ORIGINAL PAPER

International Journal of Occupational Medicine and Environmental Health 2019;32(5):723 – 733

https://doi.org/10.13075/ijomeh.1896.01428

CERVICO-OCULAR REFLEX UPREGULATION

IN DIZZY PATIENTS
WITH ASYMMETRIC NECK PATHOLOGY
EWA ZAMYSŁOWSKA-SZMYTKE1, TOMASZ ADAMCZEWSKI2, JACEK ZIĄBER3, JOANNA MAJAK4,
JOLANTA KUJAWA2, and MARIOLA ŚLIWIŃSKA-KOWALSKA5
1
Nofer Institute of Occupational Medicine, Łódź, Poland
Audiology and Phoniatrics Clinic, Balance Disorders Unit
2
Medical University of Lodz, Łódź, Poland
Clinic of Medical Rehabilitation
3
Holy Family Medical Hospital, Łódź, Poland
4
Medical center “Medicover”, Łódź, Poland
5
Nofer Institute of Occupational Medicine, Łódź, Poland
Audiology and Phoniatrics Clinic

Abstract
Objectives: The aim of this study was to investigate whether the restriction in neck rotation and increased neck muscle tension could be causally
related to vertigo and dizziness. Material and Methods: Seventy-one patients reporting vertigo and/or imbalance were divided into 2 groups: 45 sub-
jects with unilateral restriction (R+) and 26 without restriction (R–) of cervical rotation and muscle tension in the clinical flexion-rotation test. The
normal caloric test was the inclusion criterion. The control group comprised 36 healthy volunteers with no history of vertigo. The vestibulo-ocular
reflex (VOR) and the cervico-occular reflex (COR) were measured through the videonystagmography (VNG) sinusoidal pendular kinetic test in the
conditions of not inactivated head and immobilized head, respectively. The VNG-head torsion test (VNG-HTT) nystagmus was recorded. Results:
Among the reported complaints, neck stiffness, headaches and blurred vision were more frequent in the R+ group than in both the R– group and
the control group. VNG revealed an increased COR gain and the presence of VNG-HTT nystagmus in the R+ group only. Similarly, only in the R+
group a positive relationship between COR and VOR was observed. Conclusions: Patients with asymmetric restriction in neck rotation and increased
neck muscle tension reveal the tendency to have an increased response of the vestibular system, along with co-existing COR upregulation. Further
research is needed to investigate the relationships between the activation of cervical mechanoreceptors and dizziness pathomechanisms. Int J Occup
Med Environ Health. 2019;32(5):723 – 33

Key words:
muscle tension, proprioception, dizziness, afferents, cervical vertigo, COR upregulation

Funding: this study was supported by the National Centre for Research and Development (project No. Strategmed 2/266299/19NCBR/2016, part of the “Prevention
and treatment of civilization diseases” program, entitled “Innovative system for evaluation and rehabilitation of human imbalance,” project manager: Prof. Mariola
Śliwinska-Kowalska).
Received: January 13, 2019. Accepted: August 26, 2019.
Corresponding author: Ewa Zamysłowska-Szmytke, Nofer Institute of Occupational Medicine, Audiology and Phoniatrics Clinic, Balance Disorders Unit, św. Teresy 8,
91-348 Łódź, Poland (e-mail: [email protected]).

Nofer Institute of Occupational Medicine, Łódź, Poland 723

 ORIGINAL PAPER     E. ZAMYSŁOWSKA-SZMYTKE ET AL.

