This article was downloaded by: [Virginia Tech Libraries] On: 27 February 2015, At: 03:21 Publisher: Routledge Informa Ltd Registered in England and Wales Registered Number: 1072954 Registered office: Mortimer House, 37-41 Mortimer Street, London W1T 3JH, UK
Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uear20
Age-related decline in receptivity in normal, neonatally androgenized female and male hamsters a
a
Alice Farrell , Arnold A. Gerall & Mary J. Alexander
a
a
Department of Psychology , Tulane University , New Orleans, Louisiana, 70118 Published online: 27 Sep 2007.
To cite this article: Alice Farrell , Arnold A. Gerall & Mary J. Alexander (1977) Agerelated decline in receptivity in normal, neonatally androgenized female and male hamsters, Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process, 3:2, 117-128, DOI: 10.1080/03610737708257093 To link to this article: http://dx.doi.org/10.1080/03610737708257093
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages,
and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
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This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
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117
AGE-RELATED DECLINE IN RECEPTIVITY IN NORMAL, NEONATALLY ANDROGENIZED FEMALE AND MALE HAMSTERS ALICE FARRELL, ARNOLD A. GERALL and MARY J. ALEXANDER Dcfiartrnent of Psychology Tulane University New Orleans, Louisiana 701 18
Farrell, A., Gerall, A. A., & Alexander, M. J. Age-related decline in receptivity in normal, neonatally androgenized female and male hamsters. Experimental Aging Research, 1977, 3, (21, 117-128. The pattern of female sexual behavior shown by aging male and female hamsters was related to exposure to perinatal androgen. Twenty-five female and 37 male hamsters in Experiment 1 were gonadectomized on the day of birth or a t 43 days of age. They received 11 tests for receptivity between the ages of 28 and 66 wk. In Experiment 2, 83 females were implanted with a Silastic pellet containing 0, 1, 3 or 9% testosterone (T) or testosterone propionate ( T P ) by weight from the second to t h e tenth day of life, and tested approximately army 2 wk from 22 to 58 wk of age. Receptivity was induced by estradiol benzoate and progesterone injected before each 600 sec mating test. Normal females exhibited the highest lordosis scores, followed by minimally androgenized females and males castrated a t birth. High doses of exogenous or endogenous perinatal T suppressed receptivity throughout the animal’s lifespan, but did not accelerate the rate of decline in female behavior over time. Non-androgenized animals showed the greatest decrease in receptivity with advanced age.
This study was supported by Research Grant HD-00867-10 from the National Institute of Child Welfare and Human Development, USPHS. A preliminary report of part of this study was given a t the Eastern Regional Conference on Reproduction, Nags Head, North Carolina, 1975. Appreiation is expressed to Silas Brady of Dow Corning Corporation for providing Silastic 382.
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
118
FARRELL/GERALL/ ALEXANDER
This research is part of an effort to identify factors p r e p n t during the perinatal period that influence reproductive competence throughout an animal’s life-span. Other investigators have described age-related changes in the behavior of old male rats (Larsson, 1958; Larsson & Essberg, 1962) and male guinea pigs (Jakubezak, 1964), but to our knowledge, the comparable study has not been done using female hamsters. In the present study changes in the receptivity of male and female hamsters were related to two factors: the age of the animal when tested, ranging from young adulthood to advanced age, and the presence of naturally-ocurring or exogenously administered testosterone during the neonatal developmental period. Female rodents injected with relatively large amounts of testosteronejjropionate (TP) perinatally become permanently anovulatory and non-receptive (Barraclough & Gorski, 1962). Males castrated neonatally can support ovulatory ovaries and exhibit the complete receptive pattern when provided with estrogen and progesterone (Gerall, Hendricks, Johnson, & Bounds, 1967; Grady, Phoenix, & Young, 1965; Yazaki, 1960). Two actions of testosterone, one in the female and the other in the male, encourage the consideration that this hormone influences the longevity of reproductive function. First, when TP is administered in amounts less than 3 0 4 g before the eighth day of life, female rats can have a relatively long period of reproductive competence before becoming sterile (Arai, 1972; Gorski, 1968; Swanson & van der Waff ten Bosch, 1964). During the interval preceding the onset of sterility, estrous cycles become irregular and fewer offsprings are born after each pregnancy (Swanson & van der Werff ten Bosch, 1964). These characteristics are shared by many aging female rats. The terminal state of these animals consists of persistent vaginal cornification and anovulatory ovaries (Aschheim, 1976; Clemens & Meites, 1971; Mandl & Shelton, 1959). Swanson and van der Werff ten Bosch (1964) suggested that prenatal androgen prematurely ages female rodents. Secondly, the intensity of castrated males’ receptive behavior is age-dependent (Dunlap, Gerall, & Hendricks, 1972). They lose the capacity to respond to estrogen and progesterone sooner than females, perhaps because they have been exposed to prenatal androgen. The present research set
RECEPTIVITY IN ANDROGENIZED
HAMSTERS
1 19
out to describe the decline in receptivity of male and female hamsteqs with age and to determine whether exposure to T P accelerated the rate of decline induced by estrogen and progesterone.
