M.A., M.D., Lecturer on Physiology, Charing Cross Hospital Medical School, AND A. G. PITTS. (Ten Figures in Text.)
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1 THE RELATION BETWEEN THE INTERNAL TEMPE- RATURE AND THE RESPIRATORY MOVEMENTS OF HIBERNATING ANIMALS. BY M. S. PEMBREY, M.A., M.D., Lecturer on Physiology, Charing Cross Hospital Medical School, AND A. G. PITTS. (Ten Figures in Text.) (From the Physiological Laboratory, Charing Cross Hospital Medical School.) I. Introduction. II. Observations upon Dormice. III. Observations upon Hedgehogs. IV. Observations upon a Marmot and a Bat. V. Work of Previous Observers. VI. Conclusions. VII. Literature on the Subject. I. Introduction'. Since the time of Aristotle the phenomena of hibernation have attracted the attention of numerous observers and the exceedingly slow and irregular breathing of torpid animals has been frequently described. The fact that the nature of the respiratory movements varied according to the animal's activity and temperature was also recognized, but, even after the introduction of the graphic method into pbysiological investigation, few attempts were made to record these various types of breathing. The chief researches are those of Valentin and of Dubois, who experimented with Marmots; their graphic records, however, do not illustrate many of the characteristic types of respiration. No tracings appear to have been taken of the respiratory movements of hibernating dormice and hedgehogs. It is with these animals that this paper is especially concerned. II. Observations upon Dormice. The respiratory movements of torpid dormice are very readily recorded by allowing a long straw lever to rest across the middle portion of the coiled-up body of the animal. The hibernating animal remains so quiet that it is possible, by placing I The expenses of this research were defrayed by a grant from the Royal Society.
2 306 M. S. PEMBREY AND A. G. P[TTS. it each time in a definite position in relation to the lever, to obtain curves quite comparable as regards the magnitude of the movement. The dormouse is most readily awakened by periodical determinations of its rectal temperature. It is not until its temperature reaches a point about 220 that the animal fully awakes and may move about and render the observation of its respiratory movemeits difficult or even impossible. The general method of observation was this:-the torpid animal was placed under the lever and its respiratory movements recorded for a sufficiently long time to determine the character and frequency of the breathing; the bulb of a small thermometer was then inserted into the rectulm and retained until the mercury became stationary. The animal was thus partly aroused. The altered breathing was recorded, the temperature again observed and in this way the experiment was continued until the animal was fully awake. From the records of eighteen experiments upon four dormice (Myoxus avellanarius) it is possible to recognize at least four different types of respiration and these are associated with a difference in the rectal temperature. Variations in the external tenmperature do not come into play in these experiments, for the animals were kept in the room in which the observations were made; there was no fire and the temperature of the room remained fairly constant between The winter was mild and therefore it was impossible to obtain lower temperatures. The following curves are typical portions selected from a number of tracings. In some cases the record of the respiration was, apart from the short time necessary for the determination of the rectal temperature, observed continuously for an hour or more. The types of respiration often pass gradually one into the other, but four distinct types can be described. 1. When the dormouse was in a condition of marked torpidity and had been only slightly disturbed at the commencement of an experiment, the respiratory movements were often suspended for three or four minutes and this period of apncea was suddenly broken by a series of from four to fourteen well-marked respirations, followed by another long period of apncea. These respirations generally commenced and ceased suddenly and showed no waxing and waning as in the typical Cheyne-Stokes' respiration. The rectal temperature of the dormouse was during this stage. The curves 1 in Figs. 1 and 2 illustrate this type of respiration.
