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8 Rotational Vestibular Assessment
A B
D E
C
F
FIGURE 1–7. Portraits of prominent vestibular scientists from the eighteenth through the twentieth century. A. Róbert
Bárány (1876–1936). B. Ernst Josef Mach (1838–1916). C. Robert Waring Darwin (1838–1916). D. Alexander Crum Brown (1838–1922). E. Erasmus Darwin (1731–1802). F. Jan Evangelista Purkyneˇ (1787–1869). continues
notably by Charles Wells, Erasmus Darwin, and Robert Waring Darwin) (Wade, 2003), it was not until the work of Flourens in 1824 that Aristotle’s five senses officially added one more. Flourens’ research involving the extirpation of semicircular canals in pigeons finally provided the irrefutable evidence for the vestibular system’s role in the
perception of motion, thus heralding the elusive sixth sense.
The emergence of the sixth sense struggled for nearly 2000 years after Aristotle first described the five principal human senses. Therefore, it was not surprising that widespread acceptance was not ap­preciated by all scientists at the time, including Jan
1. Historical Perspective of Human Rotation and Centrifugation 9
G H
FIGURE 1–7.
Breuer (1842–1925).
continued G. Jean Pierre Flourens (1794–1867). H. Josef
Evangelista Purkyneˇ, who continued to remain hesitant in acknowledging all the available scien­tific evidence at the time (Wade, 2003).
Despite the quiescence of reports investi­gating the use of rotational chairs for the clinical diagnosis and treatment of vertigo throughout the early and mid-1800s, there were significant advancements in the understanding of vestibular physiology in the last quarter of the nineteenth cen­tury. Ernst Josef Mach, Alexander Crum Brown, and Josef Breuer (see Figure 1–7) almost simul­taneously proposed the “hydrodynamic theory of semicircular canal function” in 1874 to 1875. Ernst Josef Mach, in particular, was instrumental in this theory. During this time, Mach also pub­lished scientific reports investigating the nature of otolith responses, as well as the first reports indicating the semicircular canals responded to acceleration, not velocity (Cohen & Raphan, 2004). Between the years 1874 and 1875, Ernst Mach con­structed a rotational chair that was mounted in a rotatable frame, and examined the perception of the visual vertical during static tilt, and also the visual aftereffects of body rotation (Figure 1–8). Mach performed such studies after observing the
vertical tilting of telegraph poles when round­ing an inappropriately banked curve on a train (Cohen & Raphan, 2004). For his work on subjec­tive visual vertical, some consider Ernst Mach the “Father of Otolith Function Testing.” Despite this otological notoriety, Ernst Josef Mach, being an Austrian physicist and philosopher, is probably better known for the Mach principle, which was the precursor to Einstein’s theory of relativity.
It is also worth noting that during the time of Mach’s discoveries, Alexander Crum Brown also devised methods for measuring thresholds for detecting body movements on a rotating stool. He determined that thresholds were low­est when the head was positioned so that one of the semicircular canals was in the plane of rota­tion; a precursor to Ewald’s laws of semicircular canal function. Finally, toward the beginning of the twentieth century, Lorente de Nó (1933) first described in detail the three-neuron arc that con­nects the peripheral vestibular end organs to the ocular muscles, thus detailing the Vestibular Ocu­lar Reflex (VOR) pathways that Charles Wells eloquently described 140 years earlier (Cohen & Raphan, 2004).
10 Rotational Vestibular Assessment
A B
FIGURE 1–8.
examined the perception of the visual vertical during static tilt, and also the visual aftereffects of body rotation. Some consider Ernst Mach the “Father of Otolith Function Testing.” From Grundlinien der Lehre von den Bewe- gungsempfindungen, by E. Mach, 1875, Leipzig, Verlang von Wilhelm Engelmann.