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
METHOD Subjects One hundred and forty-five golden hamsters (Mesocricetus auratus) born to parents originally obtained from Charles River Breeding Laboratories, Wilmington, Ma. served as subjects. The 25 females and 37 males in Experiment 1, and 83 females in Experiment 2 were weaned at 21 days of age and then housed i n groups of 1 to 6 in polyethylene cages measuring 30 x 36 x 15 cm. ,A 14-10 light-dark reversed illumination cycle was used, the dark period beginning at 1300 h. Purina Lab Chow and water were available at all times. Design and Procedure I n Experiment 1, animals of both sexes were gonadectomized either within 6 h of birth using cryogenic anesthesia or 43 days after birth under ether. All animals had participated in a previous study (Gerall & Thiel, 1975) in which they had received 8 weekly tests for female sexual behavior beginning at the eighth or sixteenth week of life. In the present study, tests for receptivity were given at 28, 36, 40 and 44 wk of age. After a three-month interval, 3 weekly tests were administered at 56, 57 and 58 wk of age, followed by 4 bimonthly tests. As in any study of aging, animals died during the course of the study. From an original sample of 86 animals, 62 survived until 66 wk of age. The analyses and pictorial representation of the data are based only on these survivors. The number of animals1 in each group used in the analyses is indicated in Table 1. Receptivity was induced by injecting 6.64 g/100 g body weight estradiol benzoate (EB) 48 and 24 h and 0.5 mg/100 g body weight progesterone (P) 4 h before being placed with males. Animals were teslted under dim illumination in arenas measuring 51 x 38 x
FARRELL/GERALL/ALEXANDER
120
TABLE 1 Design and Number of Animals per Group in Experiment 1
Males
Females
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
Day of Gonadectomy Age at Initial Test
Day 1
Day 43
Day 1
Day 43
Eight weeks
6
6
10
8
Sixteen weeks
8
6
8
11
47 cm. Each animal was allowed to adapt for 2 to 3 min before introduction of a vigorous male. During each 600 sec. session, the number and duration of each lordosb were recorded on an Esterline-Angus event recorder.
Experiment 2 consisted of a series of 17 tests for receptivity in female hamster? neonatally treated with testosterone (T) , testosterone propionate ('IF) or neutral Silastic. The hormone was administered in Silastic pellets containing 0, 1, 3 or 9% T by weight; the 3 mm long and 0.8 mm diameter pellets were implanted subcutaneously on Day 2 (Day 1 being day of birth) and removed on Day 10. Animals were ovariectomized at approximately 60 days of age and given 4 tests for female behavior at 11, 12, 13 and 17 wk of age. The results of these early tests are described by Gottlieb, Gerall, & Thiel (1974). On the basis of these data, 153 females were assigned to one of 4 groups which differed in degree of receptivity. The designation and original treatments of each group and number of animals surviving to the end of the study are listed in Table 2. Only scores from animals alive at 58 wk of age were analyzed.
RECEPTIVITY IN ANDROGEWZED HAMSTERS
121
TABLE 2 Number of Animals in. Experiment 2, Using Groups Based on Initial Receptivity
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
Receptivity Level
Neonatal Treatment
Number of Animals
1 (highest)
0% androgen
2
T P 1% and T P 3%
?
3
TP 9% and T 1%
30
4 (lowest)
T 3% and T 9%
25
19
The data in the current study were obtained in tests given when the animals were between 22 and 58 wks of age. Tests were given approximately every 2 wk with two exceptions: a 5-wk interval between tests at ages 30 and 35 wk, and a 3-wk interval between 41 and 44 wk. Animals were primed with 6u g/100 g body weight EB injected 52 and 28 h and 0.5 mg/100 g body weight P 4 h before testing. Test conditions and procedures were the same as described above for Experiment 1. An unweighted means analysis of variance was performed on data obtained in both experiments.
