AMERICAN

Vol.

JOURNAL

OF PHYSIOLOGY 1975. Prinied

228, No. 1, January

in U.S.A.

Effect of hypoxia to the carotid

on vascular

responses

baroreflex

CONRAD L. PELLETIER AND JOHN T. SHEPHERD Mayo Clinic and Mayo Foundation, Rochester, Minnesota 55901

PELLETIER, CONRAD L., AND JOHN T. SHEPHERD. E$ect of hypoxia on vascular responses to the carotid barorej?ex. Am. J. Physiol. 228(I) :331-336. 1975.-The effect of systemic hypoxia on the vascular responses to the carotid baroreflex was studied in anesthetized, vagotomized, artificially ventilated dogs. One hindlimb, kidney, gracilis muscle, and paw were perfused at constant flow, and neurograms were obtained from renal sympathetic fibers. Bilateral carotid occlusions were performed while the animal was breathing a mixture of air and 02 (mean arterial Pop = 106 mm&) and again during ventilation with 10% 02 (PO, = 40 mmHg) + With occlusion, the average increase in mean aortic pressure was 36 mmHg greater during hypoxia than during normoxia and the increase in renal perfusion pressure was 87 the increase in hindlimb perfusion pressure was mmI-Ig greater; identical in both situations. Hypoxia did not change the reflex response of the paw to carotid occlusion and increased that of the muscle vessels by only 10%; the increase in renal sympathetic activity averaged 56 + 10 y$ more with hypoxia than with normoxia. When the carotid chemoreceptors were destroyed, the greater increase in aortic and renal pressure response to carotid occlusion during hypoxia as compared to normoxia was abolished. Thus systemic hypoxia markedly potentiates the reflex renal constriction caused by the barorefiex, and this effect is due to the

carotid chemoreceptor

afferent input.

carotid occlusion; chemoreceptors; hindlimb perfusion; kidney perfusion; muscle; paw; renal neurograms; peripheral resistance; sympathetic activity

OF THE INHIBITORY influence of the arterial baroreceptors induces an increase in sympathetic nerve traffic to skeletal muscle and kidney. This increase is equivalent to electrical stimulation of the sympathetic nerves to the skeletal muscles at a frequency of eight impulses per second but at a frequency, at most, of only four impulses per second to the kidney. This indicates that withdrawal of baroreceptor restraint on the vasomotor center is followed by a lower firing rate in renal vasoconstrictor fibers than in those to skeletal muscle. This appears to result from a lower level of spontaneous activity in the renal neuron pools in the vasomotor center as compared to those governing the skeletal muscles (9, I 1). However, in other circumstances, the response of the renal vessels to changes in baroreceptor activity can be greatly increased. In the cat, during hypoventilation or acidosis, the spontaneous ac tivi tY in the renal vasomotor neurons evidently increases, so th at the renal vasoconstriction in response to decreased baroreceptor activity is augmented (6, 9); in the rabbit, interELIMINATION

of aortic or vagal nerve afferents during normoxia causes a relatively greater reflex constriction of muscle than of renal vessels, whereas during hypercapnia this is reversed (12, 13). Hypothalamic stimulation also modifies the sensitivity of renal resistance vessels to carotid sinus pressure (2); it increases renal sympathetic output at low pressure and displaces the point of complete inhibition at a higher pressure ( 15). Thus it appears that the changes in renal resistance induced by the baroreflexes can be altered by other inputs converging or acting directly on the vasomotor neurons. In the current studies, the effect of hypoxia on the vascular responses to the carotid baroreflex was studied in order to examine the possibility that the carotid chemoreflex might affect the renal involvement in the baroreflex. ruption

