ORIgINAl PAPERS

orIginal papers
Adv Clin Exp Med 2013, 22, 4, 549–554
ISSN 1899–5276
© Copyright by Wroclaw Medical University
Marcin Masalski1, 2, A–F, Bartosz Banaś2, B–D, Tomasz Kręcicki1, E, F
The Influence of Eyeball Rotation on the Results
of Auditory Steady-State Responses
Wpływ pozycji gałek ocznych na wyniki badania słuchowych potencjałów
wywołanych stanu ustalonego
Department and Clinic of Otolaryngology, Head and Neck Surgery, Wroclaw Medical University,
Wrocław, Poland
2
Institute of Biomedical Engineering and Instrumentation, Wroclaw University of Technology, Wrocław, Poland
1
A – research concept and design; B – collection and/or assembly of data; C – data analysis and interpretation;
D – writing the article; E – critical revision of the article; F – final approval of article; G – other
Abstract
Background. The testing of auditory steady-state responses consists in recording the electrophysiological response
to an auditory stimulus. Due to this response, in addition to changes in electric potentials caused by neuron impulses in the auditory path, the sonomotor reflex can also be observed. The sonomotor reflex shows muscle responses to
auditory events, and in the case of auditory evoked potentials it mainly consists of post-auricular muscle responses.
When the eyes are rolled to the side during testing, the post-auricular muscle response to an auditory stimulus is
stronger, which in turn can contribute to improving response detection.
Objectives. The aim of this study was to test the influence of eyeball rotation on the results of auditory steady-state
responses.
Material and Methods. Auditory evoked potentials were tested in a group of ten people with normal hearing. Each
person was examined three times: (i) with eyes closed, (ii) with eyes open looking straight ahead and (iii) with eyes
open and rolled to the side.
Results. The median electrophysiological response amplitude recorded when the eyes were rolled to the side was
approximately 40% higher than the median response amplitude recorded in other positions (with eyes closed,
and with eyes open looking straight ahead). At the same time, during tests with the eyes rolled to the side, a 170%
increase in the noise median was observed, compared to the tests conducted with the eyes closed.
Conclusions. Rolling the eyes to the side does not improve the detection of response, as the observed increase in
noise amplitude is much higher than the increase in the amplitude of the electrophysiological response (Adv Clin
Exp Med 2013, 22, 4, 549–554).
Key words: auditory steady-state responses (ASSRs), postauricular muscle response.
Streszczenie
Wprowadzenie. Badanie słuchowych potencjałów wywołanych polega na rejestracji odpowiedzi elektrofizjologicznej na bodziec dźwiękowy. W odpowiedzi tej, oprócz zmian potencjałów elektrycznych wywołanych impulsacją
neuronów drogi słuchowej, można wyróżnić także komponent sonomotoryczny. Komponent sonomotoryczny jest
mięśniową reakcją organizmu na bodziec dźwiękowy i w przypadku słuchowych potencjałów wywołanych składa
się głównie z reakcji mięśnia zausznego. Boczne zwrócenie gałek ocznych podczas badania wzmacnia reakcję mięś­
nia zausznego na stymulacje dźwiękową i tym samym może przyczynić się do poprawy detekcji odpowiedzi.
Cel pracy. Określenie wpływu pozycji gałek ocznych na wyniki badania słuchu metodą potencjałów wywołanych
stanu ustalonego.
Materiał i metody. Badania słuchowych potencjałów wywołanych przeprowadzono na grupie 10 osób z prawidłowym słuchem. Każda osoba została zbadana trzykrotnie: (i) z zamkniętymi oczami, (ii) z otwartymi oczami, patrząc
na wprost, oraz (iii) z otwartymi oczami przy bocznie zwróconych gałkach ocznych.
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M. Masalski, B. Banaś, T. Kręcicki
Wyniki. Mediana amplitudy odpowiedzi elektrofizjologicznej zarejestrowanej w warunkach bocznego zwrócenia
gałek ocznych była wyższa o około 40% od mediany amplitudy odpowiedzi zarejestrowanej w pozostałych badaniach, tj. przy oczach zamkniętych i oczach otwartych patrząc na wprost. Jednocześnie w badaniu przy gałkach
ocznych zwróconych bocznie zaobserwowano wzrost mediany szumu aż o 170% w porównaniu do badania przeprowadzonego przy oczach zamkniętych.
