(Pco2 > 65 mmhg). Unilateral section of sympathetic nerves did not change c.b.f. or
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1 J. Phyail. (1984), 347, pp With 3 text-figure8 Printed in Great Britain EFFECTS OF ACTIVATION OF SYMPATHETIC NERVES ON CEREBRAL BLOOD FLOW DURING HYPERCAPNIA IN CATS AND RABBITS BY DAVID W. BUSIJA AND DONALD D. HEISTAD Frm the Cardivascular Divisin, Department f Internal Medicine and Cardivascular Center, University f Iwa Cllege f Medicine, and Veterans Administratin Hspital, Iwa City, IA 52242, U.S.A. (Received 25 January 1983) SUMMARY 1. Effects f unilateral and bilateral activatin f sympathetic nerves n cerebral bld flw (c.b.f.) and cerebrvascular resistance (c.v.r.) during hypercapnia were cmpared in anaesthetized cats and awake rabbits. 2. Sympathetic nerves supplying cerebral vessels were sectined n ne r bth sides in anaesthetized cats and unanaesthetized rabbits. Cerebral bld flw was measured with 15 pm radiactive micrspheres. 3. In cats, c.b.f. was greater than 11 ml/min per 1 g during hypercapnia (Pc2 > 65 mmhg). Unilateral sectin f sympathetic nerves did nt change c.b.f. r c.v.r. but unilateral electrical stimulatin decreased c.b.f. by % and increased c.v.r. by %. Bilateral sectin f sympathetic nerves decreased c.v.r. by % (P < -5, cmpared with unilateral sectin) and electrical stimulatin increased c.v.r. by % (P < -5, cmpared with unilateral stimulatin). 4. In awake rabbits, c.b.f. was greater than 11 ml/min per 1 g during hypercapnia (Pc2 > 5 mmhg). Unilateral sympathetic denervatin did nt change c.v.r. but bilateral denervatin decreased it by % (P < -8, cmpared with unilateral sectin; P < 3, cmpared with intact nerves). 5. Thus, reflex activatin f sympathetic nerves, as well as electrical stimulatin, increases c.v.r. during hypercapnia. In additin, effects f bilateral stimulatin r denervatin f sympathetic nerves are greater than unilateral effects. INTRODUCTION Cerebral vessels are innervated extensively frm sympathetic nerves arising primarily frm the superir cervical ganglia (Nielsn & Owman, 1967; Peerless & Yasargil, 1971). Althugh the distributin f this innervatin is largely ipsilateral, there is verlap in basal and medial areas f the brain (Nielsn & Owman, 1967; Peerless & Yasargil, 1971). The functinal imprtance f bilateral sympathetic innervatin n cerebral bld flw (c.b.f.) and cerebrvascular resistance (c.v.r) has nt been investigated. Bilateral activatin f sympathetic nerves may prduce a greater effect n c.b.f. than unilateral activatin if bilateral innervatin f larger arteries f the circle f Willis is f physilgical imprtance. The purpse f this study was t examine the physilgical imprtance f bilateral 2-2
2 36 D. W. BUSIJA AND D. D. HEISTAD innervatin f the cerebral circulatin. We tested the hypthesis that bilateral activatin f sympathetic nerves wuld reduce c.b.f. r increase c.v.r mre than unilateral activatin. Imprtant features f this study are that we used micrspheres t measure reginal as well as ttal c.b.f. and that we examined effects f bth electrical and reflex activatin f sympathetic nerves n c.b.f. We studied effects f activatin f sympathetic nerves during hypercapnia because effects n c.b.f. are greater under these cnditins than during nrmcapnia (Harper, Deshmukh, Rwman & Jennett, 1972), and sympathetic nerves supplying cerebral vessels are activated by hypercapnia (James, Miller & Purves, 1969; Wei, Knts & Pattersn, 198). METHODS Stimukain f sympathetic nerves in cats Twenty cats (2-s95-2 kg) were used. The cats were anaesthetized initially with ketamine (25 mg/kg I.M.) and aceprmazine (1P5 mg/kg I.M.) and supplemental chlralse-urethane (1:1, i.v.) was given as needed. They were intubated and ventilated with air and supplemental 2- Plyethylene catheters were inserted int a femral artery (fr-measurement f bld pressure and bld sampling), bth brachial arteries (fr withdrawal f reference bld samples), and a femral vein (fr injectin f drugs and fluids). After a left thractmy, a plyethylene catheter was placed int the left atrium fr injectin f micrspheres. Heparin (5 u./kg i.v.) was given fr anticagulatin. Bdy temperature was maintained at TC with a heating pad. These studies were designed t cmpare unilateral and bilateral effects f electrical and physilgical activatin f sympathetic nerves n c.b.f. during hypercapnia in cats. In twelve anaesthetized cats preganglinic fibres supplying ne superir cervical ganglin were sectined and c.b.f. was determined after 14 min f hypercapnia. Hypercapnia was induced by adding CO. t inspired air. Cerebral bld flw als was measured after 1 min f electrical stimulatin f ne superir cervical ganglin (4-1 V, 1 Hz, 4 ins) during hypercapnia (n = 8). In eight ther anaesthetized cats, c.b.f. was measured during hypercapnia (> 1 min duratin) with sympathetic nerves intact, 5 min after bilateral sectin f preganglinic fibres, and after 1 min f bilateral electrical stimulatin fsympathetic nerves (4-1 V, 1 Hz, 4 ms). Arterial bld pressure, ph, Pc, and PO, were determined at the time f each measurement. Sectin f sympathetic nerves in rabbits Furteen rabbits ( kg) were used. Surgery was perfrmed n ne grup 1 day befre experiments (n = 6) and n anther grup n the same day (n = 8). The first grup f rabbits were lightly anaesthetized with sdium thipental (36 mg/kg) administered thrugh an ear vein. Additinal anaesthesia was given as needed. Lcal anaesthesia was infiltrated int skin befre incisins. The superir cervical ganglin n ne side was remved and sham surgery was perfrmed n the ther side. A PE-9 catheter, used fr injectin f micrspheres, was inserted int the left ventricle via a femral artery. In each animal the tip f the catheter was in the left ventricle at the beginning and end f each experiment. Plyethylene catheters were inserted int anther femral artery (fr measurement f arterial bld pressure, bld sampling, and withdrawal f reference bld samples) and a femral vein (fr injectin f heparin). The catheters were exterirized with injectin caps (Becktn-Dickinsn, Rutherfrd, N.J.) placed n the back, and filled with heparin. By inserting tw needles int an injectin cap, arterial bld pressure culd be accurately mnitred during simultaneus withdrawal f a reference bld sample (-5 ml/min). On the day f the experiment a 23 g needle was inserted int an ear artery fr withdrawal f a secnd reference bld sample. The secnd grup f rabbits were anaesthetized as described abve. Catheters were inserted int the left ventricle (via a femral artery) fr injectin f micrspheres, a femral and bth brachial arteries fr measurement f arterial bld pressure, bld sampling and withdrawal f reference bld samples, and a femral vein fr injectin f heparin. The catheters were exterirized and filled with heparin. In additin, the preganglinic nerve bundles supplying bth superir cervical ganglia
3 SYMPATHETIC EFFECTS ON C.B.F. DURING H YPERCAPNIA were carefully expsed, and a lp f 2- surgical silk was placed arund each nerve and tied withut crushing the nerve. The suture was passed under the skin and exterirized thrugh the back. The rabbits were fully awake and respnsive t audible and tactile stimuli fr at least 2 h befre the experiment. On the day f the experiment, rabbits were secured in a restraining device and placed in a chamber (28 x 32 x 48 cm) made f Plexiglas and wd. Hles in the sides f the chamber allwed intrductin f varius gas mixtures. Because rabbits hyperventilated in the chamber under cntrl cnditins, a gas mixture f 3-4 % CO2 in air was intrduced at abut 3-5 I/min in rder t increase arterial Pc, twards nrmal. Heparin (5 u./kg I.v.) was given fr anticagulatin. These