Acta Oto-Laryngologica

ISSN: 0001-6489 (Print) 1651-2251 (Online) Journal homepage: http://www.tandfonline.com/loi/ioto20

Role of the Cervical and Lumbar Proprioceptors

during Stepping

Hideyuki Fukushima & Manabi Hinoki

To cite this article: Hideyuki Fukushima & Manabi Hinoki (1985) Role of the Cervical and
Lumbar Proprioceptors during Stepping, Acta Oto-Laryngologica, 98:sup419, 91-105, DOI:
10.1080/00016489.1985.12005659

To link to this article: https://doi.org/10.1080/00016489.1985.12005659

Published online: 30 Apr 2018.

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Acta Otolaryngol (Stockh) 1985; Suppl. 419:91-105

Role of the Cervical and Lumbar Proprioceptors during Stepping

An Electromyographic Study of the Muscular Activities of the Lower Limbs

HIDEYUKI FUKUSHIMA' and MANABI HINOKJ2

From the 1Department a/Otolaryngology, Shizuoka City Hospital, 2 Shimane Medical School, Japan

Fukushima H, Hinoki M. Role of the cervical and lumbar proprioceptors during stepping:
An electromyographic study of the muscular activities of the lower limbs. Acta Otolaryn-
gol (Stockh) 1985; Suppl. 419:91-105.
To obtain evidence of the role of the cervical and lumbar proprioceptors during stepping,
the following investigations were carried out. I) 10 normal, healthy subjects and vertigi-
nous patients, particularly those with lumbar pain, were examined. 2) Fukuda's stepping
test was first carried out, followed by two modified stepping tests, i.e., stepping after fixing
the waist with a corset and after fixing the neck with a collar. 3) Electromyograms (EMGs)
of the gastrocnemius muscles of the extensor of the lower limbs were analysed as regards
the foot contact with the ground. The following results were obtained. In the original way
of Fukuda's stepping test, normal subjects tended to show EMG discharges from the
gastrocnemius muscles before foot contact with the ground, whereas in the modified
stepping tests, the generation of EMG discharges was delayed, especially in the test
requiring fixing of the Waist with a corset. The results of these stepping tests were reversed
in the vertiginous patients, particularly in those with lumbar pain. We conclude that the
lumbar proprioceptors participate especially in the smooth performance of stepping by
promoting the anticipatory activity of the extensor of the lower limbs. Key words:
Fukuda's stepping test, modified stepping test, anticipatory activity.
H. Fukushima, Department of Otolaryngology, Shizuoka City Hospital, 10-93 Ohtemachi,
Shizuoka, 420 Japan.

Walking, a basic movement in daily life, is closely related with dynamic equilibrium in
humans. The centre of gravity is higher in humans than in many animals and moreover,
stepping or walking in humans consists of alternating, continuous repetition of standing on
one leg. Since this method of locomotion is unstable from the standpoint of body equilibri-
um, various equilibrium reflexes must come into play in order to achieve smooth perfor-
mance of this motion.
In tests on normal, healthy adults, Kitahara & Matsubara (l) reported that during
stepping in Fukuda's test the head inclined slightly to the right when the right foot was set
down and the left foot was lifted, and vice versa. They explained this finding on the basis
of the tonic neck and the tonic labyrinthine reflexes. We devised a new apparatus, called
the drift meter, with which we could record side to side and back-and-forth movements of
the head as an angular deviation of the head from the upright position. With this apparatus,
we investigated the relationship between movements of the head and the feet during
stepping. In a series of examinations we noted the following facts. l) Movements of the
head and the feet during stepping were correlated. This correlation could be explained on
the basis of the tonic neck reflex. 2) A rebound phenomenon was elicited in the move-
ments of the head during stepping. This phenomenon seemed to be helpful in reinforcing
the tonic neck reflex, and led to a smooth performance of stepping (2).
Tokizane et a!. (3) reported that walking or stepping was significantly influenced by the
tonic lumbar reflex elicited from the lumbar proprioceptors and which controlled the
muscle tone of the four limbs in the formation of static and dynamic postural reflexes.
Earlier, we reported that the lumbar proprioceptors were coordinated with the cervical
92 H. Fukushima and M. Hinoki

proprioceptors during stepping, resulting in a smooth performance of this action. This

conclusion was drawn from the fact that the inclination of the head to the trunk during
stepping tended to increase when the subject's waist was fixed with a corset. Furthermore,
the reason that we used corset fixation was that in normal subjects this procedure tended
to limit movement of the waist, which led to a lack of adequate activity by the lumbar
proprioceptors, and this was detrimental to the movements of the lower limbs during
stepping (4). Thus, the phenomenon seen in a normal subject with the waist fixed by a
corset indicated that compensatory reinforcement of the tonic neck reflex was induced so
that the possible occurrence of ataxic gait due to lack of adequate activity by the lumbar
proprioceptors could be inhibited. In other words, this result supported the postulation
that the lumbar proprioceptors may play a major role in the smooth performance of
stepping.
In order to carry out various movements, particularly rhythmic movements, subjects
must predict the possible situation of the motion and promote the anticipatory activities of
the eye muscles and of the trunk and limb muscles necessary for this motion.
The present investigations were undertaken to ascertain whether or not the cervical and
lumbar proprioceptors participate in the smooth performance of stepping, by promoting
the anticipatory activities of the muscles, particularly those of the lower limbs-and
moreover, which is the more important of the two proprioceptors, cervical or lumbar, with
regard to the above-mentioned promotion.

