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Pakistan Journal of Marine Sciences, Vol.3(1), 1-7, 1994. THE MYOGENIC AUTOMATISM OF THE SYSTEMIC HEART OF OCTOPUS VULGARIS (CEPHALOPODA: COLEOIDEA): EVIDENCE FOR LOCALIZED STRETCH SENSITIVITY AND PACING ACTIVITY C. Agnisola Department of General and Enviroiunental Physiology, University of Naples "Federico II", Napoli, Italy. ABSTRACT: The localization ofthe stretch sensitivity and myogenic automatism in the systemic heart of Octopus vulgaris has been studied on an isolated preparation in which the ventricle was zoned by ligatures. Each region has been submitted to two different levels of internal hydrostatic pressure (1 and 2 kPa). Only the two atrio-ventricular regions were able to contract regularly when submitted to internal pressure, with a frequency dependent from the pressure value, while the ventricle-aortic region was insensitive to the stretching by internal pressure. This result supports the hypothesis that the automatism in this heart is localized. Electrocardiogram recordings from different areas of an isolated and perfused preparation of the systemic heart ventricle are also reported, which suggest that the electrical activity of the ventricle originates in two narrow areas near the atrio-ventricular valves. KEY WORDS: Octopus- systemic heart- automatism - stretch. INTRODUCTION Coleoid cephalopods are active organisms with high metabolic rates (O'Dor and Webber, 1986), so that they must have a fast and relatively efficient blood supply system. Cephalopods have developed a closed circulatory system characterized by a high systemic pressure and a powerful single central heart, the systemic heart, situated on the oxygenated side of gills. This central pump consists of a single ventricle and two auricles (left and right). It has a relevant myocardial mass, comparable with that of fishes, (Agnisola and Houlihan, 1994) and a complex myoarchitecture (Kling and Schipp, 1987). A lacunary -vascular system for blood supply to the ventricle has been described (Agnisola eta/., 1990). This system connects the intraventricular lumen with superficial epicardial veins through a capillary bed. The systemic heart .of cephalopods is characterized by a myogenic autorhythm which is under neurohumoral control (Kling and Jakobs, 1987; Jakobs and Schipp, 1992). The isolated octopod ventricle contracts in a regular way for many hours if stretched by internal hydrostatic pressure: heart rate and contractile force are related to the input pressure (Smith, 1981a; Foti et al. 1985; Agnisola and Houlihan, 1991). The need for an internal pressure to get the regular beating of the isolated systemic heart suggests that stretch sensitivity and automatism in this heart are intimately related. The hearts of Octopus and Eledone (Smith, 198lb) as well as Sepia (Jakobs and Schipp, 1992) display well defined electrocardiogram (ECG) waves, and the existence of a precise sequence for the depolarization of the ventricular myocardial wall has been proposed (Smith, 198lb). However, it is still unknown whether there is in this heart a distinct pacemaker region, and an associated localized stretch sensitivity, or whether each myocardial cell possesses the character of pacemaker activity (diffuse myogenic automatism). 2 Pakistan Journal of Marine Sciences, Vol.3(1), 1994 In the present paper the effect of wall stretching by internal pressure on different regions of the ventricle has been studied by zoning it with ligatures. This approach allows to test if the stretch dependency of heart activity is diffuse in the ventricle or is limited to specific regions of its . wall. Moreover, a first attempt to make a surface map of unipolar ECG records of the isolated systemic heart aimed to obtain insights on the impulse propagation on the ventricle surface is reported. ' MATERIALS AND METHODS ANIMALS The study was carried out at the Zoology Station of Naples 11 A. Dohrn11 , Naples, Italy. Six specimens of either sex of Octopus vulgaris (0.5-1.5 Kg in weight) were captured in the Bay of Naples and maintained in circulating seawater pools for at least one week before use. HEART PREPARATION FOR TESTING REGIONAL STRETCHING SENSITIVITY The animals were sacrificed by decapitation and the systemic heart dissected out. The dissection was made at 4°C. The isolated ventricle was zoned in three regions of similar size by ligatures, as shown in Fig.l. Dorsal aorta and both the auricles were cannulated, while gonadal and abdominal aorta were ligatured at their bases. The dorsal aorta was cannulated forcing the aortic valve. In each preparation the cannulae were alternatively connected to an input reservoir to give a fixed head pressure. In this way each region was separately ·subjected to internal hydrostatic pressure and its mechanical activity was estimated by an isotonic transducer (UGO BASILE ~iol. Res. Apparatus) connected to a chart recorder. Two different pressure levels were used (1 and 2 kPa). The perfusion saline was filtered seawater containing 0.05% glucose, pH 8.0, gassed with oxygen. Because of the ligatures, there was no flow through the heart, apart some outflow from the coronary veins. Measures were made at room temperature. ISOLATED SYSTEMIC HEART PREPARATION AND ECG DETERMINATION The isolated systemic heart was prepared according to Agnisola eta{ (1989) with some modifications. The dissection was made at 4°C. Both the