INTRODUCTION cases. Vertigo or dizziness, cervical pain and a diminished

The cervical origin of headaches, dizziness or vertigo range of cervical motion were reported by post-traumatic
has been observed by specialists in combination with sig- patients diagnosed with atlanto-axial subluxation (AAS),
nificant controversy due to the lack of evidence for a link when atlanto-axial asymmetry was found in open-mouth
between cervical abnormalities, symptoms and objective anteroposterior (AP) radiographs. In addition, some de-
tests. In clinical practice, the cervical origin of vertigo and gree of asymmetry was noticed in the CT study on a large
dizziness is a common, even if not fully proven, explana- Chinese population of subjects with no history of trauma
tion offered to patients when no other reasons for their or other spine diseases [8]. In several more or less serious
dizziness can be established. In  consequence, symptoms diseases and clinical conditions listed above, dizziness may
of the functional origin may seriously handicap occupa- be attributed to a cervical pathology on the basis of pos-
tional practice and everyday living. Thus, there is a need sible pathophysiologic mechanisms.
for more clinical research, which could provide evidence Stimulation of the cervical afferent pathways has been
to understand the problem of cervical dizziness and help recognized as one of the possible pathomechanisms of
to develop a treatment program for the affected subjects. cervical dizziness. Unilateral stimulation of the neck with
The clinical syndrome of vertigo or dizziness that develops vibration stimuli generates a proprioceptive signal related
due to neck disorders has been named cervical dizziness. to the head-to-trunk position, which can induce illusions
Cervical dizziness may arise when pathological or inap- of head tilt, head rotation and visual motion  [9]. Weak,
propriate cervico-postural and cervico-ocular reflexes in- low-velocity nystagmus may be elicited in normal subjects
teract with vestibular and visual cues. According to Brandt by trunk rotation with the head immobilized and kept in
and Bronstein [1], symptoms of cervical dizziness would be the dark (thereby avoiding vestibular and visual stimula-
“a sensation of lightheadedness or floating unsteadiness tion). In such cases, cervico-occular reflex (COR) induces
and slight ataxia of stance and gait, perhaps more on head eye movements in response to proprioceptive signals from
turns,” and their suspected mechanism is proprioceptive. the neck. Animal studies suggest that cervical propriocep-
It has been suggested by Hulse [2] that one-third of all cas- tive afferents send collaterals directly to the ipsilateral
es of cervical dizziness are due to trauma, such as whiplash, medial and inferior vestibular nuclei and, by disynaptic
one-third have an insidious onset following spinal degener- contralateral pathways, to the medial, inferior and lateral
ation, and one-third exhibit other causes. Hain [3] has de- vestibular nuclei  [10]. Then, COR includes central ves-
scribed 3 main categories of cervical dizziness, depending tibulo-ocular reflex (VOR) pathways and is obscured by
of its origin: vascular, whiplash and cervical disorders oth- the other eye stabilization reflexes (vestibulo-ocular and
er than whiplash. Hypothetically, patients with a whiplash optokinetic) [11]. The gain of COR varies, depending on
associated disorder develop vertigo and imbalance due to the laboratory, from non-measurable [12–13] to < 0.25 at
disturbed proprioception in the facet joints of the cervical 0.1 Hz rotation [14], or even 0.65 for low velocities [15].
spine and deep muscles of the neck [4]. Cervical spondy- The COR can partially compensate for a complete loss of
losis is believed to be one of the causes of cervical dizzi- the VOR function which was observed in studies on mon-
ness although the literature contains data both for [5] and keys [16] and humans [17]. The COR gain increases with
against this theory [6]. In the study by Colledge et al. [7] age (particularly > 60), and there is a  significant nega-
investigating the causes of dizziness in the elderly, the au- tive correlation between the gains of VOR and COR in
thors attributed dizziness to cervical spondylosis in 65% of older populations [15]. An increase in the COR gain with

724 IJOMEH 2019;32(5)

 CERVICO-OCULAR REFLEX UPREGULATION IN DIZZINESS     ORIGINAL PAPER

reduced neck mobility and the lack of synergy between started with a careful neurological examination including
VOR and COR were observed in patients with whiplash- cranial nerves and cerebellar function assessment. In the
associated disorders [18]. In that group of patients, a re- case of any doubt or deficit, the MRI was performed,
duced cervical range of motion and a decreased relaxation which should be normal in order for the patient to be
ability of the cervical trapezoid muscles were observed. involved in the study. An ENT specialist performed an
Montfoort et al. [18] have hypothesized that an increased ear-nose-throat examination. Detailed questions were
COR may be caused by a reduced neck mobility while cer- asked about hearing difficulties, ear fullness and tinnitus.
ebellar disturbance may underlie the absence of adapta- Audiometric tests, such as pure tone audiometry, immit-
tion of both COR and VOR. tance audiometry and other relevant tests recommended
Cervical dizziness is a clinical syndrome which probably by specialists, were performed to rule out middle and/
incorporates multi-field cervical abnormalities. In theory, or inner ear pathologies. Those patients who present-
altered proprioception caused by damaged muscles, ten- ed hearing loss above their respective age-related val-
dons and the fibrous capsules in joints may cause postural ues were excluded from the study. Finally, information
imbalance, visual target movement and vertigo. In prac- was gathered about the potentially co-existing diseases,
tice, there is no clinical test to differentiate whether i.e., age-related cervical spondylosis, arrhythmia, hyper-
cervical dizziness develops, or does not develop, due to tension, orthostatic hypotension, thyroid disease, diabe-
neck pathology  [3]. Moreover, for the majority of neck tes, anemia, drug intake or psychiatric problems. Cardiac
symptoms, there is an absence of an identifiable under- function and blood pressure (BP) were also assessed. Pa-
lying disease or an abnormal anatomical structure. The tients with serious and unstable internal problems were
terms “mechanical neck disorder” and “non-specific neck not included in the study. A very detailed headache in-
pain” have been coined; those conditions are character- terview was performed, intended to reveal subjects who
ized by neck pain accompanied by headache, dizziness met the criteria of primary headache (migraine, tension
and a  limited range of motion, which are unrelated to headache) specified in the International Classification
any systemic problems of the cervical spine or soft tis- of Headache Disorders, 3rd edition (ICHD-3). All the
sues. It has been proposed that these problems may result patients underwent videonystagmography (VNG) assess-
from lifestyle factors, habitual posture and external neck ments: saccades, smooth pursuit, optokinetic, gaze nys-
muscle imbalance [19,20]. tagmus and bithermal Fitzgerald-Hallpike caloric tests.
Since the pathogenesis of cervical dizziness is poorly rec- The most relevant neuro-otological criteria of exclusion
ognized, and its link to the increased COR has not been from the study were as follows: vestibular imbalance in
proven, the aim of this study was to investigate whether VNG (canal paresis > 19%), benign paroxysmal position-
the asymmetric restriction in neck rotation and increased al vertigo (BPPV) signs in the Dix-Hallpike test, BPPV
neck muscle tension may activate the cervical afferent re- episodes during the previous year, Ménière’s disease, se-
sponse, which in turn could be linked to dizziness. rious head and neck traumas which involved the loss of
consciousness and long-lasting hospitalization, migraine
Description of study groups history and symptoms of cervical instability in the spe-
The study group prospectively included patients referred cialist physiotherapy examination (the Sharp-Purser and
to the Audiology Clinic or the Neurology Department Aspinall tests for transverse ligament of atlas and alar liga-
due to vertigo or dizziness. The patients’ evaluation ment stress tests).