MATERIAL AND METHODS

1. Investigation related to role of lumbar proprioceptors in the performance
of stepping in normal subjects (Investigation 1 a)
(a) Subjects examined. Ten normal, healthy adults were examined using Fukuda's step-
ping test. In these subjects, electromyograms (EMGs) were recorded during stepping,
using surface electrodes and transmitted by telemetry from the anterior tibial muscles and
the gastrocnemius muscles, the antagonists of the lower limbs.
The EMGs appearing in these subjects were classified into three types, viz., Type A,
Type B and Type C, according to the action of these muscles during stepping. In Type A,
the rest and active periods in the EMGs were clearly distinguished in the two above-
mentioned muscles and moreover, reciprocal discharges were observed in the antagonistic
muscles. This type of EMG was observed in 2 out of 10 subjects examined. In Type B, the
rest and active periods in the EMGs were clearly distinguished in the two muscle groups.
However, in the EMGs of the anterior tibial muscles their manner differed from Type A in
having the main activity of the entire period not only in the swing phase but also in the
stance phase. This type of EMG was observed in 5 out of 10 subjects examined. In Type
C, in the EMGs from the anterior tibial muscles, the rest and active periods were not
differentiated and marked EMG discharges were observed throughout the entire stepping
phase, although these two periods were clearly distinguished in the gastrocnemius mus-
cles. This type of EMG was observed in 3 out of 10 subjects examined.
(b) Method of examination and assessment of the correlation between the EMGs from
the two above-mentioned muscle groups and movements of the feet during stepping. (i)
The method of stepping used here was Fukuda's stepping test (5). The total number of
steps adopted was fifty. The test was frrst carried out in the original manner and then
performed again after fixing the waist with a corset. The reason we used the latter
procedure, i.e., waist fixing with corset, was as described in the introductory remarks.
(ii) To assess the correlation between the EMGs from the antagonistic muscles of the
lower limbs and foot movements we adopted the following method. A rectangular thin
 Role of cervical & lumbar proprioceptors during stepping 93

Fig. 1. Block diagram.

metal plate was fixed to the surface of the anterior part of the sole of each foot and
subjects were instructed to perform stepping on the 2-metre-square iron plate on the
ground. When the sole of one foot touched the plate, an electric current was triggered and
recorded as an on-signal. When the sole of one foot left the ground, the current was broken
and was recorded as the off-signal (Fig. l). In the following figures, the on-signal is
expressed by an upward movement of the pen, and the off-signal as a downward move-
ment.
The EMGs were compared in the two conditions, i.e., with and without a corset,
particularly with reference to the correlation between the onset of the EMGs of the
gastrocnemius and the moment the foot contacted the ground plate during stepping. The
reason why the EMG from the gastrocnemius was especially analysed in this investigation
was that this muscle belongs to the extensors of the lower limbs and consequently it
supports the weight of the whole body throughout stepping. With reference to the above-
mentioned correlation, generation of the EMGs from the gastrocnemius muscles was
classified into the following three patterns: Preceding (P), Simultaneous (S), and Delayed
(D). In P, Sand D, the EMGs showed the preceding, simultaneous, and delalyed genera-
tion in relation to the moment the foot contacts the ground. Thus, EMG discharges starting
more than 40 msec before foot contact were counted as P pattern and those delayed by
more than 40 msec after foot contact were counted as D pattern. EMG discharges starting
within 40 msec before or after foot contact were therefore counted as S pattern (Fig. 2).

of the foot r
On and off sognals - - . . , ' - - - - -
--,'-----~

'
EMGs of the
gastrocnem•us

contact of the contact of the contact of the

foot w•th tne foot w1th the foot with the
ground ground ground

_Ereceding .Simultaneous Delayed

(P pattern) (S pattern) To pattern)

Fig. 2. Scheme of the correlation between the onset of the EMGs of the gastrocnemius and the moment when the
foot touches the ground during stepping.
94 H. Fukushima and M. Hinoki

2. Investigation related to role of lumbar proprioceptors in performance of stepping

by vertiginous patients (Examination 1 b)
(a) Subjects examined. The test was made on 4 vertiginous patients, of whom 3 had
sustained head and neck injury. According to the results of the equilibrium tests, they
were diangnosed as having bilateral impaired labyrinthine function (case I), dysfunction of
the central nervous system, particularly the brain stem (case 3), and impairment of
labyrinthine function on the right side combined with dysfunction of the central nervous
system, particularly the brain stem (case 4). The fourth case was a non-traumatic patient
who was diagnosed as having impaired labyrinthine function on the left side (case 2).
These 4 patients complained of pain and/or stiffness in the lumbar region.
(b) Method of examination and assessment of the correlation between the EMGs from
the above-mentioned two muscles and movement of the feet during stepping. Fukuda's
stepping test was also carried out in the 4 vertiginous patients in whom the EMG recording
was made in the same way as described for the normal subjects. Results were compared in
the two above-mentioned conditions, viz., before and after fixing the waist with a corset.
Furthermore, according to Ushio & Hinoki (4), investigating vertiginous patients with
lumbar pain, fixing of the waist with a corset tended to act favorably on the impaired
activity of the lumbar proprioceptors, by which the impaired dynamic equilibrium, such as
in stepping, was significantly ameliorated. The assessment of the correlation between the
EMGs from the gastrocnemius muscles and movements of the feet during stepping was the
same as that described in Examination I a.

