Steffen, J. M. , and M. L. Riedesel " L982.

Pulmonary ventilation and cardiac activity in hibernating and arousing golden-mantled ground squirrels (Spermophilus lateralis). Cryobiology 19: 83-91.
cRYoBroLocY 19,83 91 (1982)

Pulmonary Ventilation and Cardiac Activity in Hibernating and Arousing Golden-Mantled Ground Squirrels (Spermophilus lateralis)
J. M. STEFFEN' aNo M. L. RIEDESEL
Departtnent
oJ'

Biologl', University of Net, Mexico, Albuquerque, Nev' Mexico 87131

Mammalian hibernation is characterized by a pronounced depression of body temperature. a marked reduction of wholebody metabolism, and the capacity to spontaneously arouse and rewarm to normothermia within several hours without recourse to an exogenous source of heat. The process of arousal is associated with elevated rates of oxygen consumption (1'7,34) and heat production (14). Thus the hibernating, arousing. and normothermic states,

studies have attempted to correlate ventilation with cardiac activity during hibernation or arousal (21,22). The purpose of the present study was twofold: (i) to monitor pulmonary ventilation with a modified ple-

thysmographic technique which allows the collection and analysis of end-tidal gases, and (ii) to simultaneously record ventilatory and cardiac activity in hibernating and arousing ground squirrels.
METHODS

all of which may be encountered within

several hours, are characterized by widely

differing metabolic demands. Metabolic integrity is insured by: (i) biochemical

adaptations that permit continued operation and regulation of key enzymatic reactions over a wide range of body temperatures, and (ii) individual and concerted actions of the respiratory and cardiovascular systems which insure that oxygen and substrate de-

Golden-mantled ground squirrels (Spermophilus lateralis) of both sexes were

trapped in the Jemez mountains of northern New Mexico. Following capture animals were caged singly and provided with food and water ad libitum. The diet consisted of

livery, as well as carbon dioxide elimination, are matched to the specific metabolic
requirements.

Cardiovascular parameters such as heart rate (3), blood pressure (7), cardiac output (28), and regional blood flow (1) have been examined in both hibernating and arousing animals. Quantitative evaluation of pulmonary ventilation has been hampered, how-

commercial rat chow supplemented with apples, lettuce, carrots, and peanuts. From October through April squirrels were housed in darkness in an environmental chamber al'| -1- 2"C. with food and water available. Body weights at the time of study ranged from 154 to 254 g. Oxygen uptake (Vor) was measured in a
1.0-liter closed vessel maintained at 8 +- 1"C

in a walk-in cold room. Animals were allowed a 30-min acclimation period in the vessel and thereafter gas samples were
taken at approximately 1-hr intervals. Following sampling the chamber was flushed with room air by a small pump attached to the vessel. Two or three measurements were made and averaged for each squirrel. Gas samples were introduced into an oxygen analyzer (Model S-3A, Applied Eleclrochemistry. Sunnyvale. Calii.) and Vo, calculated (STPD) from the gas concentra83 o0 1 1 -2240 I 821 0 10083-09$02. 00/0 Copyright @ 1982 by Academic Press, lnc. All rights of reproduction in any form reserved

ever, by the sensitivity of the hibernating animal to handling. This has limited the application of precise methods of investigation in this area (24.35). In addition, few
Received May 19, 1981; accepted July 31, 1981. I Present address: Dept. Physiology and Biophysics,

University of Louisville School of Medicine, Health Sciences Center. Louisville. KY. 40292.

84

STEFFEN AND RIEDESEL

Frc. 1. Diagram of the plethysmograph and instrumentation for monitoring ventilation and heart
rate-

tion, the chamber volume, and the time elapsed between closure of the chamber
and sampling.

