gestational stress: effects on open-field behaviour and heart rate reactivity in rat offspring

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Biological Psychology, 3,1975,231-236. @ North-Holland PubIishing Company GESTATIONAL STRESS : EFFECTS ON OPEN-FIELD BEHAVIOUR AND HEART RATE REACTIVITY IN RAT OFFSPRING ALAN JOLLEY* and JAN H. ADAM Department of Psychology, University College, Card& U.K. Accepted for publication 29 May 1975 Home-cage heart rate (HR) and open-field defecation, ambulation, rearing and HR, were recorded in the offspring of mothers who had been exposed to stress during gestation. Com- pared with controls, experimental animals showed no significant differences in ambulation and rearing, while defecation was significantly lower. The only significant finding on HR was an increase from home-cage level to open-field level in the experimental group. The results confirmed previous findings that illumination level is a useful independent variable in ges- tational stress studies, and suggested that different types of HR measure yield a similar picture of the HR/defecation relationship, which appears to be a negative function. These conclusions were discussed in the light of other findings in this area, and traditional assump- tions about the emotionality construct were questioned. 1. Introduction Recent work has shown that exposing pregnant rats to high-intensity illumin- ation relative to maintenance level, resulted in significant changes in off- spring behaviour (Jolley and Dreesman, 1973). More precisely, open-field HR was significantly elevated, while defecation was reduced as a result of the treatment. Ambulation scores did not differ from those of a control group. Apart from demonstrating the potential of a simpler method of administering experimental stress to the mothers than the traditional ‘conditioned anxiety’ technique, the specific results of the experiment pose some problems of inter- pretation. Defecation has long been employed as a measure of emotional reactivity in animals (Hall, 1934; Broadhurst, 1960). Similarly HR has also been trad- itionally viewed as an index of emotional state, since Cannon’s (1929) work on the ‘emergency reaction’. A positive relationship might therefore be pre- dicted between defecation and HR in an open-field situation. The findings of Jolley and Dreesman (1973) do not support this prediction. However, Archer * Address for correspondence: Dr. Alan Jolley, Department of Psychology, University College, Cardiff, U.K. 231

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Biological Psychology, 3,1975,231-236. @ North-Holland PubIishing Company

GESTATIONAL STRESS : EFFECTS ON OPEN-FIELD

BEHAVIOUR AND HEART RATE REACTIVITY IN

RAT OFFSPRING

ALAN JOLLEY* and JAN H. ADAM

Department of Psychology, University College, Card& U.K.

Accepted for publication 29 May 1975

Home-cage heart rate (HR) and open-field defecation, ambulation, rearing and HR, were recorded in the offspring of mothers who had been exposed to stress during gestation. Com- pared with controls, experimental animals showed no significant differences in ambulation and rearing, while defecation was significantly lower. The only significant finding on HR was an increase from home-cage level to open-field level in the experimental group. The results confirmed previous findings that illumination level is a useful independent variable in ges- tational stress studies, and suggested that different types of HR measure yield a similar picture of the HR/defecation relationship, which appears to be a negative function. These conclusions were discussed in the light of other findings in this area, and traditional assump- tions about the emotionality construct were questioned.

1. Introduction

Recent work has shown that exposing pregnant rats to high-intensity illumin- ation relative to maintenance level, resulted in significant changes in off- spring behaviour (Jolley and Dreesman, 1973). More precisely, open-field HR was significantly elevated, while defecation was reduced as a result of the treatment. Ambulation scores did not differ from those of a control group. Apart from demonstrating the potential of a simpler method of administering experimental stress to the mothers than the traditional ‘conditioned anxiety’ technique, the specific results of the experiment pose some problems of inter- pretation.

Defecation has long been employed as a measure of emotional reactivity in animals (Hall, 1934; Broadhurst, 1960). Similarly HR has also been trad- itionally viewed as an index of emotional state, since Cannon’s (1929) work on the ‘emergency reaction’. A positive relationship might therefore be pre- dicted between defecation and HR in an open-field situation. The findings of Jolley and Dreesman (1973) do not support this prediction. However, Archer

* Address for correspondence: Dr. Alan Jolley, Department of Psychology, University College, Cardiff, U.K.

231

232 A. Jolly and J. H. Adam

(1973) has reviewed in some detail a number of conflicting findings on the relationship between the two variables, and suggests that one important factor in determining the nature of the relationship may be the particular type of HR measure employed (whether an absolute level or degree of change).

