Physiology and Behavior, Vol. 14, pp. 13--16. Brain Research Publications Inc., 1975. Printed in the U.S.A.
Effects of Prior Aversive Stimulation on Heart Rate Responses to Open Field Exposure in the Rat a DONALD V. CHALMERS,2 SALLYEANA COYLE AND SEYMOUR LEVINE 3
Department o f Psychiatry, Stanford University School o f Medicine Stanford, California 94305
(Received 15 July 1974) CHALMERS, D. V., S. COYLE AND S. LEVINE. Effects o f prior aversive stimulation on heart rate responses to open field exposure in the rat. PHYSIOL. BEHAV. 14(1) 13-16, 1975. - Heart rate (FIR) responses to open field (OF) exposure were compared between rats previously exposed to intense, inescapable electric shock (preshock, PS) and Controls. Results indicated that (1) Control animals showed a steady increase in HR across a 3 rain exposure on each of 4 days of testing, while PS animals showed an initial HR deceleration followed by partial recovery on each day; (2) the HR response of PS animals in the OF was not related to any HR response to shock during treatment; and (3) the HR responses of both PS and Control animals were specific to the OF situation, with both groups showing steady HR deceleration across 3 min after being placed in their home cages. Results were discussed in terms of (1) the apparently altered perception of environmental change produced by PS, and (2) the possible role of HR acceleration in Controls in terms of minimizing the impact of aversive stimulation. Preshock
Open field
Heart rate
Defensereflex
PRIOR exposure to intense, unsignaled and inescapable electric shock (preshock, PS) has been shown to alter the subsequent behavior of rats in the presence of novel [8,15 ] and/or aversive [1,9] stimulation. In connection with these behavioral effects, it has also been observed that PS leads to heightened physiological reactivity as measured by increased plasma corticosterone levels [8, 9, 15] and lower basal resistance levels [ 1 ]. More recently Chalmers et al. [2] found that, although PS did not alter the amplitude of the startle reflex elicited by intense acoustic stimulation, it did alter the nature of the heart rate (HR) response to such stimulation. Thus, while control animals showed HR acceleration, animals exposed to PS showed HR deceleration to the initial stimulus presentations. In discussing these results, Chalmers et al. [2] noted that the strong deceleratory response shown by PS animals resembled the bradycardia described by Hofer [7] for wild rodents in the open field (OF). Since PS animals also show OF behavior similar to that of wild rodents [8,15], a more direct examination of the cardiovascular responses of PS animals in this situation seemed warranted. The HR deceleration observed following startle was also discussed by Chalmers et al. [2] in terms of the theoretical
account of PS effects set forth by Anderson et aL [1]. These authors argued that intense stimulation in test situations aroused pain-produced emotional responses, previo u s l y associated with PS treatment, and that these responses mediated the behavioral effects of PS. Such a mechanism was viewed as unlikely in view of the qualitatively dissimilar HR responses elicited by shock, i.e., HR acceleration, and by startle stimulation in the test situation, i.e., HR deceleration. Although this argument has a priori merit, the possibility does exist that HR deceleration mediated by parasympathetic rebound may follow PS treatment, and that the reproduction of this response in test situations might be involved in PS effects. In addition to comparing the HR responses of PS and control animals in the OF, then, the present study was also designed so that the HR responses up to 1 hr following the PS treatment could be investigated. METHOD
Animals Forty naive, male Sprague-Dawley rats were received from Simonsen Laboratories (Gilroy, CA) at approximately 90 days of age. Animals were housed individually with food
~This study was supported by Research Grant NICH & HD 02881 from the National Institutes of Health, Biological Sciences Training Grant MH 8304 and ONR Contract N00014-67-A-0112-0009. 2Present address: Psychology Department, Illinois State Univ., Normal, IL 61761. aSupported by USPHS Research Scientist Award K5-MH-19936 from the National Institute of Mental Health. Reprint requests should be sent to this author. 13
14 and water available ad lib throughout the experiment except for the brief periods during which HR was recorded in home cages.
