Quarterly Journal of Experimental Physiology (1989), 74, 493-501

Printed in Great Britain

THE EFFECT OF DISTENSION OF THE URINARY

BLADDER ON ACTIVITY IN EFFERENT VAGAL
FIBRES IN ANAESTHETIZED DOGS
MOHAMED R. M. RAMADAN, MARK J. DRINKHILL
AND DAVID A. S. G. MARY
The Department of Cardiovascular Studies, University of Leeds, Leeds LS2 9JT
(MAN U SC RI PT RECEIVED 10 NOVEM BER 1988, ACCEPTED 16 JANU AR Y 1989)

SUMMARY

Experiments were performed in anaesthetized dogs to find out whether the response of
decreases in vagus nerve activity to distension of the urinary bladder is affected by changes in
carotid sinus pressure. The carotid sinuses were vascularly isolated and perfused with blood at
constant flow. Both ureters were cannulated and the urinary bladder was distended with warm
Ringer solution. In eight dogs, all eleven efferent vagus fibres which responded to changes in
carotid sinus pressure also responded to distension of the urinary bladder by a decrease in
activity. This response of a decrease in activity was obtained at all levels of carotid sinus
pressure between 8 4 and 30 kPa, and was greater at high than at low carotid sinus pressure.
In the same vagus fibres, a relation was shown between progressive decreases in activity and
either increases in intravesical pressure up to 8-7 kPa or reductions in carotid sinus pressure
between 9 and 30 kPa. The decreases in activity were greater at high than at low carotid sinus
pressure. These findings have shown that the inhibition of vagus nerve activity caused by
bladder distension was affected by the level of carotid sinus pressure.

INTRODUCTION
Recently, it has been shown that the same efferent renal and vagus nerve fibres are affected
by distension of the urinary bladder or changes in carotid sinus pressure (Drinkhill, Mary,
Ramadan & Vacca, 1989; Hassan, Hicks, Walters & Mary, 1987 a). The magnitude of the
renal nerve response to bladder distension could be altered by changing carotid sinus
pressure (Drinkhill et al. 1989).
The present investigation was planned to find out whether the response of decreases in
activity in efferent cardiac vagus nerve fibres to distension of the urinary bladder is affected
by changing the pressure in the perfused carotid sinuses. The methods used in this study
have previously been demonstrated to the Physiological Society (Drinkhill, Hassan, Hicks,
Mary, Ramadan & Vacca, 1987).

METHODS
Eight dogs of either sex, which weighed between 15 9 and 21-0 kg, were given a subcutaneous injection
of morphine sulphate (0-5 mg kg-'). Approximately 1 h later the animals were anaesthetized with an
i.v. injection of ac-chloralose (Vickers Laboratories Ltd, Yorkshire; 100 mg kg-') and artificially
ventilated with oxygen-enriched air (approximately 40%), as described by Linden & Mary (1983).
Throughout the subsequent surgical procedures, anaesthesia was maintained by a continuous i.v.
infusion (0 5-1 0 mg kg-' min-') of a 1% solution of a-chloralose in saline. During recording of
activity in efferent vagus nerve fibres, in some animals suxamethonium chloride was administered
(BDH Ltd, Dorset; dose 0.5 mg kg-' every 30 min). Periodically, the doses of the neuromuscular

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494 M. R. M. RAMADAN AND OTHERS