3. Examination of role of cervical proprioceptors when performing stepping

in normal subjects (Investigation 11)
(a) Subjects examined. Seven normal, healthy subjects were examined, belonging to
groups A and B in the EMGs in Investigation I a.
(b) Method of examination and assessment of correlation between EMGs from the two
above-mentioned muscles and movements offeet during stepping. Fukuda's stepping test
was carried out in the 7 normal, healthy subjects, both before and after fixing the neck
with a collar. The reason for using this procedure was that in normal subjects, it tended to
limit movement of the neck, causing lack of adequate activity of the cervical propriocep-
tors, and thus detrimentally affecting the movements of the lower limbs during stepping
(4). Furthermore, in these subjects, the EMG recording was made in the same way as that
described in Investigation I a. Results were compared before vs. after fixing the neck with
a collar. Assessment of the correlation between the EMGs from the gastrocnemius
muscles on the two sides and movements of the feet during stepping was the same as that
described in Investigation I a.

RESULTS
I. Investigation 1 a
(a) Representative case. Fig. 3 shows the EMGs from the gastrocnemius on the right side
of a 36-year-old healthy man. These EMGs were recorded before and after fixing the waist
with a corset. This man showed a Type A EMG, which did not alter significantly after
fixing the waist with a corset. However, through the above-mentioned procedure, the
correlation between the onset of EMG discharge of the gastrocnemius and the moment of
contact of the right foot with the ground altered, showing a significant reduction in
generation of P pattern and frrst signs of a developing D pattern. The bar graphs (lower
part of Fig. 3) show the distribution of P, S and D patterns generated in all the EMG
discharges of the gastrocnemius muscles on the two sides during stepping. Fig. 3 shows
 Role of cervical & lumbar proprioceptors during stepping 95

without a corset with a corset

Fig. 3. EMGs from the gastrocnemius on the right side of a 36-year-old normal man and bar graphs of distribution of
P, S and D patterns of EMG discharges of bilateral gastrocnemius muscles generated throughout the period of
stepping before and after fixing the waist with a corset.

that develoment of P pattern decreased, whereas that of S pattern increased. Furthermore,

D pattern first developed after the above-mentioned procedure.
(b) Overall results in all cases. Fig. 4 and Table I show the distribution of P, S and D
patterns generated in 10 normal subjects, before and after fixing the waist with a corset. In
subjects with Type A and B EMGs, P pattern generation decreased, whereas that of S
pattern increased. Furthermore, in 4 out of 7 subjects examined, D pattern first developed
after the above-mentioned procedure, whereas one subject showed disappearance of this
pattern. In subjects with a Type C EMG, the above-mentioned tendency was not so
obvious as in those with Types A and B. In 3 subjects, there was little evidence of D
pattern throughout the examination. In 2 out of 3 subjects, P pattern generation decreased,
whereas that of S pattern increased, after fixing the waist with a corset. In the remaining
subject, P pattern increased even with the corset procedure (Table 1). Furthermore, by
using the t-test, we tested the difference between the two conditions, with and without a

,. Type A -group Type 8- group Type C- group

· -. ··-tiL JL JL lk l
PSO PSO PSO PSO PSO PSO
JL l JL l
PSD PSD PSO PSO

"

. . . . ~UiJL !_ 1_ JL l
PSO
ll>.l
PSO
lt>.1
PSO
1111..)
PSO
IIID.4
PSO
MD.!t
PSO
Ma.6
Al1L l
PSO
ta..J
PSO
No.I
PSO
MD.9
PSO
~10

Fig. 4. Bar graphs of distribution of P, Sand D patterns generated in 10 normal subjects before and after fixing the
waist with a corset.
96 H. Fukushima and M. Hinoki

on and off signals

of the foot on the
right side
Gastrocnemius (EMG)

P S D P S D

without a corset with a corset

Fig. 5. EMGs from gastrocnemius on right side of a 68-year-old man with head and neck injury. Bar graphs of
distribution of P, Sand D patterns generated before and after fixing the waist with a corset.

corset, with regard to the distribution of development of three EMG patterns. As a result
of this test, we noted that the above-mentioned difference was statistically significant in P
and S patterns (p<O.Ol). Thus, the change could be regarded as definite in P and S
patterns.

