5. A parental motivational mechanism; suppressed perinatally by androgen, activated in the adult by estrogen and by decreasing levels of progestin, and (possibly) inhibited by ACTH or corticosteroids.
Considerable research on the rat has shown that there are a number of related motor patterns shown by mothers with litters of young infants and that the occurrence of these motor patterns is greatly influenced by hormones (Rosenblatt and Lehrman, 1963; Rosenblatt, 1970; Noirot, 1972b; Lamb, 197.5). The following motor patterns are usual~ tested in these studies; nest--building, infant retrieval, assuming a nursing posture over the infants, and grooming of the self and of the infants. A closer analysis might require further differentiation of the first two into several motor patterns with different releasing and directing stimuli: thus nest-building may consist of approaching and picking up potential nest material, carrying it to the "home" area, and infant-retrieval may consist of approaching and picking up a stray pup and carrying it to the "home" area.
The many motor patterns of parental behavior require various types of releasing and directing stimuli. For this reason, they may not co-vary when considered in terms of temporal sequencing or individual differences (Slotnick, 1967a). Thus, approach to a lost pup may be released and directed by visual, olfactory, and tactile cues (Beach and Jaynes, 1956a) as well as ultrasound vocalizations by the infants (Allin and Banks, 1972; Noirot, 1972a). Carrying the pups home, on the other hand, may be influenced by still other factors such as olfactory recognition of the pup (Beach and Jaynes, 1956a) and the two motor patterns may be dissociated by particular brain lesions (Slotnick, 1967b; Terlecki and Sainsbury, 1978) that appear to disrupt the influences of relevant releasing and directing stimuli. Also, the approach components of motor patterns of parental behavior may be specifically conditioned by operant conditioning techniques; thus rats and hamsters will learn to bar press in order to obtain nest material when they are pregnant (Oley and Slotnick, 1970) , and rats will learn to bar press in order to obtain a baby for retrieval (Wilsoncroft, 1969).
All of the various motor patterns of parental behavior are affected by other stimuli which may be considered as motivating stimuli operating upon a single parental motivational mechanism (figure 1, site 5). These stimuli are responsible for a general activation of parental behavior that has been called "priming" or "sensiization" (Noirot, 1972b). The exposure to stimuli from pups can increase retrieving, licking, nest-building, and nursing in subsequent tests in both male and female mice (Noirot, 1964b) and retrieving and nest-building in naive female hamsters (Noirot, 1972b). The motivating effects of these stimuli do not depend upon hormones, since they can be elicited in virgin .female rats following surgical removal of the pituitary or ovary (Rosenblatt, 1967, 1970). Both auditory and olfactory stimuli are involved. Ultrasonic calls from the infants can serve as motivating stimuli for pup retrieval (Noirot, 1972a), nest building (Noirot, 1974) and nursing (Noirot, 1970) in mice and pup retrieval in rats (Smotherman et aI, 1978). Although grooming was only slightly increased in mice following previous "priming" with auditory stimulation from pups, the control values were already quite high and perhaps maximal, in which case the experimental values could not have been significantly increased (Noirot, 1970). Olfactory cues can also serve as motivating stimuli for grooming, pup retrieval, and nursing in mice (Noirot, 1970), and pup retrieval in rats (Smotherman et al, 1978). Noirot (1970) looked at the effects of olfactory and auditory motivating stimuli upon various motor patterns, and although she came to the conclusion that different stimuli affected motor patterns to different degrees, which would argue against the existence of a single motivational mechanism, my own examination of her published data lead me to the opposite conclusion. The effects or olfactory deafferentation upon parental behavior have been contradictory; it can abolish maternal behavior in mice (Gandelman et al, 1972), facilitate it in rats (Fleming and Roseriblatt, 1974) or have no effect upon it in rats (Beach and Jaynes, 1956b; Herrenkohl and Rosenberg, 1972). At least some of these differences may be related to the fact that rats and mice tend to eat the offspring of unfamiliar litters, as will be discussed in the !section on the female reproductive fulfillment state, It is likely that olfactory deafferentation affects this other behavior which is contradictory to parental behavior,
I have referred to a "parental" rather than a "maternal" motivational system because of the fact that all of the various parental behaviors may be obtained in male as well as female muroid rodents. This has been shown for mice (Noirot, 1964b),gerbils (Elwood, 1977), rats (Lubin et al, 1972), and voles and deermice, as discussed by Beach (1967b).
