CENTRAL BLOOD PRESSURE AND HEART OUTPUT IN SURFACED AND SUBMERGED FROGS

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1 J. Exp. Btol. (965), 42, Wth text-fgura Prnted n Great Brtan CENTRAL BLOOD PRESSURE AND HEART OUTPUT IN SURFACED AND SUBMERGED FROGS BY G. SHELTON* AND D. R. JONES* Department of Zoology, The Unversty, (Receved 4 August 964) Southampton INTRODUCTION Those anmals whch have an ncompletely dvded double crculaton have, for obvous reasons, occuped a domnant role n dscussons of the phylogeny of vertebrate crculatory systems. The poston of the present-day amphbans, ether as representatve of an early stage n the progressve separaton of two sdes of the heart or as a specalzed offshoot from ancestors wth more effectvely dvded systems, s n some doubt (Foxon, 955). Detals of the movement of blood through the amphban heart and arteral arches must be central to the dscusson as the only drect evdence to be adduced on the status of the undvded ventrcle. A great deal has been wrtten on ths subject and all workers n recent years are agreed that the classcal theory of the separaton of blood streams (Sabater, 873) s totally unsupported by expermental evdence. In spte of ths unanmty t s stll not clear whether there s ndscrmnate mxng of blood from the rght and left aurcles (Foxon, 95) or some degree of separaton of blood from the body and lung crcuts as t passes through the heart. De Graaf (957), workng on Xenopus, found a rather odd dvson wth the lung crcut carryng most of the ventrcular output. At each ventrcular systole the pulmocutaneous arch receved all of the blood comng to the heart from the body together wth much of that comng from the lungs. Smons (959) also clamed that n anurans some separaton of blood from the two sdes of the heart could be seen n the arteral arches, whereas n urodeles complete mxng occurred n the snus. Recently, Johansen (963), on the bass of X-ray photography and determnatons of oxygen concentraton n the arteral arches, decded that n Amphuma separaton of the vsceral and pulmonary blood can occur under certan crcumstances, but that t s not a permanent feature of the crculaton. Snce many Amphba can lve for long perods under water as well as n ar, they must obvously be able to undertake gross changes n the balance of ther respratory mechansms. It s unsatsfactory to regard the crculatory system as beng stable durng these changes, ndeed a pronounced dvng bradycarda has already been descrbed (Jones & Shelton, 964). It seems certan that the soluton to the problem of functon n the amphban heart must be sought n both the submerged and surfaced anmal. In the work whch has been done so far on blood dstrbuton the possblty of alteratons adaptve to dfferent envronmental condtons has not been examned. Although the effect of submerson on amphban crculaton s largely unknown, * Present address: School of Bologcal Scences, Unversty of East Angla, Wlberforce Road, Norwch, NOR 77H.

2 340 G. SHELTON AND D. R. JONES ths s not the case for the less well adapted, dvng vertebrates. Dvng s known to cause bradycarda n brds and mammals wthout, however, gvng rse to much change n the arteral pressures measured centrally (Irvng, Scholander & Grnnell, 942; Johansen & Aakhus, 963). Ths s nterpreted as beng due to vasoconstrcton n certan parts of the perphery such as the skn, vscera and muscles, thus maltng more blood and oxygen avalable to other restrcted areas, notably the bran and heart. In the allgator a smlar perpheral vasoconstrcton s thought to occur and accounts for the ncrease n blood pressure durng the early stages of the dve (Andersen, 96). Later the pressure falls substantally suggestng that blood flow s reduced n all regons. Varatons clearly exst n the crculatory responses shown to dvng by dfferent anmals. The need to mantan adequate skn crculaton for gas exchange at the body surface, and the fact that the lung crcut need not carry the same flow of blood as the body (as t must n completely dvded systems) lead one to expect that the Amphba wll also dffer n some respects from those cases already examned. METHODS The majorty of the experments were done on Rana ppens, the Amercan grass frog, but because of supply dffcultes R. temporara was also used. The only experments n whch one speces {R. temporard) was used exclusvely were those of ' smultaneous' pressure measurement. In all other cases both speces were used and no qualtatve dfference could be seen between them. There are some slght quanttatve dfferences n the behavour of the heart when anmals of the two speces are submerged (Jones, n preparaton), but these are of no sgnfcance to the results descrbed n ths paper. The text refers to the work done on R. ppens except where t s otherwse stated. The frogs were stored, and the experments were carred out, at room temperature (20 0 C.) n the wnter and early sprng of one year. No obvous dfferences n actvty of the anmals could be seen over ths perod. Before an experment the frog was deeply anaesthetzed n Sandoz MS 222 soluton (300 mg./l.) untl the breathng movements had just ceased. The clavcle and coracod were cut through near ther ventral ends and a small part of the sternum was removed. Ths allowed the conus and the roots of the arteral arches to be exposed. The anmal wth ts ventral sde uppermost was then clamped by the four lmbs to a wax block and allowed to recover to a lghtly anaesthetzed state n whch the breathng was normal. The frog was kept n ths stage of anaesthesa by perodcally mostenng the skn wth MS 222 soluton throughout the experment. The wax block was located n a Perspex tank nto whch water could be run from a reservor. To submerge the anmal water was run n to the level of the buccal cavty floor, takng care that t dd not flow over nto the body cavty. The blood pressures were measured by capactance manometers of the type desgned by Hansen (949) and manufactured by Ole Dch (Type ATH, new model). They were connected to the artery by means of a short pece of copper tube, and n the majorty of cases, a no. 20 hypodermc needle. In some cases no. 5 needles were used, but the experments were all repeated later usng the fner needles. No dfference was seen n the results. The manometers were held n manpulators and the needles were nserted nto the pulmocutaneous and systemc arches about or 2 mm. beyond