A. Ernst Mach (1838–1916). B. The rotational chair that was mounted in a rotatable frame, which
ROTATION IN THE EARLY
TWENTIETH CENTURY
day rotational chairs are sometimes referred to as “Bárány chairs.” Although modern chairs have come along way in their function, chairs similar in appearance and function to Bárány’s original
Despite the scientific evidence heralding the emer­gence of the vestibular system as the sixth sense,
chair are actually still in use today in some aero­space and military motion tolerance labs.
the application of clinical rotation withstood a slow transition from the psychiatric treatment of mental disorders to the clinical assessment of otolaryngological disease. Toward the later part
Introduction of Rotational Testing in the Assessment of Vestibular Function
of the nineteenth century and the early part of the twentieth century, the medicinal evidence for Horn’s “psychiatric centrifuge” finally gave way to more scientific evidence supporting the use of rotation as a clinical method for investigating vestibular function. Nearly a century after the well-accepted and routine use of patient rotation for the treatment of psychiatric disorders, Róbert Bárány (see Figure 1–7) introduced the applica­tion of patient rotation in 1907 as a means for the clinical assessment of the vestibular system. Bárány developed the first rotational chair that was universally adopted in otolaryngology clinics at the time (Figure 1–9). For this reason, modern
Róbert Bárány first introduced the idea of rota­tional testing in routine clinical assessment of the vestibular system in 1907. Bárány devised a method of impulse stimulation whereby an abrupt acceleration was applied to a rotational “Bárány chair,” with the patient being given 10 rotations in 20 seconds, which was then followed by an abrupt cessation of rotation applied by a manual foot brake. Immediately following cessation of rotation, the presence of post-rotary nystagmus was visualized and timed by the examiner. It was believed that the slow decay of nystagmus reflected activity of the horizontal cupulae. The
1. Historical Perspective of Human Rotation and Centrifugation 11
A B
FIGURE 1–9. A. Bárány chair. From Background and Introduction to Whole-Body Rotational Testing by A. M.
Goulson, J. H. McPherson, and N. T. Shepard, 2016. In G. P. Jacobson and N. T. Shepard (Eds.), Balance Func­tion Assessment and Management, (pp. 347–364). San Diego, CA, Plural Publishing. Reprinted with permission.
B. Use of a Bárány chair applying the past-pointing procedure following cessation of rotation. Reprinted with kind permission from http://www.goflightmedicine.com
test was then repeated in the opposite direction and the results were often compared. Although the principles of the test were believed by many early twentieth century neurologists to be very insight­ful into the function of the vestibular system, the administration and subsequent interpretation of this test was also recognized as problematic, as control of stimulus delivery was often inconsis­tent, particularly between different patients.
A few years later in 1931, Veits suggested that Bárány’s method of impulse stimulation over a 20 second period was, in fact, too short to allow
for the cupulae to return to their original position after having received such brisk accelerations. Therefore, Veits suggested that the cessation of rotation during Bárány’s impulse protocol likely occurred while the cupulae were still deviated. In an attempt to remedy this problem, Veits sug­gested delivering extremely slow accelerations until reaching a constant velocity of 180°/sec. At this velocity, Veits proposed maintaining a con­stant level of rotation until resetting of the cupulae were assured. He determined this by an absence of nystagmus and cessation of vertigo. Only after
12 Rotational Vestibular Assessment
these criteria were met, was the brake applied to the Bárány chair and the duration of the post­rotary nystagmus recorded.
In 1948, another attempt to improve upon Bárány’s impulse stimulation test was proposed by van Egmond, Groen, and Jongkees. These authors described a method similar to Veits involving the use of slow accelerations. However, van Egmond, Groen, and Jongkees slowly accelerated patients to a number of predetermined target velocities, at which time the chair was abruptly stopped and the post-rotary nystagmus and subjective vertigo was again timed. van Egmond, Groen, and Jong­kees plotted each nystagmus response against the various target velocities and coined the term “cupulometry” to describe the vestibular response over a broader range of frequencies.