blocking agent were omitted and the animal was allowed to recover from its effect, so that the depth
of anaesthesia could be gauged to assess changes required in the rate of a-chloralose infusion.
Cannulation of the femoral vessels were performed and the pressure in the right femoral artery,
urinary bladder and carotid sinuses were recorded and monitored together with the electrocardiogram
(ECG). The oesophageal temperature and the pH, Pj% and PO of arterial blood were monitored and
maintained within normal limits using techniques described gy Linden & Mary (1983).
Both carotid sinuses were vascularly isolated and perfused with arterial blood from the same
animal using a constant-flow roller pump, as described by Linden, Mary & Weatherill (1981).
Coagulation of the circulating blood was prevented by i.v. injection of heparin (CP Pharmaceuticals
Ltd, Wrexham, UK: initial dose 500 i.u. kg-'; subsequent dose 50 i.u. kg-' every 30 min).
The methods used to distend the urinary bladder have previously been described in detail (Drinkhill
et al. 1989). Briefly, the urinary bladder and both ureters were approached through a mid-line
abdominal incision; the ureters were ligated proximal to their orifice in the bladder, and both were
cannulated proximal to the ligation to ensure free urine flow from the kidneys. A wide-bore double-
lumen cannula was introduced into the urinary bladder retropubically through the urethra, to allow
distension of the bladder with warm Ringer solution, and measurement of intravesical pressure. This
method enabled the pressure inside the urinary bladder to be set to desired values and maintained at
steady levels in all experiments.
The right cervical vagus nerve was dissected free and covered in warm (38C) paraffin oil. A
binocular microscope was used to dissect fine strands from these nerves on a black Bakelite platform
under warm liquid paraffin maintained at 38C by overhead heating lamps. Efferent activity from
single- or few-fibre preparations of the vagus nerves was obtained using silver electrodes, a
preamplifier (NL104, Digitimer, Welwyn, Garden City, London) and filter (NL125, Digitimer). The
action potentials were displayed on a digital storage oscilloscope (OS4020, Gould Ltd, Hainault,
Essex) and passed on to a UV recorder (2112, SE, Laboratories Ltd). In addition, the activity
occurring in 5 s intervals was monitored using a spike processor (Dl30, Digitimer, Ltd) attached to
a chart recorder (Phillips PM8041, Pye Unicam, Cambridge) and on-line computer (BBC, Model B,
Acorn). At all times the activity was counted from single units which were assessed as previously
reported (Linden et al. 1981). Vagus nerve activity was displayed as described above, along with
pressures in the carotid sinuses, trachea, urinary bladder and in the right femoral artery, and the ECG
and was also recorded on electromagnetic tape (Teac R.71).
Experimental protocol
In all dogs, after a steady state had been attained with respect to heart rate, mean arterial blood
pressure and anaesthetic dose, the following responses were initially obtained: an increase in heart
rate and blood pressure to bladder distension, and decreases in heart rate and blood pressure to an
increase in carotid sinus pressure. The activity in the efferent vagus nerve fibres was then studied
following the prevention of the reflex changes in heart rate and blood pressure by the administration
of atropine sulphate (BDH Ltd, Dorset; 0-5 mg kg-') and bretylium tosylate (Wellcome Foundation,
London; 10 mg kg-1).
In each dog, systematic search was used to identify the efferent vagus nerve fibres which either did
or did not respond to changes in carotid sinus pressure as previously described (Hassan et al. 1987 a);
all efferent vagus fibres which responded to changes in carotid sinus perfusion pressure also
responded to stimulation of carotid body chemoreceptors and distension of the urinary bladder. The
nature of the response of efferent vagus nerves indicated that their likely destination was the heart
(e.g. Jewett, 1964; Neil, 1979). Initially, the responsive fibres were examined during distension of the
bladder for 90 s and during an increase in carotid sinus pressure for 90 s. The same protocol was used
in studying some of the efferent vagus nerve fibres which did not respond to an increase in carotid
sinus pressure. The intervention was kept constant throughout its time period. The response to each
intervention was calculated as the difference between the mean nerve activity (in impulses s-1) during
the test period, which constituted the last 60 s of the intervention, and the average of the mean nerve
activity during the two 60 s control periods immediately before and after the intervention period. As
in previous studies (Hassan et al., 1987a; Hassan, Hicks, Walters & Mary, 1987b), this protocol
ensured a steady state of the measured variables during the test period of the intervention. Any
changes in heart rate or arterial blood pressure during the interventions was calculated in a similar
manner. The experiment of bladder distension was performed at two levels of carotid sinus pressure,
a high and a low, such that the baseline vagus nerve activity was changed by at least 100%.