3 Blood pressure and heart output n frogs 34 the pont of ther orgn, the openngs n the needles pontng downstream. To prevent clots formng n the needles they were coated wth slcone, the anmal was njected wth heparn (2*5.u. heparn per 0 g. weght), and the manometers were flled wth 5 % sodum ctrate. In some later experments the anmals were not njected and the manometers were flled wth salne contanng 0.u. heparn per ml. On the whole ths latter method was more effectve but, after the ntal experments, very lttle trouble was experenced wth ether method even over extensve recordng perods. The two manometers were tested by applyng a sudden pressure change to the end of the needle. Wth a no. 20 needle on the slower of the two manometers, the whole equpment,.e. manometer, capactance detecton unt, amplfer and pen recorder, followed a sudden release of pressure wth a tme constant of 3-5 msec. The most rapd pressure change recorded (the begnnng of the pulmocutaneous pulse) was some fve tmes slower than the nstrument's response to a square wave pressure change of smlar dmensons. The electrocardogram (e.c.g.) was detected by a wre located just under the skn close to the regon of the ventrcle. The sgnal was amplfed n conventonal amplfers and dsplayed on the pen recorder. Heart output was measured by means of a cardometer. A Perspex cup was made to accommodate the ventrcle and the open top of the cup was sealed by a thn rubber membrane wth a hole through whch the ventrcle was pushed. The sze of the hole was very mportant and a fresh membrane was prepared for each experment. The cup was connected drectly to the tube of a ml. tuberculn syrnge arranged horzontally. Volume change n the salne-flled system was recorded by means of a small metal pston n the syrnge tube connected to a mechano-electrc transducer. The pston was polshed to an easy ft n the tube. The whole movng assembly weghed rg. and moved through a maxmum of 8mm. In addton the heart had to move about ml. of salne whch flled the apparatus. The nertal and frctonal losses n the cup and tube were thus qute small, though nevtably n ths type of system an extra load was placed on the heart. In the account whch follows 'left* and 'rght' always refer respectvely to the left and rght sdes of the anmal. RESULTS (a) Blood pressures n the systemc arch Typcal values for pressures measured n the systemc arch when the frog was n ar are gven n Table a, and recordngs of the pressure pulse can be seen n Fgs. b and 26. The pressure levels were hgher than those recorded by Smons (957) n R. temporara, and slghtly hgher than those determned by de Graaf (957) n Xenopus. The pulse curve conssted typcally of two parts separated by an nflexon n the fallng phase. Ths has been called the ncsura by Smons (957) who thought t was smlar to that of the mammalan pulse. In the mammal the ncsura s produced by closure of the aortc valves and pressure run-off after ths event s due to elastc recol by the walls of the arteral arch. Standng waves caused by pressure recol from the perphery also produce secondary pulses after the ncsura. In Xenopus de Graaf (957) clamed that the pressure component after the nflexon was due to contracton of the conus arterosus (bulbus cords) and our results on Rana have confrmed ths, though wthout elmnatng the possblty of a small contrbuton due to standng