2. Investigation 1 b
(a) Representative case. Fig. 5 shows EMGs from the gastrocnemius on the right side of a
68-year-old man, recorded before and after fixing the waist with a corset. This man
developed vertiginous attacks and cervical and lumbar pain after head and neck injury.
Equilibrium and neurological examinations revealed an impaired labyrinthine function on
both sides and hypertonicity of the cervical and lumbar soft supporting tissues. After
fixing the waist with a corset, particularly vertigo and lumbar pain were significantly

Table I. Change in development of P, S and D patterns in the EMGs in normal, healthy

subjects after fvcing the waist with a corset

Patterns of EMGs
Change in development
Subjects of EMG patterns P pattern S pattern D pattern

Group of types A and B Increase or 0 7 4

(subjects examined n=7) appearance
Unchanged 0 0 2G
Decrease or 7 0 1
disappearance
Group of type C Increase or 2 0
(subjects examined n=3) appearance
Unchanged 0 0 JG
Decrease or 2 1 0
disappearance
Total 10 10 10

" These subjects did not develop a D pattern either before or after fixing the waist with a corset.
 Role of cervical & lumbar proprioceptors during stepping 91

80

60

without a corset 40

20

P 5 D
lLJL_h_
P 5 D P 5 D P 5 D

80

60

with a corset 40

20

P 5 D P 5 D P 5 D P 5 D

No.1 No.2 No.3 No.4

Fig. 6. Bar graphs of distribution of P, S and D patterns generated in 4 vertiginous patients before and
after fixing the waist with a corset.

ameliorated. This was evident from the fact that after the corset procedure, his stepping
altered in nature, showing a significant decrease in ataxic features. Furthermore, as shown
in the upper part of this figure, generation of the S pattern increased, whereas the D
pattern disappeared after waist fixation. The bar graphs (lower part of Fig. 5) show the
distribution of P, S and D generation patterns in all the EMG discharges of the gastrocne-
mius muscles on both sides during stepping. These bar graphs show that the development
of P pattern increased markedly, whereas D pattern decreased following the corset
procedure. S pattern showed no significant change.
(b) Overall results in all cases. Fig. 6 and Table II show the distribution of P, Sand D
generation patterns in the 4 vertiginous patients. From these, we found that the P pattern
tended to increase, whereas the D pattern decreased and/or disappeared after fixing the
waist with a corset. No definite tendency was observed with regard to S pattern genera-
tion.

Table II. Change in development of P, S and D patterns in the EMGs in vertiginous

patients after fu:ing the waist with a corset

Patterns of EMGs
Change in development of
EMG patterns P pattern S pattern D pattern

Increase or appearance 2 2 0
Unchanged I 0 Ia
Decrease or disappearance I 2 3
Total 4 4 4

a This subject did not develop a D pattern either before or after fiXing the waist with a corset.

7-848420
98 H. Fukushima and M. Hinoki

P 5 D P 5 D

without a collar with a collar

Fig. 7. EMGs from gastrocnemius on right side of a 36-year-old normal man. Bar graphs of distribution ofP, Sand D
patterns generated before and after fixing the neck with a collar.

3. Investigation 11
(a) Representative case. Fig. 7 shows EMGs from the right side gastrocnemius muscle of a
36-year-old nonnal man (same subject as illustrated in Fig. 3). Neither abnormal deviation
nor ataxic features in stepping were observed after fixing the neck with a collar. However,
the above-mentioned procedure altered the correlation between the onset of the EMG
discharge of the gastrocnemius and the moment the right foot touched the ground, showing
a reduced generation of P pattern and first signs of the development of D pattern. The bar
graphs of distribution of development of P, S and D patterns (lower part of Fig. 7) show
that P pattern generation decreased, whereas that of S pattern increased. Furthennore, D
pattern first developed after the collar procdure. This tendency was similar to that after
fixing the waist with a corset, though the decrease in P pattern and development of D
pattern was less obvious with a collar than with a corset (cf. Fig. 3).
(b) Overall results in all cases. Table III shows the change in P, S and D generation
patterns in 7 nonnal, healthy subjects, after fixing the neck with a collar. In these subjects,
there was a tendency for the development of P pattern to decrease, whereas the S pattern
increased after fixing the neck with a collar. Furthennore, in 4 of the 7 subjects, D pattern
first developed after the collar procedure, although one subject showed complete disap-
pearance of this pattern.

Table III. Change in development of P, S and D patterns in the EMGs of normal, healthy
subjects after .fu:ing the neck with a collar

Patterns of EMGs
Change in development
Subjects of EMG patterns P pattern S pattern D pattern

Group of types A and B Increase or 5 4

(subjects examined n=7) appearance
Unchanged 1 2 (l")
Decrease or 6 I
disappearance

" This subject did not develop aD pattern either before of after fiXing the neck with a collar.
 Role of cervical & lumbar proprioceptors during stepping 99

80
80
60
60
40 40
40
20 20
20

P 5 D P 5 D P 5 D

Without a corset With a corset With a collar

and/or a collar
Fig. 8. Bar graphs of distribution of P, Sand D patterns in a 36-year-old man, generated before and
after fixing both neck and waist.

