Volume Receptors
By Louis G. WELT, M.D.
This paper reviews the coimplicated interplay which may be involved in the retention
of water and salt by the kidney. For the sake of brevity, it does not treat either the
inechanisnis which regulate the intake of water or the disposition of fluid throughout
the body. The neurohunmoral pathways by which a change in intravascular volume can
effect a retention of water by the kidney receives particular attention. The difficulties in
dissociating intrarenal from extrarenal determinants of salt and water excretion are
eonsidered in detail.
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amrlonig these several alternatives for the effereut are of a reflex. If there is a volume receptor, its preseniee eertainly does not exclude
other types of detectors. Lastly, if there is a
volume receptor, there certainly need not be
only one. It would indeed be surprising if this
function of body fluid volume, which is so
crucial to the very existence of the organisn,
were to be regulated by some simple single
control niechanisin. It is much more reasonable to approach this problem with the perspective that there are mtaniy devices through
which aim error in volume is appreciated, several means by which the kidneys are notified,
and a variety of mechanismns by which the
kidneys can compensate for the error.
The most basic of all mechanisms mnight
very well reside within the kidneys themselves.
It should not be forgotten that when the nerve
supply of a kidney has been totally interrupted,' or when the supply of salt-retaining
adrenocortical hormone can be neither increased mior decreased,2 the kidney can, nevertheless, respond immediately and appropriately to a variety of procedures which appear
to have, as the common denominator, a change
in total volunme or an alteration in its disposition.
The regulation of the excretion of water and
the role of antidiuretic hormone have already
been described in this symposium.3 With respect to the antidiuretic hormone, it is apparent that the effective osmolality of the
body fluids is the primary stimulus leading to
the elaboration of a concentrated or a dilute
urine.4 However, osmolality is only 1 aspect
of the comiposition of body fluids.
T HIS REVIEW will deal with only 1
aspect of the problem of why, on the one
hand, we donl't shrivel to clay and dust, and,
on the other, why we just don "t blow up and
bust. It will not attempt to discuss the problems which relate to the regulation of volume
among the several major and mninor fluid conpartments. Nor will it consider either the inportant determiinants which condition the distribution of volume within the vascular comzponent itself, or the factors whieh determine
our appetites for, and the ingestion of. salt
and water. The problem at hand coneerns only
those factors that control the fluid volume,
and how this volume is affected by the elimination of salt and water from the organism by
the excretion of urine. This small, but still
awe-inspiring, segment of the problem can be
defined by the question: how are the kidneys
apprised of and how do thev respond to distortions of volume in such a fashion as to
selectively augment or diminish the rate of
excretion of salt and water, so as to maintain
the volume of the body fluids within certain
narrow limits ?
The kidney 's ultimate response must be
either a primary change in hemodynamics or
an altered rate of tubular reabsorption. These
mechanisnms could be local and autonmatic; thev
could be influeneed by neural discharges or by
humoral agents. If there is a receptor which
is sensitive to some funetion of volume such
as stretch, pressure, or flow, we must still look
From the Department of Medicine, School of
Medicine, University of North Carolina, Chapel Hill,
N. C.
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A distortion of the volume of body fluids
can also promote changes in the secretion of
the antidiuretic hormnone, but these appear to
be of secondary importance.5-9 Paradoxically,
however, the best evidence for volume receptors is stretch receptors that appear to influence the secretion of antidiuretic hormone.10-17 These will be referred to later.
The regulation of the excretion of salt will
occupy our attention first, because the quantity of sodium in the body appears to be the
primary influence with respect to the volume
of fluid in the body. When salt is retained in
excess of water, thirst is stimulated. Thirst,
in turn, promotes the ingestion of water, and
the secretion of antidiuretic hormone is stiinulated, so that the urine which is elaborated
is concentrated and small in volume. The
quantity of salt that gains access to the urine
is presumably the difference between that
which is filtered at the glomerulus and that
which is reabsorbed by the tubules, assuming,
for the sake of simplicity, that there is no
significant net secretion of sodium. The quantity of salt which is excreted, then, might
readily be expected to be influenced by the
filtered load, a value which is the product of
the concentration of sodium in the filtrate and
the volume of the filtrate.