In the experiment by Jolley and Dreesman (1973) only absolute levels of open-field HR were recorded. A measure of HR reactivity (the difference between home-cage resting level and open-field level) might show a positive relationship to defecation, despite the finding that open-field HR itself does not. It is not difficult to suggest how this could come about. The effects of gestational stress might be to elevate resting HR above that of controls. HR reactivity would thus be attenuated in the experimental animals. This follows from the law of initial value which states that the higher the initial level of an autonomic function the smaller will be the increment following a standard stimulus (Wilder, 1950). In addition, the concept of emotionality seems to involve the idea of ‘degree of responsiveness’ to stimuli; a point which further suggests that HR reactivity may be a more appropriate index of emotionality than HR level.

This present study, therefore, has a twofold aim : firstly to attempt to con- firm the initial findings of Jolley and Dreesman (1973), that increased illu- mination intensity during gestation has an effect on offspring behaviour; and secondly, to investigate further the relationship between HR reactivity and defecation. In addition, open-field ambulation and rearing were recorded from the offspring, and emotional defecation was measured in the pregnant females during treatment, in an attempt to provide extra information con- cerning the emotional state of the subjects.

2. Method 2.1. Subjects

The subjects were 20 female rats of the Carworth CFE strain aged 90 days, and their offspring. Of the 20 females, 10 were randomly chosen as foster-mothers. The remainder were divided equally and randomly into an experimental and a control group.

2.2. Apparatus A circular open field 83.2 cm in dia., with an illumination level of 15.3 lx, and a 78 dB level of white noise (Broadhurst, 1960) was used for offspring testing. The open field was situated in an electrically screened cubicle, and a closed circuit television system allowed observations of behaviour to be made from outside the cubicle.

Offspring open-field HR was recorded from two stainless steel wire-loop electrodes, implanted subdermally on the back of the animal (Word, Stern, Sines and McDonald, 1959), and attached via miniature crocodile clips and lightweight screened leads to a slip-ring system mounted centrally above the

Gestational stress and offspring emotionality 233

open field. From there the signal was fed to an amplifier, and finally to a Southern Instruments UV polygraph. Details of the construction of the slip- ring system are published elsewhere (Jolley and Thomas, 1973). The same basic ‘trailing-wires’ technique was also used for recording home-cage resting HR from the animal although the slip-ring system was not required, since movement of the animal in its home cage was relatively restricted compared with the open-field situation. A stabilimeter platform (LeHigh Valley) recorded the activity of the females during treatment.

2.3. Procedure The 20 females were each placed with a male of the same age and strain for five days. After removal of the males the five females of the experimental group were exposed to an illumination level of 15.3 lx for 5 min on 14 consecutive days ceasing two days before the first possible date of parturition. The animal was transported in its home cage, from the animal house to the screened cubicle, and placed on the stabilimeter platform in the centre of the open field. The white noise generator was not switched on. Females of the control group received the same treatment except that the illumination level of the open field was set at 0.07 lx, to correspond with mean maintenance illumination intensity. The activity and emotional defecation (number of fecal boluses deposited) of both groups were recorded during the treatment each day. The treatment was carried out at approximately the mid-point of the 12-hr ‘lights- on’ period of the animal house lighting schedule. Temperature during treat- ment ranged from 20.0 to 23.O”C, with mean temperature of the animal house at 22.2’C.

All litters in the experimental and control groups were given to untreated foster-mothers at birth to control for postnatal maternal effects on offspring behaviour. At weaning (21 days old) offspring were housed three to a cage, randomly across litters, within each group. The number of offspring for testing were 39 experimental and 29 control animals.

Three males and three females from each group had electrodes implanted four days before home-cage HR recording took place. To secure these records HR leads were attached to the animals in their home cages and left for a period of 30 min before 10 set of HR recording was taken. The whole pro- cedure was repeated on three consecutive days, and a mean level of resting HR was calculated for the whole period. On the following day (at 40 days old) a IO-set sample of HR was recorded immediately after placement in the open field, and a mean level for each group was calculated. Open-field ambulation was also noted during the IO-set period.

