CARDIORESPIRATORY RESPONSE TO PROGRESSIVE HYPOXIA AND HYPERCAPNIA IN THE TURTLE TRACHEMYS SCRIPTA
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1 The Journl of Experimentl iology 22, (1999) Printed in Gret ritin The Compny of iologists Limited 1999 JE CRDIORESPIRTORY RESPONSE TO PROGRESSIVE HYPOXI ND HYPERCPNI IN THE TURTLE TRCHEMYS SCRIPT JY K. HERMN* ND NEL J. SMTRESK Deprtment of iology, University of Texs t rlington, rlington, TX 7619, US *Present ddress: Deprtment of Comprtive iosienes, 2 Linden Drive West, University of Wisonsin-Mdison, Mdison, WI 5376, US (e-mil: HermnJ@svm.vetmed.wis.edu) epted 7 Septemer; pulished on WWW 28 Otoer 1999 The ventiltory responses of helonin reptiles to hypoxi nd hyperpni stress hve een firly well desried. s turtles re ple of lrge rdi shunts, hnges in pulmonry perfusion my e n eqully vile nd potent response to these stressors. To test this hypothesis, onsious unrestrined turtles were unidiretionlly ventilted while lood flow in the left pulmonry rtery (Q. LP) nd left orti rh (Q. Lo) ws monitored. Turtles were exposed to step hnges (2.5 h step 1 ) in O 2 tension (3,, 5, 2.5 or % O 2 ; CO 2 inflow mintined onstnt) on dy 1 followed y step hnges in CO 2 tension (, 2, 4, 8 % CO 2 ; O 2 inflow mintined onstnt) on dy 2. Stedy-stte rdiorespirtory vriles were reorded for the lst 3 min of eh step hnge in gs tension. Progressive hypoxi resulted in progressive inreses in Summry ventiltion, Q. LP nd Q. Lo nd smll, ut non-signifint, inrese in hert rte. Progressive hyperpni resulted in progressive inrese in ventiltion, while Q. LP nd Q. Lo did not hnge t ny level of CO 2. These results suggest tht informtion from the O 2 -sensitive hemoreeptors ppers to e stimultory to oth the rdiovsulr nd ventiltory ontrol systems, while CO 2 hemoreeption ppers to ffet primrily the ventiltory ontrol system. These results lso suggest tht, in nimls ple of intrrdi shunting, inresing pulmonry perfusion my e n integrl omponent of the reflex response to hypoxi. Key words: lood flow, ventiltion, reptile, noxi, hypoxi, hyperpni, turtle, Trhemys sript. Introdution Semi-quti turtles re diving nimls tht exhiit n episodi rething pttern similr to tht of mny other tetrpod lower vertertes (see Shelton nd outilier, 1982; Milsom, 1991; Glss, 1992). This rething pttern ppers to e n inherent omponent of the entrl respirtory rhythm genertors, ut its output my e dynmilly ltered y vrious fferent stimuli (Douse nd Mithell, 199). The ues tht modify this respirtory pttern hve intrigued omprtive respirtory physiologists for mny yers nd, s suh, the ventiltory responses to ltered lood gs tensions re well doumented (Frnkel et l., 1969; Jkson, 1973; Hitzig nd Jkson, 1978; Silver nd Jkson, 1985; West et l., 1989). Lowered lood oxygen tensions hve een demonstrted to indue n inrese in minute ventiltion primrily through inresing ventiltory frequeny (deresing the nonventiltory period), with tidl volumes eing progressively inresed s hypoxi eomes more severe (Jkson, 1973; Milsom nd Chn, 1986). These effets re thought to e medited through O 2 -sensitive hemoreeptors loted in the rotid rteries nd in the pulmonry nd orti rhes (Frnkel et l., 1969; enhetrit et l., 1977; Ishii et l., 1985; Kuske et l., 1988). Hyperpni idosis, in ontrst, inreses ventiltion through hnges in oth frequeny nd tidl volume, pprently vi stimultion of oth entrl nd peripherlly loted hemoreeptors (Hitzig nd Jkson, 1978; enhetrit nd Dejours, 198; Milsom nd Jones, 198; Hitzig et l., 1985). During rething episodes, pulmonry lood flow (Q. pul) nd hert rte (fh) inrese to mth lung perfusion with ventiltion (urggren, 1975; Shelton nd urggren, 1976; urggren et l., 1977; Wng nd Hiks, 1996). euse turtles reth episodilly nd use their lungs s potentil O 2 store during non-ventiltory periods, n independent ontrol of pulmonry perfusion would enle finer degree of ontrol over the rte t whih O 2 is extrted from the lungs during these nonventiltory periods. Indeed, evidene exists tht supports this ide, s shown y inreses in rteril P O (nd dereses in lung P O ) during dives in the sene of ventiltion (Shelton nd urggren, 1976; urggren et l., 1989). urggren et l. (1977), using similr protool to tht used in the present study, found tht exposure to hypoxi indued muh lrger hnges in pulmonry perfusion thn in ventiltion nd therefore redued the ventiltion/perfusion (V. /Q. ) rtio, further supporting n independent ontrol of pulmonry perfusion. In