studies were designed t cmpare unilateral and bilateral effects f physilgical activatin f sympathetic nerves n c.b.f. during hypercapnia. In the grup with unilateral denervatin, c.b.f. was measured after 9-1 min f hypercapnia. In the grup t have bilateral denervatin, c.b.f. was measured after 12 min f hypercapnia; hypercapnia was maintained and bilateral sectin f sympathetic nerves was perfrmed at 14 min, and c.b.f. was measured 5 min later. Hypercapnia was induced by adding a gas mixture f 7-8% CO2 in air int the chamber at abut 3-5 I/min. Arterial bld pressure and gases were measured at the time f each masurement f c.b.f. Measurement f c.b.f. Micrspheres 15 /an in diameter were injected int the left atrium (in cats) r left ventricle (in rabbits) ver a 1-2 s perid and the injectin line was flushed with 5-7 ml f saline. The number f micrspheres injected each time varied frm 4 t 2-5 millin in cats and 1 t 1-5 millin in rabbits. The nuclides used were 46Sc, 96Nb, 86Sr, '13Sn, 14'Ce and 125I. Withdrawal f reference bld samples began befre micrsphere injectin and cntinued fr 9 s afterwards. After each experiment the animals were killed with intravenus KCI (the rabbits were anaesthetized first) and the brain and cranial muscle remved. The brain was dissected accrding t regin; the tissue was weighed and placed in cunting vials. Brain samples were classified as right and left cerebrum, crtical grey matter (sensry, visual and parietal areas), cerebral white matter (crpus callsum and centrum vale), caudate nucleus, cerebellum and brain stem (thalamus, mid-brain, pns and medulla). Tissues were cunted in a 3-inch well-type gamma cunter. Bld samples were divided int aliquts s that cunting gemetry was similar t tissue samples. The energy windws used were: 46Sc, 8-15 kev; 96Nb, 65-8 kev; "6Sr, 4655 kev; '13Sn, kev; 14'Ce, kev; 126I, kev. Nuclide separatin was perfrmed using differential spectrscpy by standard methds. Cerebral bld flw was calculated frm the equatin: c.b.f. = CB x 1 r.b.f./cr, where c.b.f. is cerebral bld flw in ml/min per 1 g, CB is cunts per gram f brain, r.b.f. is reference bld flw (rate f withdrawal f bld samples frm reference arteries) in ml/min, and CR is ttal cunts-in the reference arterial bld samples. Muscle bld flw was determined in a similar fashin. Cerebrvascular resistance was calculated as mean arterial pressure divided by bld flw t cerebrum. Statitical analy8i8 All bld flw data were analysed using paired t tests (ne-tailed), cmparing bld flw r c.v.r. n the denervated versus intact r stimulated sides, r bld flw r c.v.r. with nerves intact r stimulated and fllwing bilateral denervatin. When sympathetic nerves were intact r cut bilaterally, values fr bld flw t bth sides f the brain were cmbined. Percentage changes in c.b.f. r c.v.r. during unilateral and bilateral sympathetic stimulatin were cmpared using unpaired t tests (ne-tailed). Percentage change was calculated as (nn-stimulated minus stimulated/nn-stimulated) r (intact minus denervated/intact) fr c.b.f. and (intact minus denervated/denervated) fr c.v.r. All data are presented as means+ S.E. f mean. 37
4 38 c) c G) G) Z D. W. BUSIJA AND D. D. HEISTAD C aew r" 2 - ci 4E. e *wq.6 I G v C1 * aq I~ +l V t - 4 4a t + -- II ) Ca Ca.Q a F c +l '11 11 s IIt* CO e *~3-* b V Ca c c +1O B -.-I ^ e~-~,1 aq k cq :: : v OMCMCL V V V V v c-- a4 _- _.- * * * *l c C +1 +l aqls Q it CO ( OC k M V- -S- t l +1 +l t r- u:-c4 * mo P- aq aq $45 v V V V V6 Q.. _L _4 * * * 1-1 '- t * t T--4 --O'- +l H t- N r- 1 " t V I+J+I+I+I+I- _ O -CO O 1 'PO _-es d P:E PM)la". w "~ 5-5- e v~ a +l+l- - Ca +a+1 C Z = Ca II Y - Ca +I +1 + P. IIE