RESULTS Experiment 1 Whether the hamsters had their first mating test at 8 or 16 wk of age was not a significant factor in the pattern of scores obtained during the 11 mating tests started when they were 28 wk old, p r 0 . 0 5 . The factors of age of gonadectomy and sex as well as the interaction between them were statistically significant. Total lordosis duration was higher in females than in males, 1370.01, and in animals gonadectomized at 1 than at 43 days of age, p < 0.01. The interaction, PCO.01 was due to the much greater effect
Age (Weeks)
28 32364044485256606468
I U
@--@Females Day I and 43 U---OMales Day I 6-HMaIes Day 43
Fig. 1 . Total lordosis duration as a function of age for male and female animals in Experiment 1.
\
a?
'
\
480 .o 420 Q p 360 30C 3 24C b 18C 4 ' b 12c I? 6C C-
-2 540
-
600 -
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
w w
c
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
RECEPTIVITY IN ANDRBGENIZED HAMSTERS
123
age of gonadectomy had on males than on females. Whereas males castrated on the day of birth manifested significantly longer lordosis durations than males gonadectomized when 43 dayp old, (in the order of 300-400-ser),the difference between the females ovariectomized at 1 and 43 days was always less than 50 sec. The difference in lordosis duration between the two male groups was significant, ~ ( 0 . 0 1 , while it was not between the female groups, p 7 0 . 0 5 . Because female groups did not differ from each other and showed the same change of scores with age, ~ 7 0 . 0 5 ,their scores were averaged to simplify presentation. The change in total lordosis scores with age for the averaged female and two male groups is shown in Figure 1. Total duration of lordosis decreased gradually with age in all groups. The males castrated at 43 days showed the least decrease from their first test at 28 wk. The female and Day-1 castrated male group$. appear to be decreasing at slightly different rates, as indicated by the relatively larger difference in performance on the first series of tests than that in later ones. Inspection of these scores suggests that the 3 groups are converging toward the same low level at the older ages. The differential rate of decline among the groups is supported by a significant interaction among the factors of sex, age of gonadectomy and tests, p
Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process Publication details, including instructions for authors and subscription information: http://www.tandfonline.com/loi/uear20
Age-related decline in receptivity in normal, neonatally androgenized female and male hamsters a
a
Alice Farrell , Arnold A. Gerall & Mary J. Alexander
a
a
Department of Psychology , Tulane University , New Orleans, Louisiana, 70118 Published online: 27 Sep 2007.
To cite this article: Alice Farrell , Arnold A. Gerall & Mary J. Alexander (1977) Agerelated decline in receptivity in normal, neonatally androgenized female and male hamsters, Experimental Aging Research: An International Journal Devoted to the Scientific Study of the Aging Process, 3:2, 117-128, DOI: 10.1080/03610737708257093 To link to this article: http://dx.doi.org/10.1080/03610737708257093
PLEASE SCROLL DOWN FOR ARTICLE Taylor & Francis makes every effort to ensure the accuracy of all the information (the “Content”) contained in the publications on our platform. However, Taylor & Francis, our agents, and our licensors make no representations or warranties whatsoever as to the accuracy, completeness, or suitability for any purpose of the Content. Any opinions and views expressed in this publication are the opinions and views of the authors, and are not the views of or endorsed by Taylor & Francis. The accuracy of the Content should not be relied upon and should be independently verified with primary sources of information. Taylor and Francis shall not be liable for any losses, actions, claims, proceedings, demands, costs, expenses, damages,
and other liabilities whatsoever or howsoever caused arising directly or indirectly in connection with, in relation to or arising out of the use of the Content.
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
This article may be used for research, teaching, and private study purposes. Any substantial or systematic reproduction, redistribution, reselling, loan, sub-licensing, systematic supply, or distribution in any form to anyone is expressly forbidden. Terms & Conditions of access and use can be found at http://www.tandfonline.com/page/terms-and-conditions
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
117
AGE-RELATED DECLINE IN RECEPTIVITY IN NORMAL, NEONATALLY ANDROGENIZED FEMALE AND MALE HAMSTERS ALICE FARRELL, ARNOLD A. GERALL and MARY J. ALEXANDER Dcfiartrnent of Psychology Tulane University New Orleans, Louisiana 701 18
Farrell, A., Gerall, A. A., & Alexander, M. J. Age-related decline in receptivity in normal, neonatally androgenized female and male hamsters. Experimental Aging Research, 1977, 3, (21, 117-128. The pattern of female sexual behavior shown by aging male and female hamsters was related to exposure to perinatal androgen. Twenty-five female and 37 male hamsters in Experiment 1 were gonadectomized on the day of birth or a t 43 days of age. They received 11 tests for receptivity between the ages of 28 and 66 wk. In Experiment 2, 83 females were implanted with a Silastic pellet containing 0, 1, 3 or 9% testosterone (T) or testosterone propionate ( T P ) by weight from the second to t h e tenth day of life, and tested approximately army 2 wk from 22 to 58 wk of age. Receptivity was induced by estradiol benzoate and progesterone injected before each 600 sec mating test. Normal females exhibited the highest lordosis scores, followed by minimally androgenized females and males castrated a t birth. High doses of exogenous or endogenous perinatal T suppressed receptivity throughout the animal’s lifespan, but did not accelerate the rate of decline in female behavior over time. Non-androgenized animals showed the greatest decrease in receptivity with advanced age.
