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Sperm maturation in the male reproductive tractDevelopment of motility.

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Sperm Maturation in the Male Reproductive Tract :
Development of Motility '
Department of Biological Structure, University of Washington,
Seattle, Washington
Rabbit spermatozoa were removed from various levels of the male
reproductive tract. They were examined in Hanks' solution at room temperature with
a phase contrast microscope and their motility characteristics were recorded cinematographically.
Spermatozoa from the seminiferous tubules and ductuli efferentes show weak, vibratory movements with no forward progress. Little change in motility occurs until the
sperm reach the flexure of the caput epididymidis where some are capable of moving
more vigorously in a circular fashion. Samples from the distal caput epididymidis show
a sudden increase in sperm activity and a consistent pattern of tight, circular movement.
As the sperm traverse the corpus epididymidis, increasing numbers show progressive,
forward movement with longitudinal rotation. The proportion of such sperm becomes
significant only in samples from the upper cauda epididymidis and more distal regions.
Sperm from the ductus deferens rarely retain the circular movement.
It is concluded that rabbit spermatozoa undergo a distinct sequence of changes in
their swimming movements as they mature in the epididymis. A similar change was
noted in epididymal spermatozoa from the rat and guinea pig suggesting that this
process i s fundamental to sperm maturation in several species.
It is well known that mammalian spermatozoa undergo a change during their
passage through the epididymides which
enables them to fertilize ova (Young, '31;
Bedford, '66; Orgebin-Crist, '67b). This
maturation is accompanied by certain physiological and biochemical changes which
have been discussed extensively in earlier
reviews (Bishop and Walton, '60; Bishop,
'61). Morphological alterations in the acrosome have been noted also (Fawcett and
Hollenberg, '63; Bedford, '65).
Recently Blandau and Rumery ('64)
demonstrated that rat spermatozoa taken
from the caput epididymidis swim in a circular fashion whereas those taken from
the cauda tend to move in straight lines.
When caput spermatozoa were inseminated
into the cornu they did not go through the
utero-tuba1 junction into the oviduct and
thus the number of fertilized eggs was
negligible. In contrast, spermatozoa from
the cauda epididymidis reached the site of
fertilization readily. This experiment emphasized that rat spermatozoa must attain
a specific pattern of motility before they
reach full fertilizing capacity. Preliminary
observations indicated that rabbit spermatozoa undergo similar changes in their
swimming pattern during maturation
ANAT. REC..161: 471-482.
(Gaddum, '67). This finding prompted us
to study the motility patterns of rabbit
spermatozoa in detail as they move through
the various segments of the male reproductive tract.
Twenty-five mature male rabbits of various breeds weighing between eight and ten
pounds were used in the experiment. Each
animal was stunned by a blow on the head
and bled immediately by severing the carotid arteries. The testes, epididymides and
ducti deferentia were removed quickly and
placed in Petri dishes. Connective tissue
and blood vessels were cut away and the
fat pad over the caput epididymidis was
dissected with iridectomy scissors to expose the ductuli efferentes and the various
components of the caput epididymidis.
In a preliminary investigation involving
12 rabbits, spermatozoa were recovered
from several levels of the tract and examined in the manner described below. When
it had been established beyond doubt that
there were consistent variations in the mo1 Supported by a bio-medical fellowship from the
Population Council and, by USPHS grant HD-03464
from the National Instltutes of Health awarded to
Dr. Richard J. YA~..Y..".
2 Population Council Fellow, 1965-1968.
Fig. 1 Drawings of the right testis and epididymis of the rabbit. A. Lateral view, B. Posterior view,
C. Anterior view. D. D., ductus deferens. The numbers 1 to 9 refer to segments of the epididymis
which were chosen for sampling the sperm population.
tility pattern of spermatozoa removed from
different levels, an additional 13 rabbits
were used for a systematic study. For this
experiment, the epididymis was divided
arbitrarily into nine segments which could
be distinguished macroscopically by differ-
ences in the diameter and convolutional
pattern of the tubule, and also by their
spatial relationship to the testis (fig. 1 ) .