METHODS

Preparation

Dogs, lo-29 kg in body weight, were anesthetized with thiopental and chloralose (15 and 60 mg/kg, respectively) and artificially ventilated at 12-l 5 cycles/min. Additional chloralose (10 mg/kg) was administered hourly. Prior to cannulation of the blood vessels, gallamine and heparin (3 mg/kg each) were given intravenously and repeated hourly (1 mg/kg each). The two vagosympathetic trunks were cut in the neck. In the control condition, the dogs were ventilated with a mixture of room air and 0,. Systemic hypoxia was produced by ventilating the animals with 10 % O2 in Nz for 2 min, after which the ventilation was returned to the control condition (normoxia reached after 2 min). Blood samples were taken during the control situations before and after hypoxia and at the end of 2 min of hypoxic ventilation for measurement of arterial blood gases and pH. In the normoxic condition, arterial PO, averaged 106 mmHg (range: 77-142 mmHg); after 2 min of hypoxic ventilation it averaged 40 mmHg (range : 32-47 mmHg). Arterial Pcoz was maintained normal throughout the experiment by adjusting the tidal volume and was the same during normoxia and hypoxia, averaging 32 mmHg (range: 25-38 mmHg). The pH of arterial blood was kept normal by infusing bicarbonate as needed and averaged 7.41 (range : 7.34-7.49) during normoxia and 7.44 (range : 7.35-7.53) during hypoxia. Bilateral occlusion of the common carotid arteries (BCO) was used to study the reflex responses to decreases in carotid

331

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332

C.

baroreceptor activity. Each occlusion lasted 30-40 s and was not repeated until all pressures had returned to control level. The occlusion was done during the control condition, after 2 min of hypoxic ventilation, and 2 min after normoxic ventilation was resumed. To minimize the duration of systemic hypoxia, only one occlusion was done for each period of hypoxia, which was repeated an avcragc of 4 times in each experiment, interrupted by intervals of at least 6 min of normoxia. The left lumbar sympathetic trunk was cut at the level of Lp, and the rami at Lz, Ls, and LJ were divided. A bipolar stimulating electrode was placed on the trunk between L,, and Ls. Monophasic square-wave stimuli were given (Grass stimulator, model S-4) at 10 V, 5 ms duration, and frequencies from 1 .O to 12/s. Stimulation was maintained until the response of the hindlimb resistance vessels had reached a plateau. Between stimulations, hindlimb perfusion pressure was allowed to return to control level. Measurements

All pressures were measured with strain-gauge transducers (Statham P23 De) and recorded on a Honeywell ultraviolet Visicorder (model 1508). Aortic pressure. The pressure was measured in the aortic arch through a catheter inserted in the right brachial artery. Constant--ow perfusion. The kidney, hindlimb, gracilis muscle, and paw were perfused at constant flow with roller pumps, using arterial blood taken from the iliac artery. Depulsators and heat exchangers were interposed in the perfusion lines, and the temperature of the blood was maintained at 37°C. Perfusion pressures were measured through the side arm of T connectors immediately upstream from the inflow cannula to each bed. The perfusion pressures of the hindlimb, gracilis muscle, and paw were adjusted to approximately mean aortic pressure at the beginning of the experiment (about 150 mmHg) ; the per-

L.

PELLETIER

AND

J.

T.