IJOMEH 2019;32(5) 725

 ORIGINAL PAPER     E. ZAMYSŁOWSKA-SZMYTKE ET AL.

Finally, 71 subjects (including 15 males) with dizziness of examination did not reveal any diminished range of cervi-
an unknown origin (other than the impairment of vestibu- cal motion in this group. There were no statistically signifi-
lar function) were involved in the study. cant age differences between the R+ and C groups, while
Two study groups were created based on 2 independent ex- the subjects included in the R– group were generally older
aminations: the flexion-rotation test (FRT) performed by than those in the R+ and C groups.
a  neurologist, and the atlanto-occipital and atlanto-axial Informed consent was obtained from all the participants
mobility testing performed by a  physiotherapy specialist. in this research.
During FRT, the cervical spine was fully flexed and pas-
sively rotated to the right or left while noting the range of MATERIAL AND METHODS
motion and pain. A  one-side limited range of motion of Symptoms
> 10° measured with goniometry, and the painful restric- The patients were inquired in detail about such symptoms
tion in the joint play at the level of C0–C2, made the test as vertigo, dizziness, imbalance, headaches and neck pain,
positive in a yes–no manner. The physiotherapy examina- as well as visual disturbances (blurred vision and oscillop-
tion was performed according to the Kaltenborn-Evjenth sia). They were asked if these were head movements that in-
Orthopedic Manual Physical Therapy system in which duced these symptoms. A shortened version of the Vestibular
muscle tension was evaluated by palpation of the trapezius, Symptom Scale (VSS) was used to summarize the dizziness
elevator scapulae, sternocleidomastoideus and suboccipi- (vertigo and imbalance) and anxiety scoring. The VSS con-
tal muscles. The consistent results of these 2 tests formed sists of 15 items divided into 2 sub-scales: 8 items relating to
the basis for dividing the patients into 2 groups: vertigo-balance (VSS-V, score ranging 0–32), and 7 items re-
1) 45 R+ patients with a one-side diminished range of cer- lating to autonomic-anxiety symptoms (VSS-A, score rang-
vical motion (age (M±SD) 33.4±8.5 years), ing 0–28). The Duke Anxiety-Depression Scale (Duke-AD)
2) 26 R– patients with no limits or restrictions in cervical was used as a screening instrument for anxiety and depres-
rotation (age (M±SD) 46.1±14.8 years). sion. The Duke-AD is a 7-item brief screener for both clini-
Finally, the open mouth AP X-ray examination was per- cal anxiety and depression. The Duke-AD score cutoff point
formed in all the study patients to evaluate the functional of > 5 on a 0–14 scale was used.
findings. The area of interest included cases where the
odontoid peg was subtly rotated to the left or right with no VNG tests
anterior displacement of the atlas, and/or the lateral mass The VNG examination was performed using the comput-
C1 was rotated and asymmetric. The radiographic assess- erized videonystagmography set by VNG-Ulmer, Syna-
ment was blinded as for the clinical status of the patient. psys  SA. Real-time analysis of eye movements was per-
As a result of testing, 81% of the R+ group revealed asym- formed using light-occluded VNS Goggles (an IR high
metry in the open mouth AP X-ray examination while no resolution CCD camera). The system was connected to an
such abnormality was found in the R– group. Ulmer MED4 rotary chair and enabled the simultaneous
Additionally, VNG tests were compared to the control recordings of chair and eye movements.
group (C), which included 36 volunteers (mean age: The bithermal Fitzgerald-Hallpike caloric test was per-
30.9 years, SD 6.1) with no history of vertigo, dizziness or formed with water stimulation (30°C and 44°C). Reactivity
headaches. The exclusion criteria were the same as listed was calculated by the system as the sum of a  better ear
above for the study groups. The FRT and physiotherapy response and compared between groups.