4 342 G. SHELTON AND D. R. JONES waves. The sze of the second component n the pressure trace was varable but t became more obvous n anmals where, for some reason, there had been apprecable blood loss. Such anmals were not used for further experment but t was notced that n some cases the second wave could become larger than that due to ventrcular contracton, the latter beng qute small because of the blood loss. Clearly ths type of pulse could not be produced by elastc recol; actve contracton of some part of the Table. Blood pressures {mm. Hg) recorded from the arteral arches Systolc Dastolc Pulse Systemc pressures (a) At the surface (6 determnatons from 7 flrnmfln) Average Range (6) After 20 mn. submerson (0 determnatons from 7 nnmfll) Average Range Pulmocutaneous pressures (c) At the surface (3 determnatons from 6 flnman) Average Range (d) After 20 mn. submerson (8 determnatons from 5 anmals) Average Range o 3-* S II-I *8 4-8 I9-8-IO-6 II-O IS system must occur. In the anmals n whch the nflexon was pronounced and the second pressure component very clear t was possble to relate ths component to conus contracton. In normal anmals the delay between the conus deflexon of the e.c.g. and the begnnng of the second pressure wave was greater than that between the QRS (ventrcular) deflexons and the man pulse. There must therefore be a prolonged perod of sometrc contracton n the conus and t s possble that the actve muscle s extended n the early stages by the flow of blood from the ventrcle. These observatons are n accord wth prevously expressed vews on the functon of the conus as a pressure chamber tendng to reduce pulse sze and mantan dastolc pressure (Johansen, 963). Breathng movements dd not have much effect on the pulse or dastolc pressures when the breathng was regular. If the breathng was spasmodc then each burst of movement was followed by an ncrease n pulse pressure. The dastolc pressure was varable under these condtons but dd not consstently rse or fall. When the frogs were submerged the effect on overall systemc blood pressures was surprsngly small (Table 6), even though there was consderable slowng of the heart. In some cases the dastolc pressure hardly changed (Fg. ), although the systolc pressure nvarably fell gradually durng the perod of submerson. In many frogs, however, the effect was more pronounced and both systolc and dastolc pressures fell (Fg. 2) but only when the heart became arrhythmc after farly prolonged submerson was the dastolc pressure reduced apprecably. When the heart contnued to beat rhythmcally t was unusual for changes to be greater than those llustrated n Fe. 2.

5 Blood pressure and heart output n frogs 343 At the begnnng of the submerson perod the systemc pressures ncreased but the rse was never large or prolonged (Fg. 2) and occasonally was not seen. The heart rate frequently went up durng ths ntal perod but the ncreased pressures were mantaned after ths when the heart rate had begun to go down. Snce the systolc pressure fell more than the dastolc durng the perod under water, there was always a change n the pulse pressure (Fgs. a and 2 a). Ths change together wth the altered shape of the pulse curve, was the most obvous effect of Tme (mn ) () () (III) Fg.. (a) Systemc blood pressures and heart rate n R. ppens (29 g.). Downward and upward pontng arrows ndcate submerson and emerson respectvely, x, Heart rate; O, systolc pressure;, dastolc pressure; C, pulse pressure, (b) Pressure pulses recorded at tmes ndcated on graph. Trace, breathng movements from buccal cavty; trace 2, systemc pressure (mm. Hg); trace, 3, electrocardogram; trace 4, tme (sec). submerson. The shape of the pulse can be seen n the supermposed records of Fg. 3 where, n order to compare both the rsng and fallng phases, the same pulses have been supermposed usng (a) the begnnng, and (b) the end of the wave as the pont of concdence. The records have been chosen from experments n whch the dastolc pressures remaned approxmately constant so that the declne n peak systolc and pulse pressures followed the same course. Durng submerson the rate of pressure change went down progressvely but the tme taken for the peak pressure to be developed stayed roughly the same snce the level was fallng. It seems probable that the perod of sometrc contracton before the pressure pulse appeared n the aortc arches was also prolonged. Confrmaton was obtaned by measurng the tme

6 344 G. SHELTON AND D. R. JONES nterval between the R deflexon of the e.c.g. and the begnnng of the pulse wave. Ths gave a measure of the change n duraton of the sometrc contracton, assumng that the tme delay between e.c.g. and actvaton of the muscle and the perod for the pulse to reach the manometer remaned constant. The results are gven n Table 2 and show that submerson dd extend the sometrc contracton tme almost twofold, beyond what mght be expected on the bass of an equal expanson of all events of the cardac cycle as the heart rate decreased. In fact, as Table 2 shows, the tmng of the SO Tme (mln) , Fg. 2. (a) Systemc blood pressures and heart rate n R. ppens (24 g.). Downward and upward pontng arrows ndcate submerson and emerson respectvely, x, Heart rate; O, systolc pressure;, dastolc pressure; C, pulse pressure. (6) Pressure pulses recorded at tmes ndcated on graph. Trace, systemc pressure (mm. Hg); trace a, electrocardogram; trace 3, tune (sec.). man electrcal events of a sngle actvty sequence changed very lttle, the PR nterval ncreasng and the RT decreasng slghtly. In the mammal frst-stage anoxa of the heart muscle causes smlar changes n the e.c.g. relatonshps and a dsplacement of the ST segment whch was also seen n many of the recordngs from the frog. As the

7 Blood pressure and heart output n frogs 345 Anmals on surface (30 determnatons) Anmals submerged for at least 7 mm. (24 determnatons) Table 2. Tme ntervals {seconds) between electrocardogram components and pressure pulse (Average values calculated from data obtaned from three frogs) Cardac cycle length I-O2 6 R wave to pulse pressure PtoR wave RtoT wave TtoP wave Systemc sec ' Fg. 3. Pulses recorded from systemc and pulmocutaneous arches n R. ppens at the surface and after the perods of submerson ndcated. The same pulses are supermposed usng the begnnng and end of the pulse wave as the pont of concdence. heart rate went down the TP nterval (.e. the tme between repolarzaton of the muscle of the ventrcle and the begnnng of the next aurcular contracton) was the factor prncpally affected. In the fallng phase of the pressure pulse several mportant changes were seen. The ventrcular wave became much smaller n relaton to that of the conus and the pressure reversal from rsng to fallng phase more ponted. The nflexon begnnng the conus component moved much nearer to the peak of the dmnshng ventrcular pulse. Fnally there was a very marked decrease n the slope of the whole fallng phase