As the result of the t-test used, we found no definite statistical difference in results of
testing with vs. without the collar, with regard to development ofthe three patterns in the
EMGs during stepping. Thus, the resulting change in the development of the three patterns
due to fixation of the neck was considered not to be so definite as that due to fixation of
the waist.

4. Comparison between the two conditions, i.e., neck and waist fuation,
with regard to the resulting change in development of the three EMG patterns
during stepping
Fig. 8 shows the bar graphs of distribution of development of P, S and D patterns in the
EMGs of a 36-year-old normal, healthy man, calculated from the results of stepping before
and after fixing the neck and waist. As shown, there was a similarity between the two
types of stepping, with regard to the resulting change in the three above-mentioned
patterns in the EMGs. However, the decrease in P pattern and the development of D
pattern were more obvious in the case of fixation of the waist than in that of the neck.
Fig. 9 and Table IV show the overall results in all cases. Similar findings were observed
except in case 3 between the two above-mentioned two types of stepping, with regard to
the resulting change in the development of P and S patterns. However, development of D
pattern was more marked in the case of fixation of the waist than in that of the neck.

DISCUSSION
I. Physiological implication of the development of three types of EMG
(P, S and D patterns), particularly of the P pattern, during stepping
We have reported earlier that the neck and lumbar proprioceptors control the muscle tone
of the lower limbs via the tonic neck and lumbar reflexes, thus accomplishing a smooth
performance of stepping (2). In the present examination, we found that these receptors
participate in the smooth performance of stepping by promoting the anticipatory activities
of the extensores of the lower limbs. In other words, in normal human subjects, the
gastrocnemius muscles tended to produce preceding EMG discharges (P pattern) in
relation to the moment of contact of the foot with the ground during stepping, which led to
the induction of adequate activities of the lower limb extensors sufficient to support the
weight of the whole body with one leg. Naturally, these muscles also developed simulta-
neous EMGs in relation to the above-mentioned moment and thus an S pattern was
induced. However, the S pattern was significantly less common than the P pattern. EMG
100 H. Fukushima and M. Hinoki

Type A group Type B group

%

JL JL Ll l jl_
80
60
without
40

20

PSD PSD PSD PSD PSD PSD

80

1L 1L l JL l !
60
with a corset
40

'?C

% PSD PSD PSD PSD PSD PSD PSD

JL l 1L iL l JL
80

60
with a collar
40

20

PSD PSD PSD PSD PSD PSD PSD

No.1 No.2 No.3 No.4 No.5 No.6 No.7

Fig. 9. Bar graphs of distribution of P, Sand D patterns generated in 7 normal subjects, before and
after fixing both waist and neck.

discharges, which appeared with a delay after contact of the foot with the ground, viz. D
pattern., were seen in only one out of 10 subjects examined.
In order to carry out rhythmic movements, subjects are requested to predict the possible
situation of the movements and to promote the anticipatory activity of the eye muscles, of
the trunk and limbs, adequate for such movements. The above-mentioned results in the
present examination are considered to exemplify this postulation.
Engberg & Lundberg (6) reported that when unrestrained cats walked, the electromyo-
graphic activity in many hindlimb muscles was correlated with the angular movements in

Table IV. Comparison between results from two types of stepping, viz. stepping with a collar and/or a
corset, with regard to development of P, S and D patterns in the EMGs of normal, healthy subjects

Patterns of EMGs

P pattern S pattern D pattern

Change in
development of Fixation Fixation Fixation Fixation Fixation Fixation
Subjects EMG patterns of neck of waist of neck of waist of neck of waist

Group of types A and B More marked 0 2 3 0 3

(subjects examined n=7) increase
More marked 2 3 0 0 0
decrease
Change in equal 4 (2a)
degree

a These subjects did not develop a D pattern either before or after fixing the neck and/or the waist.
 Role of cervical & lumbar proprioceptors during stepping 101

the hip, knee and ankle joint. Furthermore, the activity is fairly uniform in all the extensor
muscles but differs between individual functional groups of the flexor muscles.
These results are instructive in understanding the possible presence of a correlation
between the lumbar proprioceptors and the activity of the lower limb extensors during
stepping. Furthermore, Lundberg (7) reported that when unrestrained cats walk, the
EMGs from the extensors of the hip, knee and ankle appeared just before (100 msec) the
contact of the feet with the ground and moreover, this phenomenon developed constantly,
not depending on the speed of walking and/or running. Thus, the above-mentioned
phenomenon is not attributed to the stretch reflex which is induced by stimulation of the
receptors of the muscles and the skin due to the contact of the feet with the ground. Hence
he assumed that the above-mentioned action of the extensors is due to a centrally
programmed alternating activation of the extensors and flexors.
Udo (8) put forward a similar postulation in which he stated that this EMG phenomenon
can be explained by the following mechanism. The phenomenon is fundamentally due to
centrally programmed alternating activation of the extensors and flexors, produced in the
rhythmic centre in the spinal cord and moreover, probably modified by the spinal reflexes
occurring in six muscles including the extensors and flexors of each leg during stepping.
Grillner (9) found that during walking, cats had a considerably increased tone in the
gastrocnemius muscles at the moment when the hindlimb touched the ground. From this,
he deduced that this phenomenon cannot be attributed to the stretch reflex of the hindlimb
muscles, since any alteration in muscle tone could be manifested first several microse-
conds after alteration in the volleys from the motoneurons of the muscles. The results
reported by Lundberg (7), Udo (8) and Grillner (9) were obtained in cats. Therefore,
results in the present examination using humans may not be directly comparable with
those obtained with quadrupeds. Stability of the body when walking or stepping is
significantly less sure in humans than in animals, since in humans the centre of gravity is
higher and the area of support for the soles, related to the body's stability, is significantly
less. Accordingly, activation of the anticipatory activity of the extensor muscles (the
gastrocnemius) is more crucial in humans than in quadrupeds, as regards maintenance of
dynamic equilibrium, such as in stepping. Thus, the fact that in many normal, healthy
subjects, the development of P pattern was far more common than other EMG patterns
can be reasonably explained from the standpoint of the body's equilibrium. Furthermore,
the above-mentioned results seem valuable, since in humans, systematic investigations
have not hitherto been carried out on this problem.