SHEPHERD

fusion pressure of the kidney was set between 100 and 110 mmHg to avoid excessively high perfusion pressures being reached in the kidney during sympathetic nerve activation and a failure to return to control levels on cessation of stimulation. After the pressures were adjusted initially, they were left unchanged thereafter. The left renal artery was cannulated at its origin from the aorta. The renal blood flow was 3.2 =t 0.3 ml/min per g of tissue (mean f SE). The hindlimb was perfused via the left external iliac artery. To eliminate other sources of arterial inflow to the limb, all branches of the terminal aorta, the deep circumflex iliac artery, and the deep caudal epigastric artery were ligated. The left gracilis muscle was isolated from the remainder of the thigh, except for its neurovascular pedicle, and its artery was cannulated. The left paw was perfused via a cannula inserted in the crariial tibia1 artery 3-4 cm above the ankle, and all other arterial branches were tied at this level. Blood flows averaged 12 ml/min in the gracilis muscle and 33 ml/min in the paw. Satisfaclory isolation of the vascular beds studied was indicated by a backflow pressure of 40 mmHg or less when the perfusion lines were occluded. Flow being constant, changes in perfusion pressure reflected changes in vascular resistance in each bed. Renal neurograms. Efferent activity was recorded from multifiber preparations of sympathetic nerves to the left kidney. Through a lateral incision, the renal nerve was dissected retroperitoneally over a length of 2 cm with the use of a dissecting microscope. Fat and connective tissue were removed, the nerve was thinned, and its distal end was crushed. The remaining fibers were placed on a pair of platinum electrodes 3-4 mm apart. The whole preparation was immersed in mineral oil to prevent nerve fibers from drying. The nerve signals were amplified (AC preamplifier P511 and power supply RPS-107, Grass Instrument Co., Quincy, Mass.) and transformed into standard pulses. At the beginning of each experiment, the activity record was inspected to determine the noise level as judged by the background activity during the quiet periods between the bursts of impulses; a discriminator was then set to eliminate the noise from being counted. The impulse frequency was integrated by a rate meter. The response-time characteristics of the equipment permitted counting of signals at intervals of 0.25 ms. Analysis

of Data

Because the tests were repeated in the same dog, the responses to BCO during normoxia and those during hypoxia were averaged separately for each dog, and these averages were used to calculate the mean results for the group. All results were expressed as means f SE. The Student paired t test was used for the statistical analysis of the data. RESULTS

Carotid Sinus Pressure

FIG. 1. Changes in aortic pressure and hindlimb and kidney perfusion pressures (constant-flow perfusion) with bilateral carotid occlusion (indicated by signals at bottom of tracing) during ventilation with room air and 10 (“c 02 in dog with vagosympathetic trunks cut.

In 6 of the 10 dogs referred to below, the changes in carotid sinus pressure with BCO were measured distal to the level of occlusion by a catheter inserted through the external carotid artery. Before occlusion, mean sinus pressure averaged 145 & 7 mmHg during normoxia and

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HYPOXIA

AND

CAROTID

333

BL4ROREFLEX

144 -_t 6 mmHg during hypoxia; mean pulse pressure was 30 and 29 mmHg and mean pulse frequency was 162 and 166/min, respectively. With BCO, carotid sinus pressure decreased to 75 + 3 and 72 & 4 mmHg, respectively, and then stabilized at 114 * 5 and 115 & 8 mmHg after approximately 15 s of occlusion.

c

A

Renal and Hindlimb Resistance Vessels In 10 dogs, the left kidnev and hindlimb were perfused simultaneously. Before BCO, mean aortic pressure was identical during normoxia and hypcxia (147 & 6 mmHg). There was no significant change in the perfusion pressures in response to hypoxia (Fig. 1). With normoxia (mean arterial PO, = 107 mmHg), BCO caused a larger increase in hindlimb perfusion pressure than in kidney perfusion pressure. Th e reverse occurred when BCO was performed during hypoxia (mean arterial PO, = 41 mmHg). The increase in mean aortic pressure averaged 36 mmHg larger with hypoxia and the renal perfusion pressure increased 3 times more than during normoxia; the response in the hindlimb was the same in both conditions (Fig. 2). In five of these dogs, the influence of the carotid chcmoreceptors was eliminated by ligating the occipital arteries at their origin from the external carotid and by dissecting and removing the immediately adjacent tissue; BCO was repeated afterward and two or three tests with hypoxia were performed. Prior to occlusion, all pressures were similar during normoxia (mean arterial PO:! = 117 mmHg) and hypoxia (mean arterial Paz = 38 mmHg). After the chemoreceptors were eliminated, the increases in aortic, renal, and hindlimb pressures caused by BCO during hypoxia did not differ in any of these dogs from those during Carotid