8 346 G. SHELTON AND D. R. JONES of the pulse as Fg. 3 shows. In general all the changes descrbed above became more marked the longer the frog was kept under water, for perods up to 30 mn. When the anmal was brought to the surface these changes were reversed, the dvng bradycarda dsappearng almost mmedately and the blood pressures recoverng over a varable perod of tme. In those anmals whch began regular breathng soon 40 x ^^ h W t v X x E "3" S 4 5 ^ V n 4Ol () Tme (mn) 40, r H) () (n) t Fg. 4. (a) Pulmocutaneou8 blood pressures and heart rate n R. ppens (23 g.). Downward and upward pontng arrows ndcate submerson and emerson respectvely, x, Heart rate; O, systolc pressure;, dastolc pressure;, pulse pressure, (b) Pressure pulses recorded at tmes ndcated on graph. Trace, pulmocutaneous pressure (mm. Hg); trace 2, electrocardogram; trace 3, tme (sec.). after the head was clear of water the recovery was rapd and complete n 2 or 3 mn, (Fg. ). If the breathng was ntermttent however, the recovery to the orgnal pressure levels took place gradually even though the heart rate was hgh rght from the end of the dve (Fg. 2).

9 Blood pressure and heart output n frogs 347 (b) Blood pressures n the pulmocutaneous arch The pressures measured n the pulmocutaneous arch when the frogs were n ar showed lttle dfference from the systemc pressures n systolc levels but the pulse pressures dffered n magntude (Table c) and to some extent n form. The pulse was nvarably larger than that from the systemc arches by vrtue of the lower dastolc pressures recorded, a dfference smlar to that descrbed by de Graaf (957) n Xenopus. The rate of change of pressure, both n the rsng and fallng phases, was greater n the pulmocutaneous arch. In the steeply fallng phase of the pulse an W Fg. 5. The effect of arrhythmc heart beat, (a) Pulmocutaneous pressure. R. ppens (33 g.). Trace, pressure (mrruhg); trace z, electrocardogram; trace 3, tme (sec.). (6) Stroke volume. R. ppens ( g.). Trace, electrocardogram; trace a, volume (p., up on trace = decrease n volume); trace 3,tme (sec). nflexon assocated wth the begnnng of the conus pressure wave could not be seen clearly (Fg. 4). There was a slght change of slope n the fallng pressure curve but the run-off remaned much more rapd than that found n the systemc arch. When the anmal was submerged the pressures changed n the same way as those measured n the systemc arch. After an ntal rse the systolc pressure decreased more than the dastolc so that there was agan a marked fall n pulse (Fg. 4). It s dffcult to make vald comparson between small dfferences usng pressure records from dfferent anmals, but t seems lkely that the fall, n dastolc pressures partcularly, was less marked n ths arch than t was n the systemc (Table ). In the majorty of experments the dastolc pressures vared very lttle. In Fg. 3 pulses obtaned from the pulmocutaneous arch are supermposed n the same way as for the systemc pulse. Agan they were chosen from a seres n whch the dastolc pressure remaned farly constant and the systolc pressures were at the same level as those of the systemc pulses gven n ths fgure. It can be seen that, as the tme under water ncreased, the pulse changed n shape as before wth the rates of change of pressure decreasng, partcularly durng the fallng phase. A clear nflexon frequently appeared, separatng the ventrcular and conus pressure components, and the peak of the ventrcular wave became more ponted. The run-off after the conus pressure became slower. It was not usually as slow as that seen n the systemc arch

10 348 G. SHELTON AND D. R. JONES even though the dastolc pressure level was on the whole much lower. However, when arrhythma developed and the heart beat nterval was qute long, the slope of the run-off decreased a great deal. The dastolc pressure never declned to zero (Fg. S«). (c) ' Smultaneous'measurement of blood pressures Because of the range n blood pressures whch exsts between dfferent ndvduals some of the dfferences suggested by the experments descrbed n the foregong sectons can only be confrmed by determnaton of pressures smultaneously n sec Fg. 6. Pressures (mm. Hg) recorded from systemc and pulmocutaneous arches n R. temporara (32 g.) and supermposed as explaned n text. The systemc pressure s the top trace n all cases. The calbraton curve and the correspondng curve on the e.c.g. trace show the wrtng radus of the pens and represent the same pont n tme: (a) at surface; (6) submerged mn.; (c) submerged 22 mn.; (d) surfaced 0 mn. sybtemc and pulmocutaneous crcuts. Two manometers were used together n three frogs (R. temporara) connected to the pulmocutaneous and ether the systemc or carotd vessels, the pressures n these latter beng dentcal. Only one capacty detecton unt was avalable and ths had to be swtched between the two manometers. The records obtaned were therefore not smultaneous but, because the e.c.g. was recorded throughout, the successve traces could be supermposed easly and accurately. Changng from one manometer to the other was done wth a swtch so that there was rarely any change n pressure characterstcs and the tmng of events durng the short recordng perods necessary. The dfference between the systemc and pulmocutaneous pulse pressures was confrmed and further ponts of dfference were found (Fg. 6). Although the dastolc pressures n the two arches were very dfferent, the pulse appeared smultaneously n both. Durng the rsng phase the rate of pressure change n the pulmocutaneous