2 326 J. K. HERMN ND N. J. SMTRESK ddition, reent reports hve indited n pprent link etween rteril oxygen ontent (C O ), when ltered either hemilly (Wng et l., 1996) or through redued hemtorit (Wng et l., 1997), nd net rdi shunt, without onomitnt hnges in ventiltion. However, with the pprent exeption of hypoxemi hypoxi, oth ventiltion nd pulmonry perfusion typilly inrese during hypoxi exposure, mking the ontrol of pulmonry perfusion diffiult to resolve from the ontrol of ventiltion (Wng nd Hiks, 1996; Wng et l., 1997). Therefore, the degree to whih the rdiovsulr nd respirtory systems re independent nd ple of eliiting seprte responses remins unler. n independently ontrolled rdiovsulr response my serve to mintin lood gs tensions during non-ventiltory periods or, lterntively, during periods of lowered O 2 -rrying pity (Wng nd Hiks, 1996; Wng et l., 1996, 1997). However, if the reltionship etween ventiltion nd pulmonry perfusion is stritly orreltive, then hyperpni stress should stimulte similr inreses in oth pulmonry perfusion nd ventiltion. The ojetives of this study were therefore to exmine the rdiorespirtory responses to ltered stedy-stte rteril O 2 nd CO 2 tensions. Mterils nd methods nimls Turtles [Trhemys sript (Gry), ody mss kg] were purhsed from Chrles Sullivn Co. (Nshville, Tennessee, US) nd housed in lrge quri with free ess to wter nd terrestril environments. The turtles were kept on 14 h:1 h L:D photoperiod for t lest 2 months prior to experimenttion to ensure helth nd sesonl (long-dy) sttus. Food ws given twie weekly in the form of Trout Chow (Purin) or rikets, ut ws withheld for 5 7 dys prior to experiments. During this time nd throughout the experimentl protool, the turtles were mintined t 25 C. Instrumenttion of turtles The turtles were nesthetized y intrmusulr injetions of Ketmine (14 mg kg 1 ). Following indution of nesthesi, 3m 5 m retngulr hole ws ut into the plstron ove the hert using Dremel tool. Doppler flow trnsduers (Triton Tehnology, Sn Diego, Cliforni, US) were pled round the left pulmonry rtery ( mm i.d.), lose to the ifurtion of the ommon pulmonry rtery, nd round the left orti rh ( mm i.d.). The leds from the flow trnsduers were pssed through n inision ut into the skin t the right dorso-lterl mrgin of the nek nd then through hole drilled into the rnil order of the rpe. The right sulvin rtery ws non-olusively nnulted (strethed PE-5 tuing) y nnulting the right ventrl ervil rtery nd dvning the nnul into the sulvin rtery. One the nnul hd een seured in ple, it ws flushed with heprinized Ringer s solution to ensure pteny nd to prevent lood lotting. The rteril nnul ws led out through the hole in the plstron nd tped into ple. The retngulr piee of the plstron ws seured k into ple using 5 min epoxy resin. To nnulte the lungs, the turtle ws returned to prone position, nd two holes were drilled on eh midpoint of the lterl order of the third dorsl sute. The lung tissue on eh side ws exposed, the underlying lung hmer ws nnulted (PE-25) nd the nnul ws seured into ple using pursestring suture. Prior to plement, the nnule were fitted through hole in ruer serum ork tht ws then seted into the hole in the rpe nd seled with 5 min epoxy resin to ensure n ir-tight sel. The two lung nnule were then onneted vi T-piee with seled end so tht norml lung ventiltion ould our s the nimls reovered. Experimentl protool The turtles were llowed h to reover fter indution of nesthesi to ensure full reovery from surgery nd pteny of flow proes. The turtles were pled into 5 l terrri 3 h prior to the strt of reording. During this time, they were unidiretionlly ventilted with the pproprite initil humidified gs (35 ml min 1 ) using gs-mixing flow meter (Cmeron Instruments). The initil ir mixture ws either hyperoxi (3 % O 2, 3.5 % CO 2, reminder N 2 ) or hypopni ( % O 2, % CO 2, reminder N 2 ), depending on the protool. differentil pressure trnsduer (Vlidyne, Northridge, Cliforni, US) ws tthed vi the side-rm of T-piee to the ir inflow nnule to mesure ventiltion frequeny nd hnges in pulmonry pressure. Lung ventiltion frequeny ws mesured vi hnges in inflow pulmonry pressure. While tidl volumes ould not e ssessed diretly, the pek pressure of tidl movements within out ws used s n index of tidl effort. The position of the differentil pressure trnsduer on the inflow nnul llowed pulmonry pressure to e monitored nd ensured tht the unidiretionl ventiltion did not indue lrge inreses in pulmonry pressure. To lter the lveolr P O (PO ) tension, the lungs were perfused for 2.5 h with 3 %, % (normoxi PO ), 5 %, 2.5 % or % O 2 while holding CO 2 tension t 3.5 % (reminder N 2 in ll ses). The O 2 onentrtions were sequentilly stepped down from 3 % to % to indue progressive delines in PO nd rteril P O (P O ) during the experiments. To indue hnges in CO 2 tension, the lungs were perfused for 2.5 h eh t, 2, 4 nd 8 % CO 2 while holding O 2 tension t % (reminder N 2 in ll ses). Mesurements of responses to CO 2 were mde y sequentilly inresing CO 2 doses euse of the long-lsting effets of id se hnge on lood ion onentrtions (ph returns to the ontrol vlue within 1 h of return to normopni, ut [HCO 3 ] remins elevted for over 48 h; Silver nd Jkson, 1985). The responses of turtles to vrying P O levels were determined first, nd the responses to hnging P CO levels were mesured the following dy. This ensured tht CO 2 -indued idifition did not onfound the P O response urves. rteril lood ws drwn (.5 ml) vi the ventrl ervil nnule during the lst 5 min of eh stedy-stte period in eh ondition to mesure P O, rteril ph (ph) nd totl CO 2 (during the CO 2 protool). Totl CO 2 (T CO ) ws