This study was supported by Research Grant HD-00867-10 from the National Institute of Child Welfare and Human Development, USPHS. A preliminary report of part of this study was given a t the Eastern Regional Conference on Reproduction, Nags Head, North Carolina, 1975. Appreiation is expressed to Silas Brady of Dow Corning Corporation for providing Silastic 382.
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
118
FARRELL/GERALL/ ALEXANDER
This research is part of an effort to identify factors p r e p n t during the perinatal period that influence reproductive competence throughout an animal’s life-span. Other investigators have described age-related changes in the behavior of old male rats (Larsson, 1958; Larsson & Essberg, 1962) and male guinea pigs (Jakubezak, 1964), but to our knowledge, the comparable study has not been done using female hamsters. In the present study changes in the receptivity of male and female hamsters were related to two factors: the age of the animal when tested, ranging from young adulthood to advanced age, and the presence of naturally-ocurring or exogenously administered testosterone during the neonatal developmental period. Female rodents injected with relatively large amounts of testosteronejjropionate (TP) perinatally become permanently anovulatory and non-receptive (Barraclough & Gorski, 1962). Males castrated neonatally can support ovulatory ovaries and exhibit the complete receptive pattern when provided with estrogen and progesterone (Gerall, Hendricks, Johnson, & Bounds, 1967; Grady, Phoenix, & Young, 1965; Yazaki, 1960). Two actions of testosterone, one in the female and the other in the male, encourage the consideration that this hormone influences the longevity of reproductive function. First, when TP is administered in amounts less than 3 0 4 g before the eighth day of life, female rats can have a relatively long period of reproductive competence before becoming sterile (Arai, 1972; Gorski, 1968; Swanson & van der Waff ten Bosch, 1964). During the interval preceding the onset of sterility, estrous cycles become irregular and fewer offsprings are born after each pregnancy (Swanson & van der Werff ten Bosch, 1964). These characteristics are shared by many aging female rats. The terminal state of these animals consists of persistent vaginal cornification and anovulatory ovaries (Aschheim, 1976; Clemens & Meites, 1971; Mandl & Shelton, 1959). Swanson and van der Werff ten Bosch (1964) suggested that prenatal androgen prematurely ages female rodents. Secondly, the intensity of castrated males’ receptive behavior is age-dependent (Dunlap, Gerall, & Hendricks, 1972). They lose the capacity to respond to estrogen and progesterone sooner than females, perhaps because they have been exposed to prenatal androgen. The present research set
RECEPTIVITY IN ANDROGENIZED
HAMSTERS
1 19
out to describe the decline in receptivity of male and female hamsteqs with age and to determine whether exposure to T P accelerated the rate of decline induced by estrogen and progesterone.
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
METHOD Subjects One hundred and forty-five golden hamsters (Mesocricetus auratus) born to parents originally obtained from Charles River Breeding Laboratories, Wilmington, Ma. served as subjects. The 25 females and 37 males in Experiment 1, and 83 females in Experiment 2 were weaned at 21 days of age and then housed i n groups of 1 to 6 in polyethylene cages measuring 30 x 36 x 15 cm. ,A 14-10 light-dark reversed illumination cycle was used, the dark period beginning at 1300 h. Purina Lab Chow and water were available at all times. Design and Procedure I n Experiment 1, animals of both sexes were gonadectomized either within 6 h of birth using cryogenic anesthesia or 43 days after birth under ether. All animals had participated in a previous study (Gerall & Thiel, 1975) in which they had received 8 weekly tests for female sexual behavior beginning at the eighth or sixteenth week of life. In the present study, tests for receptivity were given at 28, 36, 40 and 44 wk of age. After a three-month interval, 3 weekly tests were administered at 56, 57 and 58 wk of age, followed by 4 bimonthly tests. As in any study of aging, animals died during the course of the study. From an original sample of 86 animals, 62 survived until 66 wk of age. The analyses and pictorial representation of the data are based only on these survivors. The number of animals1 in each group used in the analyses is indicated in Table 1. Receptivity was induced by injecting 6.64 g/100 g body weight estradiol benzoate (EB) 48 and 24 h and 0.5 mg/100 g body weight progesterone (P) 4 h before being placed with males. Animals were teslted under dim illumination in arenas measuring 51 x 38 x
FARRELL/GERALL/ALEXANDER
120
TABLE 1 Design and Number of Animals per Group in Experiment 1
Males
Females
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
Day of Gonadectomy Age at Initial Test
Day 1
Day 43
Day 1
Day 43
Eight weeks
6
6
10
8
Sixteen weeks
8
6
8
11
47 cm. Each animal was allowed to adapt for 2 to 3 min before introduction of a vigorous male. During each 600 sec. session, the number and duration of each lordosb were recorded on an Esterline-Angus event recorder.