There are, in fact, innumerable examples of
a direct correlation between the change in the
filtered load of sodium and the change in its
rate of excretion."' Under most circumstances,
the per cent of the filtered load which is excreted is small and, for this reason, one might
readily account for many changes in the rates
of excretion of salt on the basis of very siiall
alterations in the filtered load.
Thus, at the very start, we are faced with
the problem of how we can ever exclude with
certainty a minor change in filtered load as
the determinant of most changes in the rate
of excretion of salt. This problem can sometimes be resolved, however, if the experimental design includes enough data so that a
statistical treatment may, at least, either allow one to conclude that it was unlikely that
a change in filtered load was responsible, or
else force one to conclude that the alterations
Circulation, Volume XXI, May 1960
1003
in excretion could have been due to concordant
changes in filtered load.
Eveen if this problem were surmounted,
there are still other matters concerning local
reiial hemodynamics that must be considered.
There are approximately 2,000,000 nephrons
in the 2 human kidneys, and it has recently
been emphasized by Bradley and Wheeler"'
that all of these cannot be considered to be
identical. One cannot assumue that each glomerulus filters the same volume as each of
the others. This has significance for several
reasons.
The reabsorptive activity of a nephron may
be, in part, conditioned by the volume of filtrate formed in that nephron. Furthermore,
there are reasons to view the population of
nephrons as varying, not only in certain
anatomic characteristics which include position, size and length, but in functional termus
as well. Some tubules, for example, might
reabsorb a greater fraction of filtered sodium
than others. Hence, it is conceivable that under different circumstances the total rate of
filtration from all 2,000,000 glomeruli mav
reinain unchanged, while the fraction of the
total filtration in any particular group of
nephrons may increase or decrease. In this
fashion, a change in the rate of excretion of
sodium may be effected without a change iii
the total filtered load.
Still another renal hemodynamnic alteration
that might conceivably influence the exeretion of sodium to some degree has recently
been re-emphasized by Vander, Malvin, Wilde,
and Sullivan.20 They raised the question of
whether the reabsorption of sodium in the
proximal tubule may be passive rather than
active. They suggest that the colloid osmotic
pressure of the blood in the peritubular vessels promotes a redisposition of water froin
the proximal tubular lumen into the vascular
channels. This redisposition would tend to
increase the lunminal concentration of sodium
and to promote its passive diffusion from the
tubule. Accordinig to this concept, a change
in the filtration fraction might alter sodium
reabsorption- because of changes in the colloid
osmotic pressure of the blood in the peritu-
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bular vessels. This theory has been criticized
on several grounds: (1) it has been pointed
out that it is unlikely that the colloids could
ilnfluence the distribution of water across such
a highly discriminating membrane as the proxiinal tubular epitheliuin; (2) it could not aecount for the bulk of the proximal tubular
sodium reabsorption; (3) there is evidence
that sodiuin does move against a gradienit and,
hence, must be transported by an active
process.
The first criticism must be evaluated by experiment. The fact that it cannot account for
the bulk of sodium reabsorption and the fact
that there is undoubtedly active transport do
not exclude the possibility that this transport
night be facilitated in part by this nmechanism. Thus, it is clear that altered rates of
exeretion of salt could be accounted for by
small, and what are frequently referred to as
"insignificant," changes in filtration rate, by
a redistribution of filtration among the nephrons with no net change in the total rate of
filtration, and, conceivably, by disproportionate changes in renal plasma flow and filtration rate.
This is a most difficult area to study, but
the imposing nature of the experimental challenge does not reduce the significance of these
possible physiologic regulatory devices. Furthermore, they might very well be responsive
to direct consequences of alterations in the
volume of the blood per se, and may represent
rather automatic adjustments within the renal
circulation itself.
