Exteroceptive stimulation of maternal behavior in the naive rat

Exteroceptive stimulation of maternal behavior in the naive rat

Physiology and Behavior, Vol, 8, pp, 595-598, Brain Research Publications ln¢., 1972. Printed in Great Britain. Exteroceptive Stimulation of Maternal...

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Physiology and Behavior, Vol, 8, pp, 595-598, Brain Research Publications ln¢., 1972. Printed in Great Britain.

Exteroceptive Stimulation of Maternal Behavior in the Naive Rat L. R O T H H E R R E N K O H L

A N D P. A. R O S E N B E R G '

Psychology Department, Temple University, Philadelphia, Pa. 19122, U.S.A. (Received 3 S e p t e m b e r 1971) HERRENKOHL, L. R. AND P. A. ROSENBERG. Exteroceptive stimulation of maternal behavior in the naive rat. PHYSIOL. BEHAV. $ (4) 595-598, 1972.--Systematic removal of either vision, audition or olfaction in primiparous naive rats relieved of young by Caesarean section on Days 18-22 of gestation does not eliminate maternal behavior toward foster pups; it only alters components of the total maternal response. Deafening (produced by destruction of the basilar membrane) increased the latency of retrieving and sniffing. The initiation of these two behaviors is thus facilitated by audition. Blinding by enucleation increased the duration of licking and crouching. Vision may thus be said to hamper or lessen the shortterm maintenance of maternal behavior. In contrast, anosmia (produced by removal of the olfactory bulbs) had little effect on either the initiation or maintenance of maternal behavior. In all of the animals the incidence of cannibalism was rare. Only 9~o (n=58) ate young. In general, then, maternal behavior remained intact in most of the rats. It would appear therefore that no one exteroceptive sense is necessary for maternal behavior in naive Caesarean-delivered rats.

Exteroceptive cues

Maternal behavior

Naive rats

B~ACH AND JAYN~S [2] in their classic studies on maternal behavior reported that either blind, anosmic or anaptic rats located and retrieved pups about as well as intact animals. On this basis they concluded that the " . . . female rat's retrieving behavior normally involves a multisensory pattern of stimulat i o n . . . (p. 120)" and that " . . . any single modality can be dispensed with as long as alternative routes of sensory input remain (p. 121)." Beach and Jaynes [2] used only experienced rats (lactating females with several days of experience with young). The question arises as to whether any one sensory modality is essential for maternal behavior in rats that have had no previous maternal experience. Late pregnant Caesareandelivered rats are known to be highly responsive to young in the absence of prior experience with them [4, 5, 12]. We chose therefore to reexamine the multisensory view with the use of naive Caesarean-delivered rats. The three modalities we investigated were vision, hearing and smell. Beach and Jaynes [2] had already used blind and anosmic rats but not deaf ones. The potential contribution of hearing to the regulation of maternal behavior had been suggested only in more recent years with the discoveries that (a) pups emit ultrasonic distress calls [6, 7, 8, 9, 14] and (b) adult rodents are capable of perceiving them [10]. Our primary purpose was to study the role that each of these modalities alone played in the initiation and short-term maintenance of maternal behavior. A secondary interest was to assess the contributions to maternal behavior of these modalities relative to each other.

METHOD

Animals' The animals were 58 primiparous pregnant SpragueDawley rats between 200-250 g sent from the Camm Research Institute, Wayne, New Jersey. All animals w e r e housed individually in 8½ × 11 × 5 in. opaque fibreglass observation cages with San-i-eel bedding. They were fed Purina pellets and water ad lib and kept in rooms that were maintained at a temperature of 72°F on 10 lax of light daily starting at 8 a.m. From weaning on, exposure to pups was controlled by keeping the animals in colony rooms where there were no breeding females with young.