726 IJOMEH 2019;32(5)

 CERVICO-OCULAR REFLEX UPREGULATION IN DIZZINESS     ORIGINAL PAPER

To assess VOR and COR, the sinusoidal pendular test revealed significance, the non-parametric Kruskal-Wallis
with a frequency of 0.25 Hz and an increasing-decreasing test was performed to compare the means. Then, the re-
amplitude of 0–49° was performed. The patients were test- sults were compared one-to-one between the groups, using
ed under 3 conditions: Student’s t-test or non-parametric Mann-Whitney U  test.
1) while turning around visible settings; the stimulation was Finally, the χ2 test was performed to compare the frequency
both visual and vestibular, and visual-vestibular interactions of these test results between the R+ and R– groups.
were assessed (visual-vestibulo-ocular reflex, VVOR); This project was approved by the Research Ethics Com-
2) while seated in absolute darkness, motionless; the stim- mittee of the Nofer Institute of Occupational Medicine
ulation was strictly vestibular; VOR was evaluated and (Project No. 12/2015). Clinical investigations were con-
recorded; ducted according to the principles stipulated in the Decla-
3) while seated in the absence of any visual or vestibular ration of Helsinki.
input (in absolute darkness), the patient’s head was held
manually by the technician to be motionless and the body RESULTS
was rotated by the chair (trunk-to-head rotation). Symptoms
To control the lack of head movement, a laser pointer was The main symptoms by study group are summarized in
mounted on the goggles and the still light dot was con- Table 1. The R+ group reported more frequent non-mi-
trolled by a  technician; COR was elicited and recorded. graine headaches, painful neck stiffness and blurred vi-
In  every case, the gain, i.e.,  the eye movement to chair sion, as compared to the R– group.
movement ratio, was calculated. The results of the questionnaire assessment of vestibu-
lar symptoms and psychological status are presented in
VNG head turning test Table  2. There were no statistically significant differenc-
During the VNG head turning test (VNG-HTT), the pa- es between the groups although the mean values of the
tient was sitting upright, in absolute darkness, wearing Duke-AD questionnaire scoring were slightly higher in
VNG goggles. The patient’s head was rotated gently about the R– group than in the R+ group. The frequency of the
the vertical axis to the end point of rotation (close to 90°), positive Duke-AD scoring (> 5) was 47% in the R+ group
and this position was maintained for 30 s. During this peri- and 73% in the R– group (p = 0.0044).
od, the examiner encouraged the patient to keep the eyes
in the center of the orbit. The eyes were monitored for the VNG tests
nystagmus development. The slow phase velocity (SPV) of The COR gain and the VNG-HTT SPV were significantly
nystagmus was recorded, and its horizontal, vertical and higher in the R+ group than in the R– group. Besides,
torsional components were analyzed in the last 10 s of the the COR gain, the VNG-HTT nystagmus and caloric re-
recordings to avoid vestibular stimulation. The torsional activity were higher among the R+ subjects than in the
component was used for calculations. healthy control group (Table 3). No correlations were ob-
served between the COR gains and the VNG-HTT SPVs
Statistical analysis in the study and control groups. The frequency of elevat-
The ANOVA test was used to compare the mean values of ed VNG-HTT (SPV > 1°/s) was higher in the R+ group
tested parameters between the 3 groups, and Levene’s test (56%) than in the R– group (19%, p = 0.0321) and the
was conducted before that comparison. When Levene’s test control group (22%, p = 0.0367).

IJOMEH 2019;32(5) 727

 ORIGINAL PAPER     E. ZAMYSŁOWSKA-SZMYTKE ET AL.

Table 1. Complaints reported by the patients during interviews of 71 subjects included in the study on vertigo and dizziness, Poland

R+ R–
Complaint (N = 45) (N = 26) p
n % n %
Vertigo 11 24 4 15 0.9646
Dizziness 37 82 21 81 0.8188
Imbalance 25 56 16 62 0.7188
Headache 42 93 14 54 0.0002
Head movement induced symptoms 16 36 6 23 0.3180
Blurred vision 10 22 1 4 0.0447
Painful neck stiffness 14 31 0 0 0.0000
Bolded are statistically significant differences between the R+ and R– groups for p < 0.05.
The χ2 analysis was performed to compare the frequency of symptoms and test results between the R+ and R– groups.