5 S YMPATHETIC EFFECTS ON C.B.F. DURING H YPERCAPNIA 39 RESULTS Anaesthetized cat8 During hypercapnia, c.b.f. increased t mre than 11 ml/min per 1 g. Unilateral electrical stimulatin decreased bld flw t cerebrum (12 ± 3 %), crtical grey matter ( %) and cerebral white matter (14 + 8%), andincreased c.v.r. by 15 ± 4% (Table 1, Fig. 1). Bilateral electrical stimulatin reduced bld flw t cerebrum (3 ± 5 %; P < 15, cmpared with unilateral stimulatin), crtical grey matter 1 8 *t C 'v J1 )(8) L Unilateral Bilateral stimulatin stimulatin Fig. 1. Effects f electrical stimulatin f sympathetic nerves n c.v.r. in anaesthetized cats during hypercapnia. *P < 15 fr the unilateral grup and P < 13 fr the bilateral grup, cmpared with n difference in c.v.r.; tp <-5, cmpared with unilateral stimulatin. Values are mean ±s.e. Sample sizes are in parentheses. (26 ± 8 %; P < -5, cmpared with unilateral stimulatin), cerebral white matter (25 ± 9 %), caudate nucleus (25 ± 8 %) and brain stem ( %; P < 15, cmpared with unilateral stimulatin) (Table 1). In additin, bilateral stimulatin increased c.v.r. by 66 ± 16 % (P < -5, cmpared with unilateral stimulatin) (Table 1, Fig. 1). Electrical stimulatin als decreased cranial muscle bld flw. In cntrast t electrical stimulatin, unilateral sectin f sympathetic nerves did nt change c.b.f. r c.v.r. (Table 2). Hwever, c.v.r. was % higher (Fig. 2) when sympathetic nerves were intact cmpared with bilateral sectin (P < 15, cmpared with unilateral denervatin) (Table 2, Fig. 2). Bth unilateral and bilateral denervatin f sympathetic nerves increased cranial muscle bld flw. Awake rabbit During hypercapnia, c.b.f. increased t greater than 11 ml/min per 1 g. Remval f ne superir cervical ganglin prduced an increase in bld flw t cerebrum (5 ± 2 %) and caudate nucleus (1 ± 3 %); bilateral denervatin increased bld flw t brain stem (17 ± 7 %; P <13, cmpared with unilateral ganglinectmy) (Table 3). Cerebrvascular resistance was 5+ 2 % (n.s.) higher when
6 4 D. W. BUSIJA AND D. D. HEISTAD Vv 4m I I-- Iw V C) s 15 $4 *- r"z 9P + W I-4 1 m I* I_ +1-H -H +1+1 cq (m ( 11r- c _- _- _- * +- +l C)._f c C) 4)._I 4 P 1 -H 6 km W- +1 T- V- en _- 1 T4_- -H +I -H +l+ +1 W4- t- T-4 N CO 1 _- t~- 1~_e4 1 4) I-- ' 1 e4 r. C) Ev c4) p- +1 ;s -H V- 'e4 c O * +l +1+l ++1+l +1 s = aq = 3 m cm aq _F- _F- _- _ c. CO 4+l Ca t*c - v. ce.e ) - ;, d :.2 -a Is $, 4) + k *E 9
7 SYMPATHETIC EFFECTS ON C.B.F. DURING HYPERCAPNIA sympathetic nerves were intact cmpared with unilateral denervatin and 18+8% greater cmpared with bilateral denervatin (P < -8, cmpared with unilateral denervatin; and P < 3, cmpared with intact nerves) (Table 3, Fig. 2). Bth unilateral and bilateral sympathetic denervatin tended t increase cranial muscle bld flw. 41 C -1 Cats Rabbits Unilateral Bilateral Unilateral Bilateral denervatin denervatin denervatin denervatin J- ~~ ~~161 (8) (12) (8) C g-2 C.C * CcJ~~~~~~*. -4 Fig. 2. Effects f sectin f sympathetic nerves n c.v.r. in anaesthetized cats and awake rabbits during hypercapnia. *P < 5 fr anaesthetized cats, and P < -3 fr awake rabbits, cmpared with n difference in c.v.r.; tp < 5 fr anaesthetized cats and P < -8 fr awake rabbits, cmpared with unilateral denervatin. Values are mean + s.e. Sample sizes are in parentheses. DISCUSSION The majr findings f this study are that: (1) electrical and reflex activatin f sympathetic nerves reduces c.b.f. and increases c.v.r. significantly during hypercapnia; and (2) bilateral effects f sympathetic nerves n the cerebral circulatin are much greater than unilateral effects. Althugh electrical stimulatin has larger effects, reflex activatin f sympathetic nerves has ptentially imprtant effects n c.b.f. and c.v.r. during hypercapnia. These findings prvide evidence that sympathetic nerves play a rle in regulatin f the cerebral circulatin during hypercapnia. We have shwn previusly that unilateral electrical stimulatin f sympathetic nerves des nt reduce c.b.f. during nrmcapnia in anaesthetized cats (Heistad, Marcus & Grss, 