auricles and the dorsal aorta were cannulated, while gonadal and abdominal aorta were ligatured at their bases. The perfusion apparatus was as reported by Agnisola et a!. (1989). The perfusion saline was same as described above. The perfusate was not recirculating and the two auricles received it at the same controlled input pressure. . The basal perfusion conditions were chosen to- reproduce in vivo resting afterload and stroke volume values as previously reported (Agnisola eta!. 1989; Agnisola eta!., 1994). Each heart was generating its own rhythm. Preparations were stable for at least one hour. . For the unipolar recording of the ECG preparations were enclosed in a Faraday-cage. Two platinum electrodes (0.2 mm in diameter) were used. One of the electrodes was grounded while the other was inserted into the ventricle surface where necessary. The signals were amplified and recorded with a dual beam oscilloscope (502A, Tektronic Inc.). The measures were made at room temperature. Agnisola: Octopus heart automatism 3 RESULTS STRETCH DEPENDENCE OF DIFFERENT REGIONS OF THE VENTRICLE In order to test the stretch dependence of different regions of the Octopus ventricle, this has been divided in three regions by two ligatures (Fig.l): the left and right atrio-ventricular (A- V) regions (indicated as I and II respectively) and the ventricleaortic (V-A) region (indicated as III). Each cavity in which the ventricular lumen was divided by the ligatures was separately submitted to two different levels of internal pressure (1 and 2 kPa). Two have been the main results ofthese experiments. First, only the regions J and II respond to the internal load with a regular beating. No spontaneous contraction was observed in the region III when subjected to internal auricles b ....__..... 2 sec Fig. 1. Stretch sensitivity of the isolated Octopus systemic heart. A scheme of the Octopus systemic heart showing auricles, ventricle, dorsal aorta and the two minor aortae (gonadal and abdominal) is reported. Ligatures were made along the dashed lines, so that the ventricle was. divided up in three regions: I, left atrio-ventricular; II, right atrio-ventricular; III, ventricle-aortic. Two different stretch levels were obtained by applying internal hydrostatic pressure through the cannulated left auricle, right auricle and dorsal aorta respectively. Examples of mechanograms from the regions I and II at the pressure of 1 kPa (a) and 2 kl'a (b) are also shown. Region III does not contract when submitted to the same pressure values. The determinations were repeated on three preparations: no difference in the qualitative response was observed. 4 Pakistan Journal of Marine Sciences, Vol.3(1), 1994 pressure independently from the other regions. Second, in the regions I and II both frequency and amplitude of contractions increased with increasi~g pressure. In particular the doubling ofpressurealmost doubles the heart rate (from 15± to 27.6±6 beats min" 1 in the region I, from 18±4 to 40.5±8 beats in the region II; mean of three preparations). The differences between the left and the right sides were not significant. Relatively high pressures were necessary to obtain contraction rates similar to those of the whole heart perfused preparation or in vivo (Agnisola and Houlihan, 1991; Agnisola eta!., 1994). In summary the above results seem to demo,nstrate that the stretch sensitivity and the pace control in the Octopus systemic ventricle is localized and not diffuse. In this respect the two atrio-ventricular regions seems to be qualitatively equivalent. ELECTROCARDIOGRAM IN THE ISOLATED AND PERFUSED VENTRICLE As shown in Fig.2, the isolated ventricle perfused under basal conditions simulating the resting physiological ones (Agnisola et al. 1989) displays a regular and complex ECG waveform. According to previous reports (Smith, 1981b; Jakobs and Schipp, 1992; Agnisola and Houlihan, 1994), a regular R wave, indicating the ventricular depolarization, can be observed. In some preparations a small and not constant P wave occurs (auricle depolarization, Jakobs and Schipp, 1992). Auricles do not contract regularly. The R spike is of 300-500V and it is known to precede the ventricle contraction (Agnisola and Houlihan, 1994). Interestingly, the shape ofthe R wave depends on the site of recording. In general, this wave consists of a positive-negative deflection whose relative amplitude depends on the specific region of the :ventricle from which it is recorded. An interesting result is shown in Fig.3, where the records obtained from different places of the ventral surface of the isolated perfused ventricle are reported. It can be seen that there are two limited areas, close to each atrio-ventricular junction, in which, unlike the complex waveform detectable elsewhere, only a negative wave is obtained. The absence of a positive deflection indicates these areas as sites of origin of electrical activity in the ventricle. DISCUSSION Based on the presence of a 11 P 11 -wave in the ECG of the Sepia systemic heart, Jakobs and Schipp (1992) have hypothesized the existence of a non-diffuse automatism within this heart and of a specific pacemaker function in the auricle. However, this does not solve the question of whether the ventricle possesses a localized and non-diffuse pacemaker capacity. In the isolated working heart preparations here used the auricles scarcely contribute to the heart rhythm. Their beating is irregular and not synchronous with the ventricular beating. This suggests that the ventricle must have its own pacemaker capacity. The main result reported here is the apparent regional sensitivity to pressure changes in the systemic ventricle of the octopod 0. vulgaris. The zonation of the ventricle by ligatures has clearly demonstrated that the ventricular-aortic region is insensitive to the wall stretching by internal pressure and is unable of spontaneous activity. On the other hand both the atrio-ventricular regions are able to contract Agnisola: Octopus heart automatism ~[• 5 .......