The plethysmographic setup for

mea-

surement of ventilatory parameters is illustrated in Fig. 1. Squirrels wore a closefitting hard plastic face mask (0.5 to 1.5-ml dead space) secured to the neck by a rubber diaphragm to create a tight seal. To reduce the incidence of arousal caused by placement of the mask on the animal, hibernating squirrels were handled at least three times per week for a period of several months prior to experimental use. The mask communicated with the exterior through a short length of plastic tubing. Changes in body volume resulting from inspiration and expiration resulted in intrachamber pressure

fluctuations which were monitored by a differential pressure transducer (Model MP45-1, Validyne, Northridge, Calif.) attached to a Validyne transducer indicator
and recorded. Calibration of the system was

achieved by injecting and withdrawing known volumes of air from the chamber at intervals between breaths. A uniform calibration signal throughout the experiment insured that no leaks were present in the system. Catheter tubing, attached to a small pump and placed within several millimeters of the nares, served a dual function: (i) to pull air continuously past the nares and ensure that the inspired gas was effectively room air, and (ii) to pull expired gases through an S-3A oxygen analyzer or LB-l carbon dioxide ar'alyzer (Beckman, Palo Alto, Calif.). To insure the accurate measurement of end-tidal gas pressures low sample flow rates (30 to 60 ml ' min-1) were maintained during experiments on hibernating animals with flow rates increased for arousing animals. With low-sample flow rates end-tidal plateaus were recorded for both oxygen and carbon dioxide. Therefore, end-tidal gas pressures were taken as representative of alveolar values. Gas

VENTILATION IN

Spermophilus

lateralis

85

- (l) 'Fro"), where A : alveolar (end-tidal), I : in(P^co,

analyzers were calibrated with dry room air or commercial gases. Breathing frequency (f), tid,al volume (Vr) and minute ventilation (VB) were obtained directly from the record of chamber pressure changes. Ventilatory parameters were based on expired volumes. pulmonary gas exchange ratio, R", was calculated from the equation (11): : {', Q""qr) (l - Frc)l(Prn, * Poor)

exteriorized and the ends were fastened together in a safety pin type arrangement. At the time of experimentation the silver wires were connected to a Model MK IV cardiac preamplifier (E and M Inst. Co., Houston, Tex.). This system served to monitor the heart rate and the electrocardiogram. Data were collected on eight hibernating ground squirrels for periods ranging from 4 to 30 hr. Data on the arousal process were obtained from 5 to 16 squirrels for each

spired, and F,o, is the fractional concentration of inspired oxygen. Alveolar ventilation (Vo) was calculated from the equation Va

10-min period during the

RESULTS

first hour of

arousal.

Rn'

y2(RTIP

where R : the gas constant (2.785 ml BTPS'Torr'oK.ml STPD) and 7: the absolute temperature in'K. Dead space (Vp) was calculated from the equation:
Vo

^co).

Q)

(Va

- Vo)/.f.

(3)

While observations on hibernating ground squirrels generally lasted from 4 to l0 hr, the ability to continuously record ventilation and heart rate for periods of up to 30 hr emphasizes that the techniques employed in the present study did not constitute an unduly irritating stimulus to the hibernating animal.

Calculation of the dead space allowed comparison of measured minute ventilation and calculated alveolar ventilation, and ensured that they were in acceptable agreement. In addition, because Vo was calculated from end-tidal gas pressures. comparison of Vu and Vo provided a test for the reliability of end-tidal gas pressure measurements. Skin temperature (I"u) over the scapulae was measured with a copper constantan thermocouple attached to a potentiometer.

A periodic breathing pattern

served in all hibernating ground squirrels (Figs. 2 and Fig. 3). Nonventilatory periods extending as long as 40 min were occasion-

was ob-

ally noted, though apneic intervals averaged 8 to 9 min. Ventilation was always initiated by an inspiratory movement and was