Table 2. Symptoms scoring according to the Vestibular Symptom Scale (VSS) and the Duke Anxiety-Depression Scale (Duke-AD)
in the study on vertigo and dizziness, Poland

Symptoms scoring
(M (SEM))
Scale pa
R+ R–
(N = 45) (N = 26)
Vestibular Symptom Scale
Vestibular 8.1 (0.4) 9.7 (0.7) 0.14455
Anxiety 8.8 (0.7) 10.7 (0.9) 0.10746
Duke Anxiety-Depresion Scale 6.1 (0.5) 7.8 (0.6) 0.05842
SEM – standard error of the mean.
a
R+ vs. R–.

Table 3. The videonystagmography test results in the study on vertigo and dizziness on a group of 71 subjects, Poland

Parameters
[°/s]
Videonystagmography parameter (M (SEM)) pa
R+ group R– group controls
(N = 45) (N = 26) (N = 36)
Caloric reactivity 50.7 (2.55)* 44.5 (3.80) 38.4 (2.85) 0.008
VOR gain in the kinetic test 0.49 (0.02) 0.45 (0.03) 0.49 (0.02) 0.819
COR gain in the kinetic test 0.22 (0.02)1* 0.09 (0.02) 0.10 (0.02) 0.000
VNG-HTT SPV 1.44 (0.15)2* 0.83 (0.21) 0.81 (0.15) 0.001
To compare the mean values of the study parameters between the groups, the ANOVA or Kruskal-Wallis test was used.
SEM – standard error of the mean.
COR – cervico-ocular reflex; SPV – slow phase velocity of the nystagmus elicited by head turning; VNG-HTT – head torsion test;
VOR – vestibulo-ocular reflex.
a
R+ vs. controls.
R+ vs. R–: 1 COR gain p = 0.000360; 2 VNG-HTT SPV p = 0.023544.
* Statistically significant differences between the study group and the control group.
Bolded are statistically significant differences between the study groups for p < 0.05.

728 IJOMEH 2019;32(5)

 CERVICO-OCULAR REFLEX UPREGULATION IN DIZZINESS     ORIGINAL PAPER

A positive relationship was found in the R+ group be- 0.7

a)

COR
tween the VOR and COR results (Figure 1a); no such cor- 0.6
relation was observed in the R– group (Figure 1b) and the
0.5
control group (Figure 1c). A positive correlation was also
0.4
found between the COR and VOR directional prepon-
0.3
derances (COR-DP and VOR-DP) in the R+ group only
(Spearman’s rank correlation coefficient 0.39, p = 0.003 0.2

in the R+ group, 0.14, p = 0.486 in the R– group, and 0.1

0.11, p = 0.520 in the control group). 0.0

VOR:COR: r = 0.3597, p = 0.0141
–0.1
0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
DISCUSSION VOR
Vertigo and dizziness are quite common symptoms, for b)
0.30
which cervical etiology may be suspected in some cases.
COR
0.28
VOR:COR: r = -0.1519, p = 0.4588
One of the pathophysiological theories assumes that ver- 0.26
0.24
tigo may be produced in response to distortion of vestibu- 0.22
0.20
lar and neck afferent impulses. Deep intervertebral neck 0.18
0.16
muscles and high cervical joint capsules and ligaments are 0.14
strongly responsible for proprioceptive activation; thus, the 0.12
0.10
muscle and ligament tension caused by an improper (asym- 0.08
0.06
metric) neck posture at the C1–C2 level has been assumed 0.04
0.02
to be the source of increased proprioception and, probably, 0.00
–0.02
dizziness. This study was based on the assumption that, in 0.2 0.3 0.4 0.5 0.6 0.7 0.8
the reference study group, there were signs of propriocep- VOR
tive activation caused by asymmetric increased muscle ten- 0.50
c)
COR

sion. The clinical picture in this group was also explored. 0.45 VOR:COR: r = -0.0623, p = 0.7180
The study group included patients from the Audiology 0.40

Clinic and the Neurology Department, who suffered from 0.35

0.30
vertigo and imbalance, as well as reported frequent head- 0.25
aches. The FRT and muscle palpation were used to di- 0.20
vide patients into 2 study groups. The R+ group included 0.15
patients who presented asymmetric muscle tension and 0.10
0.05
a one-side diminished range of head motion as compared
0.00
to the other side. The R– group included subjects without –0.05
muscle tension on palpation and abnormalities in FRT. 0.25 0.30 0.35 0.40 0.45 0.50 0.55 0.60 0.65 0.70 0.75
VOR
Both the R+ and R– study groups presented transient
vertigo, dizziness and imbalance, whose origin could not Figure 1. The correlation between the gains of vestibulo-ocular
reflex (VOR) and cervico-ocular reflex (COR)
be simply explained by the performed examination. Ad- in the pendular kinetic test; a) the R+ group, b) the R– group,
ditionally, a group of healthy volunteers were tested using c) control volunteers

