Differences in Maternal Responsiveness Bet ween Lactating and Sensitized Rats

ROBERT BRIDGES M. X. ZARROW

RONALD GANDELMAN VICTOR H. DENENBERG

Department of Biobehavioral Sciences The University of Connecticut

Storrs, Connecticut

Retrieval in lactating females, sensitized virgin females, and sensitized adult male rats was compared in a T-maze extension of the home cage. The percent of lactating females that retrieved was significantly greater than in either the sensitized virgin or sensitized male groups. No difference was found between the two sensitized groups. The data are discussed in terms of the hormonal involvement in maternal behavior.

Recent studies suggest that pregnancy and parturition may not be essential for the elicitation of maternal behavior in certain mammals. Beniest-Noirot (1958) reported that both virgin female and male mice exhibited maternal activities similar to those exhibited by lactating mice. Rosenblatt (1967) found that adult intact and castrate male and adult intact, hypophysectomized, and castrate virgin female rats exhibited maternal behavior after being sensitized by exposure to pups for approximately 1 week. He proposed that the nonparturient rat has a basic level of maternal responsiveness which is, ostensibly, independent of hormone action.

Both Beniest-Noirot (1958) and Rosenblatt (1967) tested for maternal behavior in the home cages. When Gandelman, Zarrow, and Denenberg (1 970) required lactating and virgin mice to traverse a runway to retrieve pups, they found that a significantly greater percentage of lactating females retrieved than did virgins, concluding that virgin female mice could be differentiated from lactating mice on the basis of maternal responsiveness.

The present study extends the findings on the mouse to the rat by comparing the maternal responsiveness of lactating animah to that of sensitized virgin females and sensitized males in the runway-retrieval situation. In addition, the design permits an examination of the stimuli involved in controlling pup retrieval by giving the subject a choice between a live and a dead pup.

Received for publication 23 March 197 1 Developmental Psychobiology, S(2): 123-127 (1972) 0 1972 by John Wiley & Sons, Inc.

123

124 BRIDGES ET AL.

Method

Subjects

Purdue-Wistar rats, aged 80-120 days, were divided into the following 3 groups of 14 animals each: pregnant, adult virgin female, and adult male. They were maintained on a free feeding schedule, were kept on a 13:11 hour light-dark cycle, and were placed into individual translucent plastic cages (9 X 17-1/2 X 6 in.) (22 X 43 X 15 cm) at least 3 days prior to testing.

Procedure

Sensitization

Ths consisted of scattering 3 fresh pups, age 3-12 days, in the home cage of the experimental animal. If the rat retrieved all 3 pups and grouped them within a 10-min observation period on 2 successive test days, the subject was considered sensitized. The 3 pups were left in the home cage with the test animal after the observation period and were removed prior to testing the following day. Three fresh pups were then put in, and the adult was observed for retrieving. If the test animal failed to become sensitized within 15 days, it was eliminated from the experiment.

Apparatus

For testing, a clear Plexiglas T-maze was attached to the home cage. The arms and stem of the maze were 4 X 14 X 3-3/4 inches high (10 X 36 X 8 cm). A removable top covered the maze. All home cages had an opening (5 X 4 in.) (13 X 10 cm) cut into one end to accommodate the insertion of the T-maze. The opening was covered with a sliding metal door between tests.

Testing

Sensitized virgin females and adult males were tested 1 day after sensitization was completed. Testing commenced for the lactating subjects, whose litters had been culled to 6 pups, 1 day after parturition.

Two test pups were obtained on each test day from a donor mother. The test pups were 2-day old on Day 1 of testing, and their ages progressively increased over the 6-day experimental period. One of the test pups was lulled with sodium pentobarbital (Diabutal, Diamond Laboratories). Five min later, both the dead pup and the live pup were placed in opposite ends of the T-maze arms, approximately 2.5 cm from the end of each arm. The positions of the live and dead pup were randomized. All pups were then removed from the home cage and the maze was inserted into it. The test session lasted for 10 min or until retrieval of both pups occurred. At the end of the testing period

MATERNAL RESPONSIVENESS 125

the T-maze was removed. The lactating females had their own pups returned while fresh pups were placed in the cages of the sensitized females and adult males.

Results and Discussion

Virgin females require an average of 5.8 days of exposure to pups (SD= 3.65 days) before reaching the sensitization criterion. The males averaged 6.67 days (SD = 3.52). These results are in good agreement with those of Rosenblatt (1967).

Each group showed an increase in percentage of animals showing retrieval over the 6-day test period in the T-maze (Fig. 1). Chi square tests of the retrieval percentages on Day 6 revealed that the lactating females had a higher incidence than either sensitized virgins (2? = 5 . 8 9 , ~ < .02) or sensitized males (X2 = 1 4 . 4 , ~ < .OOl). The 2 sensitized groups (i.e., the virgin females and males) did not differ from each other.