There are certainly many studies wherein
it is clear that a reduction of the volumne
of the body fluids decreases, and an expansion
of the body fluids augomelnts, the rate of excretion of salt. Changes in the disposition of
volume without alteration in its total quantity also promote natriuresis and antinatriuresis. The passive erect posture, sitting, cuffing
of the extremities, obstruction of the venious
return from either the inferior or the superior
vena eava, and opening an arteriovenous fistula all promote a diminished exeretion of
salt. In contrast, the relief of these obstructions and the assumption of a comfortable
WELT
supine position augment the elimination of
salt.5-9, 21
Let us deviate for the moment, to consider
which volume may be undergoing the important change. An increase in the total volume of body water, an increase in the extracellular volume as a whole, an increase in
the vascular volume, and an increase specifically in the arterial volume per se all promote
an increased exeretion of salt.
Several recent reviewers have stated6' 7 that
the infusion of iso-oncotic solutions of albumin
does not promote the excretion of salt. However, the data from the experiments quoted
did, in fact, demonstrate soime increase in the
excretion of salt when iso-olcotic solutions of
albumin in saline were infused.22 It was also
apparent that this natriuresis was no greater
than that achieved with the infusion of an
equal volume of saline. Sinee the common denominator of these 2 types of infusion was aii
expansion of the intravascular volume, it is
ilot illogical to assert that the expansiomi of the
vascular volume was at least 1 determinant of
the increased salt excretion.
This does not, of course, exclude the influence of alterations in the volume of the
interstitial space. The experiments which suggest that the volume of this latter compartment may be important are those in which
hvperoneotic solutions of albumin were found
to expand the vascular volume (at the expense
of the interstitial volume) and to diminish the
rate of salt excretion.23' 24 It may be that con-
traction of the interstitial fluid volume was
important, but it is also possible that an increase in the colloid osmotic pressure of the
plasma in the peritubular vessels was the
important alteration.
Strauss and his co-workers25 recently reported a study which emphasizes the amazing
sensitivity of some receptors to the infusion of
a salt solution. Subjects were prepared on a
salt-free regimen, so that they had eliminated
a "surfeit" of salt, and were excreting small
quantities of it. They were then studied in
a supine position, and at a time of day when
a spontaneous, diurnal increase in the renaal
excretion of salt would not be expected. After
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suitable control periods, the subjects were infused with a small volume (150 ml.) of a
100 millimolar solution of salilne over a period
of 15 minutes. There was a prompt and unequivocal increase in the rate of exeretioni of
sodium. The clearance of endogenous creatinine was said not to have changed significantly, and, since the infusate was hypotonic,
it could hardly have inereased the conieentration of sodium in the filtrate.
Since this experinlental design appeared to
be uniquely sensitive to alterations in volume,
Hollander26 has beeii utilizing this protocol
to compare the effects of the infusion of solutions which are identical in volume and conposition with the exception that in half of
the experiments, the infusate contains albumin
at an iso-oncotic level. Thus far, there are 10
experiments, in which 150 ml. has been infused over a period of 30 minutes. Half of
these have contained albumin. There is a small
natriuretic response to both infusions, and
although the mean inerement in salt excretion
is greater with the infusions which contain
albumin, the signifieance of this difference is
dubious. The question of a discriminating response to larger volumes is ulider study.
These experiments have some other interesting features. In 3 studies, it has been noted
that the infusion of a volume as small as 25
ml. in 30 minutes, that is, less than 1 ml. per
minute, will elicit a response which is identical
to that noted after the infusion of 150 ml. It
is difficult to imagine a central volume reeeptor sensitive to such minute changes, and the
question must be raised whether the stimulation of a peripheral vein or the undetected influence of some other part of the experimental
procedure may not be more important than
the volume expansion itself. The experiment
utilizing a mock infusion has not yet been
done.