Apparatus The apparatus used during the treatment phase of the experiment has been described in detail previously [3]. Briefly, it consisted of two boxes (17.8 x 17.8 x 30.5 cm) located in sound-attenuating wooden chambers. One of the boxes was wired to a Grason-Stadler Shock Generator (Model No. E1064) so that the floor and all four walls could be electrified. The OF has also been described in detail [8]. Briefly, it consists of a circular arena (74.9 cm in dia.) with 31.8 cm high walls painted flat white throughout. Black concentric circles and radii divide the floor into sectors, consisting of a central circle, an inner circle with 6 sectors and an outer circle with 12 sectors. During testing the arena was lighted by two 150 W flood lamps in 22.9 cm aluminum reflectors placed 91.4 cm above the floor, and a white noise background (70 db re 0.0002 dynes/cm 2) provided through an 8.9 cm speaker which was also placed 91.4 cm above the floor.
CHALMERS, COYLE AND LEVINE sive 30 sec intervals during each 3 min exposure; and (4) immediately following placement in the home cage and successive 30 sec intervals in the post-OF recording. The time required for each 20 beat interval was converted to beats per minute for statistical analysis. RESULTS The HR responses elicited by shock and control treatments as well as pretreatment HRs are summarized in Fig. 1. As expected, there was no significant difference between the two groups prior to treatment. HR responses to treatment also followed a predictable pattern. Thus, shocked animals showed much higher HR immediately after return to their home cages. Both PS and Control animals showed deceleration to near basal levels within 15 min, and neither group showed any significant deceleration below basal levels.
0
,. r i .
440
Procedure On Days 1 - 1 0 following arrival in the laboratory, animals were handled and weighed daily. On Day 7 animals were matched according to weight and assigned to either PS or Control groups (n = 20). On Days 1 1 - 1 5 PS and Control animals were placed individually in the shock chambers for 3.5 rain. During the last 3 rain of this time PS animals received continuous shock (4.0 mA). On Days 1 6 - 3 3 all animals were handled and weighed daily and on Days 3 4 - 3 7 OF testing was carried out. Animals were placed individually in the OF and observed for 3 min. Ambulations were scored on a minute-by-minute basis and the total number of fecal boli were counted at the end of 3 min. HR was recorded from one half of the animals from each group during the treatment phase of the experiment and from the other half during OF testing. In the case of the former animals, electrodes for EKG recording were implanted under light ether anesthesia on Day 8. Electrodes were implanted along the dorsal midline, one at the level of the shoulder blades and one immediately posterior to the rib cage. HR was also recorded from these animals on Day 10. Light flexible leads were attached to the electrodes and the animal returned to its home cage. A 10 sec EKG sample was taken 15 min later for a determination of basal or pretreatment HRs. Animals from which HR was to be recorded during OF testing were implanted with electrodes on Day 32. HR was also measured in these animals in their home cages 10 days after the completion of OF testing.
Quantification o f Data HR was determined by measuring the length of time necessary for 20 beat intervals. These measurements were made (1) 15 min after placement in the home cage for the determination of pretreatment basis; (2) immediately and every 15 min up to 1 hr following placement in the home cage during the treatment phase of the experiment; (3) immediately following placement in the OF and at succes-
400 3~
t o _ I o ~..,q ~ eol ~ u~
O--O CONTROL
I I III BASE 0 30 60 0
MINUTES DAY 1
.o.