11 Blood pressure and heart output n frogs 349 arch was much greater than n the systemc so that the two pressures approached but never qute reached the same level. The maxmum pressure occurred at the same tme n both arches but the systemc pressure was the hgher by an average -6 mm. Hg (Fg. 6 a, d). The two pressures began to dverge durng the fallng phase and the dvergence became most marked after the nflexon n the systemc pulse. These results were confrmed wth the manometers reversed to elmnate any dfference produced by nstrument characterstcs. Durng submerson of the frogs the same general relatonshps were mantaned. In spte of an ncrease n the length of tme taken for the cardac cycle, the two pulse waves agan appeared smultaneously and the pressure maxma, though lower, were reached together. The systemc pressure also remaned the hgher one, though by a smaller margn durng the later stages of the dve (Fg. 6b, c). The dfferences n the two dastolc pressures became less marked. (d) Heart output Snce the effect of submergence on aortc pressures, partcularly durng dastole, was not usually of the same magntude as the change n heart rate, t must be supposed that some other factors were nvolved n the relatonshp between total output and pressure. One of these factors must be the stroke output of the heart; an ncrease n stroke could obvously offset a decrease n heart rate. Though there has been speculaton about ths parameter n other dvng vertebrates (Elassen, 960; Johansen & Aakhus, 963) drect measurements have not been made. The other factor of major mportance whch can nfluence the relatonshp between overall heart output and aortc pressures s the perpheral resstance. Observaton of the exposed heart suggested that the stroke volume was affected by submerson of the frog though not n the sense suggested above. When the anmal was n ar aurcles and ventrcle empted farly completely at each systole. The left aurcle was more obvous and appeared to be larger than the rght as far as could be seen from the rather restrcted ventral vew. After a perod under water the chambers of the heart dd not empty to the same extent as on the surface, the stroke volume went down, and the heart became much more dstended wth blood. Experments n whch the ventrcle was enclosed n the cardometer have confrmed and extended these observatons on ventrcular volume. The cycle of actvty can be seen n the records of Fgs. 7 and 0. The ventrcular contracton began after the QRS complex of the e.c.g., there beng a short perod of exctaton and sometrc actvty before the volume slowly decreased. At ths moment the pulse appeared n the systemc arch and, rsng steeply, the pressure had ncreased over at least half ts range before the ventrcle began to decrease n volume at all rapdly. By the tme the pulse reached ts maxmum value the ventrcle had pumped out more than half the total stroke volume. The end of the perod of contracton concded roughly wth the T wave of the e.c.g. and the begnnng of the conus component n the pressure record. From ths pont the behavour of the system was somewhat varable. Usually there was a delay durng whch the aurcles flled and then, followng shortly after the P wave, came the perod of ventrcular fllng. In R. ppens, breathng n ar, we have no evdence that the ventrcle was flled other than by aurcular contracton (Fg. yd). In R. temporara, on the other hand, several records suggest that the ventrcle was

12 350 G. SHELTON AND D. R. JONES fllng slowly n the perod before aurcular contracton (Fg. jb ) and n some cases up to half the dastolc volume entered the ventrcle durng ths perod (Fg. jb). These two records were taken at an nterval of 90 mn. and though we cannot account fully for the dfferences t s possble that durng the frst record the anmal had not recovered completely from the operaton to expose the heart and arteral arches. In 20- ~ 5-2- / > <-2Kb 20 n J J N / f] J N f V / ( ) 22- I I 5 26-x.y If j k J f / u r- () () (III) P QRS T 'J. () Fg. 7. Ventrcular volume and systemc blood pressure n: (a) R. ppem (a g.) () at surface, () submerged 6 mn., () submerged II mn.; (b) R. temporara (3 g.) () and () at surface, 90 mn. apart. Trace, electrocardogram; trace, a systemc blood pressure (mm. Hg); trace 3, ventrcular volume ((/*.), n (a) up on trace = decrease n volume, n (b) down on trace = decrease n volume); trace 4, tune (sec.). Curved lnes show wrtng radus of pens and concdent ponts n tme. R. ppens ventrcular fllng before contracton of the aurcles was common durng bradycarda produced by submerson, and was more lkely the lower the heart rate became. It was nvarably seen when the heart beat became arrhythmc (Fg. 56). (I)