Experiment 2 consisted of a series of 17 tests for receptivity in female hamster? neonatally treated with testosterone (T) , testosterone propionate ('IF) or neutral Silastic. The hormone was administered in Silastic pellets containing 0, 1, 3 or 9% T by weight; the 3 mm long and 0.8 mm diameter pellets were implanted subcutaneously on Day 2 (Day 1 being day of birth) and removed on Day 10. Animals were ovariectomized at approximately 60 days of age and given 4 tests for female behavior at 11, 12, 13 and 17 wk of age. The results of these early tests are described by Gottlieb, Gerall, & Thiel (1974). On the basis of these data, 153 females were assigned to one of 4 groups which differed in degree of receptivity. The designation and original treatments of each group and number of animals surviving to the end of the study are listed in Table 2. Only scores from animals alive at 58 wk of age were analyzed.
RECEPTIVITY IN ANDROGEWZED HAMSTERS
121
TABLE 2 Number of Animals in. Experiment 2, Using Groups Based on Initial Receptivity
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
Receptivity Level
Neonatal Treatment
Number of Animals
1 (highest)
0% androgen
2
T P 1% and T P 3%
?
3
TP 9% and T 1%
30
4 (lowest)
T 3% and T 9%
25
19
The data in the current study were obtained in tests given when the animals were between 22 and 58 wks of age. Tests were given approximately every 2 wk with two exceptions: a 5-wk interval between tests at ages 30 and 35 wk, and a 3-wk interval between 41 and 44 wk. Animals were primed with 6u g/100 g body weight EB injected 52 and 28 h and 0.5 mg/100 g body weight P 4 h before testing. Test conditions and procedures were the same as described above for Experiment 1. An unweighted means analysis of variance was performed on data obtained in both experiments.
RESULTS Experiment 1 Whether the hamsters had their first mating test at 8 or 16 wk of age was not a significant factor in the pattern of scores obtained during the 11 mating tests started when they were 28 wk old, p r 0 . 0 5 . The factors of age of gonadectomy and sex as well as the interaction between them were statistically significant. Total lordosis duration was higher in females than in males, 1370.01, and in animals gonadectomized at 1 than at 43 days of age, p < 0.01. The interaction, PCO.01 was due to the much greater effect
Age (Weeks)
28 32364044485256606468
I U
@--@Females Day I and 43 U---OMales Day I 6-HMaIes Day 43
Fig. 1 . Total lordosis duration as a function of age for male and female animals in Experiment 1.
\
a?
'
\
480 .o 420 Q p 360 30C 3 24C b 18C 4 ' b 12c I? 6C C-
-2 540
-
600 -
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
w w
c
Downloaded by [Virginia Tech Libraries] at 03:21 27 February 2015
RECEPTIVITY IN ANDRBGENIZED HAMSTERS
123
age of gonadectomy had on males than on females. Whereas males castrated on the day of birth manifested significantly longer lordosis durations than males gonadectomized when 43 dayp old, (in the order of 300-400-ser),the difference between the females ovariectomized at 1 and 43 days was always less than 50 sec. The difference in lordosis duration between the two male groups was significant, ~ ( 0 . 0 1 , while it was not between the female groups, p 7 0 . 0 5 . Because female groups did not differ from each other and showed the same change of scores with age, ~ 7 0 . 0 5 ,their scores were averaged to simplify presentation. The change in total lordosis scores with age for the averaged female and two male groups is shown in Figure 1. Total duration of lordosis decreased gradually with age in all groups. The males castrated at 43 days showed the least decrease from their first test at 28 wk. The female and Day-1 castrated male group$. appear to be decreasing at slightly different rates, as indicated by the relatively larger difference in performance on the first series of tests than that in later ones. Inspection of these scores suggests that the 3 groups are converging toward the same low level at the older ages. The differential rate of decline among the groups is supported by a significant interaction among the factors of sex, age of gonadectomy and tests, p