The characteristics of the redisposition of
volume accomplished by changes in posture,
cuffing of the limbs and obstruction of the
vena cava, have suggested to several authors
that volume receptors might exist in the upper
half of the body. Some attention was drawn
to the head itself by experimentts that sugCirculation, Volume XXI, May 1960
1005
gested that the application of a cuff around
the neck might modify salt exeretion.27 However, this has not been confirmed by
others.28' 29
Stretch receptors and baroreceptors have
been known to exist in various parts of the circulatory system,30 and recently considerable
attention has been directed to those within
the thorax. It had been noted by Gauer,
Henry, Sieker, and Wendt'0 that negative
pressure breathing promoted an increase in
urine flow in dogs that began after about 10
minutes and reached its peak in 30 to 50 minutes. In contrast, Drury, Henry and Goodman31 had reported that positive pressure
breathing promoted a decrease in urine flow.
These observations have been confirmed in
man,'1' 17 and it seems reasonably clear that
this is an effect on the excretion of water and
that there is no primary effect on the rate of
excretion of sodium or other solutes. The response can be blocked with vasopressin51' 16
and there is no increase in urine flow while
the subject is under a maximum water diuresis and the secretion of antidiuretic hormone
is presumably completely suppressed.15 The
antidiuretic response to positive pressure
breathing can be partially or completely inhibited with alcohol.16 Surtshin and his collaborators12 have demonstrated that the diuresis which occurs during negative pressure
breathing is not significantly affected by renal
denervation. Thus, the efferent arm of this
reflex seems to be a diminished supply of antidiuretic hormone rather than some peripheral
neural component.
Henry and his co-workers13' 14 demonstrated
that distention of the left atrium with a balloon resulted in a pronounced diuresis, and
that the response to negative pressure breathing was either abolished or reduced by section
of, or the applieation of cold to, the vagus
nerves. They also recorded neural discharges
from the vagus nerve, and by relating peak
activity to events of the cardiac cycle, were
led to conclude that the receptors probably
respond to stretch rather than to pressure.
Henry and others'3 seemed to have excluded
distention of the pulmonary arterial and ve-
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nous system, except, perhaps, for that portion
of the pulmonary vein that lies within the
pericardium. Love and his collaborators32
demonstrated that the amplitude of the pulsation of sonie part of the intrathoracie vascular
systenm might be the important stimulus. They
reported that pulsatile pressure breathing
around a ineau pressure of zero, or a positive
pressure of 20 immn. Hg, promoted an inerease
in urine flow, whereas nonpulsatile positive
pressure breathing did not.
In assessing the significanee of this reflex,
Henry, Gauer, alnd Sieker33 reported that
changes in blood volume from -30 per cent to
+30 per cent influeneed pressure conicordantly
throughout the circulatory system, alnd concluded that stretch reeeptors in the left atrium
could therefore be influenced by changes in
volume. However, it must be einphasized that
this reflex only inifluenees the exeretion of
water. Furthermore Pearce34 has reported
that the integrity of the vagus nerve was not
essential to the diuresis which resulted from
iso-oneotic albumin infusion in dogs.
More recently, Barger and his collaborators35, 36 have conleerned themselves with
another area of the vascular tree which may
be implicated as a volumne receptor. They
noted that a decrease in blood pressure in the
carotid sinus is accompanied by a decreased
rate of excretion of sodium. They suggest that
the retention of sodiumn may be due to the
release of norepinephrine as blood pressure in
the carotid sinus decreases. This hypothesis
remains to be reconciled with the observations
of Pearce34 that denervation of the carotid
sinus does not interfere with the diuresis
which follows the infusion of iso-oneotic solution of albumin in the dog.
If volume receptors are of importance in
the regulation of salt excretion, the efferent
are would presumably be 1 or more of the following: a neural impulse, the diminished secretion of a salt-retaining hormnone, or the
secretion of some humoral agent which was
primarily concerned with increasing the excretion of salt, i.e., a natriuretic hormone.
