NAMES IN GENITOURINARY SURGERY
“ON THE PHYSIOLOGY OF MICTURITION” BY DENNY-
BROWN AND ROBERTSON: A CLASSIC PAPER REVISITED
JOEL A. VILENSKY, DAVID R. BELL,
T he 1933 article1 by the renowned neurologist,
Derek Denny-Brown (1901 to 1981)2 and
E. Graeme Robertson (1903 to 1975)3 titled, “On
the Physiology of Micturition,” has been described
as “classical,”4 presumably because of its high cita-
tion rate, which continues to this day,5 and the
authors’ novel use of two catheters to differentiate
between vesical and urethral pressures. Despite the
long history of citation, the basis of the work sup-
porting the article’s conclusions is difficult to dis-
cern from simply reading the paper. The authors
did not make clear exactly which of the four cath-
eter arrangements they used with each experiment
(Fig. 1), and most of the plates are almost impos-
sible to evaluate because the lines are faint and at
times cross each other and/or move out of view.
Moreover, the same numerically identified lines
represent data obtained from different manometers
in different experiments (ie, line 1 might be vesical
pressure in one experiment and urethral pressure
in another). Furthermore, and unfortunately,
Denny-Brown’s prose has long been recognized as
exceptionally convoluted, and this paper can be
considered a model of his style.6 For this reason we
decided to revisit this paper.
Our approach in this review is to first describe
the methods developed by Denny-Brown and Rob-
ertson and then to relate these to each of their
“summary of conclusions” listed at the end of the
article. Furthermore, we restate and/or shorten the
text Denny-Brown and Robertson used to describe
their conclusions. Finally, we have redrawn one of
their figures and developed a new figure to illus-
trate their method.
From the Departments of Anatomy and Cell Biology and Physi-
ology, Indiana University School of Medicine, Fort Wayne, Indi-
ana; and Department of Neurology, University of Michigan
School of Medicine, Ann Arbor, Michigan
Reprint requests: Joel A. Vilensky, Ph.D., Department of Anat-
omy and Cell Biology, Indiana University School of Medicine,
2101 Coliseum Boulevard East, Fort Wayne, IN 46805
Submitted: January 9, 2003, accepted (with revisions): March
11, 2003
© 2004 ELSEVIER INC.
182 ALL RIGHTS RESERVED
AND SID GILMAN
FIGURE 1. Four catheter arrangements used in the
seven experiments described in the text. Adapted from
Denny-Brown D, and Robertson EG: On the physiology
of micturition. Brain 56: 149–190, 1933. Used with
permission of Oxford University Press.
MATERIAL AND METHODS
Three subjects were used. Subjects A and B were the au-
thors7 and subject C was a volunteer. In part because of the
authors’ reluctance to cause discomfort to the volunteer, how-
ever, almost all the data presented were from the authors
themselves. During the experiments, each of the subjects lay
on a couch and was catheterized with two catheters (Fig. 2), a
small “ureteric” catheter that was inserted into a slightly larger
rubber catheter (Fig. 1). Unfortunately, the authors used in-
consistent and confusing terminology to refer to each of these
catheters. Accordingly, we refer to the smaller catheter as the
“vesical” catheter and the larger one as the “urethral” catheter.
The vesical and urethral catheters were placed in four con-
figurations relative to the bladder and proximal urethra for
different experiments in the study (Fig. 1). These configura-
tions enabled the authors to evaluate the activity of the inter-
nal and external urethral sphincters relative to each other and
to detrusor contractions. As a note of caution to the reader, the
positions of the catheters were not verified radiologically and
thus the positions depicted in Figure 1 must be considered
approximate. Each of the catheters had an inlet/outlet valve for
fluid inflow or outflow. The distal (external) end of each cath-
eter was attached as shown in Figure 2 to a “pressure cham-
ber,” and this was in turn attached to a mirror manometer. The
mirror manometer consisted of a small glass funnel over
which was secured a tight rubber diaphragm with a glued
small mirror. A light was reflected from the mirror onto mov-
ing light-sensitive recording paper so that pressure changes
UROLOGY 64: 182–186, 2004 • 0090-4295/04/$30.00
doi:10.1016/S0090-4295(03)00341-8
FIGURE 2. Experimental setup (not all drawn to same scale). The subject lay on a couch, and the catheters were
held at the glans penis to prevent movement. The assistant held the flask containing the fluid reservoir and raised
and lowered it to ensure a constant pressure as fluid entered the bladder.
within the catheters induced movements of the mirrors and
consequently tracings on the recording paper. The tracings
were calibrated in centimeters of water.