3 lood flow during hypoxi nd hyperpni 327 mesured on whole-lood smples using infrred sorption (Cpnion V, Cmeron Instruments) on 2 µl smples tken from the drwn lood. The Henderson Hssellh eqution ws used to lulte estimted vlues of P CO nd [HCO 3 ] using pk 1 nd α CO vlues derived in Niol et l. (1983) nd orreted to 25 C. rteril ph nd P O were mesured using ph nd O 2 miroeletrodes (Rdiometer, Copenhgen, Denmrk). fter mesurements hd een mde, the reminder of the lood ws reinjeted into the turtle to prevent nemi resulting from repeted lood smpling. The nnul ws then flushed with heprinized Ringer s solution to mintin pteny. The P O eletrode ws lirted using zero-oxygen solution nd wter equilirted with room ir using mgneti stir r. The ph eletrode ws lirted using stndrd uffers (ph 7. nd 1.). The eletrodes were mintined t the sme temperture (25 C) s the niml during the experiment. Dt nlysis nd sttistil nlysis lood-flow trnsduers were onneted to diretionlpulsed Doppler flow meter (ioengineering, University of Iow, model 545C-4). Signls were onverted to digitl signl using DTQ (model DI 22) /D onversion ord nd reorded t 5 Hz using WINDQ dt-quisition softwre (DTQ Instruments, version 1.13 kron, Ohio, US). Hert rte ws determined from pek-to-pek intervl nlysis of the left orti lood flow. The flow proes were lirted t five different flow rtes y exising the left ort from the niml following experiments nd perfusing this vessel with lood tht hd een previously drwn from the niml. The pressure trnsduer ws lirted using stti wter olumn prior to eh experiment. lood flow ws initilly nlyzed in 1 min ins for the lst 3 min of eh stedy-stte gs tension. Net rdi shunt (Q. shunt, ml min 1 kg 1 ) ws estimted s desried y Wng nd Hiks (1996). In short, the totl pulmonry lood flow (Q. pul) ws estimted y douling the lood flow in the left pulmonry rtery (Q. LP). Totl systemi lood flow (Q. sys) ws estimted y multiplying the lood flow in the left ort (Q. Lo) y 2.8 (the omined lood flow in the right orti rh, sulvin rteries nd rotid rteries is 1.8 times the flow in the left orti rh; Comeu nd Hiks, 1994). The differene etween Q. pul nd Q. sys yields n estimte of the net rdi shunt: negtive vlue would indite net right-to-left shunt (R-L shunt), wheres positive vlue would indite net leftto-right shunt (L-R shunt). To e sttistilly onservtive, lood flows (Q. LP nd Q. Lo), fh, the frequeny of tidl movements (f vent ; reths min 1 ), the frequeny of rething outs (f out ; outs min 1 ), the numer of tidl movements per out (reths out 1 ) nd pek tidl pressure (T P ) were verged over the lst 3 min of eh stedy-stte gs tension. While nlyzing the dt in this mnner msked the norml rdiorespirtory synhrony tht took ple during tive lung ventiltion, it gve etter estimte of the degree to whih the rdiorespirtory vriles hd hnged during the stedy-stte period. repeted-mesures nlysis of vrine (NOV) ws used to nlyze the effets of eh stedy-stte gs tension on lood flow, fh nd rething vriles. Post-ho nlysis using the Student Newmn Keuls (SNK) method ws used where signifine ws indited y the NOV. lestsqures regression nlysis ws used to determine the reltionship etween Q. LP nd f out. ll sttistil tests were performed using Sttisti (SttSoft, version 4.5). The level of signifine ws set t P<.5, nd the dt re presented s mens ±1 S.E.M. Results Crdiorespirtory responses to progressive hypoxi Ten turtles were exposed to progressive step dereses in PO while inflow P CO ws mintined onstnt. Deresing PO signifintly lowered P O (P<.1), while ph did not differ mong the different onditions (Tle 1). Crdiovsulr vriles Hert rte (fh) ppered to inrese slightly with deresing P O, ut this inrese ws not signifint (P=.7, Fig. 1). lood flow in the left orti rh inresed with deresing P O (P<.1, Fig. 1). The progressive deline in P O lso indued signifint inreses in Q. LP (P<.1, Fig. 1C). s the turtles eme progressively hypoxi, the lulted net L- R shunt flow inresed signifintly (P<.5, Fig. 1D). Respirtory vriles Redutions in P O did not lter the tidl frequeny (f vent ) (Fig. 2) ut did inrese the frequeny of rething outs (f out ) t the lowest P O level (P<.1, Fig. 2). Sine f vent did not pper to hnge while f out inresed, the numer of reths per out ws signifintly redued with redued P O (P<.1, Fig. 2C). Pek tidl pressure (T P ) inresed signifintly with deresing P O (P<.1, Fig. 2D). Crdiorespirtory responses to progressive hyperpni Ten turtles were exposed to progressive step inreses in Tle 1. rteril P O2 nd ph during the lst 3 min of stedy-stte periods of ltered lung P O2 tension in the turtle Trhemys sript erted perentge P O2 O 2 (kp) ph ± ± ± ± ± ± ±.6 d 7.677± ±.5 e 7.664±.34 Reovered 11.2± ±.33 ( ) Different letters indite signifint differenes (SNK test; P<.5). Vlues re presented s men ± S.E.M. (N=1). P O2, rteril P O2 ; ph, rteril ph.
