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Relationships between hand skill and the excitability of motoneurons

innervating the postural soleus muscle in human subjects
Üner Tan a
a
Atatürk University, Medical Faculty, Institute of Physiology, Erzurum, Turkey

Online Publication Date: 01 May 1985

To cite this Article Tan, Üner(1985)'Relationships between hand skill and the excitability of motoneurons innervating the postural
soleus muscle in human subjects',International Journal of Neuroscience,26:3,289 — 300
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 Intern. J . Neuroscience. 1985, Vol. 26, pp. 289-300 0 1985 Gordon and Breach, Science Publishers, Inc.
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RELATIONSHIPS BETWEEN HAND SKILL AND

THE EXCITABILITY OF MOTONEURONS
INNERVATING THE POSTURAL SOLEUS
MUSCLE IN HUMAN SUBJECTS
UNER TAN
A tatiirk University, Medical Faculty, Institute of Physiology, Erzurum, Turkey

(Received October 29, 1984)

The relation of hand skill to the excitability of motoneurons innervating the postural soleus muscle
was studied in normal human subjects. The motoneuronal excitability was tested by the recovery
curve of the Hoffmann reflex. The hand skill was assessed by the peg moving test. Females have been
found to be better than males in hand skill. It was established that the H response recovery curve
from the right leg was significantly lower than that from the left leg in right handed subjects. The
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opposite was found in left handers. In ambidexters, there was no significant difference between the
heights of the left and right recovery curves. The laterality quotients of the H response recovery
curves were normally distributed in the total sample with a mean significantly less than zero, indi-
cating a left shift bias in the motoneuronal excitability. The possible factors contributing to the
inverse relationship between hand skill and the excitability of motoneurons innervating the postural
soleus muscle were discussed in light of genetic determinants of brainedness and the corticospinal
inputs to postural motoneurons.

A spinal motor lateralization independent from supraspinal structures has recently

been shown to exist in cats (Tan, 1984a). However, there was no relationship between
pawedness and the excitability of motoneurons innervating the gastrocnemius-soleus
muscles performing extensor movements and the associated postural adjustments.
Nieoullon and GahCry (1978) reported that the degree of pyramidal influences on the
hindlimb motoneurons is markedly less than the amount of pyramidal input to the
forelimb motoneurons, and the coordination between hindlimb movement and the
associated postural adjustments are generally similar to that observed before pyramidal
section in cats. Accordingly, a spinal motor lateralization in the hindlimb extensor
system of cats may develop independently from the pyramidal influences. In primates,
there is a pronounced corticospinai input to hindleg motoneurons, and the motoneuron
pool of antigravity muscles receive predominantly inhibitory influences from the
pyramidal tract (Uemura & Preston, 1965; Stewart & Preston, 1967). It is then to be
expected that the excitability of motoneurons innervating the postural (antigravitiy)
soleus muscle on the right side would be lower than the excitability of motoneurons
innervating the soleus muscle on the left side of right handers. The same relationship
could be considered for the left handers, but in a reverse order, On the other hand,
there would be no difference in the excitability of motoneurons innervating the right
and left soleus muscles of ambidexters. The results of the present work are consistent
with these hypothetical considerations. A preliminary account of this study has been
presented elsewhere (Tan, 1984b).
289
 290 u. TAN
METHOD

Subjects and the Evaluation of Hand Skill

The subjects were 70 male and 27 female healthy students ranging in age from
20 to 22 years. The hand preference was assessed by the Oldfield (1971) Handedness
Inventory modified by Geschwind and Behan (1982). The hand skill was evaluated
by a slightly modified peg moving test (Annett, 1981). In this test procedure the
subjects were required to insert 25 pegs into their appropriate holes using first the
right and then the left hand. One trial consisted of the time elapsed to move 25 pegs
with one hand. This time period was accurately measured by an electronic device.
Ten trials were given to each hand, and the mean peg moving time was calculated for
each hand. The significance of the difference between the peg moving times for each
hand was tested by the Student’s t-test for paired data. According to the results of this
statistical analysis, the subjects were classified into three main groups: right, left, and
mixed handers. A laterality quotient for the hand skill was computed by using the
formula R/(R+L)x 100, where L and R refer to the mean peg moving times for the
left and right hands, respectively. Subjects also reported familial left-handedness in
at least one parent or sibling.
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H Response Recovery Curve (Testing of Motoneuronal Excitability)