2. Comparison between the role of the cervical and lumbar proprioceptors,

with regard to the resulting change in development of the three
EMG patterns (P, Sand D) during stepping
As previously mentioned, Udo (8) reported that in quadrupeds such as cats, the
rhythmic centre of the forelimbs related to walking is located in the cervical cord, whereas
that of the hindlimbs is located in the lumbar cord. In humans, the rhythmic centre is
probably located in the lumbar cord, since a similarity has been found between the activity
of the hind limb muscles of quadrupeds and that of the lower limb muscles in humans, with
regard to production of postural reflexes such as the tonic lumbar reflex (3). Thus, the
activity of the lumbar proprioceptors seems to correlate particularly with that of the
rhythmic centre in the lumbar cord, as regards the development of dynamic equilibrium,
such as in stepping. Is it possible that the present results support such a postulation? As
mentioned above, when movements of the neck and/or waist were restricted by fixing
these regions, normal, healthy subjects tended to show a decrease in P pattern and/or
increase in D pattern, respectively. It is remarkable that this tendency was more evident
102 H. Fukushima and M. Hinoki

when wearing a corset than when wearing a collar. That is, the resulting change in the
generation of P and S patterns during stepping with a corset was statistically significant
when tested with the t-test. By gross observation, a similar tendency was observed with
regard to the resulting change in generation of P, S and D patterns during stepping with a
collar (Table III). However, by using the t-test, this alteration was found to be not so
marked as in the case of stepping with a corset. Furthermore, the D pattern was more
common when wearing a corset than when wearing a collar (Table IV). These results lead
to postulation that a more important role may be played by the lumbar proprioceptors than
by the cervical proprioceptors, with regard to performance of stepping. These results also
support the postulation proposed by Lundberg (7) and Udo (8), since they stated that the
rhythmic centre of the hindlimbs related to walking is located in the lumbar cord.
Furthermore, it is compatible with the postulation of Tokizane et a!. (3), since they
reported that the lumbar proprioceptors control particularly the muscle tone of the lower
limbs via the tonic lumbar reflex, resulting in smooth stepping. The postulation that the
activity of the lumbar proprioceptors probably correlates with generation of the three
EMG patterns, particularly of the P pattern, is also supported by the following. We
examined vertiginous patients with pain and/or stiffness of the waist by observing the
resulting change in development of the three EMG patterns (P, S and D) during stepping
with a corset. In this examination, we noted that the P pattern increased, whereas the D
pattern decreased after the above-mentioned procedure. It is worth noting that quite the
opposite tendency was observed between normal subjects and vertiginous patients with
pain and/or stiffness of the waist, with regard to the resulting change in generation of P and
D patterns in the EMGs. These results also support the postulation mentioned above.

3. Comparison between results from subjects with Type A and B EMGs

and those with Type C EMGs
The question then arises: what is the difference between results from subjects with Type A
and B EMGs and those with a Type C EMG, with regard to the resulting change in the
development of P, S and D EMG patterns during stepping with a corset. As previously
mentioned, similarity was, of course, found between the two groups of subjects with
regard to results obtained in the above-mentioned stepping. However, it should be noted
here in the same type of stepping, some differences were found between these two groups
of subjects, indicating that a more marked decrease in P pattern and increase in S pattern
were observed in subjects with Types A and B than in those with Type C. Furthermore,
alteration, particularly increase in D pattern generation, was clearly observed in the
former subjects, whereas this pattern was never observed in the latter before or after fixing
the waist with a corset. All these subjects were normal, healthy adults. However, the
EMGs of Types A and B differ from those of Type C regarding the following point. In the
former types of EMG, the resting and active periods in the EMGs of the anterior tibial
muscles and gastrocnemius muscles were clearly distinguished during stepping.
In contrast, in the latter type of EMG, the resting and active periods in the EMGs of the
anterior tibial muscles were not clearly distinguished during the entire period of stepping,
although the two periods were observed in the gastrocnemius muscles.
According to Nakagawa's report of 1973 (10), development of EMGs of Types A and B
probably indicate the presence of a well developed equilibrium function when compared
with that of Type C EMGs, since the former, particularly Type A, often developed in
athletes and ball game players. In contrast, the C Type EMG was frequently observed in
infants and elderly subjects. Naturally, no definite evidence has been proposed as to
whether these differences with regard to the resulting change in development of P, S and D
patterns between the two groups of subjects are due to differences in the activity of the
 Role of cervical & lumbar proprioceptors during stepping 103

