years
(n = 54)
70–79 Years
(n = 28)
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16
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Vestibular-Evoked Myogenic
Potentials (VEMPs)
Devin L. McCaslin and Gary P. Jacobson
history and signifiCanCe
of Vestibular­myogeniC Potentials
It is now well known that the vestibular system can be stimulated using sound. In 1929, Pietro Tullio under­took the original investigations demonstrating the ves­tibular system’s sensitivity to auditory stimuli. Tullio’s experiments consisted of fenestrating the bony laby­rinth of pigeons, subjecting them to sound produced by a flute, and observing the motion of the labyrin­thine fluids (the frequency of the notes produced by the flute matched the frequency of the movement of the endolymph) and eye movements. From these experi­ments Tullio was able to determine that the vestibular system could be stimulated using sound (Tullio, 1929). Von Békésy (1935) built on the findings of Tullio and observed that when human subjects were exposed to a high-intensity stimulus (e.g., 122 to 134 dB sound pressure level [SPL]) there was a corresponding head displacement toward the stimulated ear. Von Békésy argued that this reflexive movement of the head in response to an auditory stimulus was likely due to movement of the endolymph stimulating the vestibu­lar system.
In the mid-1960s, Bickford, Jacobson, and Cody (1964) reported the presence of a sound-evoked electri­cal potential (consisting of a negative waveform peak­ing at approximately 30 ms) that could be recorded
eVoked
from an active electrode placed on the inion. Initially, this response was believed to be “neurogenic.” How­ever, the investigators demonstrated that the earlier components of the response were significantly reduced in amplitude following administration of a muscle para­lyzing agent. Additionally, it was noted that the response grew exponentially in amplitude with increases in the level of the tonic electromyography (EMG) in the neck extensors. This evoked-potential response was subse­quently named the inion potential. Further studies by this group of investigators led to the theory that the vestibu­lar system (i.e., the saccule) was the peripheral origin of the inion potential (Cody, Jacobson, Walker, & Bickford, 1964; Townsend & Cody, 1971). Finding no good clinical application for these responses, they were abandoned for almost 30 years. Then, in 1992 Colebatch and Halma­gyi reported the presence of another short-latency large amplitude myogenic potential recorded in response to a loud click with an electrode (non-inverting) placed over the belly of a contracted sternocleidomastoid muscle (SCM). This response was characterized by a positive wave (P1) followed by a negative wave (N1) occurring ipsilateral to the ear that received the stimulus (Cole­batch & Halmagyi, 1992; Colebatch, Halmagyi, & Skuse,
1994). There were several lines of evidence suggesting that the vestibular system, and more specifically the sac­cule, was the peripheral origin of this evoked response (Colebatch & Halmagyi, 1992; Colebatch et al., 1994). As with the inion potential, this sonomotor response represented a sound-evoked attenuation of tonic EMG
399
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activity in the SCM (Bickford et al., 1964; Colebatch & Halmagyi, 1992). It has been suggested that the sound­synchronized decrease in the tonic level of EMG that occurs during the response is interpreted by the central nervous system as a sudden loss in postural tone. The reflexive response from the vestibular system to com­pensate for this perceived decrease in muscle activity is to increase extensor muscle tone and decrease flexor muscle tone (Carey & Amin, 2006). Therefore, the amplitude of this inhibitory muscle response repre­sents an interaction between the level of tonic EMG and the size of the inhibitory postsynaptic potential (IPSP) initiated at the end organ (Colebatch & Rothwell, 2004; Figure 16–1). Colebatch and Halmagyi (1992) referred to this response as a vestibular-evoked myogenic potential (VEMP). Since this response is recorded from the SCM it is now referred to as the cervical VEMP (cVEMP). This early work led to the description of the ocular VEMP (oVEMP), which will be discussed in the second half of this chapter. Our objective for this chapter is twofold. First, we will describe how the cVEMP and oVEMP are recorded and measured. Second, we will present how different recording and stimulating parameters effect the responses.