4 328 J. K. HERMN ND N. J. SMTRESK Q. LP (ml min -1 kg -1 ) fh (ets min -1 ) C,,, Q. shunt (ml min -1 kg -1 ) Q. Lo (ml min -1 kg -1 ) D,,, Numer of reths per out fvent (reths min -1 ) C,,,, TP (kp) fout (outs min -1 ) D, P O2 (kp) P O2 (kp) Fig. 1. Men vlues of rdiovsulr vriles versus rteril P O (P O ) for the lst 3 min of eh stedy-stte P O period in the turtle Trhemys sript (N=1). () Hert rte (fh). () Left orti rh lood flow (Q. Lo). (C) Left pulmonry rtery lood flow (Q. LP). (D) Clulted net shunt lood flow (Q. shunt). Different letters indite signifint differenes (SNK test; P<.5). Vlues re presented s mens ± S.E.M. PCO while mintining inflow P O onstnt. While there ws no diretionl hnge in P O, there ws signifint differene in P O etween the 2 % nd 8 % CO 2 tretments (P<.5, Tle 2). Inresing the P CO of the unidiretionl gs strem indued signifint derese in ph (P<.1) nd signifint elevtion in T CO (P<.1) nd in estimted P CO (P<.1) nd [HCO 3 ] (P<.1, Tle 2). Crdiovsulr vriles ltering the PCO indued signifint hnges in fh (P<.1) ut not in diretionl mnner (Fig. 3). Q. Lo did not pper to hnge signifintly s the turtles eme inresingly hyperpni, lthough the NOV results were mrginl (P=.53, Fig. 3). Q. LP (Fig. 3C) nd lulted net Q. shunt (Fig. 3D) lso did not hnge with inresing P CO. Respirtory vriles Inresing PCO hd signifint effets on ll the respirtory vriles (Fig. 4 D). Tidl frequeny (f vent ) P O2 (kp) P O2 (kp) Fig. 2. Men vlues of respirtory vriles versus rteril P O (P O ) for the lst 3 min of eh stedy-stte P O period in the turtle Trhemys sript (N=1). () rething frequeny (f vent). () out frequeny (f out). (C) Numer of reths per out. (D) Pek tidl pressure (T P). Different letters indite signifint differenes (SNK test; P<.5). Vlues re presented s mens ± S.E.M. inresed in n lmost liner fshion with progressive hyperpni (P<.1, Fig. 4). out frequeny (f out ) lso inresed with eh suessive inrese in CO 2 level (P<.1, Fig. 4). The numer of reths per out inresed initilly (P<.1) ut then remined unhnged with further inreses in PCO (Fig. 4C). Pek tidl pressure lso inresed in n lmost liner fshion with progressive hyperpni (P<.1, Fig. 4D). Correltion etween respirtory events nd Q LP out frequeny nd Q. LP inresed similrly during hypoxi nd therefore their reltionship ws signifintly orrelted (r 2 =.2285, P<.1, Fig. 5). This orreltive reltionship ws not mintined during hyperpni stress (r 2 =.439, P=.1941, Fig. 5). Comprison etween experimentl dys The rdiorespirtory vriles from the % O 2 level on dy 1 were ompred with the 2 % nd 4 % CO 2 vlues (normoxi/ner-normopni) from dy 2. Hert rte ws
5 lood flow during hypoxi nd hyperpni 329 Tle 2. rteril P O2, ph, T CO2 nd P CO2 during the lst 3 min of eh stedy-stte period of ltered lung P CO2 tension in the turtle Trhemys sript Perentge P O2 T CO2 P CO2 [HCO 3 ] CO 2 (kp) ph (mmol l 1 ) (kp) (mmol l 1) 1.4±.5, 8.423± ± ± ± ± ± ± ± ± ±.5, 7.592± ± ± ± ± ±.49 d 35.25±.41 d 5.43±.53 d 33.62±.55 Different letters indite signifint differenes (SNK test; P<.5). Vlues re presented s men ± S.E.M.; N=1 exept for T CO2, P CO2 nd [HCO 3 ] where N=5). Clultions for P CO2 nd [HCO 3 ] re derived from Niol et l. (1983). P O2, rteril P O2 ; ph, rteril ph; T CO2, totl CO 2; P CO2, rteril P CO Q. LP (ml min -1 kg -1 ) fh (ets min -1 ) C Q. shunt (ml min -1 kg -1 ) Q. Lo (ml min -1 kg -1 ) D Numer of reths per out fvent (reths min -1 ) C TP (kp) fout (outs min -1 ) d D ph ph ph ph Fig. 3. Men vlues of rdiovsulr vriles versus rteril ph (ph) for the lst 3 min of eh stedy-stte P CO period in the turtle Trhemys sript (N=1). () Hert rte (fh). () Left orti rh lood flow (Q. Lo). (C) Left pulmonry rtery lood flow (Q. LP). (D) Clulted net shunt lood flow (Q. shunt). Different letters indite signifint differenes (SNK test; P<.5). Vlues re presented s mens ± S.E.M. slightly elevted on the seond dy of experiments, ut this did not result in signifint elevtions in Q. LP or Q. Lo or in ltertions in net Q. shunt. The respirtory vriles were lso not ffeted y the dy of experiments. The only respirtory Fig. 4. Men vlues of respirtory vriles versus rteril ph (ph) for the lst 3 min of eh stedy-stte P CO period in the turtle Trhemys sript (N=1). () rething frequeny (f vent). () out frequeny (f out). (C) Numer of reths per out. (D) Pek tidl pressure (T P). Different letters indite signifint differenes (SNK test; P<.5). Vlues re presented s mens ± S.E.M. vrile tht differed etween dys ws f out, whih ws slightly lower on dy 1 thn t the 4 % CO 2 level on dy 2. Disussion Progressive hypoxi nd progressive hyperpni were used