These segments were chosen for convenience of sampling rather than to correspond with regional differences in their
cellular characteristics. They do not correspond with the segments of the rabbit
epididymis described by Nicander (’57).
As each segment of the epididymis was
separated from the rest of the tissue, it
was rinsed thoroughly in Hanks’ solution,
placed in the well of a Maximow slide with
a few drops of Hanks’ solution and incised
carefully with iridectomy scissors. If the
spermatozoa were not released in sufficient
numbers by this method, the tubules were
pressed gently with a fine dental probe to
express their contents. In order to examine
the spermatozoa, they were mounted in
vaseline rings prepared in the following
manner. A ring of vaseline slightly smaller
than a no. 1 round coverslip (18 mm) was
made on the center of a specially cleaned
microscope slide. A 2-3 mm gap was left
in the circumference of the ring. After a
few drops of the sperm suspension had
been deposited in the center of the ring,
the coverslip was lowered carefully onto
the preparation and the gap was then
sealed with a drop of mineral oil. The purpose of the vaseline ring was to raise the
coverslip approximately 0.5 mm from the
surface of the slide and thus ensure sufficient depth in the preparation so that the
spermatozoa could display their normal
swimming activity. All preparations were
maintained at room temperature.
Preparations of spermatozoa were made
in this way from epididymal segments one
to nine (fig. 1); from the seminiferous
tubules dissected from the testis; from the
ductuli efferentes and from the ductus deferens. In addition, short segments of the
ductuli efferentes were mounted intact in
vaseline ring preparations in order to examine the activity of cilia lining their walls.
Suspensions of spermatozoa from the ductus deferens were obtained by flushing
them from the lumen with Hanks’ solution.
The preparations were examined in detail with the phase contrast microscope and
the movements of the spermatozoa were
recorded cinematographically on 16 mm
motion picture film at a speed of 24 frames
per ~econd.~
tive tract. The following terms will be
used to denote the various types of swimming movement which were observed in
the in vitro preparations:
( 1) Vibratory movement. The flagellum moves rapidly from side to side in an
oscillatory, or quivering motion. This
movement does not result in forward progress. For the most part, the spermatozoon
remains in the horizontal plane with the
flat surface of the head parallel with the
surface of the slide. Often the amplitude
of movement is so small as to be barely
perceptible, but in some cases, the amplitude has increased significantly. Thus, two
types of vibratory movement are distinguished, namely “weak and “vigorous.”
( 2 ) Circular movement. The flagellum
is bent in the shape of a curve and the
spermatozoon moves in a tight circle rather
than forward (figs. 1-5). The diameter of
the circular orbit appears to be related to
the degree of flagellar curvature. The head
of a spermatozoon moving in this fashion
apparently remains in one plane through
many swimming “strokes.” Such sperm
may be seen moving in either a horizontal,
oblique or perpendicular plane with respect
to the glass surface. When many sperm
in a preparation show the circular movement, they may swim in either a clockwise
or a counterclockwise direction.
( 3 ) Darting movement. The head of
the spermatozoon is propelled in an irregular, zigzag fashion. Forward movement
is minimal and highly erratic.
( 4 ) “Tuning forh” movement. The
spermatozoon moves forward but its path
is a wide arc rather than a straight line.
The head does not rotate and the flagellum
appears to vibrate so rapidly that it resembles the oscillations of a tuning fork.
(5) Rotatory movement (fig. 6 ) . Undulations of small amplitude pass down the
flagellum swiftly and the whole sperm rotates about its longitudinal axis. As the
head rotates, one observes the well-known
“flashing” effect which is due to periodic
changes in light scattering as the head
changes its position. The sperm makes
rapid forward progress in a relatively
straight line. This appeared to be the most
Rabbit spermatozoa display characteristic patterns of behavior when recovered
from specific regions of the male reproduc-
3 A research film demonstrating the various types of
sperm movement is available upon request from the
University of Washington Press, Seattle, Washington
efficient form of movement observed in
this study and we consider it to be the
motility pattern of fully mature spermatozoa.