Wnioski. Boczne zwrócenie gałek ocznych nie przynosi poprawy detekcji odpowiedzi, ponieważ obserwowany
wzrost amplitudy szumu jest dużo większy od wzrostu amplitudy odpowiedzi elektrofizjologicznej (Adv Clin Exp
Med 2013, 22, 4, 549–554).
Słowa kluczowe: słuchowe potencjały wywołane stanu ustalonego, odruch z mięśnia zausznego.
The testing of auditory evoked potentials consists in recording electrophysiological responses
to auditory stimuli. The auditory evoked potentials make it possible to evaluate the transmission
of nerve impulses in the auditory path. On the basis of electrophysiological responses to auditory events the hearing thresholds of the examined
person can be estimated. In addition to changes
in electric potentials caused by neuron impulses
in the auditory path, the electrophysiological response also shows the sonomotor reflex, which is
the muscle response to auditory events. On the one
hand, the existence of the sonomotor reflex in the
recorded auditory steady-state responses can make
the evaluation of transmission in the auditory path
difficult due to overlapping muscle and auditory
potentials, but on the other, it can make the detection of responses to auditory stimuli easier, since
the total muscle and auditory potential is easier to
identify in the signal registered during testing. In
the case of auditory evoked potentials the sonomotor reflex mainly consists of post-auricular muscle
responses (PAMRs) [1, 2]. PAMRs are unstable responses, varying from patient to patient [3, 4], but
they can be strengthened when the eyes are rotated to the side [5, 6].
Auditory evoked potentials can be divided into
transient responses (electrophysiological responses to short auditory stimuli), and steady-state responses (SSRs: electrophysiological responses to
a series of stimuli presented at high repetition
frequency).
Some previous researchers have proposed that
the detection of transient responses may be improved when the eyeballs are rolled to the side [7, 8].
According to those authors, in most subjects it is
possible to objectively reconstruct a pure tone audiogram in this way.
The aim of the current study was to determine
the influence of eyeball rotation on the results of
auditory steady-state responses, especially on the
possibility of improving the detection of responses
recorded when the eyeballs are rolled to the side.
Auditory steady-state responses (SSRs) are
a sinusoidal wave generated by the overlapping
of transient responses due to a high stimulation
frequency. The frequency of a SSR is equal to the
frequency of a sound stimulus. SSRs can be obtained by applying a short sound stimulus at a high
repetition frequency or a continuous modulated stimulus [9]. The detection of steady-state responses can be made on the basis of EEG signals by
comparing the signal’s amplitudes at the stimulation frequency with the amplitude of adjacent frequency bands. In this case PAMRs will be observed
as an increase in the response amplitude [10].
The influence of eyeball rotation on SSR results was tested for multifrequency steady-state
responses (MF-SSRs). MF-SSRs are responses to
stimuli presented simultaneously with a modulation frequency in the 70–100 Hz range [9]. They
are often used to evaluate the hearing threshold.
Material and Methods
Auditory evoked potentials were tested in
a group of 10 subjects (age from 25 to 33) with
normal hearing. Each person was examined three
times: (i) with eyes closed, (ii) with eyes open looking straight ahead and (iii) with eyes open and
rolled to the side. During all the examinations the
subjects were lying comfortably on their backs and
were asked not to fall asleep. During the first examination the patients’ eyes were closed, during
the second they were looking straight ahead, and
during the third their eyes were fixed on points located to the side, within the scope of binocular vision. As looking to one side for a long time is uncomfortable, the subjects switched from looking
toward one side to the other every minute, which
was signalled by a touch of the hand. The examination was conducted with the use of a diagnostic
system for objective audiometry [11].
Stimulus
Auditory stimulation was performed binaurally. Eight stimuli were presented at the same
time, four on the right side and four on the left
side. On both sides the fundamental frequencies
fc of the stimuli were set to 500 Hz, 1 kHz, 2 kHz
and 4 kHz respectively. Each stimulus had unique
modulation frequency fm; on the right side these
551
Eyeball Rotation and the Results of Auditory Steady-State Responses
were (respectively) 73.37 Hz, 81.52 Hz, 89.67 Hz,
and 97.83 Hz; and on the left: 77.45 Hz, 85.60 Hz,
93.75 Hz and 101.90 Hz. Each stimulus represented an intensity of 50 dBHL determined by amplitude A. All the stimuli s were generated according
to the formulas below:
ϕ(i) =
mf fc
2 fm
sin(2πfm τi ) s (i ) = A(1 + ma sin(2π fm ti )) sin(2π fm ti + ϕ(i)),
(1)
(2)
where:
mfis the frequency modulation index determined
at the level of 20%
mais the amplitude modulation index determined
at the level of 100%
t is the signal sample time of 1/48 kHz
The sound stimulus was generated by the
sound system of a personal computer and presented
through audiometric earphones TDH-39. Calibration of sound generation system was performed using a type 4153 artificial ear made by Brüel & Kjær.
response aresp to a stimulus is the amplitude of the
spectrum at the modulation frequency of the stimulus [13] and was calculated according to the formula below:
aresp =
cresp
N
,
(3)
where:
cresp is the FFT combined coefficient at resp index
representing the modulation frequency fm, and
N is number of samples in a sweep (N = 4096).