0~
_ 320
•
I I 30 60
1~1 I 30 60
I t II1 0 30 60 0
I I 30 60
MINUTES MINUTES MINUTES MINUTES DAY 2 DAY 3 DAY 4 DAY 5
FIG. 1. Pretreatment base HRs and HR in the home cage during the first hour after treatment for PS and Control rats. OF ambulation scores are shown in Fig. 2. The marked suppression of activity previously found in PS animals is apparent in this figure and was reflected in a highly significant treatments effect, F(1,32) = 48.5, p
Effects of Prior Aversive Stimulation on Heart Rate Responses to Open Field Exposure in the Rat a DONALD V. CHALMERS,2 SALLYEANA COYLE AND SEYMOUR LEVINE 3
Department o f Psychiatry, Stanford University School o f Medicine Stanford, California 94305
(Received 15 July 1974) CHALMERS, D. V., S. COYLE AND S. LEVINE. Effects o f prior aversive stimulation on heart rate responses to open field exposure in the rat. PHYSIOL. BEHAV. 14(1) 13-16, 1975. - Heart rate (FIR) responses to open field (OF) exposure were compared between rats previously exposed to intense, inescapable electric shock (preshock, PS) and Controls. Results indicated that (1) Control animals showed a steady increase in HR across a 3 rain exposure on each of 4 days of testing, while PS animals showed an initial HR deceleration followed by partial recovery on each day; (2) the HR response of PS animals in the OF was not related to any HR response to shock during treatment; and (3) the HR responses of both PS and Control animals were specific to the OF situation, with both groups showing steady HR deceleration across 3 min after being placed in their home cages. Results were discussed in terms of (1) the apparently altered perception of environmental change produced by PS, and (2) the possible role of HR acceleration in Controls in terms of minimizing the impact of aversive stimulation. Preshock
Open field
Heart rate
Defensereflex
PRIOR exposure to intense, unsignaled and inescapable electric shock (preshock, PS) has been shown to alter the subsequent behavior of rats in the presence of novel [8,15 ] and/or aversive [1,9] stimulation. In connection with these behavioral effects, it has also been observed that PS leads to heightened physiological reactivity as measured by increased plasma corticosterone levels [8, 9, 15] and lower basal resistance levels [ 1 ]. More recently Chalmers et al. [2] found that, although PS did not alter the amplitude of the startle reflex elicited by intense acoustic stimulation, it did alter the nature of the heart rate (HR) response to such stimulation. Thus, while control animals showed HR acceleration, animals exposed to PS showed HR deceleration to the initial stimulus presentations. In discussing these results, Chalmers et al. [2] noted that the strong deceleratory response shown by PS animals resembled the bradycardia described by Hofer [7] for wild rodents in the open field (OF). Since PS animals also show OF behavior similar to that of wild rodents [8,15], a more direct examination of the cardiovascular responses of PS animals in this situation seemed warranted. The HR deceleration observed following startle was also discussed by Chalmers et al. [2] in terms of the theoretical
account of PS effects set forth by Anderson et aL [1]. These authors argued that intense stimulation in test situations aroused pain-produced emotional responses, previo u s l y associated with PS treatment, and that these responses mediated the behavioral effects of PS. Such a mechanism was viewed as unlikely in view of the qualitatively dissimilar HR responses elicited by shock, i.e., HR acceleration, and by startle stimulation in the test situation, i.e., HR deceleration. Although this argument has a priori merit, the possibility does exist that HR deceleration mediated by parasympathetic rebound may follow PS treatment, and that the reproduction of this response in test situations might be involved in PS effects. In addition to comparing the HR responses of PS and control animals in the OF, then, the present study was also designed so that the HR responses up to 1 hr following the PS treatment could be investigated. METHOD
Animals Forty naive, male Sprague-Dawley rats were received from Simonsen Laboratories (Gilroy, CA) at approximately 90 days of age. Animals were housed individually with food
~This study was supported by Research Grant NICH & HD 02881 from the National Institutes of Health, Biological Sciences Training Grant MH 8304 and ONR Contract N00014-67-A-0112-0009. 2Present address: Psychology Department, Illinois State Univ., Normal, IL 61761. aSupported by USPHS Research Scientist Award K5-MH-19936 from the National Institute of Mental Health. Reprint requests should be sent to this author. 13
14 and water available ad lib throughout the experiment except for the brief periods during which HR was recorded in home cages.