Motility o f sperm f r o m the seminiferous
tubules and ductuli efferentes
Most sperm from the seminiferous tubules and the ductuli efferentes show
weak, vibratory movements. Their flagella
are often curved slightly and maintain this
state during movement. On very rare occasions, the position of the head changes
so that its thin, lateral edge comes into
view. This rotation occurs so rarely that
it is impossible to be certain whether it is
a simple oscillation of the head from side
to side or a complete rotation about the
longitudinal axis of the sperm.
In preparations from the seminiferous
tubules, sperm are either free in the medium or attached by their heads to Sertoli
cells. The flagellar movements of the attached sperm are more varied than those
of the free sperm, for they are capable of
wide, sweeping movements as well as restricted vibratory motion. Occasionally,
the distal tips of the flagella have small
“blebs” on them which appear to be either
remnants of cytoplasm or the end-pieces
of the flagella in a tightly folded condition.
Intracellular flagella in spermatids are
capable of whiplash movements which are
similar to those observed in preparations
of rat spermatids by Austin and Sapsford
(’51) and by Blandau (unpublished observations).
Whole mounts of portions of the ductuli
efferentes reveal the remarkable activity of
the cilia lining these ducts. The ductuli
are so tortuous that each appears to consist of many distinct compartments. The
cilia lining their walls create strong currents which move the contents around in
a brisk, circular fashion. On many occasions, the contents of one compartment
may be seen moving off gradually into the
adjacent one. A further demonstration of
the intense ciliary activity may be obtained
by slitting the tubules longitudinally and
observing the strong currents in the surrounding fluid. Both motile and non-motile
spermatozoa which come into contact with
the ciliated epithelium are swept briskly
over its surface.
Motility o f sperm f r o m the epididymis
Segment 1
Spermatozoa from segment 1 (fig. 1 )
show similar motility characteristics to
those from the seminiferous tubules and
ductuli efferentes. An occasional sperm
shows vigorous vibratory movements. Only
a small number of sperm can be recovered
from this segment.
Segment 2
Spermatozoa are more numerous in segment 2 (fig. 1 ) and there is a significant
increase in their activity. Nearly all show
vigorous vibratory movements, although
forward progress is still extremely limited.
The flagellum in many cases appears
slightly curved and stiff.
The bending of the flagellum is very
pronounced in a few spermatozoa, and they
move in a slow, spasmodic, circular fashion. The proportion of sperm moving in
this manner vanes between animals. In
some cases, only an occasional sperm
shows circular movement while in others,
approximately one-third move in this fashion.
On rare occasions a few spermatozoa
show the rotatory movement so typical of
fully mature spermatozoa but forward
progress in these sperm is very slow. They
appear to be continuously bent in one direction, so that their forward movement
is erratic.
Segment 3
There is not only a sudden increase in
the over-all motility of spermatozoa in segment 3 but also a variety of swimming
movements. In most preparations, the circular movement seen only occasionally in
segment 2 is now the primary pattern.
The vibratory motion is still common and
in a few preparations it is the dominant
The circular movement itself shows interesting variations. Some spermatozoa
maintain the slow, abrupt form of movement seen in segment 2, while others complete each orbit rapidly and smoothly with
a minimum of swimming “strokes.” An
occasional sperm may show peculiar darting movement, and a few move forward
in a rotatory fashion. The swimming behavior of the rotating sperm is very similar
to that of mature sperm except that forward progress is slower and the undulatory
waves passing down the flagellum are of
greater amplitude.
a few show the darting or “tuning f o r k
Segment 6
The dominant form of movement in segment 6 is still circular but the width of the
orbit shows significant variation. An increased proportion of sperm now display
forward movement of either the rotatory
or “tuning f o r k type, although forward
progress is rarely as rapid as that shown
by mature rabbit sperm. There are also a
few sperm which show the darting movement.
There is considerable variability in the
type of swimming movement shown by
individual spermatozoa from segment 6.