6 321 J. K. HERMN ND N. J. SMTRESK Q. LP (ml min -1 kg -1 ) Q. LP (ml min -1 kg -1 ) f out (outs min -1 ) Fig. 5. Stterplots demonstrting the reltionship etween left pulmonry rtery lood flow (Q. LP) nd out frequeny (f out) during () progressive hypoxi nd () progressive hyperpni. During the progressive hypoxi protool, there is signifint orreltion etween Q. LP nd f out. During the progressive hyperpni protool there is no signifint orreltion etween Q. LP nd f out. seprtely in the present study to test the hypothesis tht the ontrol of pulmonry perfusion my e independent of the ontrol of ventiltion in the response to ltered rteril lood gs tension. If the ontrol of pulmonry perfusion is direted y output from respirtory ontrol enters, then hnges in pulmonry perfusion should mth hnges in respirtory output. Therefore, during oth hypoxi nd hyperpni, ventiltion nd pulmonry perfusion should inrese in proportionl mnner. The hypoxi ventiltory response of turtles tends to e firly moderte ompred with their hyperpni ventiltory response (Jkson, 1973; urggren et l., 1977; Hitzig nd Jkson, 1978; Glss nd Wood, 1983). Therefore, pulmonry perfusion should e higher during hyperpni, refleting the higher respirtory drive of hyperpni stimultion. The mjor oservtion of the present study is tht this is not the se nd tht entrl lood flow regultion my e unoupled from ventiltory ontrol during times of hyperpni stress. The gs onentrtions used to hieve normoxi ( % O 2 ) nd normopni (3.5 % CO 2 ) onditions were hosen euse they represent the P O nd P CO levels tht hve een reported in the lungs of turtles during moderte periods of pne (urggren nd Shelton, 1979; Shelton nd outilier, 1982). This perentge CO 2 resulted in P CO nd ph levels tht were omprle with the norml rnge reported in other studies (Frnkel et l., 1969; Jkson et l., 1974). The vlues of 5 % nd 2.5 % O 2 were hosen in n ttempt to enompss the erythroyte P 5 vlue of kp reported for this speies (urggren et l., 1977). The inflow rte of the unidiretionl gs strem ws mintined t 35 ml min 1 to try to ensure onstnt lveolr gs tension. euse turtles hve lrge multimerl lungs (Perry, 1978; Jones nd Milsom, 1982), this flow rte ould e used without generting lrge intrpulmonry pressures (<.98 kp for ll turtles). However, with this type of lung, it is possile tht unidiretionl ventiltion is not s effiient s norml ventiltory movements t equilirting gses within the lung. lso, euse the unidiretionl flows were not orreted for ody mss, lung wshout during unidiretionl ventiltion in lrger nimls my not hve een suffiient to overome the inresed ventiltory movements oserved during the severely hypoxi periods. Therefore, despite the reltively high unidiretionl flow rte used, ventiltory movements y some turtles were still suffiient to elevte the P O ove the expeted vlue. During the noxi unidiretionlly ventilted period, despite n inflow P O of less thn.4 kp, this protool redued P O elow 1.33 kp in only four of the 1 turtles. Ventiltory frequeny nd mplitude inresed with progressive hypoxi, s reported previously for other reptiles (Jkson, 1973; enhetrit et l., 1977; e nd Johnsen, 1987). rething frequeny inresed primrily through derese in the non-ventiltory period, s evident from n inrese in f out rther thn n inresed numer of tidl movements (f vent ). In the present study, the inreses in T P preeded ltertions in ventiltion frequeny, suggesting tht tidl volume hnges my e prt of the initil ventiltory response to hypoxi exposure. Unlike the response reported in erlier studies (i.e. urggren et l., 1977; Wng et l., 1997), fh did not pper to inrese s muh with hypoxi exposure s did Q. LP. The pprent lk of response in the present study is proly due to inter-niml vriility euse the NOV results were mrginl (P=.7). The results of the present study lso differed from those of previous reports (i.e. Wng nd Hiks, 1996; Hiks nd Wng, 1998) in tht net L-R shunt previled during normoxi/normopni onditions. This differene my hve risen, in prt, euse fh nd Q. sys were lower in the present study during these onditions thn vlues reported previously. However, even when fh ws slightly elevted, s during the ner-normopni onditions of the 2 nd 4 % CO 2 protools, the net L-R shunt flow previled in these turtles. Despite these differenes, the reltionship etween Q. pul nd P O is similr to tht reported y urggren et l. (1977) during hypoxi nd to tht reported y Hiks nd Wng (1998) during the trnsition to noxi. Furthermore, progressive hypoxi led to n inrese in the net L-R shunt flow nd, therefore, to lrger proportionl pulmonry stroke volume, response similr to tht reported in previous studies (urggren et l., 1977; West et l., 1992; Hiks nd Wng,