During some experiments (or parts thereof), the inlet/outlet
valves associated with the catheters were closed and the vesi-
cal/urethral pressures were measured within a closed system.
At other times, fluid was allowed to flow out of the distal ends
of the catheters (open system). The value of the closed system
was that any detrusor contractions occurred almost at a con-
stant muscle fiber length, thereby reflecting isometric condi-
tions. According to the authors, this avoided distorted pres-
sure recordings that might occur with muscle shortening, gave
clearer indications of relaxation, and allowed a more direct
relationship between the recordings and vesical contractions.
Supporting their assertion, it is well established that pressure
changes under isometric conditions are easier to assess than
under isotonic conditions in which the force and length
change simultaneously during changes in muscle activity.
In addition to recording the vesical and urethral pressures
using two catheter cystometry, Denny-Brown and Robertson
used three other manometers (Fig. 2): (a) attached to a balloon
inserted into the rectum (as a measure of intra-abdominal
pressure); (b) attached to a balloon secured to the abdominal
wall (to measure abdominal wall movements associated with
micturition); and (c) attached to a balloon secured to the per-
ineum (as an indirect measure of perineal muscle activity).
However, not all of the five recording instruments were used
in all of the experiments.
To keep the pressure of input fluid relatively constant at 50
cm H2O, an assistant held a fluid reservoir, and raised or low-
ered the reservoir as necessary to maintain this pressure. Dur-
ing the experiments, one of the investigators held a gloved
hand at the glans penis to maintain the internal positions of
the catheters. Finally, the subject under study indicated events
(eg, restraint of micturition) by pressing a switch that resulted
in a mark on the recording paper.
UROLOGY 64 (1), 2004
COMMENT ON DENNY-BROWN AND
ROBERTSON’S CONCLUSIONS
CONCLUSION 1
The human bladder reacts to distension by con-
traction of its walls.
Although the evidence for this conclusion can be
derived from experiments with both the closed and
the open systems, its clearest support is derived
from Section 3, “The Reaction to Distension.” In
these experiments, the investigators assumed that
the catheters were in configuration “A” in Figure 1
(ie, the apertures for both were in the bladder).
Saline was allowed to flow into the bladder by way
of the vesical catheter in approximately 100-mL
units, after which vesical pressure recordings were
made using the same catheter under approximate
isometric conditions. Saline did not flow out of the
system because it was a closed, pressurized system
once the spigot was closed. For both of the subject-
authors, the bladders were filled to about 700 mL
during an approximately 10-minute period.
Denny-Brown and Robertson showed that under
normal conditions (ie, in the absence of prior blad-
der distension), the intravesical pressure exhibited
a fairly linear increase with increases in volume
until high volumes were reached (see their Fig. 3).
The increased pressure could be correlated with
irregular vesical contractions that were not associ-
ated with any detectable sensation at the lower vol-
umes. Because a slight fall in vesical pressure oc-
183
curred during the “rest” intervals (ie, between
contractions), the authors suggested a process of
active adaptation had occurred (ie, a process in-
volving detrusor relaxation). At the time of this
study, the authors had no means of determining
conclusively whether the decreases in pressure
that occurred during the rest intervals were due to
active contraction/relaxation waves or passive
stress relaxation, common to visceral connective
tissue. They reached their conclusion by compar-
ing their observations with those reported for ca-
daver bladders. Nonetheless, they accurately de-
scribed what is now considered a true phasic
contraction (ie, an active contraction followed by
subsequent relaxation of the bladder detrusor mus-
culature). Finally, the authors suggested that the
normal bladder has a pressure of 5 to 10 cm H2O.