lumbar proprioceptors and/or that of the rhythmic centre related to stepping in these
subjects. However, the fact that results obtained in the subjects with Type C EMGs was
between those of normal, healthy subjects with Types A and B and vertiginous patients
with pain and/or stiffness of the lumbar region is worthy of consideration.

4. Correlation between activity of lumbar proprioceptors and rhythmic centre

related to walking and/or stepping
With reference to fibre connections in the central nervous system and electrophysiological
results previously reported (7), possible connections between the lumbar proprioceptors
and rhythmic centre related to walking and/or stepping are considered as follows:
(i) lumbar proprioceptors-posterior roots of the spinal nerves at the level of the lumbar
cord-lumbar cord-rhythmic centre of the lumbar cord related to walking and/or
stepping-motoneurons in the lumbar cord-muscles, particularly the extensors of the
lower limbs;
(ii) limbar proprioceptors-posterior roots of the spinal nerves-limbar cord-ventral
and posterior spinocerebellar tracts (VSCT, PSCT)-cerebellar vermis-Purkinje cells of
the cerebellar vermis, Deiters' nucleus-Deitero-spinal tract, red nucleus-rubrospinal
tract, motor cells in the reticular formation-reticulospinal tract, rhythmic centre in the
lumbar cord-muscle, particularly the extensors of the lower limbs.
With reference to the mode of the connections described in (ii), the following reports
must be referred to. Shik et al. (11) reported that of the spinocerebellar tract, the posterior
spinocerebellar tract (PSCT) conveyed centripetal impulses from the peripheral receptors
to the cerebellar vermis. By contrast, the ventral spinocerebellar tract (VSCT) conveyed
centripetal impulses from both the peripheral receptors and rhythmic centres related to
walking to the cerebellar vermis. Furthermore, they stated that centrifugal pathways from
the cerebellum to the motoneurons of the spinal cord were considered to include the
Deiterospinal tract, ruburospinal tract and reticulospinal tract. This postulation is based on
their experimental results where, in the origin of the red nucleus, Deiters' nucleus and
motor nuclei of the reticulospinal tract, motor neurons generated discharges synchronous-
ly with movements of the lower limbs during walking and moreover, these discharges
disappeared when the cerebellar vermis was ablated surgically. Furthermore, Purkinje
cells in the intermediate part of the cerebellar vermis showed discharges similar to those
observed in the motor neurons in the origins of the above-mentioned nerve tracts. It is
therefore probable that the inputs from the peripheral receptors, particularly the lumbar
proprioceptors, reach the cerebellar vermis whereupon they act favorably on the activity
of the rhythmic centres related to walking and/or stepping, which eventually leads to a
smoothly performed stepping.
Udo (8), in a series of experiments using cats, determined whether or not the EMG
discharges of the four limbs during stepping could be altered when the activity of the
cortex of the cerebellar vermis, particularly area V, was inhibited. Furthermore, in order
to block the activity of the cerebellar cortex, the cortex was cooled temporally by
attaching a metal tube into which a cold catalyst was poured. Udo found that the amplitude
of the EMGs of the extensors of the fore and hind limbs ipsilaterally increased when the
above-mentioned procedure was applied to area V. In contrast, the same procedure did
not show any significant effects on the amplitude of the EMGs of the flexors of the same
limbs. He further studied how the activity of Deiters' nucleus during stepping altered when
the same procedure was applied to area V of the cerebellar vermis. Before the experiment,
he confirmed that cells of Deiters' nucleus from which the electrical activity was recorded
exerted an excitatory effect on the activity of the extensors of the hind limbs. In contrast,
he also confirmed that Purkinje cells of area V exerted an inhibitory effect on the activity
104 H. Fukushima and M. Hinoki

of the above-mentioned extensors. In a series of experiments, he found that during the