1978; Busija, Marcus & Heistad, 1982a). Hwever, during hypercapnia, unilateral sympathetic stimulatin reduces c.b.f % and increases c.v.r. by %. This ptentiatin f respnses t sympathetic stimulatin ccurs despite acidsis, which inhibits release f nradrenaline (Puig & Kipekar, 1971; Verhaeghe, Lrenz, McGrath, Shepherd & Vanhutte, 1978) and inhibits respnses f pial arteries t tpical applicatin f nradrenaline (Navari, Wei, Knts & Pattersn, 1978). During nrmcapnia, sympathetic stimulatin causes a 7-12 % decrease in pial artery diameter (Kuschinsky & Wahl, 1975; Wei, Knts & Pattersn, 1975; Busija et al. 1982a) in cats but c.b.f. des nt change (Heistad et al. 1978; Busija et al. 1982a). Results frm ur labratry (Busija et al. 1982a) suggest that althugh diameters f large pial arteries (> 25 /an) decrease during sympathetic stimulatin in cats during nrmcapnia, c.b.f. des nt fall because f a cmpensatry increase in bld
8 42 D. W. BUSIJA AND D. D. HEISIPAD. V I 1V c c bh ~~~~~k e w t- c O X e P ) O - -- _-_ - IO~~1 lcv W O) 9._ c XXe - -~~~i i a) I.II Ca) < ] ** s sd L I+I+I+H +I t s *g O b e cqq--cq ec c q cqcq-s a +l +H +l1+1+1+l +1+l C) tq Q O Z-> _X X ~ ~~-g. CX _~~~~~~~~~ v S *- Oa)
9 S YMPATHETIC EFFECTS ON C.B.F. DURING H YPERCAPNIA velcity whicn may be due t a reductin in dwnstream resistance. This finding supprts the hypthesis (Harper et al. 1972) that pial artery diameter may decrease withut changing c.b.f. if dwnstream, pssibly parenchymal, arteries dilate. During hypercapnia, a cmpensatry fall in dwnstream resistance during sympathetic stimulatin prbably des nt ccur because the vessels are already prfundly dilated. Under these cnditins, stimulatin f sympathetic nerves reduces c.b.f. James et al. (1969) reprted that unilateral reflex activatin f sympathetic nerves during hypercapnia in anaesthetized babns reduced crtical grey matter bld flw by apprximately 6 %. Hwever, a serius limitatin f this study is that c.b.f. was measured with the 133Xe clearance methd, which may be inaccurate when c.b.f. is high and when the cmpartmental analysis is used (Marcus, Bischf & Heistad, 1981). In additin Harper et al. (1972), als using the 133Xe clearance methd but with the mre accurate stchastic analysis, fund that c.v.r. was reduced by 11 % after bilateral sympathetic denervatin during hypercapnia in anaesthetized babns. Recently, Wei et al. (198), using the cranial windw methd, fund that vasdilatatin f large pial arteries during hypercapnia was reduced by intact sympathetic nerves in anaesthetized cats. Assuming that this vascular segment cntributes 25% f the ttal c.v.r. (Knts et al. 1978), the magnitude f this effect n c.v.r. wuld be in agreement with ur findings with bilateral denervatin in cats. We fund that sympathetic nerves cntribute apprximately 2 % t c.v.r. hypercapnia in anaesthetized cats and awake rabbits. The magnitude f this effect suggests that sympathetic nerves play a significant rle in regulatin f the cerebral circulatin during hypercapnia. A new finding frm these experiments is that effects f bilateral activatin f sympathetic nerves n c.b.f. and c.v.r. during hypercapnia are larger than effects f unilateral activatin. If sympathetic nerves frm the superir cervical ganglia supplied nly the ipsilateral hemisphere, sympathetic vascnstrictin wuld affect that hemisphere, and ne wuld nt expect bilateral stimulatin t have greater effects n c.b.f. than unilateral stimulatin. In cats and rabbits, sympathetic innervatin is primarily ipsilateral, except t vessels in basal and medial areas f the brain (Nielsn & Owman, 1967; Peerless & Yasargil, 1971). Functinal characteristics f this verlapping innervatin n c.b.f. have nt been examined systematically befre. There are at least tw pssible explanatins fr ur findings. The first is that differences in effects f unilateral and