Although the authors at one point suggested that
bladder distension was similar among the subjects,
they also noted that the degree of tonic contraction
differed from subject to subject at comparable vol-
umes and also within the same subject. For exam-
ple, in contrast to Subject A, when Subject B’s blad-
der was filled to 675 mL, it did not show strong
contractions. Furthermore, when the bladder was
filled after a previous distension, it exhibited lower
pressures than before distension.
CONCLUSION 2
Bladder contractions are controlled at low volume
by subconscious restraining. At high volumes, the
restraint becomes conscious.
This conclusion was primarily based on the same
experiments as for Conclusion 1. The authors re-
corded their desire to micturate at high volumes
and the resulting actions on bladder contractions
as they tried to restrain the feeling of “imminent”
micturition. The authors showed some ability for
this restraining process at least initially to reduce
or eliminate waves of painful bladder contractions.
They suggested, however, that with increased fill-
ing, micturition eventually becomes involuntary.
At low volumes, the authors suggested that during
ontogeny, cortical inhibition of bladder function
develops and becomes subconscious in the same
manner as the musculature coordination involved
in walking becomes subconscious.
CONCLUSION 3
Normal bladder sensations are perceived only
when bladder contractions reach a threshold in-
tensity. Furthermore, sensation from the bladder
is related to pressure only to the extent that pres-
sure produces stretch of the bladder wall beyond a
given threshold, that is, it is not pressure itself that
causes the sensation or “awareness” but instead
the amount of stretch caused by a given pressure.
184
Thus, small amounts of active contraction are
more likely to produce an “awareness” sensation if
the bladder is already stretched.
These observations were based on the same ex-
periments as for Conclusions 1 and 2. The subjects
did not feel the sensation of bladder filling until it
contained 250 to 300 mL. Both subjects then felt a
mid-perineal sensation that they related to feeling
like “rivulets running down the urethra.” This sen-
sation did not resemble any sensation normally ex-
perienced. This sensation occurred intermittently
and was not associated with pressure waves, which
the authors considered to be highly significant.
With increased filling, the sensations increased
and the intervals between sensations decreased. At
about 400 mL, a feeling of abdominal distension
began. At 600 mL, perineal and abdominal sensa-
tions increased with some feeling of urgency and
concomitant knee extension. At 675 mL, the peri-
neal feeling was definitely painful, and this pain
was relieved by micturition, with the feelings dis-
appearing in reverse order of their appearance. The
authors could not determine the relevance of the
“rivulets” feeling to normal sensation.
CONCLUSION 4
Other than a slight tonic background, vesical con-
tractions occur in rhythmic waves of activity.
This finding is self-explanatory and again was
based on the recordings of vesical pressure in the
first set of experiments.
CONCLUSION 5
Voluntary effort to micturate results in powerful
contractions of the bladder with a short latency of
development. These contractions are identical to
those that occur spontaneously.
Conclusion 5 was based on the experiments de-
scribed in Section 4, “Modification of vesical pres-
sure by willed effort.” The authors did not clearly
identify the catheter arrangement for these exper-
iments, but, because these experiments were simi-
lar to those in the next section, we assume the
arrangements are those shown by Figure 1B, C.
The bladders were slightly filled (100 to 200 mL),
and the subjects performed one of three processes:
(a) thought about micturating; (b) tried to mictur-
ate (which they actually could not do because the
system was closed); or (c) tried to restrain micturi-
tion after attempting to initiate it. The authors con-
cluded that vesical pressure rises on voluntary ef-
fort to micturate owing to a fusion of detrusor
contraction waves. The authors specifically sug-
gested that the detrusor muscle develops tetanic
contractions in which wave after wave fuses with
its predecessor. Once a contractile “wave” has be-
UROLOGY 64 (1), 2004
gun, voluntary restraint cannot prevent the con-
tractile process from following its typical course.