During the 1940s, vestibular scientists were also beginning to investigate the effects of linear acceleration on the vestibular system. Modified human centrifuges were used by various research­ers during the mid-1900s. Graybiel and Hupp (1946), and Graybiel, Niven, and Walsh (1952) devised a method to apply centripetal force to study the effects of linear acceleration on the utri­cle. Aside from Ernst Mach’s experiments, these are perhaps some of the earliest vestibular studies using “modern” human centrifuges and eccentric rotation. However, detailed ocular measures of nystagmus were lacking, and reports were often confined to patient reports of apparent subjective tilting of the body, as well as the ostensible visual tilting of surrounding objects in space.
Some of the earlier successor chairs to the Bárány chair were the Hallpike, Hood, and Byford chair (1952) (Figure 1–10), the Tönnies apparatus (1955) (Figure 1–11), the Frenckner and Preber chair (1956) (Figure 1–12), the Fluur chair (1960) (Figure 1–13), the Johnson and Taylor table (1961) (Figure 1–14), the “Girograph of Montandon” (Geneva, Switzerland, 1955; Montandon & Russ­bach, 1955), the Stille-LKB Rotating chair (Stille­Werner, Stockholm), and the Heidelberg chair (Ey & Feldman, 1964; Figure 1–15) (McNally & Stuart,
1967). For an excellent review of the rotational chairs used during the mid-twentieth century from military institutions, domestic hospitals and laboratories, as well as foreign laboratories, the
FIGURE 1–10. Hallpike, Dix, and Byford rotational
chair, 1952. From “The Design, Construction and Perfor­mance of a New Type of Revolving Chair Some Experi­mental Results and Their Application to the Physical Theory of the Cupular Mechanism” by C. S. Hallpike, J. D. Hood, and G. H. Byford, 1952, Acta Oto-Laryngologica, 42(6), 511–538. Reprinted with permission.
reader is encouraged to read Guedry and Gray­biel’s (1961) report entitled Rotation Devices, Other
Than Centrifuges and Motion Stimulators: The Ratio­nale for the Special Characteristics and Use. In general,
from 1907 until the 1960s, rotational assessments using the Bárány chair and its successors were essentially confined to impulse stimulation and cupulometry protocols. Early attempts were fre­quently proposed in an attempt to improve testing and provide better outcome measures; however, results were plagued with unreliability and poor sensitivity at identifying vestibular pathology.
A
B C
FIGURE 1–11. Early model of Tönnies apparatus rotational chair. Chair orientation could be modified to study
horizontal nystagmus (A), vertical nystagmus (B), and torsional nystagmus (C). From “On Acceleratory Stimula­tion,” 1955, Acta Oto-Laryngologica, 45(Suppl. 122), 22–44. Reprinted with permission.
13
A
B C
FIGURE 1–12. Frenckner and Preber chair. Rotational chair (A), computer console (B), and nystagmus printout
(C). From “Relationship Between Vestibular Reactions and Vegetative Reflexes, Studied in Man by Means of a Revolving Chair of New Design” by P. Frenckner, and L. Preber, 1956, Acta Oto-Laryngologica, 46(3), 207–220. Reprinted with permission.
14
A
B
FIGURE 1–13. The Fluur rotational chair. A. Chair positioned for
nasion-occipital eccentric rotation. B. Chair positioned for interaural axis eccentric rotation. From “A Novel Rotary Chair” by E. Fluur, 1960, Acta Oto-Laryngologica, 52:1–6, 210–214. Reprinted with permission.
15
FIGURE 1–14. The Johnson and Taylor rotational chair. From “The
Importance of the Otoliths in Disorientation” by W. H. Johnson, 1964, Aerospace Medicine, 35, 874–877. Reprinted with permission.
FIGURE 1–15. Heidelberg chair. From “Der Heidelberger Planeten-
Drehstuhl, eine neuartige Mehrzweck-Drehstuhlanlage für Vestibular­isreflexprüfungen” by W. Ey, and H. Feldman, 1964, Archiv Ohren-, Nasen- u. Kehlkopfheilk. 184, 73–80. Reprinted with permission.