__.. 2 sec Fig. 2. Typical unipolar electrocardiogram recorded from the isolated and perfused Octopus systemic heart . •2 sec Fig. 3. R -waves recorded from different sites of the ventral surface of the isolated and perfused Octopus systemic heart. The determinations were repeated from the same points on three different preparations: no qualitative differences in the R-wave shape were observed. 6 Pakistan Journal of Marine Sciences, Vol.3(1), 1994 regularly when submitted to a pressure load. Interestingly, heart rate in these regions seems to be related tq the internal pressure, These results strongly support the number of previously reported indications of a ventricular myogenic automatism localized in the vicinity of A-V valves. A "particular sensitivity" in the atrio-ventricular junctions in the Octopus heart has b~een reported (Skramlik, .1941) and spontaneous contractions within this area inunperfused heart preparations of octopods (Smith, 198lb) have been observed. Some authors have reported that the A-V areas seem to be the origin of the ventricular contraCtions both in vivo and in vitro (Wells, 1979; 1983). In other molluscs (e.g. Dolabella anricularia, Kuwasawa, 1979) the myocardium within the A-V valve possesses both the ultrastructural and electrophysiological characteristics of a pacemaker. The conclusion of a localized pacemaker activity in the Octopus ventricle is also supported by the unipolar ECG records in the whole isolated and perfused heart preparations. The analysis of the R-wave shape in different points of the ventricular surface indicates that there is a precise sequence of depolarization of the ventricle, according to the hypothesis of a non-diffuse origin of the activity, and that the probable sites for a localized ventricular pacemaker are the A-V junctions. The results reported here do not allow to identify specific nodal areas for which a combination of both, histological and electrophysiological studies are necessary (Jones, 1983). However, they are consistent with a non-diffuse automatism in this heart. REFERENCES Agnisola, C. and D.F. Houlihan. 1991. Oxygen supply and in vitro performance of the systemic heart of Octopus vulgaris: effects ofhaemocyanin. Journal9[ Experimental Biology 157: 523-541. Agnisola, C. and D.F. Houlihan. 1994. Some aspects of cardiac dynamics in Octopus vulgaris (Lam.). Marine Behaviour and Physiology, in press. Agnisola, C., G. Zummo and B. Tota. 1990. Coronary drainage in the Octopus vulgaris systemic heart. Journal ofExperimental Zoology 253: 1-6. Agnisola, C. T., Cariello, A. De Santis, A. Miralto and B. Tota. 1989. Chronotropic andinotropic effects of atrial peptides on the isolated systemic heart of Octopus vulgaris. Journal of Comparative Physiology B 158: 637-641. Agnisola, C., R. Venzi, T.,Mustafa and B. Tota. 1994. The systemic heart ofOctopus yulgaris: effects of exogenous arachidonic acid and capability for arachidonate metabolism. Marine Biology, in press. Foti, I., T. Trara Genoino and C. Agnisola. 1985. In vitro cardiac performance in Octopus vulgaris (Lam). Comparative Bioch(3mistry and Physiology 82C: 483-488. Jakobs, P.M. and R. Sch.ipp. 1992. The electrocardiogram of Sepia officinals L. (Cephalopoda: Coleoidea) and its modulation by neuropeptides of the FMRFamide group. Comparative Biochemistry and Physiology 103C: 399-402. Jones, H.D. 1983. The circulatory systems of gastropods and bivalves. In: The molluscaVol.5 Physiology Part II (Eds. Saleuddin, A.S.M. and K.M. Wilbur). Academic Press, New York. Pp. 189-238. Kling, G. and P.M. Jakobs. 1987. Cephalopod myocardinalreceptors: pharmacological studies on the isolated heart of Sepia officinalis (L.) Experientia 43: 511-525. Kling, G. and R. Schipp. 1987. Comparative and cytochemical analysis of the cephalopod systemic heart and its innervation. Experientia 43: 502-511. Kuwasawa, K. 1979. Effects of ACh and Lips on the AV valve and the ventricle ofDolabella auricularia. American . Zoologist 19: 129-143. O'Dor, R.K. and D.M. Webber. 1986. The constraints on cephalopods: why squids aren'tfish. Canadian Journal o[Zoology 64: 1591-1605. Skramlik. F.V. 1941. Uber den Kreislaufbei den Weichteiren. krgeonrsse aer mologie 18: 88-286. Smith, P.J.S. 1981a. The role of venous pressure in regulation of output from the heart ofthe Octopus, Eledone cirrhosa (Lam). Journal ofExperimentalBiology 93· 243-355. · Agnisola: Octopus heart automatism 7 Smith, P.J.S. 1981b. The octopod ventricular cardiogram. Comparative Biochemistry andPhysiology70A: 103-105. Wells, M.J. 1979. The heart beat of Octopus vulgaris. Journal ofExperimental Biology 78: 87-104. Wells, M.J. 1983. Circulation in cephalopods. In: TheMollusca Vol.5 Physiology Part II (Eds. Saleuddin. A. S.M. and K.M. Wilbur). Academic Press, New York. Pp.239-290. (Received: 13 January 1994)