IJOMEH 2019;32(5) 729

 ORIGINAL PAPER     E. ZAMYSŁOWSKA-SZMYTKE ET AL.

this study protocol. No one in the volunteers group suf- In order to reveal specific neck pathology, this study
fered from vertigo, dizziness, imbalance, painful neck stiff- focused on 2 clinical tests: FRT and muscle palpation.
ness or chronic headaches. Moreover, FRT and palpation Additionally, open-mouth X-ray scans were performed
did not reveal any abnormalities in this group; thus, the in the study groups to confirm the functional findings.
authors could not single out a non-symptomatic reference Flexion-rotation test is a simple clinical test used to as-
group that would be FRT positive. The mean age and age sess dysfunction at the C1–C2 motion segment [23] and is
distribution were similar in the R+ and control groups, characterized by high sensitivity and specificity to detect
while the R– group was significantly older. the presence or absence of cervical joint dysfunction [24].
As Brandt and Bronstein [1] have suggested, cervical dizzi- Although patients with serious conditions such as cervi-
ness may be suspected if other known reasons for vertigo, cal instability were excluded from the study, a  subtle
unsteadiness and oscillopsia are ruled out. In  this study, asymmetry at the C1–C2 level was observed in > 80%
the most common labyrinthine and vestibular nerve lesions of the R+ group, and in no subject in the R– group, on
were excluded by careful clinical examination, VNG ca- X-ray scans. These findings confirmed the assumptions
loric, kinetic tests and, if required, neuroimaging in both of asymmetric cervical abnormalities being the basis for
study groups. Migraine and psychogenic vertigo were taken functional asymmetry found in clinical tests. The upper
into consideration in the questionnaire and neurological cervical region is highly equipped with proprioceptors;
assessment. Patients with migraine were excluded from the thus, asymmetry in rotation restriction at this level could
study. Studies of patients with dizziness suggest that pri- be linked to a disturbed and asymmetrical proprioceptive
mary anxiety disorders cause dizziness in about 30% of the input.
dizzy population, anxiety and depression may be a result The objective signs of cervical pathology were investi-
of dizziness as well [21]. In this study, the anxiety level was gated by VNG kinetic and VNG-HTT tests. The ocular
measured with the Duke-AD. This simple questionnaire stabilization reflexes serve the purpose of stabilizing the
has been shown to be an effective brief screener for clinical visual image on the retina during head movements. COR
anxiety and depression [22]. According to the Duke-AD, is a week reflexive eye response that is elicited by rotation
the anxiety level was slightly higher in the R– group than of the neck with the head still, in darkness. The trunk-to-
in the R+ group. Concerning the possible vertigo explana- head movements stimulate the proprioception of muscles
tion, anxiety or depression might explain dizziness in 73% and the facet joints of the cervical spine. Some studies
of the R– group, and only in 47% of the R+ group. have outlined that in healthy subjects the COR gain may
The main clinical differences between the R+ and R– be absent or not higher than 0.1 [13], depending on the
study groups concern the frequency of neck pain and/or frequency and velocity of body rotation and the recording
stiffness, headaches other than migraine and transient technique. It is believed that COR can compensate for the
episodes of blurred vision. Frequent headaches which loss of vestibular function, particularly in low frequencies
were observed in > 90% of the R+ group were linked to of motion, which was observed in labyrinthine defective
increased muscle tension and a diminished cervical range patients [25]. The significant negative correlation between
of motion. Some headaches which originate in cervical the VOR and COR gains was found in healthy subjects
structures (including the C1–C2 junction) are classified as whose VOR decreased with age  [15]. In  this study, the
secondary cervical headaches according to ICHD-3 when COR gain was higher in the R+ group than in the R– and
the cervical background is proven. control groups, while the mean values of the kinetic VOR