3 RESPIRATION AND HIBERNATION The animal is disturbed by the insertion of the thermometer into its rectum and its respiration changes. The periods of apncea Fig. 1. Dormouse No. I. 1. Hibernating. The period of apncea lasted 80 seconds before the first respiration. Rectal temperature 5 minutes later was Stage of Cheyne-Stokes' respiration, 6 minutes later rectal temperature was Stage of continuous breathing, 6 minutes later rectal temperature was Stage of continuous breathing with shivering, 30 seconds later the rectal temperature was 24. Rect. Temp. at 1.23 p.m. = 110. Reet. Temp. at 1.34 p.m.= ,, =130.,,,,,, 2.8,, = ,, =24.,,,,,, 3.12.,= Time-mark in seconds. All the curves read from left to right. become shorter, the respirations more frequent, so that typical Cheyne- Stokes' respiration follows or, as already stated, the respiration may show no waxina or waning, Biot's' respiration. The rectal temperature during this stage is 130 to 16, the animal is inactive, its eyes are closed and it remains coiled up. The curve in Fig. 3 shows Cheyne- Stokes' respiration, the curve 2 in Fig. 1 is an example of Biot's respiration. PH. XXIV. Lyon rnddical, xxiii. p
4 308 M. S. PEMBREY AND A. G. PITTS. Sometimes there are slight tremors of the muscles of the body as in the case of the curve in Fig The next stage is one in which the periods of apncea become Fig. 2. Dormouse No. I. 1. Animal very quiet, 40 seconds later the rectal temperature was The animal showed well-marked Cheyne-Stokes' respiration and moved slightly during the periods of marked respiration, 7 minutes later the rectal temperature was Time-mark in seconds. very short and infrequent and continuous breathing begins. The dormouse is beginning to awake; its eyes are partly open and its rectal temperature is 16'-19'. The curves 3 Fig. 1, 2 Fig. 2 and 1 Fig. 4 illustrate this stage. Fig. 3. Dormouse No. III. Well-marked Cheyne-Stokes' respiration. The respiratory movements increase in force and then gradually die away into a slight quivering movement. Rectal temperature 5 minutesj later was 160. Time-mark in seconds. 4. The last type of respiration which it is possible to" record by this simple method is one of continuous breathing often accompanied by marked shivering; the dormouse shakes with the violenace of these contractions, which, numbering 6 to 10 per second, are superimposed upon the tracing of the respiratory movement. The animal is now almost wide awake, its rectal temperature is rising rapidly and at this stage is from 21'-290. The dormouse begins to move about and thus
5 RESPIRATION AND HIBERNATION. 309 it is impossible to continue the record of the respiration. This stage is illustrated by curve 4 Fig. 1 and curves 2 and 3 Fig. 4; the rate of respiration is from 350 to 450 per minute Fig. 4. Dormouse No. I. 1. Beginning to awake. Rectal temperature 2i minutes later was Marked shivering, rate of shivers about 10 per second. Rectal temperature was Shivers are less marked. Rectal temperature, Time-mark in seconds. Temperature of air, Fig. 5. Dormouse No. III. Dormouse quiet, but beginning to awake. The respirations are about 2 per second and occur in groups followed by periods of apncea; during this stage there was a slight tremor of the muscles of the body, especially of the forelimbs; these involuntary contractions cause slight curves in the period of apncea and are superimposed upon the curves of the respirations immediately following, where the rate of contraction is seen to be about 10 per second. A minute or two later the respirations became continuous, and about 5 minutes later the rectal temperature of the dormouse was 150; the temperature of the air was 110. Time-mark in seconds. It is interesting to note that the rapid rise in the internal temperature of the dormouse is associated with shivering,. Such involuntary 21-2