bilateral stimulatin n c.b.f. are due t differential respnsiveness ftw sets f cerebral resistance vessels - arteries prximal t and including the circle f Willis, and relatively large pial arteries distal t these vessels. Respnses t unilateral stimulatin may reflect primarily respnses f distal cerebral arteries; althugh ipsilateral prximal arteries may cnstrict during stimulatin, unilateral cnstrictin fprximal arteries may be accmpanied by an increase in bld flw thrugh the cntralateral prximal artery, s that reductins in hemispheric bld flw are small (Fig. 3). During bilateral stimulatin, prximal and distal arteries cnstrict n bth sides, s that a cmpensatry increase in prximal artery bld flw cannt ccur. Thus, the respnse t unilateral stimulatin may reflect effects n arteries distal t the circle f Willis, and the respnse t bilateral stimulatin may reflect effects n arteries prximal and distal t the circle f Willis. An alternative pssibility t accunt fr ur findings is that simultaneus activatin 43
10 44 D. W. BUSIJA AND D. D. HEISTAD f sympathetic nerves arising frm the cntralateral side may ptentiate cerebral vascnstrictin during activatin f ipsilateral sympathetic nerves. Effects f unilateral sympathetic stimulatin n c.b.f. during hypercapnia differ in tw majr aspects frm effects during hypertensin. First, the effects f unilateral stimulatin n c.b.f. are much greater during hypertensin (Heistad & Marcus, 1979; Busija, Heistad & Marcus, 198) than during hypercapnia. Acidsis assciated with Middle cerebral artery Superir cervical ganglin; Cartid artery Fig. 3. Schematic diagram f distributin f sympathetic nerves t prximal cerebral arteries (cartid artery and circle f Willis) and distal cerebral arteries (branches f anterir and middle cerebral arteries). hypercapnia prbably attenuates effects f sympathetic stimulatin n the cerebral circulatin (Puig & Kipekar, 1971; Navari et al. 1978; Verhaeghe et al. 1978); in cntrast, several mechanisms appear t ptentiate sympathetic effects during hypertensin (Busija, Sadshima, Marcus & Heistad, 1982b). Secndly, effects f sympathetic stimulatin n distributin f c.b.f. differ during hypercapnia and hypertensin. Sympathetic stimulatin during hypercapnia prduces a hmgeneus effect, as reductins in bld flw t cerebral grey and white matter are similar, while in cntrast, sympathetic stimulatin during hypertensin reduces bld flw much mre in cerebral grey than white matter (Heistad & Marcus, 1979; Busija et al. 198). This difference may be related t the primary site f sympathetic effects n the cerebral vasculature. During hypercapnia, sympathetic vascnstrictin f arteries prximal t and including the circle f Willis wuld be expected t reduce c.b.f. t the same degree in all areas served by these vessels. Hwever, during hypertensin, sympathetic vascnstrictin f arteries distal t the circle f Willis culd attenuate increases in bld flw t sme areas f the brain mre than thers. In additin, the primarily unilateral cerebral vascnstrictin prduced by sympathetic nerves during hypertensin prbably reflects majr respnses distal t the circle f Willis. In summary, electrical and physilgical activatin fsympathetic nerves decreases c.b.f. and increases c.v.r. during hypercapnia. These effects are greater with bilateral sympathetic activatin. The magnitude f the respnses indicates that sympathetic nerves play a rle in regulatin f the cerebral circulatin during hypercapnia. We thank Dnald Piegrs, Peter Prestn and Lri Panther fr technical assistance, and Anne Brwn and SuzAnne Ralph fr typing the manuscript. Supprted by New Investigatr Research Award HL-28932, Research Grant HL-326, Research Grant HL-1666 and Prgram Prject Grant HL frm the Natinal Heart, Lung and bld Institute, and by a Medical Investigatrship and Research Grant frm the Veterans Administratin.