For each stimulus the amplitude of the ipsilateral response (the response from the channel collecting the EEG signal on the same side as the stimulus) and of contralateral response (the response
from the channel collecting the EEG signal on the
opposite side from the stimulus) were calculated.
Then, for each response, the average noise in the
adjacent frequency bands was calculated according
to the formula below:
anoise =
1 n /2 cresp +i
∑
n i = − n /2 N 2
2
,
(4)
i ≠0
Registration of the EEG Signal
The EEG signal was measured using a twochannel measurement system. In each channel
changes in the electric potentials between an electrode placed on the top of the head and an electrode placed behind the auricle were registered.
The latter electrodes were placed on the post-auricular muscle, approximately 2 cm above their
normal location on the mastoid process in order
to increase the sonometric reflex [4–6]. The EEG
signal registration was carried out using a TuckerDavis Technologies system consisting of an HS4
pre-amplifier and a DB4 amplifier. The signal was
recorded in the 70–200 Hz band, with a sampling
frequency of 48 kHz, and was subject to x92 decimation. Epochs with a length of 0.49 s, in which
the maximum amplitude exceeded the level of
8 µV, were regularly removed from the registered
signal. The remaining epochs were combined into
7.85 second sweeps.
Analysis of the EEG Signal
For each examination (eyes closed, eyes open
looking straight ahead and eyes open with the
eyeballs rolled to the side) a 10 minute EEG signal consisting of 7.85 second sweeps was registered. The sweeps were averaged with the use of
weights which are the reciprocal of a variance of
the averaged sweep [12]. Then, on the basis of the
Fast Fourier Transform (FFT), the spectrum of the
averaged signal was obtained. The amplitude of
where:
n is the number of adjacent frequency bands (n = 16)
Next, for each response/noise pair, the signalto-noise ratio (SNR) was calculated according to
the formula below:
 aresp
SNRdB = 20 log 10 
 anoise

 
(5)
2
 aresp 
 represents the F statistic
The ratio 
 anoise 
used in the detection of steady-state responses [14].
Results
Figure 1 presents the amplitude of responses,
the average noise and signal-to-noise ratio for tests
conducted on subjects with their eyes closed, with
their eyes opened looking straight ahead and with
their eyeballs rolled to the side. The median of the
electrophysiological response amplitude recorded
when the eyes were rolled to the side was higher by
approximately 40% than the median of the response
amplitude recorded in the other cases (i.e., with the
eyes closed and with the eyes open looking straight
ahead). These differences were statistically significant (p = 0.001 – the Wilcoxon signed-rank test).
Simultaneously, during tests with the eyes rolled to
the side, there was a statistically significant increase
(p = 0.001) of the noise median by 170% compared
552
M. Masalski, B. Banaś, T. Kręcicki
(a)
(b)
50
averange noise amplitude [nV]
amplitude of response [nV]
150
100
50
0
eyes closed
eyes open
40
30
20
10
0
eyes roled
to the side
eyes closed
eyes open
eyes rolled
to the side
(c)
50
40
SNR [dB]
30
20
10
0
-10
eyes closed
eyes open
eyes rolled
to the side
Fig. 1. Amplitude of response (a), average noise (b) and signal-to-noise ratio (c) for examination conducted with eyes
closed, with the eyes open and with the eyeballs rolled to the side (a cross – outlier, a square – lower quartile Q1 and
upper quartile Q3, horizontal line – median, wavy line – the biggest and the smallest value within the range
〈Q1 – 1.5IQR, Q3 + 1.5IQR〉, where IQR = Q3 – Q1)
Ryc. 1. Amplituda odpowiedzi (a), średni szum (b) oraz stosunek sygnału do szumu (c) dla badań przy oczach
zamkniętych, oczach otwartych i gałkach zwróconych bocznie (krzyżyk – pomiar odstający, prostokąt – dolny kwartyl
Q1 i górny kwartyl Q3, linia pozioma – mediana, wąsy – najmniejsza i największa wartość w przedziale 〈Q1 – 1.5IQR,
Q3 + 1.5IQR〉, gdzie IQR = Q3 – Q1)
to the tests conducted with the eyes closed. Due to
the significantly higher increase of noise than of the
amplitude of response, the signal-to-noise ratio decreased during tests conducted with the subjects’
eyeballs rolled to the side, compared to tests conducted with the subjects’ eyes closed (p = 0.001) and
to the tests conducted with the subjects’ eyes open
and looking straight ahead (p = 0.05).