7 lood flow during hypoxi nd hyperpni ). During normoxi ventiltion, hnges in Q. pul pper to e etter orrelted to f out thn to the numer of reths tken within out (Wng nd Hiks, 1996). In the present study, s in the study of Wng et l. (1997), euse oth Q. pul nd f out inresed similrly with deresing levels of P O, the orreltive reltionship etween ventiltion nd pulmonry perfusion ws qulittively mintined. During noxi unidiretionl ventiltion, Q. LP nd fh were mximl. This differs from reent report tht pulmonry lood flow delines nd fh dereses during hroni (>2 h) noxi exposure (Hiks nd Wng, 1998). There re two possile resons for these differenes. Hiks nd Wng (1998) mesured these vriles in sumerged turtles in whih rething ws mesured using n inverted funnel onneted to pneumothogrph. Mny mphiins (Jones nd Milsom, 1982), helonin reptiles (Wng et l., 1997) nd diving mmmls nd irds (see Jones nd Milsom, 1982; Signore nd Jones, 1996) show prsymptheti rdyrdi during sumergene. To test this possile influene on Q. LP, we exposed four turtles to the step hnges in PO while they were sumerged in pproximtely 1 m of wter (dt not shown). The lood flow responses to hypoxi in immersed nd emersed turtles were not signifintly different, suggesting tht P O ppers to e more ritil determinnt of lood flow thn does the immersion/emersion stte of the niml. Reently, Crossley et l. (1998) reported tht, in nesthetized turtles, pulmonry vsulr resistne inreses drmtilly t P O of pproximtely 1.5 kp, level tht is lower thn the men P O hieved in the present study. In the study of Hiks nd Wng (1998), P O in the noxi turtles ws redued to elow.3 kp. In the four turtles from the present study in whih P O ws redued elow 1.3 kp, Q. LP ws redued elow the level mesured t 2.5 % P O, ut not elow tht reorded t the % O 2 level. t this low P O level, fh ws lso irregulr, whih my result from noxi impirment of rdi funtion or from vglly medited derese in rdi output (Jkson, 1987). Thus, the more severe noxi exposure in the study of Hiks nd Wng (1998) proly ounts for the oserved differenes. Tken together, this series of findings suggests tht there my e set point t whih lood flow to the lungs is no longer vile option, so tht shunting lood to the systemi irultion is enhned. This level (<1.5 kp P O ) ppers to e elow the reported P 5 for this speies (urggren et l., 1977; West et l., 1989) nd is nerer to the ritil P O for the mintenne of stndrd metoli rte (see Ultsh nd nderson, 1988). This set point my lso e n importnt determinnt in the unoupling of the rdiorespirtory systems, s demonstrted in Fig. 2 from the study of Hiks nd Wng (1998) in whih the ventiltory movements of this turtle during noxi were not ompnied y hnges in Q. pul. We did not oserve ny turtles exhiiting this ehvior in the present study, ut this my one gin reflet the P O differenes during noxi exposure etween the present study nd tht of Hiks nd Wng (1998). Numerous studies hve shown tht hyperpni exposure indues inreses in helonin ventiltion (Frnkel et l., 1969; Jkson et l., 1974; urggren et l., 1977; Hitzig nd Jkson, 1978; enhetrit nd Dejours, 198; Silver nd Jkson, 1985). The inrese in ventiltion with hyperpni is due to stimultion of oth peripherl nd entrl hemoreeptors in reptiles (Hitzig nd Jkson, 1978; Hitzig et l., 1985). With the levels of CO 2 delivered to the turtles nd the hnges seen in the lood gs vriles, there is little dout tht oth sets of reeptors prtiipted in the hyperpni responses. ssuming tht pulmonry perfusion is orrelted with, nd possily modified y, output from the respirtory enters in turtles, the inrese in respirtory drive nd respirtory output should lso stimulte lrge inreses in Q. LP. This ws not the se in the present study. Indeed, Q. LP did not differ s the nimls were stepped up from severe hypopni ( %) to severe hyperpni (8 %) despite n lmost liner inrese in the ventiltory