Ambient temperature inside the plethysmograph was monitored with a telethermometer (Model 46, Yellow Springs Inst. Co.. Yellow Springs, Ohio). At the termination of each experiment both rectal (I...) and cheek pouch (2"1) temperatures were measured with a Yellow Springs telethermometer. For measurement of Zr", the telethermometer probe was inserted a minimum of 3 cm. Several weeks prior to each experiment,
two 3-cm pieces of silver wire were inserted subcutaneously over the scapular region of hibernating squirrels. The inserted end was

generally completed with an expiration (Fig. 3). Breathing frequencies during ventilatory periods ranged from as low as 10 to as high as 40 breaths min-r. Due to the extended length of apneic intervals the overall breathing frequency was low during hibernation (Table 1). In the hibernating
animal V.. fluctuated markedly during individual breathing periods (Fig. 3). The larger tidal volumes were frequently noted at the onset of ventilation (Fig. 3.4,). Values for Vo and Vo represented 60 and 407o, respec-

tively, of the tidal volume. Hibernating

ground squirrels also exhibited CheyneStokes respiration, with a waxing and waning of the tidal volume during periods of ventilation (Fig. 38). In any given period of ventilation the ini-

86

STEFFEN AND RIEDESEL

HIBERNATION

{93

ARLY AROUSAL

Ftc. 2. Representative breathing and heart rate patterns during hibernation, early arousal, and at I hr into the arousal process. The upper recording in each section is ventilation while the lower recording is heart rate. lnspiration is represented by an upward pen deflection.

tialP"",,, was low whilePu",.o, was high. As a series of breaths continued Pu.,..,,,, decreased (COz washout) while Po,ro, increased. The initial Pu,rco,, was in the range of 26 to 32 Torr and the initial Pn".,, was 90 to 95 Torr. As end-tidal plateaus were obtained for both gases, the end expiratory
values (Table 1) were taken as representative of alveolar gas pressures and were used to calculate other parameters. Individual measurements of V,-,, ranged

averaged 10.3

The heart rate of hibernating squirrels beats min I (Fig. 4). Cardiac rhythms which were typically seen

during hibernation are illustrated in Fig. 3C. Prior to ventilation, pairing of heart beats is evident. This is followed by a marked increase in heart rate prior to and during ven-

tilation. Cardiac activity wanes to below

the preventilatory rate as breathing ceases. In addition to variable cardiac rhythms, the

from 0.358 to 0.862 ml STPD'Kg'min 1. The V6o, (Table 1) was calculated from the V6, utilizing the mean Ru value obtained from the end-tidal gas pressures.

electrocardiogram was also altered by hibernation, with a lengthening of the P-R and abbreviation of the R-T intervals
(Table 2).

During the monitored period of arousal

VENTILATION IN

Spermoplrilus lateralis

87

r1ml

t-.]"lmin

It*l
Frc.3.
Recordings ofrespiratory and cardiac activity in hibernating S. lateralis. Inspiration is
represented by an upward pen deflection. The lower recording in C is heart rate. Note the preventilatory pairing of heart beats, increase in heart rate prior to and during ventilation, and waning of heart

rate as ventilation ceases.

r.r

rose from 9.6 to 12.5"C. Final 7"r, and 7."

averaged 15.8 and 12.8'C, respectively. The onset of the arousal process was characterized by several respiratory adjustments. Apneas quickly disappeared and respiration

in heart rate and breathing frequency during arousal resulted in a marked change in the ratio of heart beats per breath (Fig. 5).
DISCUSSION

became continuous. Additionally, Vt became quite uniform in contrast to the variability of this parameter during the periodic

Oxygen consumption is markedly reduced during hibernation (17). The y,,2 measurements of hibernating S. lateralis
TABLE
.l

ventilatory bursts in hibernation (Fig. 2). By the end of the first hour of arousal yF had increased 25-fold. Adjustments in heart rate qualitatively paralleled those of breathing frequency during arousal (Fig. a). Quantitatively. however, heart rate increased only 7-fold during the monitored arousal period compared with a 26-fold increase in breathing frequency. The increase in V" during the first hour of arousal is therefore completely accounted for by an increase in breathing frequency with V1
remaining unchanged. The disparate changes

Respiratory Parameters of Hibernating S. lateralis

(min-,) ') kg ')

Vn (ml BTPS'kg

2.1 + 0.2' (8)a 4.8 * 1.1 (8)

1.3 (8) (8) 24.4 * 2.7 (8) 106.6 - 1.4 (8) 23.8 1.0 (81 0.71 + 0.04 (8)

(ml BTPS (ml BTPS kg min 1) Vu (ml BTPS.kg.min 1) Poto" {Torrr P.r, f , tTorrt
V_n

v,

11.6 14.3

+ 0.8

RE

Vu, rml STPD.kg.min r v,;" {ml STPD kg min 't Number of animals

- 0.009(ll) 0.148 0.015 (ll)

0.541

" Mean :! SEM.