At first it was thought that there were three hormones involved in the facilitation of parental behavior around the time of parturition in the female rat: prolactin, estrogen, and progestin. This was based on a study by Moltz et a1 (1970) in which it was showm that the latency for parental behavior in response to test pups for an inexperienced and ovariectomized female rat was speeded up by appropriate hormone manipulations. Regimens of estrogen and prolactin administration, or estrogen administration plus withdrawal from previous progestin administration were each effective, but the most effective combination consisted of prolactin and estrogen administration and withdrawal from progestin.
More recent work on the rat has confirmed that estrogen and progestin play roles in the increased parental behavior during pregnancy, but have not confirmed that prolactin plays such a role. Estrogen facilitates parental behavior following ovariectomy and hysterectomy (Rodriguez-Sierra and Rosenblatt, 1977), and is apparently responsible for the parental behavior shown following hysterectomy (Siegel and Rosenblatt, 1975), leading the authors to suggest that it is essential to the increased pa.rental behavior seen during normal pregnancy and lactation. Under certain extreme experimental conditions, however, estrogen may also disrupt parental behavior (Leon et al, 1975). Progestin plays a dual role, facilitating parental behavior early in gestation and inhibiting it late in gestation; thus declining levels of progestin in late gestation are necessary to release the parental behavior associated with parturition (Bridges et al, 1978). Earlier findings on the role of prolactin have not been confirmed in more recent experiments. Blockade of prolactin does not alter either the onset (Bridges et al, 1974; Rodriguez-Sierra and Rosenblatt, 1977) or the maintenance (Numan et al, 1972) of parental behavior in the rat
Parental behavior may be blocked by pituitary-adrenal activation in the rat (Steele et &1, 1976). The relevant hormone in this case is not known but is apparently not progestin (Steele et al, 1976) which leaves open the possibility that ACTH or corticosteroids may be involved. If so, this could explain the frequently observed fact that under conditions of social stress muroid rodent mothers may abandon their young (Calhoun, 1962b; Brown, 1953).
The neural substrate for parental behavior is apparently organized by gonadal hormones around the time of birth. If male rats are castrated on the date of birth, they show more parental behavior when adult, and if females are given neonatal testosterone, they show reduced parental behavior when adults (Quadagno and Rockwell, 1972). This suggests that perinatal androgens suppress development of the parental motivational mechanism.
The hormonal regulation of parental behavior in other muroid rodent species is not as well known as in the rat. In the hamster, nest-building increases during early pregnancy, apparently as a :function of increasing levels of estrogen and progestin (Richards, 1969). Although estrogen levels during pregnancy are higher in absolute terms in the hamster than in mice or rats, there is no further increase in estrogen near the time of parturition (Baranczuk and Greenwald, 1974), and one recent study failed to find any facilitation of parental behavior by injected estrogen or progestin in the hamster (Siegel and Greenwald, 197.5). In the laboratory mouse, one study has shown that prolactin injections can facilitate pup retrieval, nest building, and pup-grooming (Voci and Carlson, 1973). Also in the mouse, estrogen and progestin have different effects on nest-building (Lisk, 1971; Lisk et aI, 1969) with estrogen inhibitory while progestin is facilitative. In the Mongolian gerbil, there is an increase around the time of parturition in nest-building, pup-retrieval, and nursing, but hormone studies have not been done (Thiessen and Yahr, 1977, p. 114). Some of' the contradictory findings, especially those in the mouse, may be due to other influences upon nest-building behavior, such as changes in thermoregulation which may be influenced by hormones (Lynch and Possidente, 1978). Other findings suggest that the hormonal bases of parental behavior may be different in different muroid rodent species. This must be considered a tentative conclusion, however, since there were literally hundreds of studies on the hormonal basis of parental behavior in the rat, many of them contradictory, before the present state of knowledge was attained, and there have been only a handful of studies on other muroid rodents.
The site of the parental motivational mechanism is probably in the medial preoptic area of the hypothalamus. Both the hormonal effects and the effects of pup stimuli upon parental behavior in the rat apparently act upon a neural substrate in this area (Numan et al, 1977).