The role of the central nervous system in
the regulation of salt excretion continues to
WELT
be enigmatic. There is a considerable distribution of neural elements to the kidneys, but
there is no convincing evidence that any of
these fibers terminate within renal tubular
cells.37 The renal nerves appear to be involved
primarily with the vascular systemn. On the
other hand, there are both patients and experimental animals in whom lesionis of the central
and peripheral nervous system may be accompanied by anl increased excretion of salt in
the urine.
Schwartz and his co-workers38 have explainied "salt wastinig" in 1 group of patients
as beimig due to aii inappropriate secretion of
the antidiuretic hormone, the retention of
water, expansion of body fluid volume, and a
consequent augmeiited rate of exeretion of
salt. These patients, and others who appear
to represent the same renal disorder, have
had central nervous system lesions. The experimnental denervation diuresis provoked by seetiomi of the splanchnic nerves may be due
solely to an influence on renal vessels and altered hemodynamics.6 9 Jungmann and
Meyer39 and, more recently, Wise40 have provoked an increased renal excretion of salt by
producing lesions in the brain stem. Finally,
some patients have been seen with coexistent
central nervous system lesions of recent origin,
hyponatremia and dehydration; in this group,
which has been designated " cerebral salt
wasters, it seenms virtually impossible to implicate the administration, and the retention.
of water.9 The influence of the central nervous
system on the kidney remains to be elucidated.
Again, it should be stated that the denervated
kidney can still respond in a normal fashion
to stimuli which ordinarily promote the excretioii or retemition of salt.
The most recent phase of the development
of this problem conieernis the influence of volume on the secretion of the hormnone, aldosterone. Dr. Farrell and Dr. Bartter will unidoubtedly coneern themselves wvith this aspect, so I shall not dwell on this problem in
any detail. However, assuming that changes in
volume are somehow appreeiated by a receptor mechanism anld translated into an altered
rate of secretion of aldosterone, we must still
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raise the question of the significance of this
hormone in the regulation of the excretion of
salt.
There is no doubt that aldosterone does
have a profound influence on the renal tubular
reabsorption of salt.9 However, its effects cannot always be demonstrated, and when they
do occur, they appear only after a lapse of
time.41 The prompt, acute alterations in the
excretion of salt in response to absolute
changes in blood volume or to redisposition of
volume can occur in the adrenal-insufficient
animal and human.
In summary, there are undoubtedly many
mechanisms that influence the excretion or
retention of salt, and thereby control the volume of body fluids within narrow limits. As
of this time, one might list them as follows:
1. Basic mechanisms, which are intrinsic to
the kidney itself, which are determined by
filtered load, distribution of this load among
various nephrons, and perhaps changes in
filtration fraction. These mechanisms are most
likely responsible for the acute adjustments,
and it is probable that the volume of the blood
influences these determinants by minor variations in blood flow and perfusion pressure.
Furthermore, it is difficult in many circumstances to prove that these minor changes were
not responsible for an observed alteration in
the excretion of salt.
2. Neural regulators which probably express
themselves in filne hemodynamic adjustments.
The possibility of some other influence is not
resolved.
3. Hormonal influences which, in turn, may
be responsive either to changes in volume or
to some function thereof. The evidence that
volume influences antidiuretic hormone secretion has been presented. The probability that
volume influences the secretion of aldosterone
will be considered in a subsequent paper.
4. The existence of a natriuretic hormone is
highly speculative. It should be and is being
sought. Until it is found, it does not seem
profitable to speculate further on how its secretion may be altered.
Throughout this discussion, I have not
meant by any means to underestimate the imCirculation, Volume XXI, May
1960
portance or the significance of mechanisms
that have an extrarenal origin. However, the
certain exclusion of renal hemodynamic influences is not easy and must always be considered. Perhaps new and better tools must
be applied to these problems.
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Circulation, Volume XXI, May
1960
Volume Receptors
LOUIS G. WELT
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Circulation. 1960;21:1002-1008
doi: 10.1161/01.CIR.21.5.1002
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