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 URINARY BLADDER DISTENSION AND VAGUS NERVE FIBRES 495

30
20 2.0
10 00
- -2-0 t
-10 t r -4
-20
-60.0
-30
-40 -8-
-50 < -10.0
-60*-10*
UBP CSP UBP CSP
Fig. 1. Histograms showing responses of heart rate (left) and arterial blood pressure (right) to distension of the
urinary bladder (UBP), or increases in carotid sinus pressure (CSP). The drugs included bretylium tosylate and
atropine sulphate. The histograms represent the mean values of the responses, and S.E.M. is represented by the
bars. Statistically significant responses: *P < 0-0005; tP < 001. *, before drugs; U, after drugs.

In the same fibres, vagus nerve activity was obtained at five levels of intravesical pressure in steps
each of about 2 kPa, as previously described by Drinkhill et al. (1989). Each of the steps lasted 90 s,
their sequence was in a random order and they were repeated at two levels of carotid sinus pressure.
Measurements were made during the last 60 s of each step. Finally, vagus nerve activity was obtained
at five levels of carotid sinus pressure in steps of about 5 kPa, with and without bladder distension.
Student's t test for paired data was used for statistical analysis and group data are presented as
mean +S.E.M.

RESULTS
In eight dogs, recordings commenced approximately 4 h after the initial dose of
anaesthetic had been given. The mean initial heart rate was 129 beats min-1 (range 89-173)
and arterial blood pressure was 18 2 kPa (mean; range 150-21 0). The mean pH, P12 and
PO2 of arterial blood respectively were 7-415 (range 7T360-7A448), 4 99 kPa (range 3 60-5 60)
and 34-2 kPa (range 24 4-46'3). The haematocrit was 39-4% (mean; range 38-41).
In each animal, distension of the urinary bladder to a mean intravesical pressure of
6 6 kPa (range 5 3-8&0) was performed as previously described by Drinkhill et al. (1989).
This distension resulted in an increase in arterial blood pressure and in heart rate; these
increases (Fig. 1) were statistically significant (P < 0O0005). Incrementing the pressure in the
carotid sinuses from a mean of 10-2 kPa (range 8-412) to a mean of 29-8 kPa (range
26-7-30*9) caused significant (P < 00d05) decreases in arterial blood pressure and heart
rate (Fig. 1). Following the administration of bretylium tosylate and atropine sulphate, the
above responses to the same levels of stimuli were drastically reduced or abolished (Fig. 1).
A total of 104 efferent vagus nerve fibre preparations were examined, following
prevention of changes in heart rate and blood pressure as described above. Of these fibres,
eleven responded to changes in carotid sinus pressure and ninety-three fibres did not
respond. The latter group was not considered any further, In this group, the mean activity
during the control period was 1[353 impulses s-1 (range 026-290). This activity was not
significantly altered during increases in carotid sinus pressure from a mean of 10'2 kPa
(range 8'4-12 0) to 29-0 kPa (range 26 7-30 6). The measured alterations amounted to 0 043

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496 M. R. M. RAMADAN AND OTHERS

Before distention During distention After distention

Resp. P 0
(kPa) 2J
20 -

FAP
(kPa) K\<<X%\XN\J\<
12 j
Mean CSP
(kPa)
-
8 - 10
Mean UBP
(kPa)
A -
p

Action potential pftm. 00

L-L O' I I
f I - "-T'-'-

ECG -1--j- 1.Iii 11 A 1L.

Resp. P 0
(kPa) 21
20 -

FAP
(kPa)
27 - 2
Mean CSP
(kPa) 10 -
211-
Mean UBP
(kPa)
A -

Action potential ---] 1-1-11 11- 1__ I ----I -1 -'I I L I -II

0
4T__T
---

__..f 11-T-7 fIT-ir-T -

II-I T. -7 1,

ECG I 1 I-1-I
A 111

Is
Fig. 2. Example of experimental records at low (top) and high (bottom) carotid sinus pressure, following the
administration of bretylium tosylate and atropine. Records shown were taken before, during and after
distension of the urinary bladder; from above down are records of tracheal pressure (Resp. P), femoral arterial
pressure (FAP), mean carotid sinus pressure (CSP), mean bladder pressure (UBP), activity in an efferent vagal
nerve fibre (Action potential) and electrocardiogram (ECG). Distension of the urinary bladder, in this example,
at the two levels of mean CSP, caused decreases in activity in the efferent vagal nerve fibre, and this decrease
was unaccompanied by changes in arterial blood pressure, carotid sinus pressure or in heart rate.

impulses s-' (mean; range -0-90-0 50; P > 0 15). Similarly no significant effect was found
during bladder distension. The measured alteration during bladder distension to a mean
intravesical pressure of 6-5 kPa (range 4 2-8&3) amounted to 0 01 impulses s-' (mean; range
-030-040; P> 035).