For example, the flagellum of a spermatozoon swimming in tight circles occasionally straightens out, causing the sperm to
swim in wide arcs in the “tuning fork”
manner. On the other hand, a sperm moving forward in a rotatory manner occasionally stops and begins the circular motion
once more.
Segment 4
Segment 4 is the principal portion of the
caput epididymidis. The tubules are wide
and packed with spermatozoa. On release
into a fluid medium, nearly all of them
show much greater activity than those from
preceding segments. They move in a
highly localized, circular fashion. In a
few spermatozoa, the bend in the flagellum
is not so conspicuous and these move in
rather wider circles.
Only a few sperm show a pattern of
movement other than the circular one. An
occasional one swims forward with rotation of the head but its progress is rarely
as rapid as that of a mature sperm recovered from the ductus deferens. Indeed a
sperm such as this sometimes stops moving forward and shows restricted vibratory
motion, or begins swimming in a circular
fashion. There are a few sperm which
show either the “tuning f o r k or darting
movement, and an occasional one which Segment 7
More than half of the spermatozoa restill shows the weak, vibratory motion so
characteristic of sperm recovered from seg- covered from segment 7 still move in a
circular fashion, but the proportion movments 1 and 2.
The cytoplasmic droplet is located at the ing in wide circles has increased sigjunction of the midpiece and the mainpiece nificantly. The tendency to move in wide
in most sperm. Often it is arranged asym- circles is accompanied by a noticeable inmetrically and the flagellum appears to crease in the rate of flagellar movement.
Several spermatozoa now move forward
curve towards the side to which the dropwith either the rotatory or the “tuning
let is attached.
f o r k movement but the proportion showSegment 5
ing forward progress varies considerably
Fewer spermatozoa can be recovered between animals. The speed of forward
from segment 5 than from segment 4. The movement varies also but it is rare to find
primary swimming movement is again cir- sperm moving forward as rapidly as those
cular, but the diameter of the circular orbit recovered from the ductus deferens.
shows more variation than in sperm from
segment 4. While most sperm still move Segment 8
Segment 8 is a transitional zone in which
in tight circles, a significant number now
swim in rather wider circles. This change a variety of movements may be seen. For
is associated with a lesser curvature of the the first time the greater proportion of
flagellum. In some preparations, the dif- spermatozoa are now moving forward
ference between segments 4 and 5 is re- rather than in a circular fashion. Forward
markable in that all the sperm appear to movement of both the rotatory and the
“tuning fork” type occurs. Circular swimbe moving in wider circles.
Whatever the width of the circle, the ming activity is still present and the width
heads of the spermatozoa do not generally of the circular orbit varies considerably.
rotate. Only an occasional spermatozoon It is noteworthy that some sperm still swim
moves forward with the head rotating and in tight circles. Nearly all preparations
contain a few sperm showing the darting
Segment 9 and ductus deferens
from these
show no appreciable difference in their
pattern of motility. The majority of them
move forward. The circular and darting
movements occur rarely and in several
preparations they are limited to only a few
individuals in each microscopic field.
The dominant type of forward movement varies from one animal to another.
In many cases the rotatory and the "tuning f o r k types occur in approximately
equal numbers, but in some the rotatory
type predominates.
As rabbit spermatozoa pass through the
male reproductive tract they undergo a
remarkable change which enables them to
move forward rapidly and efficiently. The
relative proportion of sperm showing the
typical forward movement increases only
gradually as they pass through the epididymis. The achievement of mature swimming behavior in an individual spermatozoon is apparently a slow process. In
samples from the caput and corpus epididymidis, for instance, spermatozoa may be
seen which are capable of moving forward
but only in an abrupt, inefficient manner,
with a tendency to revert occasionally to
the circular swimming pattern.
Even though the change in swimming
movements is a gradual one, the over-all
pattern of sperm motility in a given segment is sometimes remarkably different
from one segment to the next. For example, the spermatozoa from the caput flexure
(segment 3 ) show a dramatic increase in
activity when compared to those from preceding segments. Sperm from the distal
limb of the caput epididymidis (segment 4 )
show an even greater increase in motility.