vriles. Thus, P CO ppers to e potent respirtory stimulnt, ut is unlikely to e involved in rdiovsulr ontrol. Therefore, with this stimulus modlity, the orreltive nture etween f out nd Q. pul ws not mintined. These findings differ from tht reported y urggren et l. (1977). These uthors, using similr protool to the present study, reported tht in n quti turtle, Pelomedus suruf, nd in tortoise, Testudo prdlis, oth hypoxi nd hyperpni inresed pulmonry lood flow. The differene in the hyperpni responses my e due to slight differene in experimentl protool etween the two studies. urggren et l. (1977) exposed the turtles to eh new gs onentrtion until n pprent stedy stte ws rehed in the ventiltion nd lood flow tres; typilly, this ourred within minutes. With this protool, it is oneivle tht lood gs tensions nd id se lne were not yet t stedy stte. Studies y Silver nd Jkson (1985) hve shown tht id se djustments tke over n hour to equilirte when the turtle is exposed to 5.7 % CO 2. Thus, the differenes in the pulmonry lood flow response etween these two studies my hve risen, in prt, from id se equilirtion differenes. However, despite these differenes, the results of the study of urggren et l. (1977) re similr to those of the present study in tht oth demonstrte tht hyperpni ws muh more potent ventiltory thn rdiovsulr stimulus. Furthermore, pulmonry lood flow in the tortoise (urggren et l., 1977) nd in T. sript (present study) inresed more vigorously during hypoxi thn during hyperpni exposure. These similrities further support the hypothesis tht pulmonry perfusion nd ventiltion my e differentilly modified in the response to ltered rteril lood gs tension. The question tht still needs to e ddressed is why lood flow is responsive to O 2 ut not to CO 2. The V. /Q. rtio in turtles tends to e skewed towrds ventiltion when the turtles re rething normoxi nd normopni ir (urggren et l., 1977; Hopkins et l., 1996). This rtio is rought loser to unity in response to hypoxi nd inreses in ody temperture (urggren et l., 1977; Kinney et l., 1977). The lile nture of the V. /Q. rtio is suggestive of two independent yet tightly oupled systems. The present study further demonstrtes this
8 3212 J. K. HERMN ND N. J. SMTRESK tight oupling in tht, with respet to O 2 homeostsis, oth ventiltion nd Q. pul re similrly modified. The min finding of the present study is tht the orreltive nture of the rdiorespirtory output is not oligtory, therey demonstrting tht the two systems re independent nd my e unoupled. Thus, the findings of the present study support the onept tht oxygen homeostsis is more dependent on hnges in pulmonry perfusion thn is id se lne nd provide sis for further neurophysiologil investigtion of the sensory ontrol of lood flow in turtles. The uthors would like to thnk Dr K. D. O Hllorn for ritilly reviewing this mnusript. J.K.H. ws in reeipt of University Sholr s Fellowship from the University of Texs t rlington. Referenes e,. S. nd Johnsen, K. (1987). Gs exhnge nd ventiltory responses to hypoxi nd hyperpni in mphisen l (Reptili: mphiseni). J. Exp. iol. 127, enhetrit, G., rmnd, J. nd Dejours, P. (1977). Ventiltory hemoreflex drive in the tortoise, Testudo horsfieldi. Respir. Physiol. 31, enhetrit, G. J. nd Dejours, P. (198). Ventiltory CO 2 drive in the tortoise Testudo horsfieldi. J. Exp. iol. 87, urggren, W. W. (1975). quntittive nlysis of ventiltion thyrdi nd its ontrol in two helonins, Pseudemys sript nd Testudo gre. J. Exp. iol. 63, urggren, W. W., Glss, M. L. nd Johnsen, K. (1977). Pulmonry ventiltion: perfusion reltionships in terrestril nd quti helonin reptiles. Cn. J. Zool. 55, urggren, W., Hhn, C. E. W. nd Foëx, P. (1977). Properties of lood oxygen trnsport in the turtle Pseudemys sript nd the tortoise Testudo gre: Effets of temperture, CO 2 nd ph. Respir. Physiol. 31, urggren, W. W. nd Shelton, G. (1979). Gs exhnge nd trnsport during intermittent rething in helonin reptiles. J. Exp. iol. 82, urggren, W., Smits,. nd Evns,. (1989). rteril O 2 homeostsis during diving in the turtle Chelodin longiollis. Physiol. Zool. 62, Comeu, S. C. nd Hiks, J. W. (1994). Regultion of entrl vsulr lood flow in the turtle. m. J. Physiol. 