Bodies

Intocf

(IO

Dogs

HINO LIME

AORTA

KIDNEY

/t / /,/

/

)

/

/

//

/t

I /

/

: CPS

P

t

-

CPS

CPS

FIG. 3. Increase in perfusion pressure (perfused at constant flow) in one hindlimb with electrical stimulation of.. lumbar sympathetic chain during normoxia and hypoxia in 3 dogs at different frequencies of stimulation. For comparison, mean response to bilateral carotid occlusion (BCO) in each dog is shown by black triangle. Hypoxia did not affect response to sympathetic stimulation, and maximal perfusion pressure was always higher than that reached with BCO.

normoxia (Figs. 1 and 2). No apparent damage to baroreceptor fibers or loss of reactivity occurred after surgical destruction of the chemoreceptors because the increases in aortic pressure and in hindlimb and renal perfusion pressures with BCO during normoxia were similar to those obtained prior to these manipulations, averaging 63, 61, and 39 mmHg, respectively (Fig. 2). Maximal

Lumbar

Symjdh&

Activation

In three dogs, the left lumbar sympathetic trunk was electrically stimulated at frequencies of 1. O-l 2 cycles/s. Stimulus-response curves were obtained during normoxia and systemic hypoxia, and the maximal increases in hindlimb perfusion pressure were compared to the maximal pressure achieved with BCO in the same dog (Fig. 3). There was no difference in the curves for stimulations performed under normoxic or hypoxic conditions. The maximal perfusion pressures with electrical stimulation were 25, 78, and 59 mmHg higher than the maximal hindlimb perfusion pressure achieved during BCO in each dog.

/

I

1

/

Muscle and Paw Resistance Vessels Carotid

-

Bodies

Excluded

(5

Dogs)

25Or

Con frol

Bile terol Carotid Occlusion

C

BCO

C

EC0

PIG. 2. Effete of bilateral carotid occlusion on mean aortic pressure and hindlimb and kidney perfusion pressures (constant-flow perfusion) during normoxia and hypoxia in dogs with vagosympathetic trunks cut. Note larger responses in aortic and kidney pressures with hypoxia when carotid bodies are intact. After elimination of carotid bodies, responses during normoxia and hypoxia are similar.

In four dogs, the gracilis muscle and the paw were studied simultaneously. Before occlusion, mean aortic pressure averaged 137 s+: 6 mmHg during normoxia (mean arterial Peg = 110 mmHg) and 142 & 7 mmHg during hypoxia (mean arterial Paz = 35 mmHg). Hypoxia did not cause any change in perfusion pressure of the paw but it increased that of the muscle by an average of 9 mmHg (Fig* 4). With systemic hypoxia, the increase in aortic pressure due to BCO averaged 31 mmHg greater than during normoxia ; the increase in muscle perfusion pressure was also significantly greater (1’ < O-05), averaging 19 mmHg more, but the response in the paw did not change significantly+ When computed as percentage of control pressure, the increase in perfusion pressure of the muscle with BCO was only 10% greater during hypoxia than

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C. L. l

Aorta

Normoxio

0 “ypoxre

Grocilis Muscle

Paw

I

100’

I BilOterOl Care tid Occlusion

’ C0ilir0l

/

C

I

I

I

BCO

C

BCO

PELLETIER

AND

J.

T.