There are relatively few changes in motility
pattern in segments 5 , 6 and 7. In segment
8, however, a large proportion of spermatozoa show forward movement.
As this study has shown, the maturation
of the swimming pattern in rabbit spermatozoa involves a change from a weak, localized, vibratory movement to a swift,
circular one and later to a rapid, progres-
sively forward movement. A similar observation has been noted briefly by OrgebinCrist ('67b). This sequence of changes is
mirrored closely in the maturation of both
rat sperm (Blandau and Rumery, '64) and
guinea pig sperm (personal observation),
despite obvious differences in the mechanism of forward movement shown bv the
mature sperm of all these species. This
suggests that the essential nature of the
change in swimming activity, as described
in this paper, may not be confined to rabbit
sperm but may be fundamental to the maturation of other mammalian sperm as well.
Blandau and Rumery ('64) proceeded to
correlate the change in swimming movements of rat sperm with the acquisition of
fertilizing capacity. Recently, studies have
been completed on the fertilizing capacity
of rabbit epididymal sperm as well (Bedford, '66; Orgebin-Crist, '67b). By inseminating spermatozoa removed from various
levels of the epididymis into either the oviduct (Bedford, '66) or the cornua (Orgebin-Crist, '67b), these authors have shown
independently that fertilizing capacity of
rabbit sperm is developed only as they
reach the lower half of the corpus epididymidis. The development of fertilizing
capacity in the lower corpus epididymidis
is remarkable, for the rate of fertilization
reported with these sperm was never less
than 57%. Our studies did not reveal a
noticeable change in the motility pattern
in this segment which could account for
this sudden rise in fertility.
Nevertheless, both reports provided some
evidence that significant numbers of the
spermatozoa in the lower corpus are still
not fully mature. When sperm from this
segment were used for oviductal insemination, a 97% fertilization rate was achieved
but the ova recovered from these oviducts
did not possess as many accessory spermatozoa as those which had been exposed to
a similar number of sperm taken from the
cauda epididymidis (Bedford, '66). The
author suggested that the cauda contains
a higher percentage of mature spermatozoa
than the lower corpus. Orgebin-Crist ('67b)
performed inseminations via the cornua
and found that the fertilization rate increased from 57% when spermatozoa from
the lower corpus epididymidis were used,
to 95% when spermatozoa from the distal
cauda epididymidis were inseminated. As
seen in this study, the greater proportion
of sperm in the lower corpus still swim in
a circular fashion, providing additional
evidence that full maturity is not attained
in this segment. The development of competent forward movement by large numbers of sperm occurs only as they enter
the upper coils of the cauda epididymidis.
When observed changes in swimming
movements are correlated with fertilizing
capacity, it becomes obvious that the vibratory and circular movements of sperm
from the upper portions of the epididymis
are associated with infertility. In contrast,
the progressive, rotatory motility found at
lower levels of the tract is associated with
fertilizing ability. Forward movement may
be important for transport through certain
portions of the female tract, or for establishing contact with the egg, or both.
Blandau and Rumery ('64) showed that
rat spermatozoa from the head of the epididymis do not pass through the uterotubal junction. Orgebin-Crist ('67b), on the
other hand, believes that rabbit sperm from
the caput epididymidis may enter the oviduct readily, suggesting that the uterotubal junction in this animal is less effective as a barrier to sperm transport than
it is in the rat. In any event, it seems
highly unlikely that the localized, circular
movements of immature rabbit spermatozoa would allow frequent collisions with
the eggs. Even when such sperm are put
in the vicinity of the eggs by intra-tuba1
insemination, they do not effect fertilization (Bedford, '66).
Despite the apparent significance of progressive movement for fertilization, this
alone is insufficient to ensure full fertilizing capacity. When sperm are trapped by
ligation within the first portion of the epididymis (segments 1 and 2, fig. 1) many
become capable of rapid, progressive movement in vitro, but they rarely become fertile (Bedford, '67; Orgebin-Crist, '67a).