730 IJOMEH 2019;32(5)

 CERVICO-OCULAR REFLEX UPREGULATION IN DIZZINESS     ORIGINAL PAPER

gain were similar in all groups. High vestibular response HTT nystagmus was produced in static conditions, when
in the R+ group was confirmed by high caloric reactiv- the head was rotated to one side and kept in that position.
ity, which was significantly higher in the R+ group than Moreover, the literature concerning the efficacy of HTT
among healthy controls. Moreover, Figure 1a presents as a test for cervical dizziness is very sparse.
a statistically significant positive relationship between the
kinetic VOR in the sinusoidal pendular test and COR in CONCLUSIONS
this test for the R+ group, which was not observed either Patients with asymmetric restriction in neck rotation and
for the R– group or for healthy controls. A similar propri- increased neck muscle tension reveal the tendency to have
oreceptive overstimulation was found in whiplash injury an increased response in the vestibular system, with co-
patients [18], as a result of reduced neck mobility and/or existing asymmetric COR upregulation. Clinically, such
cerebellar disturbances. The positive correlation between patients might develop blurred vision spells, painful neck
COR asymmetry and VOR asymmetry, assessed by direc- stiffness and headaches. Increased cervical afferent pro-
tional preponderance, was observed in the R+ group only, prioception could be an explanation for these symptoms
which may suggests some interaction between reflexes. in patients with neck pathologies, but further research is
The asymmetric modulation of VOR may, in some people, needed to investigate the relationships between the activa-
result from a transient blurred vision, vertigo or dizziness tion of cervical mechanoreceptors and dizziness.
and imbalance.
Nystagmus elicited by persisted head torsion was observed REFERENCES
in R+ patients in VNG-HTT. This test is also known as the 1. Brandt T, Bronstein A. Cervical vertigo. J Neurol Neurosurg
vertebral artery test. The nystagmus observed after torsion Psychiatry. 2001;71:8–12, https://doi.org/10.1136/jnnp.71.1.8.
of the head could be caused by changes in neck muscles, 2. Hulse M. Disequilibrium caused by a functional disturbance
joints, vascular structures or somatosensory innervation. of the upper cervical spine, clinical aspects and differential
It has been suggested that when the vertebral artery test re- diagnosis. Manuelle Medizin. 1983;1(1):18–23.
veals strong nystagmus, it may originate from vascular im- 3. Hain T. Cervicogenic causes of vertigo. Curr Opin Neu-
pingement, but weak horizontal nystagmus may be caused rol.  2015;28:69–73, https://doi.org/10.1097/WCO.0000000000
by alterations in the cervical root tone [3]. L’Heureux-Le- 000161.
beau et al. [26] have found that subjects with cervicogenic 4. Gimse R, Tjell C, Bjørgen I, Saunte C. Disturbed eye move-
dizziness exhibit > 2°/s nystagmus during the cervical tor- ments after whiplash due to injuries to the posture control
sion test, which is significantly more than in subjects with system. Clin Exp Neuropsychol. 1996;18:178–86.
benign paroxysmal positional vertigo. Weak nystagmus 5. Cevik R, Bilici A, Nas K, Demircan Z, Tekin RC. Non-inva-
observed in this study could be rather categorized as af- sive evaluation of vertebral artery blood flow in cervical spon-
ferent in origin. The increased muscle and joint tension dylosis with and without vertigo and association with degen-
might produce the response in the mechanism of central erative changes. Clin Rheumatol. 2015;29:541–6, https://doi.
mishmash between the expected and supplied impulsa- org/10.1007/s10067-010-1385-7.
tion. The lack of correlation between COR assessment 6. Bayrak IK, Durmus D, Bayrak AO. Effect of cervical spon-
and VNG-HTT may be caused by the testing conditions: dylosis on vertebral arterial flow and its association with ver-
COR was measured in dynamic conditions, when impulses tigo. Clin Rheumatol. 2009;28:59–64, https://doi.org/10.1007/
elicited by the left/right side movement were compared; s10067-008-0983-0.

IJOMEH 2019;32(5) 731

 ORIGINAL PAPER     E. ZAMYSŁOWSKA-SZMYTKE ET AL.