All the other offspring in the experiment were also tested at 40 days old. Subjects were given a 3-min trial in the open field. The temperature of the open field was set at 22.2”C (mean maintenance temperature) prior to each trial. The number of fecal boluses deposited was counted as a measure of emotional

234 A. Jolley and J. H. Adam

elimination. Ambulation was recorded by counting the number of floor segments entered during the trial. Frequency of rearing was also noted. After each trial boluses were removed, and the floor wiped over with a damp cloth.

3. Results From table 1 it is clear that activity of the experimental females was not a confounded variable in determining offspring effects. It is also evident that the independent variable chosen acted as a stressor to the pregnant females, as indicated by the emotional defecation scores. Open-field defecation in the experimental offspring was significantly lower than in the control group, while ambulation and rearing appeared unaffected by the maternal treatment (table 2). Table 3 suggests that the only significant effect of the treatment on offspring HR was an increase from resting level to open-field level in the experimental group. In addition, no between-group differences in ambulation were found during HR recording in the open field (U = 12, p > 0.05).

4. Discussion The results confirm those of Jolley and Dreesman (1973), and strengthen the

Table 1. Median values of activity (stabilimeter movements) and defecation (fecal boluses) of pregnant females recorded during treatment over 14 days.

Experimental Control Mann- P group group Whitney (two-tailed

(N=5) (N= 5) test test)

Activity 224 242 U=8 > 0.05 Defecation 5 1 u=o 0.004

Table 2. Median values of defecation (fecal boluses), ambulation (open-field seg- ments crossed) and rearing (number of times forefeet leave ground)

during offspring open-field test.

Mann- Whitney

Experimental Control test P group group (z value (two-tailed

(N = 33) (N= 23) when nz > 20) test)

Defecation 2 5 z = 2.77 0.006 Ambulation 69 68 z = 0.94 > 0.05 Rearing* 12 18 lJ=73 > 0.05

* Data available for only 13 subjects in each group.

GestationaI stress and offspring emotionality 235

Table 3. Mean values (beatslmin) of offspring heart rate.

Resting HR

P Open-field Wilcoxon (two-tailed

HR test test) -

Experimental group (N = 6) Control group (N = 6)

390 425.3 T=O < 0.01

390 385.3 T=l > 0.05

proposition that illumination level is a useful independent variable in the investigation of prenatal maternal stress effects on offspring behaviour.

The finding of no between-group differences in ambulation and rearing argues against the possibility of increased physical activity producing the HR changes. It also suggests that open-field ambulation and rearing are not very sensitive measures of emotionality differences, at least in the prenatal stress

context. There is no support from the HR data for the hypothesis that gestational

stress attenuates HR reactivity via changes in resting level : mean resting HR in each group of offspring was identical. An interesting aspect of these results concerns the complete non-reactivity of HR in the control group, where no significant difference was found between resting level and open-field HR. This suggests that increased HR is not always a simple direct response to stressful stimuli. Indeed, although Graham and Clifton (1966) and Blizard (1971a, 1971b) have reported instances of HR acceleration in response to stimuli similar to those of the open field, others (Holdstock and Schwarzbaum, 1965; Horvath, Kirby and Smith, 1971) have found decreases. And Archer (1973), in discussing these discrepancies also points out, paraphrasing Lacey (1967), ‘ . . . that some situations normally associated with alertness and arousal produce cardiac deceleration or stabilization in human subjects’. The factors responsible for these discrepancies in findings are not clear, although obvious candidates are the level of physical activity, genotype of subjects, and the precise nature of the stressful stimuli. In this experiment, the HR data of the control group suggest an instance of cardiac stabilization in CFE rats. On the other hand, HR changes in the experimental offspring indicate that prenatal stress sensitizes the cardiovascular system to the effects of the open field.

In any event, it is clear that the type of HR measure employed (level or response) in this context, has no bearing on the nature of the defecation/HR function, which appears to be an inverse relationship. The interpretation of this relationship, in terms of the emotionality construct, has still to be under- taken.

236 A. Jo&y a&J. H. Adam

AS a first step, the assumption that emotiona~ity is simpiy reflected by a

unified change in autonomically innervated end-organs must be discarded.

Acknowledgement The authors would like to thank Mr. Russell Thomas for his help in carrying

out the experiment.

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205-235. Blizard, D. (1971a). Autonomic reactivity in the rat: etfects of genetic selection for emotion-

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Horvath, T., Kirby, H. W. and Smith, A. A. (1971). Rat’s heart rate and grooming activity in the open field. Jouwzal of Comparative and Physiolugical Psychology, 76,449-453.

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