Figure 2a shows the medians of response amplitudes obtained from the examination series in
relation to the fundamental frequency of the stimuli. The biggest increase in response during tests
with eyes rolled to the side occurred at high levels of fundamental frequencies of the stimulus,
which is consistent with the observations of other authors [6, 7]. For the frequencies of 2 kHz and
4 kHz, it is above 50% higher than in other test
positions (i.e., with the eyes closed and with the
eyes open looking straight ahead). However, this
increase is insufficient to compensate for the increase of noise and to improve SNR.
The amplitudes of ipsilateral and contralateral responses obtained during tests when the subjects had their eyeballs rolled to the side are similar
(Fig. 2b). The increase in the amplitude of the contralateral response tested with the eyeballs rolled
to the side is slightly higher than the increase in
the ipsilateral response; this difference results from
smaller amplitudes of contralateral response in the
other positions.
During the examinations it was noticed that
the value of the response with the eyeballs rolled
to the side is characterized by significant variability from subject to subject. Figure 3 presents the
553
Eyeball Rotation and the Results of Auditory Steady-State Responses
(a)
(b)
60
the median of response amplitude [nV]
the median of response amplitude [nV]
60
50
40
30
20
10
0
500 Hz
1000 Hz
2000 Hz
4000 Hz
fundamental frequency of the stimulus
eyes closed
eyes open
eyes rolled
to the side
50
40
30
20
10
0
ipsilateral
contralateral
type of response
Fig. 2. The median of the response amplitudes in the examination series in relation to the fundamental frequency (a)
and type of response (b)
Ryc. 2. Mediana amplitudy odpowiedzi w poszczególnych badaniach w zależności od częstotliwości podstawowej (a)
oraz rodzaju odpowiedzi (b)
the median of response amplitude [nV]
250
Subjects initials
PW
MM2
KJ
AT
AK
BB
PO
LW
MC
MM
200
150
100
50
0
eyes closed
eyes open
eyes rolled
to the side
Fig. 3. Amplitudes of the responses with eyes closed, eyes open and eyes rolled to the side reordered in relation to the
subjects tested
Ryc. 3. Amplituda odpowiedzi w badaniu przy oczach zamkniętych, otwartych i gałkach ocznych zwróconych bocznie
w podziale na osoby badane
amplitude of response in relation to the subjects
tested. The subject with the initials MM demonstrated a significantly higher response than the
other patients, and only in his case did the SNR increase during the examination conducted with his
eyes rolled to the side.
Discussion
The median of the electrophysiological response amplitude recorded when the subjects’ eyes
were rolled to the side was approximately 40%
higher than the median of response amplitude recorded in other cases (i.e., with the subjects’ eyes
closed and with their eyes open looking straight
ahead). However, this increase is insufficient to
compensate for the increase in noise amplitude,
which is 170% higher than in the tests conducted
with eyes closed. For this reason, moving the eyes
to the side does not lead to improvement in the detection of evoked potential responses. The increase
in noise amplitude is connected with stimulation
of the optic centers [15] and activation of the eye
movement system [16].
The examinations showed that the increase in
the amplitude of the sonomotor reflex from the
post-auricular muscle is characterized by high intersubject variability. Moreover, forced movement
of the eyeballs to the sides was uncomfortable for
the examined subjects and cannot be successfully
applied in the case of young children.
The tests were performed while registering MFSSRs with eight stimuli presented simultaneously
554
M. Masalski, B. Banaś, T. Kręcicki
at modulation frequencies within the 70–100 Hz
range. Steady-state responses can be also obtained
by stimulation at frequencies of approximately
40 Hz. The 40 Hz responses have different properties, which limits their application in hearing
threshold detection; for example, their amplitude
significantly decreases in the presence of other
stimuli or during sleep [17, 18]. However, the influence of eyeball rotation on 40 Hz responses may
turn out to be higher, because the PAMR amplitude increases with the decrease in the stimulation
frequency [4]. Therefore, it seems reasonable to
conduct analogical tests for a single stimulus modulated with a frequency of about 40 Hz.