To record the H wave of Hoffmann reflex, Ag-AgCl recording electrodes were placed
over the lower part of the gastrocnemius muscles. The subjects were lying comfortably
and relaxed in a prone position with their legs extended and fixed on the table. The
stimulating electrodes were fixed over the posterior tibial nerve in the popliteal fossa,
and a ground electrode was placed between the stimulating and recording electrodes.
The stimulus strength was adjusted so as to elicit maximal H response with no or little
M response. Then double shocks were delivered to the tibial nerve at intervals from
40 to 1000 ms every five seconds, the stimulus strength for the maximal H response
being kept constant. At least three trials were alternated between the right and left
legs.
To construct the H response recovery curve, the ratio of the amplitude of the test
H wave (Hz) to the amplitude of the first H wave (HI) was estimated and expressed
as a percentage (H2/Hl%). The mean value of this ratio for each leg was then plotted
versus stimulus interval. In each subject, the significance of difference between the
right and left recovery curves was assessed by using analysis of variance. To express
the laterality quotient of the H response recovery curves, an index was computed
using the equation (R-L)/(L+R)x 100, where L and R refer to the mean Hz/HlO/,
values from the left and right recovery curves, respectively.

RESULTS

I-land Skill in Male and Female Subjects

A summary of the mean peg moving times for the left and right hands of the male and
female subjects is given in Table I. In the left and right handed subjects the mean peg
moving times for the left and right hands differed from each other significantly
( p = 0.01 ). There was no significant difference between the mean peg moving times for
 HAND SKILL AND HOFFMANN REFLEX 29 1

TABLE I
Mean peg moving times for right and left hands in right, left and mixed handers

Males Females

Right Left Right Left

_____
Subjects Mean SD Mean SD Mean SD Mean SD
-
Right handed 34.5 4.4 39.4 5.2 29.5 3.6 34.1 4.0
( N - 38, 54.3 %) ( N = 18, 66.7%)

Mixed handed 34.4 4.2 35.7 4.1 31.5 3.7 32.3 3.1
(N=27, 38.6%) (N-9, 33.3%)

Left handed 40.5 6.2 35.5 5.4 - -

(N=5, 7.1%) (N=O)
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the left and right hands of the mixed handed subjects ( t =0.48 <tt ; o . o ~= 1.98). The
mean peg moving time for the left and right hands of females were significantly less
than those of males (p=O.OI).
There was an exponential relationship between the differences in left-right peg
moving times and the laterality quotients for hand skill. As seen in Figure 1 , the
regression lines of male (closed circles, straight line) and female (open circles, dashed
line) were different so that the regression line fitted to the females data indicated a
more right shift than the males regression line.

Relation of H Response Recovery Curve to Hand Skill

Right handed subjects. The H response recovery curve from the left leg was
usually found to be higher than that from the right leg in these subjects. Figure 2
illustrates the original H1 and Hz responses at indicated stimulus intervals in a right
handed male subject. There was no M response in these records, indicating that only
Group I muscle afferents were stimulated without contamination of motor fibers.
As can be clearly seen from this Figure, The Hz/H1 ratio was always larger on the left
side (8)than the right side (A), at all stimulus intervals. This was a representative
picture for almost all the right handers. Of 38 right handed males, 26 had no familial
left-handedness, and in all these subjects, the left recovery curve was significantly
higher than the right recovery curve. The remaining 12 right handed male subjects
had familial left handedness. In six of them, the left recovery curve was significantly
higher than the right one, in three the opposite was the case, and three had equal
recovery curves from the left and right sides. This analysis indicates a 15.8 % deviation
from the main bias.
Out of 18 right handed female subjects, 11 had no familial left handedness, and the
recovery curve from the left leg was significantly higher than that from the right leg in
these subjects. This result was consistent in five of seven right handed females with
familial left-handedness. The remaining two had higher recovery curves from the right
side than the left side. Thus there was a 1 1.1 deviation from the main bias.
Downloaded By: [TÜBTAK EKUAL] At: 12:58 7 August 2009

292
u. TAN
 HAND SKILL AND HOFFMANN REFLEX 293
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FIGURE 2 H waves produced by conditioning and test stimuli in right handed male subject.
The H responses in the left (A) and right (B) columns were elicited by double shocks (SI and Sa)
to the right and left tibia1 nerves, respectively. Stimulus intervals are indicated in the middle column.