88

STEFFEN AND RIEDESEL

6.O

70 U

I F
@

5.O

?oo

-t 40
a an F u
m

950
I

Boo
@

E
U

2.O

530

t.o

3
U
m

2zo k
to

30 40 50
sn"urt

60

'o *ni.,or* FIc. 4. Heart rate and breathing frequency during arousal of S. Iateralis. The 0 time value represents hibernating squirrels. Vertical lines represent SEM numbers in parentheses indicate number of animals.

lo

oo 50

60

FIc. 5. Relationrhip u"l.l['.tn .ut" and breathing frequency during arousal. The 0 time value represents hibernating squirrels. Vertical lines represent SEM. Numbers in parentheses indicate number of
animals.

hibernating l3-lined ground squirrel. Jame-

son (15) has reported apneas offrom 2to 20 min in hibernating S. lateralis. Similarly, are in accord with previously reported valHammel et al. (14) have observed apneic ues for a variety of ground squirrel species intervals of approximately 10 min in the (10. 16. 28. 341. The V.rfalls at lhe lower hibernating golden-mantled ground squirend of the range reported for the hibernatrel. Thus neither breathing pattern nor ing golden-mantled ground squirrel by timing appears to be affected by the Hammel ('t al . (l 4). The V.o,. eslimate<J plethysmographic technique. from oxygen uptake and respiratory exIn hibernating squirrels periods of ventichange values, also agrees well with previlation were invariably initiated with an inous reports (17). spiration. As suggested by Guy and Patrick Observations of a number of species (2, (13) inspiratory termination of apneic peri19, 20, 27, 32),'including ground squirrels (14, 15, 22), have documented a pattern of ods may serve to dissipate the nonchemical (neural) component of the drive to breathe periodic ventilation during hibernation simaccumulated over the period of apnea. The ilar to that reported in the present study. relative contribution of chemical versus Landau and Dawe (22) observed nonvennonchemical influences to the control of tilatory periods of from 3 to 5 min in the

ventilation during hibernation is not known.

Sensitivity to the level of inspired CO, is

TABLE
2

Duration of Electrocardiographic Intervals

Recorded from Hibernating Ground Squirrels

retained in the hibernating ground squirrel (23). The length of apneic periods in the

Duration
Interval
u

(sec)

P.T

PR RT
o

8Rs

0.62 0.13 0.32 0.29

+ + + +

0.090

0.03 0.10 0.06

N - 60 for each interval. 'Mean + SEM.

hibernating ground squirrel coupled with the greatly reduced rate of CO2 elimination (and presumably production) argues against the importance of carbon dioxide in regulation of ventilation in this group of hibernating animals. This does not rule out the potential importance of CO2 in the control of breathing in species known to exhibit much longer apneic periods (l*2 hr) such