Furthermore, because the bladder is a hollow or-
gan, every part of the bladder must contract simul-
taneously. Thus, each contractile wave represents
an active contraction that occurs evenly through-
out the bladder wall. Although their analysis was
correct, the authors did not know that the basis of
the simultaneous contraction is the electrical and
anatomic connections between the smooth muscle
cells in the bladder and that smooth muscle, unlike
striated muscle, can exhibit graded contractions.
Thus, on the basis of their knowledge of skeletal
muscle control, the authors suggested incorrectly
that the variation in the force of the bladder con-
tractions resulted from the number of muscle lay-
ers participating in the process, and by the firing
frequency of the motor neurons.
CONCLUSION 6
Relaxation of the perineum appears inseparably
related to voluntary micturition. It is not an essen-
tial factor, rather it is an “associated movement”
not accompanied by relaxation of the external
sphincter. Contraction of the abdominal wall is a
less directly associated movement that can be to-
tally disconnected from micturition. A tendency
toward spontaneous activity of the rectum is not
typically associated with micturition.
Conclusion 6 was not based on any single set of
experiments, but resulted from observations on the
manometers associated with the rectal, perineal,
and abdominal balloons. The authors found that
the most consistent measurable event associated
with the onset of micturition was relaxation of the
perineal musculature. They reached the same con-
clusion by “introspection.”
CONCLUSION 7
Voluntary control can restrain vesical contrac-
tions. Contraction of the perineal musculature
and immediate closure of the external urethral
sphincter are also associated with voluntary
restraint.
For studies supporting this conclusion, the cath-
eters were arranged as in Figure 1C. The urethral
catheter was located distal (superficial) to the ex-
ternal urethral sphincter, with the external outlet
for the urethral catheter opened slightly to allow
for micturition. The vesical catheter was located
within the bladder. Under these conditions, ure-
thral discharge could be stopped immediately, and
the authors attributed this to the external sphinc-
ter. Also, the cessation of micturition was associ-
ated with contraction (presumed) of the perineal
musculature.
UROLOGY 64 (1), 2004
CONCLUSION 8
The internal (involuntary) sphincter contracts
and relaxes reciprocally with the detrusor. The
sphincter’s activity is totally dependent on detru-
sor activity (i.e., it is not under voluntary control).
The closure of this muscle is complete and it is
continually closed during periods of slight or ab-
sent vesical contraction.
This highly cited finding was based on experi-
ments in which the catheters were arranged as in
Figure 1B, with the vesical catheter inside the blad-
der and the urethral catheter between the internal
and external urethral sphincters. The subjects were
discharging their bladder contents through the
urethral catheter, and, when they were instructed
to restrain micturition, there was no immediate
change in discharge pressure. After one or two
brief interruptions in flow, however, the flow
stopped completely 7 to 9 seconds after the sub-
jects began trying to restrain micturition. Flow ces-
sation occurred concomitantly with a decline in
vesical pressure. The authors concluded that this
type of closure is secondary to vesical relaxation.
The data further provided conclusive evidence for
the existence of an internal sphincter in humans,
which had been doubted previously on the basis of
anatomic evidence.
CONCLUSION 9
The external sphincter is normally closed, and
opens during micturition only after the internal
sphincter. The external sphincter closes sponta-
neously at the termination of micturition, before
the internal sphincter has closed. Although the
sphincter can be closed voluntarily, opening does
not appear to be under voluntary control.
With the catheters arranged as in Figure 1D,
fluid was introduced into the proximal urethra by
way of the vesical catheter. With the bladder only
slightly filled (70 mL) in a closed system, no im-
mediate change in the pressure was recorded from
the urethral catheter, which was situated more su-
perficially in the urethra, beyond the external
sphincter urethra. This situation remained even
when the subject attempted to micturate by relax-
ing the perineum and straining the abdomen. After
continued effort to micturate and an accompany-
ing increase in vesical pressure occurred, the ure-
thral pressure rose. Similarly, with the same cath-
eter disposition, but a filled bladder and both outlet
valves opened, the internal sphincter opened ear-
lier than the external sphincter, and in a more
gradual manner (although the authors did note
that the small lumen of the vesical catheter may
have distorted the actual release). With voluntary
restraint, the external sphincter closed rapidly and
the internal sphincter pressure declined slowly.