13 Blood pressure and heart output n frogs 35 When the frogs were submerged the stroke volume decreased, usually to a greater extent than the reducton n the heart rate. The combnaton of these two factors meant that the volume of blood pumped per mnute by the heart fell to levels between v u 20 E -* o f 5 ^ 5 o o ~ OS 5 - X»_ I " A--A V t m - -m m _ t V ; Ac x! ' VA t ( I t kf T ^ j h X V Kt % X V * * " XT r I < ^ ' *** ;! IL t I t % ', t» V f X! - ^ J.' - 70 "I 40s Tme (mln.) Fg. 8. Stroke volume, mnute volume, and heart rate n R. ppens (2 g.). Downward and upward pontng arrows ndcate submerson and emerson respectvely, x, Heart rate; A, stroke volume;, mnute volume. I I I I, 40 Fg. 9. The effect of surfacng on the total and stroke volume of the ventrcle of R. ppens (2 g.). Trace, electrocardogram; trace 2, stroke volume ((/tl.), up on trace = decrease n volume); trace 3, tme (sec.), mark ndcates emerson. one-half and one-ffth of those found on the surface (Fg. 8). The cardometer readngs showed that as the stroke volume went down the ventrcular volume ncreased not only after systole but also after dastole. Ths fllng took place over a long tme course and the DC level of the cardometer had to be readjusted to make recordng possble. Ths together wth long-term fluctuatons n level n the equpment made measurement 23 Exp. BoL 42, 2

14 0 Tme (mln) 5 20 (0 (II) Fg. o. (a) Heart output, carotd blood pressure and heart rate n R. temporara (35 g.). Downward and upward pontng arrows ndcate submerson and emerson respectvely, x, Heart rate, O, systolc pressure;, dastolc pressure; A, stroke volume;, mnute volume. (6) Pressure pulses (mm. Hg) and stroke volumes ((/*!.), down on trace = decrease n volume) recorded at tmes ndcated on graph.

15 Blood pressure and heart output n frogs 353 of the total volume change mpossble. When the anmal was surfaced recovery from the bradycarda and low stroke volume was rapd as was the decrease n operatng volume of the ventrcle (Fg. 9). The frst few beats of the recovery usually occurred at a slghtly greater ventrcular volume. It was estmated that durng recovery the total decrease n end dastolc volume was 0-5 /^- m tne anmal from whch Fgs. 8 and 9 were obtaned. Fnally, to confrm that the large fall n stroke and mnute volume was not accompaned by an equally large fall n blood pressure, smultaneous measurements were made of ventrcular output and systemc pressures. In both R. ppens and R. temporara these experments demonstrated that consderable change n mnute volume occurred wth lttle or no change n blood pressure. In the experment from whch the records of Fg. 7 a were taken the dastolc pressure n the systemc arch was no lower than the level recorded at the surface though the mnute volume had fallen to one-ffth after 7 mn. under water. A smaller fall n output to one-half the presubmergence level can be seen n Fg. 0, but agan there was very lttle change n the dastolc pressure. The frst few mnutes of ths experment were noteworthy, n that heart rate and stroke volume were both fallng, but systolc and dastolc pressures were rsng. Ths suggests that perpheral vasoconstrcton may be a more rapd reacton to submergence than the response of the heart tself. DISCUSSION Features of the pulse and ventrcular output curves whch have some bearng on the movement of blood through the frog heart are: () The smultaneous appearance of the pulse wave n both systemc and pulmocutaneous arches even though the absolute pressure level s dfferent. (2) The slght dfference n pressure whch s mantaned between the two arches rght through systole, the systemc pressures beng greater. De Graaf (957) found a smlar dfference n Xenopus, but Smons (957) workng on frogs and toads clamed that there was no dfference between the two pressures. Johansen (963), recordng the pressures somewhat more perpherally n Amphuma, found that the systolc values were smlar on both sdes of the crculaton and that no consstent dfference was measurable. (3) When the ventrcular contracton s complete, pressures n the two arches begn to dverge wth the pulmocutaneous pressure reachng the lower dastolc level. Ths pressure pattern was also found by de Graaf (957) and sometmes by Johansen (963). Smons (957) thought that the dastolc pressures were not sgnfcantly dfferent. (4) As most of the recent workers have found, the peak systolc pressure s reached smultaneously n the two arches. (5) In the ar-breathng anmal a marked second pulse, attrbutable to conus contracton, appears n the systemc pressure record. Ths s absent from the pulmocutaneous pressure wave though t appears here after the anmal has been submerged for some tme. It s convenent to thnk of the cycle of actvty as consstng of two dstnct perods, the frst when the pulmocutaneous and systemc crcuts are n contnuty wth the