SHEPHERD

and short duration was used, and arterial PCO~and pH were maintained normal throughout the experiments. An arterial Paz of 40 mmHg is known to activate the carotid chemoreceptors and cause a reflex vasoconstriction when the carotid bodies are selectively perfused in vagotomized dogs with the activity of the carotid baroreceptors maintained constant (14). In the present experiments, systemic hypoxia did not cause such circulatory changes with the carotid baroreceptors operative, although the POTaveraged 40 mmHg at the time of carotid occlusion. It also has been found by others (3,5), in the dog and the rabbit, that such a degree of systemic hypoxia does not change the limb or muscle vascular resistances. Presumably, this results from

FIG. 4. Effect of bilateral carotid occlusion on mean aortic pressure and gracilis muscle and paw perfusion pressures (constant-flow perfusion) during normoxia and hypoxia in 4 dogs with vagosympathetic trunks cut shown as means f SE.

during normoxia, due perfusion that occurred

to the shift in control with hypoxia.

pressure

of

Renal Nerve Activity In six dogs, the changes in impulse frequency in the renal sympathetic nerve were measured in response to BCO. Before occlusion, mean aortic pressure was 155 rfr: 7 mmHg with normcxia (mean arterial Paz = 100 mmHg) ; after 2 min of hypoxia (mean arterial Paz = 40 mmHg) it was significantly lower (P < 0.05), averaging 142 f 6 mmHg. The average increase in aortic pressure with BCO was 34 mmHg greater in the latter condition. In normoxia, the renal sympathetic nerve displayed almost no activity before occlusion, and only a slight increase in impulse frequency occurred after 2 min of hypoxic ventilation (Fig. 5). During hypoxia, BCO always caused a much larger increase in nerve activity than during normoxia. Upon release of the occlusion, the activity ceased abruptly in the two situations. In order to standardize the results, the mean nerve activity measured during BCO in normoxia was taken as 100% (average, 98 impulses/s). The mean impulse frequency with BCO averaged 56 f 10% greater during hypoxia than during normoxia (Fig. 6).

FIG. 5. Changes in renal sympathetic nerve activity with bilateral carotid occlusion (BCO) in dog with vagosympathetic trunks cut. Note larger increase in mean nerve impulses during hypoxia and complete inhibition on release of occlusion (small burst in standard pulses after BCO in upper panel was artifactual because there was no actual traffic).

, / /0

BCO

Sympathetic Blockade or Denervation In three experiments, ganglionic blockade was obtained by the intravenous infusion of 100 mg of pentolinium tartrate (Ansolysen). In three other dogs, the sympathetic nerves to the kidney and hindlimb were cut. In all these experiments, the responses to BCO were abolished, indicating that they were reflexly induced through the sympathetic nervous system. Con DISCUSSION

Normoxia

This study attempted to determine if the reflex vascular responses to the carotid baroreflex could be modified by systemic hypoxia. Severe asphyxia was avoided to prevent deterioration of the animals and intense stimulation due to cerebral anoxia (6). Rather, hypoxia of moderate degree

irol

Hypoxia

FIG. 6. Effect of bilateral carotid occlusion (BCO) and hypoxia on mean renal nerve activity as percentage of mean activity during BCO in normoxia in 6 dogs with vagosympathetic trunks cut shown as means i SE. Hypoxia caused slight increase in activity in control situations, and much larger increase in activity was seen with BCO during hypoxia than during normoxia.