6 310 M. S. PEMBREY AND A. G. PITTS. muscular contractions are accompanied in other mammals, as Rich et', L6wy2 and Pembrey3 have shown, by a rise in the temperature of the body and a great increase in the output of carbon dioxide; in fact L6wy found that shivering in the human subject may increase the respiratory exchange by 900/0. Hale White4 observed that the temperature of a dormouse awakening from hibernation rose gradually until a point about 14 was reached, when the rapidity of the ascent was greatly increase(l. This observation was confirmed by Pembrey and Hale White5, who found that the rise in temperature was associated with a great increase in the discharge of carbon dioxide. In the present research the same peculiarity was again observed in connection with the relation between the temperature and the respiratory movements of the animal. The period of the greater rise in temperature was accompanied by great muscular activity or even violent shivering. The following figures show some of the results. Fo. of IRectal Time Condition of Type and frequency Rate of rise of Dormouse temp. p.m. animal of respiration rectal temperature Torpid Type I. 3 per min Inactive Type II. Biot's respiration, 20 per min. 10 in 11 mins Inactive Type II. Biot's respiration, 29 per min. 1 in 11 mins. I Awaking Type III. 150 per min in 23 mins. continuous Awake, shiver. s Type IV. 240 per min in 14 mins. continuous Active Animal too active for 950 in 50 mins. record '32 Torpid Type I. Apncea for 5 mins. IV Inactive Type I. Biot's respiration 1-2 in 11 mins Inactive Type II. Biot's respiration, 120 per min. 30 in 24 mins Torpid Type I. Apncsa for 1; I III Q l mins. Inactive Type II. Biot's respiration, 5 per min. Awake, moves and Type IV. Continuous. shivers 300 per min. Inactive Type I. Biot's respira. tion Eyes partly open Type III. Continuous. 180 per min. Eyes open, mouse Type IV. Continuous. moves activel 240 per min in 30 mins in 30 mins in 5 mins. 60 in 18 mins. I Conipt. rend. soc. de biol. Paris, 1892, p Arch. f. d. ges. Physiol., XLV Bonn, 1889; and xrvi. S This Journal, xv. p This Journal, xiii. p This Journal, xix. p
7 RESPIRATION AND HIBERNA TION. 311 III. Observations upon Hedgehogs. The hedgehogs (Erinaceus europaeus) althouigh kept in the same room as the dormice, showed a less complete hibernation; they awoke frequently, moved about their cage and took food. The temperature of the room, 10 12, was probably not low enough to ensure longer periods of hibernation. The observations were also rendered the more difficult by marked changes in the tone of the orbicularis panniculi and other cutaneous muscles, by the action of which the animal coils itself up in a ball. The respiratory movements were recorded by fixing one or two of the spines, which moved most in respiration, to a vertical straw connected with a straw lever. Owing to the protection afforded by the sharp spines of the animal and to the strength of its cutaneous muscles, it was difficuilt to obtain records of the rectal temperature. The hedgehog during its awakening from hibernation shows several types of respiration, but it differs considerably from the dormouse in its breathing. Besides changes in the frequency there are marked alterations in the depth of respiration; the hedgehog, when it has been disturbed or is awakening natutrally, gives from time to time a deep sighing respiration. It is possible to recognize four types of respiration. 1. When the hedgehog is torpid and has been disturbed as little as possible, there are long periods of apncea, lasting even several minutes and broken only by two or three deep respirations. The rectal temperature was from 10 to 16 during, this stage. The curve in Fig. 6 illustrates this type of respiration. Fig. 6. Hedgehog No. HI. The animal was quiet, but had moved once or twice. The rectal temperature was 16.50; the temperature of the room was 120. Time-mark in seconds. 2. The periods of apncea become shorter and the respirations more frequent and more regular, but of less depth. The hedgehog is inactive and its rectal temperature is above 120. The nature of the respiratory movements during this stage is shown by curve 1 in Fig. 7.