185
The authors concluded that the external sphincter
not only closes first, but also remains closed even
when the experimental subject makes an effort to
micturate and the perineum relaxes. This sphincter
opens only when vesical contractions have begun
and these contractions have induced an intravesi-
cal pressure sufficient to cause the opening of the
internal sphincter, which is followed then by the
opening of the external sphincter.
CONCLUSIONS
Denny-Brown and Robertson did not find any
significant relationships between either the rectal
or the abdominal sensors and the process of mic-
turition. They did, however, report both a rectal
and an abdominal contraction associated with the
“final” event in micturition (ie, sudden closure of
the external sphincter and slow closure in the in-
ternal sphincter). The absence of pressure changes
in these structures during micturition demon-
strated that increases in abdominal pressure do not
occur during normal micturition, a finding not in-
cluded among their conclusions.
Denny-Brown and Robertson also omitted from
their conclusions their attempts to replicate the
1921 findings of Barrington8 in the cat that the
introduction of fluid into the posterior urethra
caused a reflex facilitation of micturition. With the
catheters arranged as in Figure 1D, and the bladder
containing 70 mL of fluid, which the subjects pre-
viously could easily micturate, fluid was intro-
duced into the urethra by way of the vesical cath-
eter at a pressure of 100 cm. This distension was
totally ineffective in provoking reflex micturition.
Denny-Brown and Robertson’s findings have been
confirmed by recent studies in humans, although
the negative finding in humans may reflect de-
scending inhibitory control not found in other spe-
cies rather than absence of the reflex.9
Although this study was conducted on normal
individuals, Denny-Brown and Robertson’s ulti-
186
mate goal was to illuminate human bladder physi-
ology to help patients with neurologic disorders
that affected micturition. Accordingly, 3 years after
publication of this article, Denny-Brown pub-
lished10 in the New England Journal of Medicine,
“Nervous Disturbances of the Vesical Sphincter,”
in which he reported the results of analysis of blad-
der function using a “delicate cystometric appara-
tus” in a patient with a complete cauda equina le-
sion destroying all nerve roots inferior to L3.
We hope the information we have provided will
lead to a better appreciation of the impressive re-
search method and deductions produced by two
young, dedicated neurologists during the first half
of the 20th century. Clearly, they set the standards
for future definitive research leading to clarifica-
tion of the processes involved in normal and defi-
cient human micturition.
ACKNOWLEDGMENT. To Roberta Shadle for her work on Fig-
ures 1 and 2.
REFERENCES
1. Denny-Brown D, and Robertson EG: On the physiology
of micturition. Brain 56: 149 –190, 1933.
2. Vilensky JA, Gilman S, and Dunn E: Derek E. Denny-
Brown (1901–1981): his life and influence on American Neu-
rology. J Med Biography 6: 73–78, 1998.
3. Denny-Brown D: Edward Graeme Robertson. Ann Neu-
rol 2: 173, 1977.
4. Borrs E, and Comarr AE: Neurological Urology: Physiol-
ogy of Micturition, Its Neurological Disorders and Sequelae. Bal-
timore, University Park Press, 1971.
5. Science Citation Index Expanded, Institute for Science
Information (www.isinet.com/isi/). Accessed 1/10/03.
6. MacDonald WI: Brain in the twentieth century. Brain
123: 3–8, 2000.
7. Foley JM: Derek Ernest Denny-Brown, 1901–1981.
Ann Neurol 11: 413–419, 1981.
8. Barrington FJF: Nervous control of micturition. Q J
Exp Physiol 33: 3–71, 1915.
9. Robain G, Combrisson H, and Maziėres L: Bladder re-
sponse to urethral flow in the awake ewe. Neurourol Urodyn
20: 641–649, 2001.
10. Denny-Brown D: Nervous disturbances of the vesical
sphincter. N Engl J Med 215: 647–652, 1936.
UROLOGY 64 (1), 2004