period of walking, which started just before the feet touched the ground and lasted
throughout the stance phase, i.e., the period of activation of the hind limb extensors, the
frequency of volleys from the above-mentioned cells of Deiters' nucleus was significantly
increased. These results suggest that in humans, Purkinje cells of the cerebellar vermis,
particularly those of area V, probably exert an inhibitory effect on the activity of the
Deiters' nucleus, through which the activity of the rhythmic centres for walking is
controlled.
With reference to these results, it is probable that promotion of the anticipatory
activation of the extensor muscles of the lower limbs during stepping can be accomplished
on the basis of a close correlation between the activity of the lumbar proprioceptors and
that of the central nervous system, particularly the cerebellar vermis.
One may now ask whether or not the other part of the brain may participate in the
promotion of anticipatory activity of the extensor muscles of the lower limbs during
stepping, and with close collaboration of the lumbar proprioceptors. In our clinical
experience on vertiginous patients with head and neck injuries, patients suffering from
pain and/or stiffness of the waist often showed abnormal EMGs in the lumbar region,
indicating the presence of over-excitement of the lumbar proprioceptors. Furthermore,
when either the waist was fixed with a corset or procaine was infiltrated into a tender spot
in this region, these abnormal EMGs weakened or disappeared, together with amelioration
or abolition of lumbar pain. Parallel with this, dysfunction of the eyes and body, particular-
ly abnormal optokinetic nystagmus, as indicated by hypoactive nystagmus, was ameliorat-
ed (12). This fmding indicated that recovery of the activity of the lumbar proprioceptors
led to amelioration of the activity of the reticular formation of the brain stem. The
spinoreticular tract originating in the lumbar cord was noted to terminate in the reticular
formation of the medulla oblongata, the pons and the mid-brain, connecting with Deiters'
nucleus (13, 14, 15). Furthermore, the spinoreticular tract was thought to have a close
functional correlation with the reticulospinal tract (13). The reticulospinal tract and the
Deiterospinal tract were, according to Shik et al. (11), important in promoting a smooth
walking performance. According to these reports, the brain stem also seems important,
together with the lumbar proprioceptors, with regard to accomplishing smooth stepping.
In brief, our opinion has been that the activity of the lumbar proprioceptors is closely
correlated with the activity not only of the cerebellum, but also of the brain stem and
moreover, these parts of the brain control the activity of the rhythmic centre related to
walking and/or stepping. Thus, the lumbar proprioceptors are responsible for promoting
the anticipatory activity of the lower limbs, i.e., generating the above-mentioned P pattern
EMG during stepping. This naturally leads to a smooth performance of stepping and/or
walking.
We conclude as followings:
1) The lumbar proprioceptors participate in the smooth performance of stepping by
promoting the anticipatory activity of the extensors of the lower limbs during stepping;
2) The cervical proprioceptors show a similar action to that of the lumbar proprioceptors,
with regard to promotion as described in l), though this action is less obvious than that of
the lumbar proprioceptors.

REFERENCES
I. Kitahara M, Matsubara H. Head movement while "marching in place". In: Hood JD, ed.Vestibu-
lar mechanisms in health and disease. London: Academic Press, 1978:335-341.
2. Fukushima H, Hinoki M. Role of the proprioceptors in the performance of stepping and the
 Role of cervical & lumbar proprioceptors during stepping 105

theory of the tonic neck and/or tonic lumbar reflex. Pract Otol (Kyoto) 1983; 76 (Suppl. 1):
64CHi57 (in Japanese with English abstract).
3. Tokizane T et al. Electromyographic studies on tonic, lumbar and labyrinthine reflexes in normal
person. Jap J Physiol 1951; 2: 130-146.
4. Ushio N, Hinoki M. Role of the cervical and lumbar proprioceptors in body equilibrium;
physiological meaning of fixation of the neck and waist with a collar and/or corset, with regard to
maintenance of static and dynamic equilibrium in humans (in preparation).
5. Fukuda T. The stepping test. Two phases of the labyrinthine reflex. Acta Otolaryngol (Stockh)
1958; 50: 95-108.
6. Engberg I, Lundberg A. An electromyographic analysis of muscular activity in the hindlimb of the
cat during unstrained locomotion. Acta Physiol Scand 1969; 75: 61~30.
7. Lundberg A. Reflex control of stepping. The Nansen Memorial Lecture, Universitetsforlaget,
Oslo. 1969 Cit. by Udo M. Central program for stepping. Medical Science 1975; 26:420-432 (in
Japanese).
8. Udo M. Central program for stepping. Medical Science 1975; 26:420-432 (in Japanese).
9. Grillner S. The role of muscle stiffness in meeting of changing postural and locomotor require-
ment for force development by the ankle extensors. Acta Physiol Scand 1972; 86:92-108.
10. Nakagawa M. Electromyographic studies on the activities of the antagonists of the lower limbs
during stepping; comparison with results obtained by Fukuda's stepping test. Pract Otol (Kyoto)
1973; 69 (Suppl. 3): 1492-1~18 (in Japanese and English abstract).
II. Shik ML et al. Control of walking and running by means of electrical stimulation of the mid-brain.
Biofizyka 1966; 4:659-666.
12. Hinoki M et al. Studies on ataxia of lumbar origin in cases of vertigo due to whiplash injury.
Equilibrium Res 1973; 3: 141-152.
13. Brodal A. The reticular formation of the brain stem. Edinburgh: Oliver & Boyd, 1957: I.
14. Terada S. Course and termination of the long ascending spinal tracts and of the medialleminiscus
in cats, with special reference to the relation of these tracts to the reticular formation. J Chiba
Med Soc 1960; 36: 1065.
15. Niimi Ketal. An experimental-anatomical study on spinothalamic tract in the cat. Okajima Fol
Anal Jap 1968; 44: 255.