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 URINARY BLADDER DISTENSION AND VAGUS NERVE FIBRES 497

Table 1. Comparison of the decreases in vagus nerve activity in response to distension of the
urinary bladder at two levels of carotid sinus pressure
Low CSP High CSP Difference P
CSP 10-8+0-45 243+115
(kPa) (84-12-0) (19-5 30 6)
Mean control vagus nerve 1-34 + 034 4 45 + 090 3-11 + 0-84 < 0 0005
activity (impulses s-1) (0 11-4-27) (0 62-7-82) (0 24-706)
Response 0-62 + 011 1-46 + 0-26 0-83 + 0-27 < 0 0005
(impulses s-1) (0 09-1 18) (0 24-275) (0 29-2 66)
Response 18 29 + 3-20 38 04 + 5-10 19-75 + 5-90 < 0-0005
(% normalized) (250-36 7) (20 8-77 9) (30-75 4)

The responses are expressed as absolute values in the third line and as normalized values (see text) in the fourth
line. The values shown are mean+ S.E.M (range). CSP, carotid sinus pressure. Number of fibres = 11.

In each of the eleven efferent vagus nerve fibres which responded to carotid sinus pressure
changes the following experimental procedures were completed.
Responses of vagus nerve activity
An example of experimental recordings obtained during examination of the effect of
changing carotid sinus pressure on the responses of vagus nerve activity to bladder
distension is shown in Fig. 2. The experiment of distension of the bladder to 7 0 kPa was
completed twice in the same nerve fibre, once with the carotid sinus pressure at 11.0 kPa,
and again at 24-0 kPa. The control levels of nerve activity respectively were 1b33 and 3-00
impulses s-1; at both levels of carotid sinus pressure, bladder distension resulted in the
response of a decrease in activity which was unaccompanied by changes in femoral arterial
pressure, carotid sinus pressure and heart rate.
In this manner, in each of the eleven nerve fibres experiments of bladder distension to an
intravesical pressure of 6-4 kPa (mean; range 4 2-8 3) were completed at high and low levels
of carotid sinus pressure (Table 1). The low levels of carotid sinus pressure were set such
that bladder distension did not completely abolish vagus nerve activity. A response of a
decrease in activity was obtained in each of the fibres, irrespective of the carotid sinus
pressure used. The control activity and the magnitude of responses to bladder distension
were always greater at high than at low carotid sinus pressure; group differences were
statistically significant (Table 1).
To allow for the difference in control frequencies between different preparations of vagus
nerves, the responses of the activity were normalized as previously reported (Linden et al.
1981; Drinkhill et al. 1989). The responses were expressed as percentage of the highest
control frequency obtained at high carotid sinus pressure in each nerve fibre examined. The
mean normalized responses were significantly greater at high than at low carotid sinus
pressure (Table 1). Similar results were obtained using normalization and expression of
responses as a percentage of the lowest control activity obtained at low carotid sinus
pressure.
Relation between intravesical pressure and vagus nerve activity
During each of five steps of intravesical pressure, vagus nerve activity was obtained in
the same eleven fibres at two levels of carotid sinus pressure (Fig. 3). The lowest carotid

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498 M. R. M. RAMADAN AND OTHERS

4 QA
(U
B
3
E
C
D
* E
2

'U*
CT

t
t
0 ~t t
0 2.3 4.2 6.1i 8-1
1-4-33 26-49 4-69 668-7
UBP (kPa)
Fig. 3. The effect of low (U, 9 9 kPa; range 84- 13 2) and high (M, 24-4 kPa; range 18-30) carotid sinus pressure
(LCSP and HCSP) on the relation between vagus nerve activity and four step increases (B-E) in urinary bladder
pressure (UBP) over the undistended state (A); UBP is shown as mean and range. The height of the columns
depicts mean values, and S.E.M. is indicated by the bars. Reduction in vagus nerve activity was always greater
at HCSP than at LCSP (at least P < 0 0025). t Indicates statistically significant difference in vagus nerve activity
between LCSP and HCSP at all steps of UBP (at least P < 0 0025). * Indicates statistically significant difference
between E, the highest UBP and the other steps (at least P < 0 005). t Indicates statistically significant difference
in vagus nerve activity at LCSP between E and other steps.