267, R569 R578. Crossley, D., ltimirs, J. nd Wng, T. (1998). Hypoxi eliits n inrese in pulmonry vsulture resistne in nesthetised turtles (Trhemys sript). J. Exp. iol. 21, Douse, M.. nd Mithell, G. S. (199). Episodi respirtory relted dishrge in turtle rnil motoneurons: in vivo nd in vitro studies. rin Res. 536, Frnkel, H. M., Spitzer,., line, J. nd Shoener, E. P. (1969). Respirtory response of turtles (Pseudemys sript) to hnges in rteril lood gs omposition. Comp. iohem. Physiol. 31, Glss, M. L. (1992). Ventiltory responses to hypoxi in etothermi vertertes. In Physiologil dpttions in Vertertes: Respirtion, Cirultion nd Metolism. (ed. S. C. Wood, R. E. Weer,. R. Hrgens nd R. W. Millrd), pp New York: Mrel Dekker, In. Glss, M. L. nd Wood, S. C. (1983). Gs exhnge nd ontrol of rething in reptiles. Physiol. Rev. 63, Hiks, J. W. nd Wng, T. (1998). Crdiovsulr regultion during noxi in the turtle: n in vivo study. Physiol. Zool. 71, Hitzig,. M., llen, J. C. nd Jkson, D. C. (1985). Centrl hemil ontrol of ventiltion nd response of turtles to inspired CO 2. m. J. Physiol. 249, R323 R328. Hitzig,. M. nd Jkson, D. C. (1978). Centrl hemil ontrol of ventiltion in the unnesthetized turtle. m. J. Physiol. 235, R257 R264. Hopkins, S. R., Wng, T. nd Hiks, J. W. (1996). The effet of ltering pulmonry lood flow on pulmonry gs exhnge in the turtle Trhemys (Pseudemys) sript. J. Exp. iol. 199, Ishii, K., Ishii, K. nd Kuske, T. (1985). Eletro-physiologil spets of reflexogeni re in the helonin, Geolemys reevesii. Respir. Physiol. 59, Jkson, D. C. (1973). Ventiltory response to hypoxi in turtles t vrious tempertures. Respir. Physiol. 18, Jkson, D. C. (1987). Crdiovsulr funtion in turtles during noxi nd idosis: In vivo nd in vitro studies. m. Zool. 27, Jkson, D. C., Plmer, S. E. nd Medow, W. L. (1974). The effets of temperture nd ron dioxide rething on ventiltion nd id se sttus of turtles. Respir. Physiol. 2, Jones, D. R. nd Milsom, W. K. (1982). Peripherl reeptors ffeting rething nd rdiovsulr funtion in non-mmmlin vertertes. J. Exp. iol. 1, Kinney, J. L., Mtsuur, D. T. nd White, F. N. (1977). Crdiorespirtory effets of temperture in the turtle, Pseudemys floridn. Respir. Physiol. 31, Kuske, T., Ishii, K. nd Ishii, K. (1988). Dense grnuleontining ells in rteril hemoreeptor res of the tortoise (Testudo hermnni). J. Morph. 197, Milsom, W. K. (1991). Intermittent rething in vertertes. nnu. Rev. Physiol. 53, 87. Milsom, W. K. nd Chn, P. (1986). The reltionship etween lung volume, respirtory drive nd rething pttern in the turtle, Chrysemys pit. J. Exp. iol. 12, Milsom, W. K. nd Jones, D. R. (198). The role of vgl fferent informtion nd hyperpni in ontrol of the rething pttern in heloni. J. Exp. iol. 87, Niol, S. C., Glss, M. L. nd Heisler, N. (1983). Comprison of diretly determined nd lulted plsm ironte onentrtion in the turtle Chrysemys pit ellii t different tempertures. J. Exp. iol. 17, Perry, S. F. (1978). Quntittive ntomy of the lungs of the redered turtle, Pseudemys sript elegns. Respir. Physiol. 35, Shelton, G. nd outilier, R. G. (1982). pnoe in mphiins nd reptiles. J. Exp. iol. 1, Shelton, G. nd urggren, W. W. (1976). Crdiovsulr dynmis of the Cheloni during pnoe nd lung ventiltion. J. Exp. iol. 64, Signore, P. E. nd Jones, D. R. (1996). utonomi nervous ontrol of hert rte in muskrts during exerise in ir nd under wter. J. Exp. iol. 199, Silver, R.. nd Jkson, D. C. (1985). Ventiltory nd id se responses to long-term hyperpni in the freshwter turtle, Chrysemys pit ellii. J. Exp. iol. 114, Ultsh, G. R. nd nderson, J. F. (1988). Gs exhnge during
9 lood flow during hypoxi nd hyperpni 3213 hypoxi nd hyperri of terrestril turtles: omprison of fossoril speies (Gopherus poyphemus) with symptri nonfossoril speies (Terrpene rolin). Physiol. Zool. 61, Wng, T. nd Hiks, J. W. (1996). Crdiorespirtory synhrony in turtles. J. Exp. iol. 199, Wng, T. nd Hiks, J. W. (1996). The intertion of pulmonry ventiltion nd rdi shunts on rteril oxygen levels. J. Exp. iol. 199, Wng, T., Hiks, J. W. nd Milsom, W. K. (1996). Chnges in rteril O 2 ontent ffet rdi shunt ut not ventiltion in turtles. (strt). Physiologist 39, 187. Wng, T., Krosniuns, E. H. nd Hiks, J. W. (1997). Control of entrl vsulr lood flows in turtles. m. Zool. 37, West, N. H., utler, P. J. nd evn, R. M. (1992). Pulmonry lood flow t rest nd during swimming in the green turtle, Cheloni myds. Physiol. Zool. 65, West, N. H., Smits,. W. nd urggren, W. W. (1989). Ftors terminting nonventiltory periods in the turtle, Chelydr serpentin. Respir. Physiol. 77,
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