Other factors besides competent motility
must be essential in the maturation process. There is some evidence, for instance,
that the plasma membrane remains in an
immature state in sperm confined within
the upper segments of the epididymis, despite the attainment of a progressive motility pattern. This factor may prevent the
sperm from establishing contact with ova
(Bedford, '67).
The circular movements shown by immature rabbit spermatozoa cannot be fully
explained as yet, although the motility patterns of mature sperm have been studied
in some detail in several species. It has
been shown that the swimming motion of
mature sperm has two major components,
lateral bending and rotation about the
longitudinal axis (Bishop, '62). In many
species, the primary bending waves are
slightly asymmetrical; that is, the amplitude is greater on one side of the flagellum
than on the other (Gray, '55; Bishop, '58;
van Duijn, van Rosmalen and van Voorst,
'66). When a spermatozoon of this type
comes close to a glass surface or to the
interface between fluid and air, it is prevented from rotating around its longitudinal axis. Then the asymmetry of the
bending waves causes the spermatozoon to
move along the arc of a circle rather than
in a straight line. This may be the explanation for the "tuning f o r k type of movement described above, particularly since
the spermatozoa displaying this type of
movement are found mainly near the glass
The rotational component of flagellar
movement normally counteracts the tendency to be propelled in a circle. In the present study, rotation was evident only in those
spermatozoa which were moving forward;
those that moved in tight circles did not
rotate. It may be possible that the two
components of sperm movement, lateral
bending and longitudinal rotation, are controlled by separate mechanisms which develop at different time intervals during
maturation. Perhaps spermatozoa from
the head of the epididymis move in tight
circles because they are capable of effecting only the lateral bending movements.
The rotational component which would
correct this asymmetry had not developed.
The tendency to swim in circular orbits
with no longitudinal rotation is not confined to epididymal spermatozoa. It has
been reported as occurring occasionally in
spermatozoa from the ductus deferens of
guinea pigs (Cody, ' 2 5 ) and in a small
proportion of the sperm in human and
bovine semen (Farris, '50; Rikmenspoel,
’62; Tampion and Gibbons, ’63). Such
sperm are generally considered to be pathological, for even sperm which are swimming normally in bovine ejaculates can be
induced to swim in circles by subjecting
them to cold shock (Rikmenspoel, ’62).
Van Duijn (’66) has observed that stiffness
in the midpiece of ejaculated spermatozoa
leads to circular movement with no rotation, and he believes that this stiffness is
often due to some kind of pathological
change in the midpiece.
The circular movement observed by
these workers appears to be similar to that
described for spermatozoa from the caput
epididymidis in this paper. The possibility
that caput spermatozoa are merely “cold
shocked is remote since all specimens
were prepared at the same temperature. In
addition, it has been shown that epididyma1 spermatozoa in a number of species
are more resistant to cold shock than ejaculated spermatozoa (Mann, ’64) and that
spermatozoa from the caput, in the boar
at least, are even more resistant than those
from the lower levels of the tract (Lasley
and Bogart, ’44). A more likely explanation may be that in ejaculated spermatozoa
which have undergone cold shock, the
mechanism controlling rotation has been
seriously disturbed, whereas in immature
spermatozoa from the caput epididymidis,
the mechanism simply has not been developed. We believe that the few spermatozoa
showing circular movement in the ejaculate may be immature forms which have
passed through the entire epididymis without attaining the mature type of swimming
The significance of the changes in motility which occur as sperm pass through
the male reproductive tract will not be fully
appreciated until further experiments reveal the biochemical or biophysical alterations within the flagellum, or in the environment, which affect the motility pattern.
The author wishes to thank Dr. Richard
J. Blandau for his valuable advice and help
in this study and also Mr. Roy Hayashi for
his skilled technical assistance in the filming of the sperm movements.
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~ undert
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Sequences in the circular movement of a spermatozoon recovered
from the caput epididymidis. (Original magnification X 1060).
Penelope Gaddum
Penelope Gaddum
A spermatozoon recovered from the ductus deferens which was showing normal, progressive rotatory movement. (Original magnification
X 1060).
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malen, maturation, motility, tractdevelopment, sperm, reproduction
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