DESCRIPTION OF THE cVEMP RESPONSE
The cVEMP is characterized by a biphasic waveform that begins with a primary positive waveform followed by a negative waveform (Figure 16–2). The mean peak latency of the positive deflection in response to a click stimulus is ~13 ms and is referred to in the literature as either P1 or p13. The negative deflection occurs at ~23 ms and is commonly referred to as N1 or n23 (Cole­batch & Halmagyi, 1992). The direction of the initial deflection (i.e., positive) suggests that the cVEMP is an inhibitory response (i.e., moving from a state where there is increased EMG activity to a state where there is decreased EMG activity) (Colebatch & Rothwell, 2004; Wit & Kingma, 2006). The response is primarily ipsilateral.
CERVICAL VEMP PATHWAY
The sacculo-collic response is a reflexive adjustment of the musculature in the neck triggered by activation of the saccule. A reflex consists of an afferent limb (i.e.,
Figure 16–1. The figure shows surface and single motor unit (intra­muscular-sternocleidomastoid muscle) recordings that have been recorded simultaneously in response to a click stimulus. The initial response is a decrease in single unit activity and is represented by “il.” From Colebatch, J. G., and Gothwell, G. (2004). motor unit excitability changes mediating vestibulocollic reflexes in the sternocleidomastoid muscle. Clinical Neurophysiology, 115(11), 2567–2573. Used with per­mission from the International Federation of Clinical Neurophysiology.
16. VESTIBULAR-EVOKED MYOGENIC POTENTIALS (VEMPS) 401
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Figure 16–2. Left and right cervical evoked myogenic potential waveform evoked using a 95 dB nH
L 500 tone-burst.
representing the activation of the peripheral end organ and ending at the brain center where these signals are received), central processing (i.e., where the affer­ent activity is routed to the central origin of the efferent limb), and an efferent limb (i.e., where the efferent activity terminates at an end muscle). The afferent limb of the cVEMP extends from the saccule (i.e., receptor organ) to Scarpa’s ganglion where neural projections course through the inferior branch of the vestibular nerve (McCue & Guinan, 1995; Murofushi & Cur­thoys, 1997; Figure 16–3). The inferior vestibular nerve becomes part of the VIIIth cranial nerve and the fibers projecting from the saccule terminate on interneurons within the medial and lateral vestibular nuclei. The efferent limb of the cVEMP reflex descends from the vestibular nucleus through the vestibulo-spinal tract to the motonucleus of CN XI. From there the activity is routed through CN XI to terminate on the SCM (Fitzger­ald, Comerford, & Tuffery, 1982). CN XI originates in the anterior horn of the first five cervical segments of the spinal column and is the solitary motor input to the SCM (Krause, Bremerich, & Herrmann, 1991) (Figure 16–4). This neural pathway has been confirmed by attenuation or ablation of the VEMP response fol­lowing selective neurectomies, neural pathologies, or local anesthetic delivered to SCM (Colebatch & Halma­gyi, 1992; Murofushi, Matsuzaki, & Wu, 1999).
STIMULUS VARIABLES
Type of Stimuli
A summary of cVEMP stimulus parameters is pre­sented in Tables 16–1 and 16–2.
Air-Conducted Stimuli
An acoustical stimulus (click or tone burst) is the stimulus most commonly used in the clinic (Papatha­nasiou, Murofushi, Akin, & Colebatch, 2014). When a high-intensity, low-frequency (e.g., 500 Hz), acousti­cal transient is introduced to the ear canal, the sound pressure is routed through the middle ear system to the oval window into the vestibule (Lysakowski et al.,
1998). This creates a situation where the endolymph in the vestibule is moved and the vestibular hair cells (type I and type II) are sheared, resulting in transduc­tion (Murofushi et al., 1995). It is worth reiterating that since sound is being used as a hydromechanical force to activate the vestibular end organ the patient need not have hearing to stimulate the vestibulocollic reflex (VCR) and generate a cVEMP. A requirement for recording a robust response is that the sound conduct­ing system (i.e., middle ear mechanism) be intact. When
figure 16–3. Anatomy of the vestibular labyrinth.
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figure 16–4. Presumed pathways responsible for generating the cervical and ocular vestibular-evoked myogenic potential. Note: IO = inferior oblique; MLF = medial longitudinal fasciculus; toid muscle.