Procedure All animals were relieved of fetuses by Caesarean section between Days 18-22 of gestation and then randomly assigned to one of the six following groups: experimental vision, hearing, smell groups and three corresponding control groups. The experimental vision animals ( n : 8 ) were blinded by the method of enucleation. Vision control animals (n=8) only received wound clips around the eyes. The experimental hearing animals (n=12) were deafened by destruction of the basilar membrane. This was d o n e by first cutting longitudinally along the auditory meatus to expose the inner ear. Next a sharp probe was forced through the typmanic membrane into the region of the cochlea and rotated vigorously to destroy the basilar membrane. Hearing

tWe gratefully acknowledge the support of our research by Research Grant 4715 from the National Institute of Child Health and Human Development awarded to LRH as Principal Investigator. 595

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control animals (n=10) sustained preparatory meatus incision but the tympanic membrane and cochlea remained intact. After the experiment, the animals were killed and the cochlea was pried open. In all cases the connection of the basilar membrane to the cochlea had been severed. Experimental smell animals (n=10) sustained bilateral bulbectomy by the method of aspiration. Animals were first placed into a Kopf stereotaxic instrument. A ½ mm circle above the sultura nasofrontalis was then transcribed using a dental drill and the skull was lifted to expose the olfactory bulbs. Aspiration of that region was done by visual inspection. Control smell animals (n=10) sustained sham operations in which the skull area above the bulb was removed but the bulbs were left intact. At the end of the experiment the animals were killed and their brains removed for histological examination. Frozen sections at 80 ~ revealed that in all cases a sufficient amount of olfactory bulb tissue had been removed to completely sever the connection between nerve fibers and the bulb. In most animals the olfactory tubercles remained intact. All operations were performed under ether anesthesia. Enucleation and deafening were performed immediately after the Caesarean section. Bilateral bulbectomy preceded the Caesarean section by about two days since performance of both surgical procedures on the same day resulted in a high mortality rate. Two days after the Caesarean section, animals were scored for maternal reactions toward 3 one-day foster pups in a daily 15-min test for three consecutive days. The test began when the pups were presented, scattered about the cage. For the next 15 min, the ongoing behavior (maternal and non-maternal) was scored continuously and analyzed in 10-see blocks of time. Latency of a behavior was defined as the time that elapsed between the presentation of pups and contact with the first pup. Duration of a behavior was the amount of time during the test period that the behavior occurred. The maternal behaviors we scored were: carrying or retrieving of pups, sniffing and licking the pups, and assuming a lactation-like posture or crouching over them. The non-maternal behaviors (e.g. sitting away from the pups, exploring the cage, self-grooming and digging) provided an index of general health and activity which across all groups proved to be quite normal. The measures of maternal behavior are presented as if each of the behaviors scored is independent of each other. We do not address ourselves in this report to the question of whether, and to what degree, these behaviors are in fact independent. Further analyses of the sequential order can provide those results. RESULTS

Figure la shows the mean latency of maternal behavior in naive rats deprived of either vision, hearing or smell. Of the four behaviols we observed, there were significant differences among the groups only with regard to retrieving and sniffing of the young. A one-way analysis of variance revealed a significant F for both behaviors (retrieve, F----4.72,dr= 5,43, p <0.01 ; sniff, F----3.74, dr----5,51, p <0.01 : the differences in df reflect the differences in n since mean latency, unlike duration, was based only on those animals which exhibited the behavior). However, the only significant difference between an experimental group and its respective control, as shown by the Newrnan-Keuls test [13], appeared with the hearing groups. Deafened animals were significantly slower to begin retrieving