7. Collegde NR, Barr-Hamilton RM, Lewis SJ, Sellar RJ, Wil- modifications of the cervico-ocular (COR) and angular
son JA. Evaluation of investigations to diagnose the cause of vestibulo-ocular (aVOR) reflexes after canal plugging.
dizziness in elderly people: A community based controlled Exp Brain Res. 2011;5(3–4):549–60, https://doi.org/10.1007/
study. Br Med J. 1996;313:788–92, https://doi.org/10.1136/ s00221-011-2558-6.
bmj.313.7060.788. 17. Bronstein AM, Morland AB, Ruddock KH, Gresty MA.
8. Chen Y, Zhuang Z, Qi W, Yang H, Chen Z, Wang X, et al. Recovery from bilateral vestibular failure: implications for
A  three-dimensional study of the atlantodental interval in visual and cervico-ocular function. Acta Otolaryngol Suppl.
a  normal Chinese population using reformatted computed 1995;520:405–7, https://doi.org/10.3109/00016489509125283.
tomography. Surg Radiol Anat. 2011;9(33):801–8, https:// 18. Montfoort I, Van Der Geest JN, Slijper HP, De Zeeuw CI,
doi.org/10.1007/s00276-011-0817-7. Frens MA. Adaptation of the cervico- and vestibulo-oc-
9. Biguer B, Donaldson IM, Hein A, Jeannerod M. Neck mus- ular reflex in whiplash injury patients. J Neurotrauma.
cle vibration modifies the representation of visual motion 2008;25:687–93, https://doi.org/10.1089/neu.2007.0314.
and direction in man. Brain. 1988;111:1405–24, https://doi. 19. Bryans R, Decina P, Descarreaux M, Duranleau M, Mar-
org/10.1093/brain/111.6.1405. coux H, Potter B,  et  al. Evidence-based guidelines for the
10. Sato H, Ohkawa T, Uchino Y, Wilson VJ. Excitatory con- chiropractic treatment of adults with neck pain. J Manipu-
nections between neurons of the central cervical nucleus and lative Physiol Ther. 2014;37:42–63, https://doi.org/10.1016/
vestibular neurons in the cat. Exp Brain Res. 1997;115:381– j.jmpt.2013.08.010.
6, https://doi.org/10.1007/pl00005708. 20. Guo LY, Lee SY, Lin CF, Yang CH, Hou YY, Wu WL, et al.
11. Gdowski GT, McCrea RA. Neck proprioceptive inputs Three-dimensional characteristics of neck movements in
to primate vestibular nucleus neurons. Exp Brain Res. subjects with mechanical neck disorder. J Back Musculoske-
2000;35:511–26, https://doi.org/10.1007/s002210000542. let Rehabil. 2012;1(25):47–53, https://doi.org/10.3233/BMR-
12. Huygen PL, Verhagen WI, Nicolasen MG. Cervico-ocular 2012-0309.
reflex enhancement in labyrinthine-defective and nor- 21. Staab JP, Ruckenstein MJ. Which comes first? Psychogenic
mal subjects. Exp Brain Res. 1991;87:457–64, https://doi. dizziness versus otogenic anxiety. Laryngoscope. 2003;113:
org/10.1007/bf00231863. 1714–8, https://doi.org/10.1097/00005537-200310000-00010.
13. Schubert MC, Das V, Tusa RJ, Herdman SJ. Cervico-ocular 22. Parkerson GR, Broadhead WE. Screening for anxiety and
reflex in normal subjects and patients with unilateral vestibu- depression in primary care with the Duke Anxiety-Depres-
lar hypofunction. Otol Neurotol. 2004;1(25):65–71. sion Scale. Fam Med. 1997;3(29):177–81.
14. Sawyer RN, Thurston SE, Becker KR, Ackley CV, Seid- 23. Hall TM, Robinson KW, Akasaka K. Intertester reliability
man SH, Leigh RJ. The cervico-ocular reflex of normal hu- and diagnostic validity of the cervical flexion-rotation test.
man subjects in response to transient and sinusoidal trunk J Manipulative Physiol Ther. 2008;31:293–300, https://doi.
rotations. J Vestib Res. 1994;4(3):245–9. org/10.1016/j.jmpt.2008.03.012.
15. Kelders WP, Kleinrensink GJ, Van Der Geest JN, de Zee­ 24. Ogince MH, Hall T, Robinson K, Blackmore AM. The diag-
uw CI, Frens MA. Compensatory increase of the cervico-oc- nostic validity of the cervical flexion-rotation test in C1/2-re-
ular reflex with age in healthy humans. J Physiol. 2003;553: lated cervicogenic headache. Man Ther. 2007;8(12):256–62,
311–7, https://doi.org/10.1113/jphysiol.2003.049338. https://doi.org/10.1016/j.math.2006.06.016.
16. Yakushin SB, Kolesnikova OV, Cohen B, Ogorodnikov DA, 25. Carmona S, Nieto D. The specificity and sensitivity of un-
Suzuki J, Della Santina CC,  et  al. Complementary gain inhibited COR in labyrinthine-defective patients. Ann NY

732 IJOMEH 2019;32(5)

 CERVICO-OCULAR REFLEX UPREGULATION IN DIZZINESS     ORIGINAL PAPER

Acad Sci. 2005;1039:508–12, https://doi.org/10.1196/annals. dizziness. Otol Neurotol. 2014;12(35):1858–65, https://doi.

1325.055. org/10.1097/MAO.0000000000000506.
26. L’Heureux-Lebeau B, Godbout A, Berbiche D, Saliba I. Eval-
uation of paraclinical tests in the diagnosis of cervicogenic

This work is available in Open Access model and licensed under a Creative Commons Attribution-NonCommercial 3.0 Poland License – http://creativecommons.org/
licenses/by-nc/3.0/pl/deed.en.

IJOMEH 2019;32(5) 733