FIGURE 1. Relation of left-minus-right hand peg moving time to laterality quotient for hand skill.
Abscissa: !eft-minus-right hand peg moving time (sec) ; Ordinate: laterality quotient for hand skill.
Straight line refers to the regnession line fitted to the data of male subjects (closed circles): y=yo.e-hZ
where y0=49.95 and X=0.013; r=0.98>rt;o.oo1=0.33. Dashed line refers to the regression line
fitted to the data of female subjects (open circles): y=yo.e-hz where y0=49.96, and X=0.016;
r =O.99>rt ;O.OOI= 0.49.
 194 u. TAN
130
T

s
2%
\
X
L
!
100

90

80
I
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I
I
70 I
I
I
I
I

7
60

50

40

30

20

10

a r I I I 1 I I I 1 I 1 1 1 I

40 60 100 200 LOO (Ins I1000

FIGURE 3 Mean H response recovery curves from right and left legs in right handed subjects.
Abscissa: stimulus interval. Ordinate: mean Hz/H1% from the right (open circles) and left (closed
circles) legs of the right handed male and female subjects ( N = 5 6 ) .
 HAND SKILL AND HOFFMANN REFLEX 29 5
Figure 3 shows the mean H response recovery curves from the right (open circles)
and left (closed circles) legs of all the right handed subjects including male and females
with or without familial left-handedness. Statistical analysis showed that the mean
recovery curve from the left leg was significantly higher than that from the right leg of
these subjects (F= 50.80>Ft ; o . o ~= 3.85).
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0 40 GO 100 200 400 ( m s ) 1000

FIGURE 4 Mean H response recovery curves from right and left legs in left handed subjects.
Abscissa and ordinate as in previous Figure.
 296 u. TAN
A

u
E 5
a

-48 0 +48

:i
B
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10

5
0

- 48 0 + 48

40-
c
35-

3 0-

2 5-

2 0-

15-

10-

5-

0-
- 48 0 +48
FIGURE 5 Distributions of recovery curve laterality quotients. A, total sample; B. right handed
subjects; C, Ambidexters.
 HAND SKILL AND HOFFMANN REFLEX 291

Left handed subjects. All of the left handers consisted of males (N=5).It was
consistently found that the H response recovery curve from the left leg was significantly
lower than that from the right leg in each of these subjects. All of them had familial
left-handedness. Figure 4 shows the mean Hz/H1% values from the right (open circles)
and left (closed circles) legs in this sample. The statistical analysis showed that the
mean recovery curve from the left legs was significantly lower than that from the
right legs (F= 36.77> Ft ; o . o ~ =6.8 1).

Mixed handed subjects. (Ambidexters). The recovery curves from the right and left
legs of the male and female mixed handed subjects did not differ from each other
significantly. There was also no significant difference between the mean Hz/H1 "/o
values from the left and right H responses in this sample (F= 0. I 5 <Ft ;0.05 = 3.86).

Distribution of the Recovery Curve Laterality Quotients

The histograms in Figure 5 show the distributions of laterality quotients of the H
response recovery curves in the total sample (A), right handers (B), and mixed handers
( C ) . The statistical analysis showed that the total sample was distributed in a normal
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manner (xz=2.01 <X2t;0.05= 14.10) with a mean of -5.52 5 14.86, which was signifi-
cantly different from zero ( t = -3.42>tt ;o.Ool=2.64). The distribution of the re-
covery curve laterality quotients in right handers also fitted to a normal curve (x2=
2.71 <x$;o,n5 = 14.07) with a mean of - 9.30 k 16.03, which was significantly less than
zero (t=4.26>tt ; O . O O ~= 3.50). The mean recovery curve laterality quotient of ambi-
dexters was found to be -0.71 k 8.68, which did not significantly differ from zero
( t =0.42<tt;0.05= 2.06). The distribution of the recovery curve laterality quotients
in these subjects fitted to a normal curve ( ~ ~ = 2 . 0 5 < ~ ~ t ; 0 . 0 5 = 7 . 8 1 ) .