References
  [1] Davis H, Lowell E, Goldstein R: Sonomotor reflexes: Myogenic evoked potentials. Acta Otolaryngol 1965, 206,
122–128.
  [2] Bochenek W, Bochenek Z: Postauricular (12 ms latency) responses to acoustic stimuli in patients with peripheral,
facial nerve palsy. Acta Otolaryngol 1976, 81, 264–269.
  [3] Picton TW, Hillyard SA, Krausz HI, Galambos R: Human auditory evoked potentials. I: Evaluation of components. Electroencephalogr Clin Neurophysiol 1974, 36, 179–190.
  [4] Jacobson GP, McCaslin DL: The Vestibular Evoked Myogenic Potential and Other Sonomotor Evoked Potentials.
In: Auditory evoked potentials: basic principles and clinical application. Eds.: Burkard RF, Eggermont JJ, Don M,
Lippincott Williams & Wilkins, Baltimore 2007, 572–598.
  [5] Patuzzi RB, O’Beirne GA: Effects of eye rotation on the sound-evoked post-auricular muscle response (PAMR).
Hear Res 1999, 138, 133–146.
  [6] O’Beirne GA, Patuzzi RB: Basic properties of the sound-evoked post-auricular muscle response (PAMR). Hear
Res 1999, 138, 115–132.
  [7] Patuzzi RB, Thomson SM: Auditory evoked response test strategies to reduce cost and increase efficiency: the
postauricular muscle response revisited. Audiol Neurootol 2000, 5, 322–332.
  [8] Purdy SC, Agung KB, Hartley D, Patuzzi RB, O’Beirne GA: The post-auricular muscle response: an objective
electrophysiological method for evaluating hearing sensitivity. Int J Audiol 2005, 44, 625–630.
  [9] Picton TW, John MS, Dimitrijevic A, Purcell D: Human auditory steady-state responses. Int J Audiol 2003, 42,
177–219.
[10] Picton TW, John MS, Purcell DW, Plourde G: Human auditory steady-state responses: Effects of recording technique and state of arousal. Anesth Analog 2003, 97, 1396–1402.
[11] Masalski M, Giżewski S: System diagnostyczny do obiektywnego badania słuchu metodą słuchowych potencjałów
wywołanych stanu ustalonego. Przegl Elektrotech 2009, 85, 45–48.
[12] John MS, Dimitrijevic A, Picton TW: Weighted averaging of steady-state responses. Clin Neurophysiol 2001, 112,
555–562.
[13] Lins OG, Picton TW: Auditory steady-state responsem to multiple simultaneous stimuli. Electroencephalogr Clin
Neurophysiol 1995, 96, 420–432.
[14] Dobie RA, Wilson MJ: A comparison of t test, F test, and coherence methods of detecting steady-state auditory-evoked potentials, distortion-product otoacoustic emissions, or other sinusoids. J Acoust Soc Am 1996, 100,
2236–2246.
[15] Barry RJ, Clarke AR, Johnstone SJ, Magee CA, Rushby JA: EEG differences between eyes-closed and eyes-open
resting conditions. Clin Neurophysiol 2007, 118, 2765–2773.
[16] Iwasaki M, Kellinghaus C, Alexopoulos AV, Burgess RC, Kumar AN, Han YH, Lüders HO, Leigh RJ: Effects of
eyelid closure, blinks, and eye movements on the electroencephalogram. Clin Neurophysiol 2005, 116, 878–885.
[17] Van Maanen A, Stapells DR: Comparison of multiple auditory steady-state responses (80 versus 40 Hz) and slow
cortical potentials for threshold estimation in hearing-impaired adults. Int J Audiol 2005, 44, 613–624.
[18] Van der Reijden CS, Mens LH, Snik AF: Frequency-specific objective audiometry: tone-evoked brainstem
responses and steady-state responses to 40 Hz and 90 Hz amplitude modulated stimuli. Int J Audiol 2006, 45,
40–45.
Address for correspondence:
Marcin Masalski
Department and Clinic of Otolaryngology, Head and Neck Surgery
Wroclaw Medical University
Borowska 213
50-556 Wrocław
Conflict of interest: None declared
Poland
Tel.: +48 71 734 37 00
Received: 7.02.2012
Mobile: +48 515 086 252
Revised: 6.07.2012
E-mail: [email protected]
Accepted: 12.08.2013