16 354 G. SHELTON AND D. R. JONES ventrcle, and the second when the valves at the base of the conus are closed. The frst perod begns as the pressure rses smultaneously n both arches and contnues throughout ventrcular contracton. As the output curves show, contracton occurs durng the rsng and ntal fallng phases of the pulse curve and stops at the tme of the nflexon n the systemc curve. Snce the two arches open from the sngle pressure source the slght dfference n recorded pressure durng ths perod wll depend on the product offlow rate and the resstance offered by the length of vessel stuated between the ventrcle and recordng needle. The value of ths product must be greater for the pulmocutaneous arch than for the systemc, though wth the avalable data t s mpossble to say whether flow rate, resstance, or both are the sgnfcant factors. In dssecton that sde of the spral valve whch leads to the pulmocutaneous arch looks small and the openng at the base of the conus s partally occluded by the spral valve tself. Openng the conus obvously has a profound effect on the spatal relatonshps of these structures. The smplest explanaton of the smultaneous pressure rse at the begnnng of the frst perod s that the ventrcle s capable of producng a step-lke pressure change at least untl the tme that blood begns to leave the chamber. There would therefore be no detectable tme nterval between reachng the dastolc levels n the two arches. It s lkely that the pressure rse n the ventrcle s not a step functon and that t becomes even less so after a perod of submergence. The pulses stll appear together and ths lends support to the alternatve suggeston that a valve, perhaps the spral valve tself, shuts off the openng to the pulmocutaneous crcut untl the tme that blood begns to flow nto the systemc chamber. The second perod begns when the ventrcular contracton s completed. Durng ths perod the progressve dvergence of pressures ndcates that the two arches are anatomcally separate not only n the truncus and more perpheral vessels but also n the conus snce blood s known stll to be leavng ths part of the system. The only structure whch can dvde the conus s the spral valve and the mplcaton s that, although t s attached along one of ts sdes only, t s nevertheless capable of sustanng some dfference n pressure n the two chambers leadng to systemc and pulmocutaneous vessels. In the second perod the pressure falls more slowly n the systemc than n the pulmocutaneous arch. De Graaf (957) suggested that n Xenopus ths was due to a smaller perpheral resstance n the lung crcut but ths s not necessarly the case. Snce the propulsve force from the ventrcle plays no part at ths tme, the pressures are mantaned above zero level by the muscular contracton of the conus and elastc recol of extended artery walls. Both of these can be regarded as makng the system complant, though the effect of actve conus contracton s to ntroduce a dscontnuty nto what would otherwse be an exponental fall n pressure due to elastc recol. The slope of the fallng pressure curves wll depend on the combnaton of the complance of the system and the resstance of the perphery to flow. Clearly the perpheral resstance of the lung crcut need not be excessvely low f the complance of the conus and arteral reservor s small on that sde, as may be the case. It s the product of these two factors whch s suffcently small to make the run-off rapd and conus pressure pulse neglgble n the pulmocutaneous arch. Conversely, the complance of the post-ventrcular reservor or the resstance of the perphery or both must be greater on the systemc sde of the crculaton.

17 Blood pressure and heart output n frogs 355 Because evdence as to actual flow rates s lackng t s mpossble to complete the analyss of ths stuaton n a satsfactory manner. As the left aurcle appears to be carryng more blood than the rght we would suggest tentatvely that the resstance offered by the lungs s lower than that of the body crcut. Ths agrees wth de Graaf's (957) conclusons. Even f the resstances of the arteral bases are not apprecably dfferent, the flow rates wll result n the slghtly hgher systolc pressures recorded n the systemc arch. Fnally, observaton of the four major arteres on the body sde of the crculaton suggests a greater complance than n the two vessels to the lungs and ths, together wth the greater perpheral resstance, wll produce the relatvely slow run-off. These conclusons are summarzed dagrammatcally n Fg.. XKAC Systole Dastole Fg.. Dagram to show relatonshps between resstance, complance and flow n the body and lung crcuts whch wll result n the characterstc pulse curves. For further explanaton see text. The adjustments whch are made when the anmal s submerged do not change the overall relatonshp of the two pulse curves to one another. Ventrcular changes, though profound, appear to affect both systems equally. Decreased output n face of ncreasng dastolc volume argues n favour of a consderable fall n contractlty of the cardac muscle snce normally the usual length-tenson relatonshp exsts. There s an accompanyng ncrease n the duraton of sometrc contracton and a gentler slope to the rsng pulse wave. We have carred out no experments to show how these changes are produced though the drect effect of oxygen shortage on the heart muscle may be an mportant factor as we have suggested prevously (Jones & Shelton, 964). As the dastolc pressure vares surprsngly lttle durng submerson t follows that there must be an ncrease n perpheral resstance of both lung and body crcuts of approxmately the same magntude as the fall n heart output. The purely elastc 23-3