8 312 M. S. PEMBREY AND A. G. PITTS. 3. At the end of the last stage the animal was forcibly uncoiled and its rectal temperature was observed. This procedure partly Fig. 7. Hedgehog No. I. 1. Animal quiet. Two minutes later the animal was forcibly uncoiled and rectal temperature taken, Animal breathing more deeply. Rectal temperature taken at the end of this curve= 130. Time-mark in seconds. awakes the hedgehog, but it remains quiet and coiled up; its respirations become more rapid, about thirty per minute, and are also deeper. The breathing is continuous. The rectal temperature begins to rise above 130. This type of respiration is shown by curve 2 in Fig The hedgehog is awake and may partly uncoil itself. Its rectal temperature is and it feels distinctly warm to the Fig. 8. Hedgehog No. I. 1. Animal from time to time gives a deep sighing respiration. Rectal temperature 3 minutes later was 33. The animal was partly uncoiled during this record. 2. Respirations vary greatly in depth and frequency. Rectal temperature 7 minutes before was Time-mark in seconds.
9 RESPIRATION A ND HIBERNATION. 313 hand. The breathing is continuous and the type of respiration is peculiar; there are periods of rapid respirations, two or three per second, and from time to time single deep respirations, accompanied by an audible sighing noise. Such a deep respiration may last three seconds. This stage is well shown in the curves in Fig. 8. Sometimes at the beginning of this stage tremors are observed (curves 1 and 2, Fig. 9). Fig Hedgehog No. II. The animal had been forcibly awakened before the record was commenced. Temperature of the air Time-mark in seconds. 2. Hedgehog No. I. Animal quiet, but shows signs of awakening. Temperature of the air Time-mark in seconds. On both of the curves of respiration small secondary curves due to tremors are to be seen. Attempts to take the rectal temperature were unsuccessful. The great difficulty in the experiments on the hedgehog was the determination of the rectal temperature. The force necessary to uncoil the animal often aroused it so much that its respirations became more frequent and of a type more advanced than that characteristic of its teinperature at the time. IV. Observations upon a IMIarnot and a Bat. These hibernating animals also show a marked relation between their temperature and respiratory movements, but, owing to other experiments upon the respiratory exchange during hibernation, it has been possible to obtain only a few graphic records. This deficiency is the less important owing to the fact that the respiratory movements of the marmot have been graphically recorded by Valentin, Dubois and Patrizi. We are couvinced, however, that there are several types in the respiration of the marmot which are unrecorded by these observers. In the bat the types of respiration somewhat resemble those seen in the dormice: of these we give two examples. Curve 1 of Fig. 10 shows the respiratory movements of the bat when it was very inactive, but not in a condition of marked torpidity; the respirations are
10 314 M. S. PEMBREY AND A. G. PITTS. irregular and have a frequency of about 60 per minute; the rectal temperature was 13-15o. The second curve was taken upon the same animal when it was awake and about a minute before it flew away from the recording lever; the respirations are regular and have a frequency of about 180 per minute; the rectal temperature was about 300. Fig. 10. Bat. 1. Animal very inactive. Rectal temperature was '. 2. Animal active and at end of this tracing flew away. When the bat was caught 15 minutes later its rectal temperature was 340* The further observations we might make uipon the respiration in the marmot and bat are reserved until a series of graphic records can be obtained during another winter. V. Work of Previous Observers. The only graphic records of the respiratory movements of hibernating animals, which we have been able to find in the literature of hibernation, are those of Valentin, Dubois, and Patrizi' who made observations uipon marmots. There are, however, many references to the variations in the frequency and the nature of the breathing in hibernating animals. These, however, were mostly made before the introduction of the graphic method and are therefore naturally incomplete. The first exact observations upon the variations in the respiration of hibernating mammals in relation to their activity and temperature appear to be those of Mangili and Saissy; next in order are those of Edwards and of Marshall Hall., who observed the "deep and 1The original paper, "IContributo allo studio dei movementi respiratorii negli ibernanti, Nota critica experimentale," we have been unable to obtain at present.