sinus pressure was 84 kPa; pressures below 8 kPa are reported to excite carotid
chemoreceptors (Biscoe, Bradley & Purves, 1970).
Increments in intravesical pressure always caused significant decreases in vagus nerve
activity at low and high levels of carotid sinus pressure (at least P < 0 0025). The vagus
nerve activity obtained at all levels of intravesical pressure was always greater at high than
at low carotid sinus pressure (Fig. 3). The decrease in vagus nerve activity of 1P77 impulses
s-1 (mean; range 0 55-3 34), caused by incrementing intravesical pressure to a mean of
8 1 kPa at high carotid sinus pressure, was significantly greater (P < 0 025) than that of
0 72 impulses s-1 (mean; range 0-33-1 69) at low carotid sinus pressure.
Relation between carotid sinus pressure and vagus nerve activity
During each of five levels of carotid sinus pressure, vagus nerve activity was obtained
in the same eleven fibres against two backgrounds, with and without bladder distension
(Fig. 4).
Increments in carotid sinus pressure always resulted in significant increases in vagus
nerve activity in the presence or absence of bladder distension (at least P < 0 05). The vagus
nerve activity obtained over the range of carotid sinus pressure examined (Fig. 4) was
always significantly lower with bladder distension than without. In the presence of bladder
distension, the increase in vagus nerve activity of 5 30 impulses s-1 (mean; range 0 47-26 7)

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 URINARY BLADDER DISTENSION AND VAGUS NERVE FIBRES 499

10

8
E

0 .
t | E

1 1-5 16-0 20-6 25-4 29-8

9-13-2 16D17-4 20213 23-7-26*7 28-3-30
CSP (kPa)
Fig. 4. Histograms showing the effect of the absence and presence of bladder distension on the relation between
vagus nerve activity and five step levels (A-E) of carotid sinus pressure (CSP); CSP is shown as mean and range.
The height of the columns depicts mean values, and S.E.M. iS indicated by the bars. Symbols as in Fig. 3.
Increments in CSP always resulted in significant increases in vagus nerve activity in the presence or absence of
bladder distension (P < 0 05). In the presence of bladder distension, the increase in vagus nerve activity caused
by increasing CSP from A to E was significantly less than that obtained in the absence of bladder distension
(at least P < 0 01). *, UBP 0 0 kPa; *, UBP 6-1 kPa (range 4-6 8).

caused by incrementing carotid sinus pressure between means of 11 5 and 29-8 kPa was
significantly less (P < 0 01) than that of 6-80 impulses s-I (mean; range 0 85-29 7) obtained
in the absence of bladder distension.

DISCUSSION
Distension of the urinary bladder has been shown to cause the reflex responses of an
increase in heart rate and arterial blood pressure, and respectively increases and decreases
in activity of efferent cardiac sympathetic and vagus nerve fibres (Taylor, 1968; Hassan et
al. 1987 a, b). The efferent effects of reflexes related to the bladder and carotid baroreceptors
have been shown to converge on the same cardiac or renal nerve fibres (Hassan et al.
1987 a, b; Drinkhill et al. 1989). In particular, the magnitude of response of increases in renal
nerve activity could be altered by changes in carotid sinus pressure (Drinkhill et al. 1989).
The present study has examined the possibility of an effect of changing carotid sinus
pressure on the response of a decrease in activity in efferent vagus nerve fibres to distension
of the urinary bladder. A total of 165 interventions of increments in intravesical pressure
in all eight dogs (see Table I and Figs 2, 3 and 4) caused a decrease in efferent vagus nerve