Another way to analyze these data is by means of the analysis of variance. Each animal was given a score of 1 for each day, out of 6 , that it retrieved. The mean number of days that lactating mothers retrieved was 4.07; the sensitized virgin mean was 1.14; and the mean for the sensitized males was .21. The analysis of variance of these data found a significant difference beyond the .01 level ( F = 20.68; df= 2/39). The lactating mothers differed from the other 2 groups which did not differ from each other.

Paralleling the retrieval data above, the lactating females entered the arms of the maze more often than did either sensitized group. The mean number of days that

DAYS

Fig. 1. Percent retrievai obtained in lactating females, sensitized virgin females, and sensitized males over a 6day test period. The rat pups were placed in the arms of the T-maze and the subjects observed for 10 min daily.

i26 BRIDGES ET AL.

lactating mothers entered one or both arms was 4.57; the sensitized virgin mean was 1.21; and the mean for the sensitized males was S O (F = 24.97; df = 2/39; p < .01). The 2 sensitized groups did not differ from each other.

Table 1 summarizes the retrieval data. There are 76 instances in which 1 or 2 pups were retrieved if all the trials and animal groups are summed. In 65 cases (86.7%) if one pup wzs retrieved, the second pup was also retrieved. In 5 1 cases (67.1 %) the live pup was picked first. This differs significantly from a chance expectancy of 5Q%? (P = 8.22; p <.Ol).

These data indicate that the sensitized rat is less maternal when compared with the lactating rat. It might also be argued that the sensitized animals are more “fearful” since they entered the arms of the maze less often than did the lactating subjects. However, the notion of fearfulness can only be meaningfully discussed within the more general context of maternal responsiveness since the lactating animals did retrieve the pups more than the other 2 groups. Thus, these findings suggest that the physiological events which accompany pregnancy and parturition act to reduce this fear thereby permitting the lactating animal to overcome certain environmental obstacles in order to care for her young (e.g., entering strange territory to retrieve the

The finding that the live pup was consistently retrieved first indicates that it emits certain cues which attract the adult. These cues may act on the auditory, visual, or olfactory systems, or, a combination of them. In the mouse, it appears that odor may be the primary maternal-eliciting cue (Gandelman; Zarrow, Denenberg, & Myers, 1971).

In conclusion, the results indicate that certain changes which accompany pregnancy and parturition act to enhance maternal responsiveness. Although a myriad of changes are brought about by pregnancy and parturition (e.g., metabolic, neural, endocrine, behavioral), it is tempting to speculate that a change in the endocrine system is the causal agent in the enhancement of maternal behavior seen in the parturient rat (see Moltz, Lubin, Leon, & Numan, 1970, for a discussion of the hormonal control of maternal behavior in the rat).

Table 1. Retrieval Performance for the Lactating Females, the Sensitized Virgin Females and the Sensitized Males over the 6-Day Test Period.

PUPS).

Number of Trials Number of Trials Total in which 1 or 2 in which both First Choice

Group Number of Trials F’UPS Were Retrieved Pups were Retrieved Live Dead

Lactating Females 84

Sensitired Virgin Females 84

Sensitized Adult Males 84

51

16

3

50 38 19

12 11 5

3 2 1

MATERNAL RESPONSIVENESS 127

Notes

This research was aided in part by Research Grant MH 19716, NIMH awarded to V. H. Denenberg and M. X. Zarrow, a University of Connecticut predoctoral fellowship and Traineeship BCEM, PHS, DHEW awarded to Robert Bridges, and ,I

postdoctoral fellowship HD-43413 from the National Institute of Child Health and Human Development, National Institutes of Health awarded t o R. Gandelman, who 1s now at Rutgers University. Mailing address: M. X. Zarrow, Department of Biobehav- ioral Sciences, Box U-154, The University of Connecticut, Storrs, Connecticut 06268.

References

Beniest-Noirot, E. ( 1958). Analyse du comportement dit “maternal” chez la souris. Mongr. Franc. Psycho/., Paris, No. I .

Gandelman, K., Zarrow, M. X., and Denenberg, V. H. (1970). Decreased retrieval of pups by virgin mice as a function of the testing procedure. Develop. Psychobiol.,

Gandelman, R., Zarrow, M. X., Denenberg, V. H., and Myers, M. (1971). Olfactory bulb removal eliminates maternal behavior in the mouse, Science, I 71: 2 10-2 1 1 .

Moltz, H., Lubin, M., Leon, M., and Numan, M . (1970). Hormonal induction O F maternal behavior in the ovariectomized nulliparous rat. Physiol. Behav., 5;

Rosenblatt, J. (1967). Nonhormonal basis of maternal behavior in the rat. Scierzce.

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