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HYPOXIA

AND

CAROTID

335

BAROREFLEX

the interaction of a number of excitatory and inhibitory effects of the hypoxia. With the hypoxia, there was no significant difference in mean aortic pressure, pulse pressure, and pulse frequency before the occlusion, as compared to normoxia, in 14 of the 20 animals studied. Likewise, the changes in carotid sinus pressure during occlusion were similar to those in normoxic conditions. However, in the six dogs in which renal sympathetic nerve activity was determined, there was a small but significant decrease in mean aortic pressure (from 155 + 7 to 142 + 6 mmHg) when the animals were made hypoxic. Our results demonstrate that moderate hypoxia markedly increases the reflex response of the kidney to the baroreflex, while that of the extremity is unchanged. When the two major components of the extremity were separately investigated, it was found that hypoxia did not affect the reflex responses of the cutaneous resistance vessels and increased only slightly those of the muscle vessels. Because of the shift in control perfusion pressure of the latter during hypoxia, it is not possible to determine whether the 10 % increase in the response was due to increased neurogenic activity or to the change in vessel wall tension consequent to hypcxia. At any rate, the difference in the response is at most modest and would support the results obtained with the perfusion of the whole hindlimbthat the response of this vascular bed to the baroreflex is affected little or not at all by hypoxia. The local effect of the lack of oxygen on the vascular smooth muscle of the limb could not have prevented the increase in the constrictor response because the vascular responses to electrical stimulation of the lumbar chain were similar during normoxia and sympathetic hypoxia. With electrical stimulation, the hindlimb perfusion pressure could be increased by 25-78 mmHg above that achieved by carotid occlusion, indicating that further vasoconstriction was possible. In contrast, the constrictor response of the kidney to carotid occlusion was markedIy potentiated by systemic hypoxia, increasing by approximately threefold. This increase occurred from the same control value as that present during normoxia. The increase in sympathetic nerve activity to the kidney caused by carotid occlusion was also markedly enhanced during hypoxia, confirming that the potentiation of the response was neurogenic. On release of bilateral carotid occlusion, the sympathetic nerve activity decreased abruptly to zero, both during normoxia and hypoxia. This suggests that the effect of hypoxia was mediated through the same pool of central neurons as those affected by the carotid baroreceptors. The SYStemi C hyper tension resulti ng from the carotid than during occlusi ons was aIways greater with hypoxia normoxia (by 3 1-36 mmHg). ITt has been shown that the cardiac output is little affected by the carotid baroreflex (4). Thus, the hypertension would be due mostly to changes

in peripheral resistance, and the larger response during hypoxia could reflect the enhancement of the renal vasoconstriction; however, it is possible that other vascular beds behave similarly to the kidney. Elimination of the carotid chemoreceptors did not affect the reflex resp onses to carotid occlusion during normoxi a, indicating that this procedure caused no apparent damage to the baroreceptor fibers and that the carotid chemoreceptors did not contribute to the reflex response to bilateral carotid occlusion. During hypoxia the potentiation of the renal and aortic pressure responses to carotid occlusion was abolished. Our experiments do not remove the possibility that oxygen deprivation might affect directly the cerebral or spinal neurons to alter their level of spontaneous activity, as suggested by other authors (1, 6), but, at the level of hypoxia used in the present stud y, such a central action bodies did not seem to occur, because after the carotid were destroyed a 11 the hemodyna mic changes in response to bilateral caroti d occlusion were similar during normoxia and hypoxia. Thus, the potentiation of the renal responses to the carotid baroreflex would appear to be due to the carotid chemoreceptors. Similarly, Gellhorn et al. (7) have shown that the blood pressure increase in response to hypothalamic stimulation w ‘as greater with anoxia and that this was due to the afferent ac tivity from the sinoa ortic chemoreceptors. Our results support the hypothesis that the intrinsic level of activity of the neurons governing the renal circulation is normally low (9, 11). Stimulation of the carotid chemoreceptors would result in an increase in activity that would not become manifest until these neurons were released from the restraint exerted by the carotid baroreceptors. When the latter occurs, there is a much larger increase in sympathetic outflow to the kidney than there is in the absence of chemoreceptor stimulation. This would also account for Korner’s findings (10) that, in arterial hypoxia, the increase in renal resistance is evoked through the combination of chemoreceptor and baroreceptor input, while sustained renal vasoconstriction cannot be obtained from the latter alone. Hypothalamic stimulation (2, 15), stimulation of afferent fibers from somatic muscles (8), CO2 (13), or acidosis (9) would exert a similar excitatory action on this neuron pool. In contrast, the neurons controlling the resistance vessels of the extremities appear to discharge at a near-maximal level when released from the inhibitory effect of the baroreceptors, and little further increase would be expected by addition of another excitatory afferent input. The authors Mrs. Joan This investigation 5883 from the and by a grant and

Received

for

thank Mr. Gary F. Burton, Mr. Robert R. Lorenz, Y. Troxell for their assistance. was supported in part by Research Grant HLNational Institutes of Health, Public Health Service, from the hledical Research Council of Canada.

publication

18 March

1974.