(p<0.01) and sniffing pups (p <0.05) than their respective control rats. It should be mentioned that the experimental hearing group also had significantly longer latencies for retrieving and sniffing when compared with all the other groups (p <0.05). Figure lb gives the mean duration of maternal behavior. Analyses of variance revealed significant differences for all but sniffing behavior (retrieve, F----4.49, df----5,52, p<0.01; lick, F----6.66, df----5,52, p<0.01; crouch, F:3.77, df----5,52, p<0.05). The only significant differences between experimental groups and their respective controls, as shown by the Newman-Kenls test [13], appeared with the smell groups with respect to retrieving, and with the vision groups with respect to licking. Anosmic animals spent significantly less time in retrieving pups than did their respective control animals (p<0.01). Conversely, blinded animals spent significantly greater time licking young than did control animals (p <0.05). Of all the other paired comparisons possible with the Newman-Keuls test [13], the only differences that were significant with regard to retrieving involved the smell control group. This group spent significantly more time retrieving pups than did all the other groups (p <0.01). With regard to licking, the experimental vision animals spent more time licking pups than did all the other groups (p<0.01). With regard to crouching, the experimental vision group spent significantly more time crouching over young than did either the experimental smell group (p<0.01) or the experimental hearing group (p <0.05). The incidence of cannibalism was rare across all groups. It occurred only in 5 animals (9 % of the 58 animals), 3 in the experimental smell group and 1 each in the control smell and the experimental hearing groups. At the start of each test this last rat immediately pounced upon the young and proceeded to eat throughout the entire test. One of the three experimental smell rats and the control smell animal retrieved pups first and then ate for about 75 % of the total test time. The two animals remaining in the experimental smell group behaved alike in that on the first test they mostly explored the cage and only occasionally bit into the young. On the days that followed, they ignored pups. DISCUSSION

Our results with naive rats support the earlier work of Beach and Jayncs [2] with experienced rats in that no one sensory modality was essential for maternal behavior. Systematic removal of either vision, hearing or smell did not eliminate maternal behavior; it only altered components of the total maternal response. For the most part, however, maternal behavior remained intact in most of our rats. Deafening rats, for example, only increased the latency for retrieving and sniffing, all other behaviors were normal. The initiation of retrieving and sniffing behaviors thus appear dependent upon exteroceptive cues associated with audition. In animals with audition intact, even in the absence of vision or smell, hearing may be said to facilitate the onset of some maternal behaviors by enabling the female to better locate young at a distance. Latencies for crouching and licking behaviors were unaffected by the removal of hearing, or for that matter, of either vision or smell. This suggests that the initiation of these behaviors is not mediated by exteroccption but depend instead upon direct contact with the young. Beach and Jaynes [2] did not test for the role of audition. The recent discoveries that pups emit ultrasonic distress calls [6, 7, 8, 9,14] and that adult rodents are capable of perceiving

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FIG. 1. Mean latency (a) and duration (b) of maternal behavior in naive rats deprived of either vision, hearing or smell. Scores from 15-min tests for three consecutive days. Vertical bars indicate S.E.M. Probability values (p) shown for analyses of variance (F) and for mean differences between respective experimental (E) and control (C) groups.

them [10] suggest, however, that hearing plays a role in the regulation of maternal behavior. Most recently, Allin and Banks [1] found that adult rats can orient in the dirvction of recorded pup calls. Moreover, the significance of ultrasonic signals for the elicitation of retrieving has been repeatedly emphasized by Noirot in her review [6] and reports [7, 8, 9].

Blinding rats increased the duration of licking and crouching behavior. Interestingly enough, whereas deafening and anosmia cause little alteration or, at best, some deficits in maternal behavior, blinding appears to facilitate it. In animals with vision intact, sight may interfere or compete with input from other sensory systems in sustaining some

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maternal behaviors. To some extent, therefore, we can say that vision lessens the short-term maintenance of maternal behavior. Beach and Jaynes [2] also reported an advantage for blinded over sighted rats. In tests for pup preference, only 75% (18/24) of their normal experienced animals chose a restraining cage containing a pup rather than an empty cage, whereas all 9 blind rats investigated the restraining cage with the pup. They concluded that "blind females . . . showed a higher degree of discrimination than did sighted animals (p. 109-110)." The advantage of which Beach and Jaynes speak can best be viewed as an effect on retrieving. Contrary to their report, we found no effect on retrieving as a function of enucleation. The difference between our result and theirs is difficult to interpret due to differences not only in animals (naive versus experienced rats) but also in procedures. They tested for pup preference in a choice cage situation whereas we scored duration of ongoing responses to unrestrained young. Anosmia left maternal behavior relatively intact. Only the duration of retrieving was changed in the direction that control rats spent significantly more time in retrieving pups than animals in the other groups. In animals with smell intact, odor cues, at least taken alone, do not appear to contribute to the short-term maintenance of maternal behavior. Beach and Jaynes [2] found a similar result. Whereas only 25 % (1 out of 4) anosmic rats preferred a cage containing a pup to an empty cage, 100% (6/6) readily retrieved free pups within 5 rain. They concluded that the " . . . sense of smell is not essential for recognition and transportation of the young (p. 110)."