VENTILATION IN
as the dormouse (27) and

.Sperzopft ilus lateralis

hedgehoE$2).In

man, periodic ventilation of the Cheyne-

Stokes type has been associated with a primarily hypoxic ventilatory drive (5, 30). Blood of hibernating animals is bright red and appears well oxygenated. In addition, hibernators are highly resistant to anoxia (17). In view of the duration of the apneic periods and greatly reduced V.,, in the hibernating ground squirrel, hypoxia would not be predicted to play a central role in the regulation of ventilation during hibernation. The effect of reduced body temperature during hibernation on the medullary and pontine respiratory centers has not been well studied. In this context, however, Cherniack et al. (4) have induced periodic respiration (Cheyne-Stokes) in the anesthetized cat by ventral medullary cooling. Depression of body temperature has also been reported to lengthen apneic periods in reptiles (11). The values for both breathing frequency and tidal volume are similar to previous reports on other hibernating species (8, 12, 22, 25, 35). Tidal volume did not change significantly during the process of arousal. This is in contrast to observations of the arousing pocket mouse (35). Eliassen (7) and Bullard (1) have reported a constant stroke volume in arousing hibernators. In view of the relatively small absolute volume changes which could be accommodated by the heart and lungs of these smaller mammals, it is conceivable that both changes in cardiac output and minute ventilation are mediated primarily by adjustments of frequency. This hypothesis is supported by the present finding that the increase in Vu during arousal can be quantitatively accounted for by an increase in breathing frequency.

arterial blood samples taken from hibernating S. lateralis (33). An arterial P.o, of 26.5 Torr was observed by Tahti (32) in the hibernating hedgehog immediately following a period of ventilation. Other investigators have likewise reported arterial P"o, values below 30 Torr in hibernating animals (18,29,31). There have been only two reports of arterial Po, in hibernating animals. A value of 88 Torr has been reported for the l3-lined ground squirrel (26), while a value of 120 Torr has been observed in the hibernating hedgehog (32). The P"ro, of 107 Torr in the hibernating golden-mantled ground squirrel approximates these values. The reliability of the end-tidal gas pressure measurements is also reflected in the value of Ro, 0.71, which was calculated assuming that end-tidal samples were representative of alveolar gas. This value is con-

sistent with previous determinations by other investigators (17), and points to a lipid-based metabolism in the hibernating ground squirrel. Thus it appears that samples of end-tidal gas can reasonably be used

The end-tidal gas pressures reported in

the present study correlate well with previous measurements of blood gases in hibernating animals. TheP"r"o, of 24Torr agrees

the hibernating ground squirrel. In agreement with previous work (3, 19, 22) the heart rate is low in the hibernating animal. Pairing of heart beats in the hibernating golden-mantled ground squirrel is similar to previous observations of the hibernating hedgehog and arctic ground squirrel (6). The increased cardiac activity observed during ventilatory periods has not previously been reported. However, this observation is reminiscent of the "bursts of hearl beals" reported to occur at regular intervals in the hibernating arctic ground squirrel (6). These simultaneous changes in ventilatory and cardiac activity may represent yet another example of the physiologic integrity of mammals during natural hibernation. Enhanced cardiac activity during lung ventilation may illustrate a parallelism between mammalian hibernators and diving
mammals and reptiles.

to predict arterial gas pressures in

well with the value of 28 Torr reported for

The qualitative correlation between

90

STEFFEN AND RIEDESEL

breathing frequency and heart rate during arousal is apparent from Fig. 4. Initially during arousal the ratio of heart beats to breaths is reduced markedly, but thereafter

remains steady at this new level. This suggests that arousal from hibernation requires the establishment of a new functional relationship between the respiratory and cardiovascular systems. The lengthened P-R interval of the ground squirrel electrocardiogram confirms previous reports of some degree of A-V dissociation in the heart of the hibernating mammal (6, 9). The relatively short R-7 interval recorded from hibernating squirrels. however, indicates that the ventricular tissue is still capable of rapid repolarization
even at greatly reduced body temperatures. In conclusion. an assessment of ventilation in the hibernating mammal without al-

the hibernating ground squirrel was characIerized by arrhythmias which correlated with ventilation and by alterations in the electrocardiogram typically seen in hibernating animals. Arousal from hibernation was accompanied by: (i) a replacement of

periodic by continuous ventilation, (ii) a 25-fold increase in Vu in the first hour which was accounted for by the increment in breathing frequency. and (iii) a marked decrease in the ratio ofheart beats to breaths. The techniques developed in the present study will permit further quantitative investigations of pulmonary ventilation and its control in hibernating animals.
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Bullard, R. W. Changes in regional blood flow and blood volume during arousal from hibernation. Ann. Ar;ad. S<;i. Fenn. Ser. A4'71.65-'76
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SUMMARY

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