SCM = sternocleidomas-
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16. VESTIBULAR-EVOKED MYOGENIC POTENTIALS (VEMPS) 403
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table 16–1. cVEMP Air-Conducted Stimulus Protocol
Frequency 400–700 Hz or click
Level 120 dB pSPL or greater, caution above
140 dB p
Gating Blackman-weighted, 7 ms maximum
duration
Rate 5 per second
table 16–2. cVEMP Bone-Conducted Stimulus Protocol
Frequency 100–500 Hz
Level 31.6 newtons peak
Gating Blackman-weighted, 7 ms maximum
duration
Rate 5 per second
SPL
a conductive impairment is present, the magnitude of the stimulus reaching the vestibule may be attenuated to a degree where the response is eliminated. In situa­tions such as this, the preferred stimulus is vibratory or mechanical (i.e., vibration produced by a Bruel & Kjaer 4810 Mini-shaker or a mechanical stimulus produced by a specially outfitted tendon hammer). Calibration of acoustic stimuli for cVEMP testing should be accom­plished using dB peak SPL (Papathanasiou et al., 2014).
Bone-Conducted Vibration
lateral response (i.e., bone vibrator placed on one side of the head) being larger. The authors also reported that the contralateral response occurred, on average, 1 ms later than the ipsilateral cVEMP. Thresholds for cVEMPs generated using the bone conduction stimulus were better than those obtained using air-conducted stimuli (i.e., 114 dB SPL versus 97.5 dB SPL; Welgam­pola et al., 2003). The authors also reported that the optimal placement for delivery of BCV was 3 cm pos­terior and 2 cm superior to the external auditory canal. In a similar study investigating BCV, Sheykholeslami and associates (2000) recorded cVEMPs using BCV applied to the mastoid. Tone bursts (i.e., 100, 200, 400, 800, 1600, and 3200 Hz) were used with a stimulus intensity of 70 dB nHL. The investigators reported that the largest amplitude VEMPs were in response to 200­Hz stimuli. Reliable cVEMP responses were unable to be obtained when 1600- and 3200-Hz stimuli were used. Recently, a number of clinical bone oscillators capable of generating enough output to consistently generate VEMPs have been made available to clinical investigators. Håkansson et al. (2018) recorded ocular and cervical VEMPs using the B81, B250, and Bruel and Kjaer 4810 Mini-shaker and compared the results with air-conducted responses. Their findings showed that for cervical VEMPs, thresholds were significantly lower with bone conduction than with air conduction (30–40 dB). The authors also reported that responses obtained to both ipsilateral and contralateral stimula­tion at 250 Hz were similar. They suggested that this finding indicated that it might not be necessary to switch the bone oscillator from one side to the other when obtaining responses.
Impairments in the middle ear conductive mechanism can reduce the amplitude or abolish the cVEMP (Bath, Harris, McEwan, & Yardley, 1999). Bone-conducted vibration (BCV) is an alternative stimulus to air­conducted stimuli that has been used successfully to stimulate the otolith organs and subsequently activate vestibular afferents (i.e., irregular neurons; Goldberg,
2000). Vibratory stimuli can be delivered to the skull with an audiometric bone vibrator. The stimuli may be either a click or a tone burst (McNerney & Burkard,
2011). In this regard, bone-conducted tone bursts have been shown to be capable of generating consistent cVEMP responses (Sheykholeslami et al., 2000; Yang & Young, 2003). Interestingly, cVEMPs in response to BCV have larger amplitudes when lower-frequency stimuli are used (i.e., 200–250 Hz) (Sheykholeslami et al., 2000; Welgampola et al., 2003). Welgampola and colleagues (2003) showed that cVEMP responses using BCV stimulation were present bilaterally, with the ipsi-
Skull Taps
The otolith mass also can be translated by lightly tap­ping the head. In this regard, it has been shown that cVEMP responses can be initiated using a commer­cially available tendon hammer that connects to the trigger input of a clinical evoked potential machine (Brantberg, L
öfqvist, Westin, & Tribukait, 2008; Jacob­son & McCaslin, 2007; Figure 16–5). The hammer (e.g., from Nicolet Biomedical, Madison, Wisconsin) con­tains an inertial trigger. Each time the hammer strikes the patient’s head, a trigger pulse is initiated and this pulse commands the evoked potential system to signal average one sweep of, for example, 100 ms. Halmagyi, Yavor, and Colebatch (1995) reported that cVEMPs could be consistently recorded by tapping the head in the frontal region using a similarly outfitted tendon reflex hammer. Recording the cVEMP in response to mechanical stimulation requires a slightly different