DISCUSSION

Hand Skill in Male and Female Subjects

According to the results of statistical analysis concerning the left-right differences in
hand skill, three groups were distinguished: right (57.773, mixed (37. I%), and left
(5.2%) handers. These proportions are in accordance with Annett's data (1981).
In general, the females tended to be more dextral and better in hand skill than males
for the following reasons: (i) There was no left handed female in the total sample;
(ii) The proportion of right handers was higher in females (66.7%) than males (54.3%).
(iii) The regression line expresing the relationship between left-right peg moving time
and the laterality quotient for hand skill of the female subjects was different from that
of males and followed a right shift course: (iv) The mean peg moving times for the
left and right hands were significantly shorter in females than males. The latter
finding is inconsistent with that of Kilshaw and Annett (1983) that males were faster
than females in all age groups except 10-1 1 years of age. This discrepancy may be
accounted for by the cultural differences. The right handed female subjects in this
study all used to make fancy work such as embrioidery since their childhood. For
this reason, the females may be faster than males in hand skill. Nevertheless, Annet
and Kilshaw (1983) also reported that females tended to be more dextral than males
in hand skill.
 298 u. TAN
H Response Recovery Curve in Relation to Hand Skill
Distribution of the H response recovery curve laterality quotients. The H reflex
recovery curve reflects the motoneuronal excitability (Zander-Olsen & Diamantopoulos,
1967; Taborikova & Sax, 1968, 1969; Goode et al., 1980). Accordingly, the laterality
quotient of the H response recovery curve can be expressed as the motoneuronal
excitability quotient. The excitability quotients in the total sample were distributed
in a unimodal and normal manner with a mean of -5.52+ 14.86. Borod et al. (1981)
described a similar distribution of the mean facedness ratings for emotion. A left
shift bias of the excitability quotients mean a sinistrality in the excitability of moto-
neurons innervating the postural soleus muscle, in contrast to a right shift bias in
hand skill as reported by Annett (1976). A left shift bias in the motoneuronal excita-
bility might be caused by the same gene, i.e., Annett’s RS factor (1981), favoring the
left brainedness in the majority of the population. A more detailed analysis of this
relationship will be presented below.
The distribution of the motoneuronal excitability quotients in right handed subjects
also fitted to a normal curve with a mean of -9.30+ 16.03, indicating a more left
shift than the mean of the total sample. Thus the excitability of motoneurons inner-
vating the left soleus of right handers was much more pronounced than that inner-
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vating the right soleus in comparison to the total sample. In ambidexters, the mean
of the normal distribution of the motoneuronal excitability quotients did not signifi-
cantly differ from zero, i.e., it was unbiased t o either side. But why are the excitability
quotients in right handers biased to sinistrality whereas the distribution of hand skill
is biased to dextrality ? The possible mechanisms of this apparently paradoxical
finding will be dealt with in the following section.

The course of H response recovery curves in three handedness groups. Statistical

analysis indicated that the mean H response recovery curve from the left leg was
significantly higher than that from the right leg in right handed subjects, and vice
versa in left handed subjects. There was no significant difference between the heights of
the left and right recovery curves in ambidexters. Thus the excitability of motoneurons
innervating the postural soleus muscle is equally distributed in both sides, indicating a
complete correspondence with hand skill. However, there was an inverse relationship
between hand skill and the excitability of these motoneurons on the left and right sides
of the left and right handed subjects. An inverse relationship between facedness and
foot and hand preference was also reported for the expression requiring unilateral
facial movements (Chaurasia & Goswami, 1975; Borod et al., 1981).
Actually, the above results confirm the working hypothesis. The crucial point
concerns what mechanisms would play a role in the decreased motoneuronal excita-
bility on the preferred side. In the present work, the H response was recorded from
the soleus muscle which is mainly involved in postural adjustments of the body.
Uemura and Preston (1965) and Stewart and Preston (1967) found that the antigravity
muscles responsible for postural mechanisms receive predominantly inhibitory influ-
ences from the pyramidal tract, whereas the proximal flexor motoneurons were
generally excited by the same input. These patterns reflected the need of the motor
cortex to decrease the activity of the antigravity muscles to permit volitional move-
ments. Accordingly, it was also reported that the small-tonic motoneurons responsible
for the activity of postural muscles are inhibited by a recurrent inhibitory circuit
originating from the large-phasic motoneurons innervating the fast muscles in the
gastrocnomius-soleus group (Eccles, et al., 1961 ; Tan, 1972, 1974, 1975).
 HAND SKILL A N D HOFFMANN REFLEX 299

Considering the above findings it is conceivable that the excitability decrease in the
extensor motoneurons innervating the postural soleus muscle on the right side of right
handers might have been developed as a result of the predominantly corticospinal
inhibitory input to these motoneurons, in order to permit comparatively rapid
volitional movements on the right side. Furthermore, the more pronounced excita-
bility of extensor motoneurons innervating the postural soleus muscle on the left side
of right handers will be essential for a support of the body to facilitate the volitional
movements on the right side. These mechmisms would function in a reverse order in
left handers, who had higher motoneuronal excitability on the right side than the left
side.
The relationship between hand skill and motoneuronal excitability showed a 8.2 %
deviation (91.8 % correlation) from the total sample. These exceptional cases did not
influence the main bias significantly. The following factors may contribute to this
deviation: (i) The foot skill cannot be assessed as accurately as the hand skill; (ii) The
hand preference and hand skill both undergo to a strong cultural control during
development, but the feet are not influenced by cultural pressures as much as the
hands. Therefore, the feet may reflect spinal motor lateralization better than the
hands. Actually, a complete correspondence between hand and foot preference was
not reported in the literature. A correspondence of 91.8 % between hand skill and
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motoneuronal excitability lies within the range of 86.7 % and 97.0 % hand-foot
correspondence reported by Merrel (1957) and Groden (1969), respectively.

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