Apparatus The apparatus used during the treatment phase of the experiment has been described in detail previously [3]. Briefly, it consisted of two boxes (17.8 x 17.8 x 30.5 cm) located in sound-attenuating wooden chambers. One of the boxes was wired to a Grason-Stadler Shock Generator (Model No. E1064) so that the floor and all four walls could be electrified. The OF has also been described in detail [8]. Briefly, it consists of a circular arena (74.9 cm in dia.) with 31.8 cm high walls painted flat white throughout. Black concentric circles and radii divide the floor into sectors, consisting of a central circle, an inner circle with 6 sectors and an outer circle with 12 sectors. During testing the arena was lighted by two 150 W flood lamps in 22.9 cm aluminum reflectors placed 91.4 cm above the floor, and a white noise background (70 db re 0.0002 dynes/cm 2) provided through an 8.9 cm speaker which was also placed 91.4 cm above the floor.
CHALMERS, COYLE AND LEVINE sive 30 sec intervals during each 3 min exposure; and (4) immediately following placement in the home cage and successive 30 sec intervals in the post-OF recording. The time required for each 20 beat interval was converted to beats per minute for statistical analysis. RESULTS The HR responses elicited by shock and control treatments as well as pretreatment HRs are summarized in Fig. 1. As expected, there was no significant difference between the two groups prior to treatment. HR responses to treatment also followed a predictable pattern. Thus, shocked animals showed much higher HR immediately after return to their home cages. Both PS and Control animals showed deceleration to near basal levels within 15 min, and neither group showed any significant deceleration below basal levels.
0
,. r i .
440
Procedure On Days 1 - 1 0 following arrival in the laboratory, animals were handled and weighed daily. On Day 7 animals were matched according to weight and assigned to either PS or Control groups (n = 20). On Days 1 1 - 1 5 PS and Control animals were placed individually in the shock chambers for 3.5 rain. During the last 3 rain of this time PS animals received continuous shock (4.0 mA). On Days 1 6 - 3 3 all animals were handled and weighed daily and on Days 3 4 - 3 7 OF testing was carried out. Animals were placed individually in the OF and observed for 3 min. Ambulations were scored on a minute-by-minute basis and the total number of fecal boli were counted at the end of 3 min. HR was recorded from one half of the animals from each group during the treatment phase of the experiment and from the other half during OF testing. In the case of the former animals, electrodes for EKG recording were implanted under light ether anesthesia on Day 8. Electrodes were implanted along the dorsal midline, one at the level of the shoulder blades and one immediately posterior to the rib cage. HR was also recorded from these animals on Day 10. Light flexible leads were attached to the electrodes and the animal returned to its home cage. A 10 sec EKG sample was taken 15 min later for a determination of basal or pretreatment HRs. Animals from which HR was to be recorded during OF testing were implanted with electrodes on Day 32. HR was also measured in these animals in their home cages 10 days after the completion of OF testing.
Quantification o f Data HR was determined by measuring the length of time necessary for 20 beat intervals. These measurements were made (1) 15 min after placement in the home cage for the determination of pretreatment basis; (2) immediately and every 15 min up to 1 hr following placement in the home cage during the treatment phase of the experiment; (3) immediately following placement in the OF and at succes-
400 3~
t o _ I o ~..,q ~ eol ~ u~
O--O CONTROL
I I III BASE 0 30 60 0
MINUTES DAY 1
.o.
0~
_ 320
•
I I 30 60
1~1 I 30 60
I t II1 0 30 60 0
I I 30 60
MINUTES MINUTES MINUTES MINUTES DAY 2 DAY 3 DAY 4 DAY 5
FIG. 1. Pretreatment base HRs and HR in the home cage during the first hour after treatment for PS and Control rats. OF ambulation scores are shown in Fig. 2. The marked suppression of activity previously found in PS animals is apparent in this figure and was reflected in a highly significant treatments effect, F(1,32) = 48.5, p