11 RESPIRATION AND HIBERNATION. 315 sonorous inspiration" of the hedgehog when it is aroused. Valentin published numerous papers upon the marmot and recorded graphically the respirator.y movements of that animal; the curves, however, only show the irregular breathing and several types of the characteristic respiration are not represented. The next important contribution is that of Horvath, who made many observations upon the spermophiles. Mosso noticed that the type of breathing known as " Cheyne-Stokes respiration " was normal in the hibernating dormouse. The general conclusion of all these observers is that the respiratory movements become fewer and more irregular as the animal passes into a condition of torpidity. Recently Dubois has published a valuable monograph upon the marmot, in which he gives many tracings of the respiratory movements and records the deep sighing respiration which the marmot gives when it is disturbed or is awaking naturally. There is no typical Cheyne- Stokes respiration such as that seen in the hibernating dormouse. Patrizi criticises some of Dubois' results and maintains that some of the types of respiration have not been recorded. We have also noticed the absence of several typical forms of respiration, but any criticisms we inight make must be reserved until we have obtained a series of tracings upon the marmot under various conditions. VI. Conclusions. There is a relation between the internal temperature and the nature of the respiratory movements of hibernating dormice, hedgehogs, marmots and bats. Four distinct types of respiration may be described:- (i) In the torpid animal with a temperature below 120 there are long periods of apncea lasting several minutes and broken only by a few respirations. (ii) In the inactive animial with its temperature rising above 130 the periods of apncea become sborter and the respiration of Biot's type with a sudden commencement and cessation of breathing, or of the Cheyne-Stokes' type with a gradual waxing and waning. (iii) The animal is beginning to awake and its temperature is about 160, the periods of apncea are very short and infrequent; the respiration becomes continuous. (iv) The animal is awake; the respiration is continuous, very rapid and accompanied by slight tremors or marked shivering. The rectal temperature is rising rapidly and is above 200. The above stages refer especially to the dormouse. In the hedgehog
12 316 M. S. PEMBREY AND A. G. PITTS. there are in stage (iv) a short series of rapid respirations often followed by a single deep sighing respiration. This is also observed in the marmot. These types of respiration are observed in animals upon which no operation has been performed. The animal was awaking naturally or had been disturbed by the observation of its rectal temperature. Cheyne-Stokes' respiration and the modification described by Biot are normal in some of the stages of hibernation. The former type is generally seen when the dormouse is less torpid and with a higher tenmperature than in those cases when the latter type obtains. The latter, however, may gradually pass into the former. Marked disturbance of the hibernating animal causes the respiration to pass more rapidly to the continuous type of breathing, even in advance of the temperature characteristic of that stage. The heat of the body is, however, in such cases rising more rapidly. The period of most rapid rise in temperature is associated with tremors of the body, or even with violent shivering. The different types of respiration are accompanied by differences in the respiratory exchange; but upon this, and other points, further experiments are in progress. VII. Literature on the Subject. Spallanzani. Memoirs on Respiration, edited by Senebier Mangili. Annales du Mus6um d'histoire Naturelle, x. p Paris, Saissy. Recherches exp4rimentales anatomiques, chimiques, etc. 1808, p. 34. Arch. f d. Physiol. xxi. S (translation of above). Reeve. An Essay on the Torpidity of Animals. London, Edwards. De l'influence des agens physiques sur la vie. Paris, Marshall Hall. Phil. Trans. London, 1832s p Article "Hibernation" in Todd's Cyclopeadia of Anatomy and Physiology, ii. p Barkow. Der Wintersehlaf Here numerous additional references are given. Valentin. Untersuchungen zur Naturlehredes Menschenund der Thiere von Moleschott, x. S Horvath. VerhandL d. phys.-med. Gesellsch. in Wurzburg. xii. 1878; xiii. 1879; xv. 1880; xv Mo sso. Archivio per le Scienze mediche, ii. p Torino, Dub ois. Physiologie compar6e de la Marmotte. Paris, This contains an excellent bibliography. Patrizi. Centralblatt fur Physiol. xi. S Pembrey and Hale White This Journal, xix. p
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