18 356 G. SHELTON AND D. R. JONES complance n. the system wll not change durng submerson. It s reasonable to expect that the contractle component of the conus may be affected though the evdence suggests that t s stll very mportant. The complance therefore makes a relatvely larger contrbuton n the submerged anmal where blood output s low and perpheral resstance hgh. Under these crcumstances the pulse s small, the run-off prolonged, and a conus pulse appears n the pulmocutaneoua arch. In all the cases we have examned these changes have been suffcent to overcome the drect effect of bradycarda, whch alone would lead to a larger pulse. The ncreased resstance must be produced by perpheral vasoconstrcton and ths has n fact been seen n the lmb muscles durng submerson. Other regons have not been examned and the work on perpheral blood pressures s stll gong on. The pattern looks very smlar to that descrbed n other vertebrates and t may be expected that the vasoconstrcton s not unform n all parts of the body. In the pulmocutaneous crcut vasoconstrcton and almost complete stoppage of blood flow has been seen n deflated lungs and t s known that the lungs do deflate to some extent when the anmal s submerged. From the functonal pont of vew the reduced blood flow should be conducted largely to the cutaneous artery but ths has not been confrmed. Though the present experments cannot show drectly what s the fate of blood enterng rght and left aurcles they do demonstrate that the conus can be regarded as a dvded vessel durng ventrcular dastole and probably durng systole. The spral valve turns clockwse through somethng more than 80 towards the dstal end of the conus and prevous work (de Graaf, 957; Smons, 959) suggests that t s responsble for conveyng blood from the left sde of the ventrcle to the ventral, carotco-systemc vessel and that from the rght sde to the dorsal, pulmocutaneous one. Durng submerson there appears to be no radcal reorganzaton of ths pattern of blood flow through the heart and arteral arches. The changes whch do occur are due to selectve perpheral vasoconstrcton and a gradual decrease n heart output. The functonal mplcatons of these changes and the mechansms of ther control hold exceptonal nterest but as yet are largely unexplored. SUMMARY. The systemc blood pressure of Rana ppens and R. temporara s slghtly hgher than the pulmocutaneous pressure at systole and much hgher at dastole. The pulses dffer n shape and a conus component can be seen n the systemc wave. 2. Submerson of the anmal causes a fall n systolc pressure n both arches, the dastolc pressure remanng relatvely constant. The shape of the pulse wave changes, the conus component beng accentuated and vsble n recordngs from both arches. 3. Heart rate and stroke volume fall durng submerson so that after 30 mn. under water the mnute volume may be % of the value at the surface. The heart becomes ncreasngly full of blood. 4. The dfferences n systemc and pulmocutaneous pressures are explaned n terms of resstance, complance and flow n lung and body crcuts. The same general relatonshps persst durng submerson but selectve ncreases n perpheral resstance must occur to mantan the central blood pressure n face of fallng heart output.

19 Blood pressure and heart output n frogs 357 We are ndebted to Mr B. H. Vennng of the Department of Electroncs, Southampton Unversty, and Dr R. H. J. Brown of the Department of Zoology, Cambrdge Unversty, for ther generous help wth the manometer electroncs. D. R. J. wshes to thank the Department of Scentfc and Industral Research for fnancal support. REFERENCES ANDERSEN, H. T. (96). Physologcal adjustments to prolonged dvng n the Amercan allgator. Acta pkysol. scand. 53, ELIASSEN, E. (960). Cardovascular responses to submerson asphyxa n avan dvers. Arbok Unv. Bergen. {Mat.-nat. sere), a, -00. FOXON, G. E. H. (95). A radographc study of the passage of blood through the heart of the frog and toad. Proc. Zool. Soc. Lond. la, FOXON, G. E. H. (955). Problems of the double crculaton n vertebrates. Bol. Rev. 30, DE GRAAF, A. R. (957). Investgaton* nto the dstrbuton of blood n the heart and aortc arches of Xenopus taevt. J. Exp. Bol. 34, 43^72. HANSEN, A. T. (949). Pressure measurement n the human organsm. Acta pkysol scand. 9, Suppl. 68. IHVINO, L., SCHOLANDER, P. F. & GRINNELL, S. W. (942). The regulaton of arteral blood pressure n the seal durng dvng. Amer. J. Phystol. 35, JOHANSEN, K. (963). Cardovascular dynamcs n the amphban Amphuma tndactylum. Acta pkysol. scand. 60, Suppl. 27. JOHANSEN, K. & AAKHUS, T. (963). Central cardovascular responses to submerson asphyxa n the duck. Amer.J. Pkysol. 205, JONES, D. R. & SHELTON, G. (964). Factors nfluencng submergence and the heart rate n the frog. J. Exp. Bol. 4, SABATIER, A. (873). Etudes sur le coewr et la crculaton centrale dans la she da Verttbrs. Montpeller et Pans. (Quoted by de Graaf, 957.) SIMONS, J. R. (957). The blood pressure and the pressure pulses n the arteral arches of the frog and the toad. J. Pkysol. 37, 2-2. SIMONS, J. R. (959). The dstrbuton of the blood from the heart n some amphba. Proc. Zool. Soc. Lond. 33,

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