Taken together, our results support the view that maternal behavior in the rat is under multisensory control. We can extend the Beach and Jaynes [2] statement about the multisensory dependency of retrieving behavior (10. 120) to include sniffing, licking and crouching behaviors as well. The generality of the multisensory view to other mammalian species, however, or for that matter, to rats in other reproductive states, must be viewed with constraint. In a recent report on mice [3], olfaction alone was found to be a necessary condition for maternal behavior in both naive and experienced mice. F o r the most part, animals made anosmic by removal of the olfactory bulbs ate the young or at least ignored them. Whereas olfaction is not critical for maternal behavior in the hormonally-primed experienced [2] or naive rat (our results), it does appear to be necessary for the maternal behavior of the hormonaUy-unprimed naive rat. In a recently completed work (Fleming and Rosenblatt, personal communication), removal of the olfactory bulbs induced naive virgin rats to cannibalize foster young. It should be mentioned that, similar to our results, it was also found that olfactory bulb removal in hormonally-primed rats did not affect maternal behavior. Rats bulbectomized during late pregnancy responded maternally toward foster pups presented after their own young were born and subsequently removed. It was also found that hormonally-unprimed experienced rats (virgin rats sensitized to foster young by the methods of Rosenblatt, [11]) were capable of maternal behavior after removal of the olfactory bulbs. With regard to the rat, therefore, it would appear that maternal behavior independent of previous experience can be under multisensory control only in the presence of appropriate hormone states.

REFERENCES

|. Allin, J. T. and E. M. Banks. Functional aspects of ultrasound production by infant albino rats. Am. Zool. 10: 480, 1970. 2. Beach, F. A. and J. Jaynes. Studies of maternal retrieving in rats. III. Sensory cues involved in the lactating female's response to her young. Behavior. 10: 104-125, 1956. 3. Gandelman, R., M. X. Zarrow, V. H. Denenberg and M .Myers. Olfactory bulb removal eliminates maternal behavior in the mouse. Science 171: 210-211, 1971. 4. Lott, D. F. and J. S. Rosenblatt. Development of maternal responsiveness during pregnancy in the rat. In: Determinants of Infant Behavior, Vol. IV, edited by B. M. Foss. London: Methuen, 1969, pp. 61-67. 5. Moltz, H., D. Robbins and M. Parks. Caesarean delivery and the maternal behavior of primiparous and multiparous rats. J. comp. physiol. Psychol. 61: 455-460, 1966. 6. Noriot, E. Ultrasons et comportements maternels chez les petits rongeurs. Annls. Soc. r. zool. Belg. 95: 47-56, 1966a.

7. Noirot, E. Ultrasounds in young rodents. I. Changes with age in albino mice. Anim. Behav. 14: 459--462, 1966b. 8. Noirot, E. Ultrasounds in young rodents. II. Changes with age in albino rats. Anim. Behav. 16: 129-134, 1968. 9. Noirot, E. Changes in responsiveness to young in the adult mouse. V. Priming. Anita. Behav. 17: 542-546, 1969. 10. Rails, K. Auditory sensitivity in mice: Peromysc~ and Mus musculus. Anita. Behav. 15: 123-128, 1967. I I. Rosenblatt, J. S. Nonhormonal basis of maternal behavior in the rat. Science 156: 1512-1514, 1967. 12. Rosenblatt, J. S. The development of maternal responsiveness in the rat. Am. J. Orthopsychiat. 39: 36-56, 1969. 13. Winer, B. J. Statistical Principles in Experimental DesSert, New York: McGraw-Hill, 1962. 14. Zippelius, H. M. and W. M. Schleidt. Ultraschallaute bei jungen matisen. Naturwissenschaften 43: 508, 1956.