11 SYMPATHETIC EFFECTS ON C.B.F. DURING HYPERCAPNIA 45 REFERENCES BuSIJA, D. W., HEISTAD, D. D. & MARCUS, M. L. (198). Effects f sympathetic nerves n cerebral vessels during acute, mderate increases in arterial pressure in dgs and cats. Circulatin Re8. 46, BUSIJA, D. W., MARcus, M. L. & HEISTAD, D. D. (1982a). Pial artery diameter and bld flw velcity during sympathetic stimulatin in cats. J. Cerebral Bld Flw Metab. 2, BUSIJA, D. W., SADOSHIMA, S., MARCUS, M. L. & HEISTAD, D. D. (1982b). Functinal significance f sympathetic innervatin f cerebral vessels. Can the issue nw be reslved? In Trend8 in Autnmic Pharmaclgy, vl. II, ed. KALSNER, S., pp Baltimre, Urban & Schwarzenberg. HARPER, A. M., DESHMUKH, V. D., ROWMAN, J.. & JENNETT, W. B. (1972). The influence f sympathetic nervus activity n cerebral bld flw. Arch. Neurl. 27, 1-6. HEISTAD, D. D. & MARCUS, M. L. (1979). Effects f sympathetic stimulatin n permeability f the bld-brain barrier t albumin during acute hypertensin in cats. Circulatin Re8. 45, HEISTAD, D. D., MARCUS, M. L. & GROSS, P. M. (1978). Effects f sympathetic nerves n cerebral vessels in dg, cat, and mnkey. Am. J. Phy8il. 235, H544-H552. JAMES, I. M., MILLER, R. A. & PURVES, M. J. (1969). Observatins n the extrinsic neural cntrl f cerebral bld flw in the babn. Circulatin Re8. 25, KONTOS, H. A., WEI, E. P., NAVARI, R. M., LEVASSEUR, J. E., ROSENBLUM, W. I. & PATTERSON, J. L., JR (1978). Respnses f cerebral arteries and arteriles t acute hyptensin and hypertensin. Am. J. Physil. 3, H371-H383. KUCHINSKY, W. & WAHL, M. (1975). Alpha-receptr stimulatin by endgenus and exgenus nrepinephrine and blckade by phentlamine in pial arteries f cats. Circulatin Re8. 37, MARCUS, M. L., BISCHOF, C. J. & HEISTAD, D. D. (1981). Cmparisn f micrsphere and xenn clearance methd in measuring skeletal muscle and cerebral bld flw. Circulatin Res. 48, NAVARI, R., WEI, E. P., KONTOS, H. A. & PATTERSON, J. L., JR (1978). Cmparisn f the pen skull and cranial windw preparatins in the study f the cerebral micrcirculatin. Micrvascular Re8. 16, NIELSON, K. C. & OWMAN, CH. (1967). Adrenergic innervatin f pial arteries related t the circle f Willis in the cat. Brain Res. 6, PEERLESS, S. J. & YASARGIL, M. G. (1971). Adrenergic innervatin f the cerebral bld vessels in the rabbit. J. Neursurg. 35, PUIG, M. & KIPEKAR, S. M. (1971). Inhibitry effect f lw ph n nrepinephrine release. J. Pharmac. exp. Ther. 176, VERHAEGHE, R. H., LORENZ, R. R., MCGRATH, M. A., SHEPHERD, J. T. & VANHOUTTE, P. M. (1978). Metablic mdulatin f neurtransmitter release - adensine, adenine nucletides, ptassium, hypersmlarity and hydrgen in. Fedn Prc. 37, WEI, E. P., KONTOS, H. A. & PATTERSON, J. L., JR (1975). Determinants f respnse t pial arteries t nrepinephrine and sympathetic nerve stimulatin. Strke 6, WEI, E. P., KONTOS, H. A. & PATTERSON, J. L., JR (198). Dependence f pial arterilar respnse t hypercapnia n vessel size. Am. J. Physil. 283, H697-H73.
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