16
1. Historical Perspective of Human Rotation and Centrifugation 17
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This was largely due to the fact that stimulus delivery was manually generated, or electrically driven through inefficient motors and turntables. It was not until the late 1960s and early 1970s, when the advent of computer-controlled precision torque motors were able to deliver more consis­tent and reliable stimuli, thus improving the vari­ous outcome measures.
The slow advancement of rotational research and its use in clinical assessments in the early twentieth century may have also been due to one of the most (if not the most) significant discovery in clinical vestibular physiology. In 1906, Róbert Bárány published, “Untersuchungen ueber den vom Vestibularapparat des Ohres reflektorisch ausgel Begleiterscheinungen” (“Investigations of Rhyth­mic Nystagmus and Its Accompanying Manifesta­tions Arising From The Vestibular Apparatus of the Ear”) (Nylen, 1965). In this work, he described the caloric response for which he was later awarded the Nobel Prize in Physiology and Medicine in 1914. In fact, no other Nobel Prize has been awarded in the field of vestibular medicine (noting that George von Békésy also received the Nobel Prize in Physiology and Medicine in 1961, although this was for his work in the field of hearing science on the cochlear traveling wave). The caloric test became an otolaryngological breakthrough for the discovery of labyrinthine disease and identify­ing normal vestibular function. Given the caloric test’s success and the concomitant unreliability of rotational data at the time, the rotational test was likely overshadowed by the simplicity and wide­spread acceptance of caloric irrigations.
östen rhythmischen Nystagmus und seine
ROTATION IN THE MID-TO-
LATE TWENTIETH CENTURY
During the mid-twentieth century, the caloric test flourished due to its increased diagnostic sensi­tivity for vestibular disease, while rotational chair testing received only a moderate degree of atten­tion, secondary to its inherently unreliable nature. However, with the advent of “personal” comput­ing in the later quarter of the twentieth century, and the increased knowledge regarding vestibular
physiology (such as the discovery of the neural integrator and the velocity storage mechanism by Raphan, Matsuo, and Cohen in 1979), research and development in the field of rotational testing was once again about to flourish and emerge as a highly specialized vestibular test, both in clinical and research settings.
The introduction of smaller (personal) com­puters in the late 1960s and early 1970s signifi­cantly changed the clinical canvas of nearly every physiologic test, and rotational testing was no exception. With the personal computer came sig­nificant advancements in the ability to deliver exacting stimuli through new torque motors with a higher degree of precision and low vibration noise, thus eliminating the immeasurable variability and clinical uncertainty associated with manually pro­duced brake-rotations common with the Bárány chair. Moreover, the discovery of the corneoretinal potential by Emil du Bois-Reymond (1818–1896) in 1948 opened the door for the objective measure­ment of nystagmus (Brey, McPherson, & Lynch, 2008a). Recording of the corneoretinal potential through electrooculography (EOG) allowed for the quantification of nystagmus, rather than the subjective timing of the post-rotary nystagmus decay response, which introduced much needed sensitivity to rotational analyses.
The number of accounts of rotational investi­gations beginning in the late 1960s into the 1970s was exponential in growth. From the development and application of new linear sleds, to the devel­opment of more advanced yaw angular rotational chairs (and rooms), numerous published reports detailing the various vestibular ocular response parameters and new stimulus paradigms, occurred at a rapid pace. Niven, Carroll Hixson, and Cor­reia (1965) devised the “Coriolis Acceleration Platform,” which was able to produce 16 feet/sec linear accelerations with a peak linear acceleration of 3-gravitational forces (McNally & Stuart, 1967). This study is often cited as the first investiga­tion to show nystagmus with linear acceleration. However, the use of linear sleds was extraor­dinarily expensive due to the shear size of the laboratory needed to build and use such equip­ment. To address the massive size requirements needed for such linear sled experiments, Johnson and Taylor (1961) devised an electrically driven