REFERENCES 1. ALEXANDER, R. S. The effects of blood flow and anoxia on spinal cardiovascular centers. Am. J. Physiol. 143: 698-708, 1945. 2. BAGSHAW, FL J., M. LIZWKA, AND L. H. PETERSON. Effect of interaction of the hypothalamus and the carotid sinus mechanoreceptor system on renal helnodynamics in the anesthetized dog. Circulation Hes. 29 : 569-585, 1971. 3, CHALMERS, J. P., P. I. KORNER, AND S. W. WHITE. The control

of the circulation in skeletal muscle during arterial hypoxia in the rabbit b J. physiol., London 184: 698-716, 1966. 4. CORCONDILAS, A., D. E. DONALD, AND J. T. SHEPHERD. Assessment by two independent methods of the role of cardiac output in the pressor response to carotid occlusion. J. Physiol., London 170: 250-262, 1964. Ei. DAUGHERTY, R. hf., JR., J. B. Scocq AND F. J. HADDY. Effect

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of generalized hypoxemia and hypercapnia on forelimb vascular resistance. Am. J. Physiol. 213 : 111 l-l 114, 1967. 6. FOLKOW, B., B, JOHANSSON, AND B. L~FVING. Aspects of functional differentiation of the sympatho-adrenergic control of the cardiovascular system. Med. &+. 4 : 32 1-328, 1961. 7. GELLHORN, E., R. CORTELL, AND H. B. CARLSON. Fundamental differences in the excitability of somatic and autonomic centers in response to anoxia, Am. J. Physiol. 135 : 641..-649, 1942. 8. JOHANSSON, B. Circulatory responses to stimulation of somatic afferents: with special reference to depressor effects from muscle nerves. Acta Phy~iol. &and. 57, Suppl. 198 : l-91, 1962. 9. KENDRICK, E., B. ~BERG, AND G. WENNERGREN. Vasoconstrictor fibre discharge to skeletal muscle, kidney, intestine and skin at varying Physiol. 10.

KORNER,

levels &and. P. I.

of arterial 85 : 464-476, Central

baroreceptor 1972. nervous

control

activity of autonomic

in

the

cat. function-

Acta

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PELLETIER

AND

J+ T.

possible tion Res.

11.

12.

13.

14.

15.

SIIEPHERD

implications in the pathogenesis of hypertension. Cz’rculu27, Suppl. 2 : 159-168, 1970. L~FVING, B. Cardiovascular adjustments induced from the rostra1 cingulate gyrus: with special reference to sympatho-inhibitory mechanisms. Acta Physiol. &and. 53, Suppl. 184 : l-82, 1961. OTT, N. T., R. R. LORENZ, AND J. T. SHEPHERD. Modification of lung-inflation reflex in rabbits by hypercapnia. Am. J. Physiol. 223: 812-819, 1972. OTT, N. T., AND J. T. SHEPHERD. Modifications of the aortic and vagal depressor reflexes by hypercapnia in the rabbit. Circulation Res. 33: 160-165, 1973, PEILLETIER, C. L. Circulatory responses to graded stimulation of the carotid chemoreceptors in the dog. Circulation Res. 3 1: 431443, 1972. WILSON, h/T. F., I. NINOMIYA, G. N. FRANZ, AND W. V. JUDY. Hypothalamic stimulation and baroreceptor reflex interaction on renal nerve activity. Am. J. Physiol. 221 : 1768-1773, 1971.

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Effect of hypoxia on vascular responses to the carotid baroreflex.

The effect of systemic hypoxia on the vascular responses to the carotid baroreflex was studied in anesthetized, vagotomized, artificially ventilated d...
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