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500 M. R. M. RAMADAN AND OTHERS

activity. The decreases in vagus nerve activity could be graded according to increments in
intravesical pressure up to 8 7 kPa. Such decreases occurred despite changes in carotid sinus
pressure over the range of 84-30 kPa, which markedly altered baseline vagus nerve
activity. However, the high levels of carotid sinus pressure were shown to augment the
decreases in vagus nerve activity caused by increases in intravesical pressure. The levels of
intravesical pressure used in this study include those previously reported in man under
physiological conditions (Denny-Brown & Robertson, 1933; Tanagho & Miller, 1970;
Walter, Olesen, Nordling & Hald, 1979) of spontaneously filled bladder at 1 8-2 5 kPa, and
at micturition at 2 3-106 kPa.
The results of the present study were based on a systematic search of efferent vagus nerve
fibres. In addition, the type of response of vagus nerve activity to changes in carotid sinus
perfusion pressure and distension of the urinary bladder suggested that the nerves
examined were destined to innervate the heart. The response of these fibres to changes in
the level of carotid sinus baroreceptor activation, a stimulus known to have a profound
effect on cardiac vagus efferent discharge (e.g. Kirchheim, 1976), produced changes in the
predicted direction for cardiac vagus fibres and has previously been used in the definition
of such efferent vagus nerve fibres (e.g. Jewett, 1964; Neil, 1979). In a previous study, it was
shown that all the responsive efferent vagus nerve fibres also responded to stimulation of
carotid body chemoreceptors in a manner suggesting a cardiac destination, and had
conduction velocities similar to those reported for cardio-inhibitory vagus efferent fibres
(Hassan et al. 1987a).
These results have important implications. For instance, the graded effect of bladder
distension on vagus nerve activity constitutes further evidence for the bladder reflex. It has
previously been shown that increases in intravesical pressure which stimulate bladder
mechanoreceptors have a graded effect on afferent hypogastric and pelvic nerve activity and
on efferent renal nerve activity (Floyd, Hick & Morrison, 1976; Floyd & Lawrenson, 1979;
Bahns, Enrsberger, Janig & Nekle, 1986; Drinkhill et al. 1989). These findings indicate that
the response of an increase in heart rate to bladder distension is reflex in nature, and
involves increases and decreases in activity, respectively, of efferent sympathetic and vagus
cardiac nerves. In the present study, the heart rate reflex was abolished by bretylium
tosylate and atropine sulphate.
The graded effect of changes in carotid sinus pressure on efferent vagus nerve activity
indicates grading of activation of the carotid baroreflex (e.g. Iriuchijima & Kumuda, 1964).
The effect of such activation on the response of vagus nerve activity to increases in
intravesical pressure has suggested interaction between the effects of the carotid baroreflex
and bladder distension on the same efferent vagus nerve fibres. According to the definition
of Kirchheim (1976) and Korner (1979), interaction is said to occur when the combined
efferent effect of stimuli is different from the algebraic sum of each. In the present study,
activation of the carotid baroreflex resulted in greater responses to bladder distension; their
average magnitude increased by 1-3. Also, this activation resulted in augmentation of the
graded effect of incrementing intravesical pressure on vagus nerve activity; overall, the
magnitude of decreases in vagus nerve activity were at least doubled in association with
increases in carotid sinus pressure. In addition, bladder distension was found to affect vagus
responses to activation of the baroreflex. The graded effect of increases in carotid sinus
pressure on vagus nerve activity was attenuated in the presence of bladder distension;
overall, the magnitude of increases in vagus nerve activity was attenuated by about 20 %
in association with bladder distension.
The present results, and those previously reported (Hassan et al. 1987a, b), could be
argued hypothetically to provide a mechanism for micturition syncope (e.g. Proudfit &
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 URINARY BLADDER DISTENSION AND VAGUS NERVE FIBRES 501
Forteza, 1959). The emptying of the bladder would lead to reductions in arterial blood
pressure and heart rate.
The present study has shown that increases in intravesical pressure caused inhibition of
efferent vagus nerve activity. The inhibition was augmented by increasing carotid sinus
pressure.

The authors wish to express their gratitude for the excellent technical help by Messrs D. Kaye,
P. Berry and P. Warburton.

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