2. An exploration/marking motivational mechanism; activated by androgen and estrogen.
The existence of a motivational mechanism of exploration and marking in muroid rodents was postulated on the basis of a sequence analysis of. intermale encounters in laboratory rats (Lehman and Adams, 1977) and developed on the basis of a comparative review of social behaviors of well-studied muroid rodents (Adams, submitted for publication). The behaviors activated by this motivational mechanism include the patrol behaviors normally seen in dominant males and the enhanced locomotor and marking behavior of estrous females. It also includes a great deal oŁ behavior often considered as sexual in nature, particularly the behavior called "proceptivity" in a recent review of sex behavior by Beach (1976a).
The organization of exploration and marking appears to be the following. There are three type s of motivating stimuli: testosterone-dependent pheromones (in females), estrogen-dependent pheromones (in males), and unfamiliar conspecific odors (in both males and females). The outputs of the motivational mechanism activate both approach locomotion and general undirected locomotion, and stop-and-sniff, along with various types of scent-marking patterns which vary greatly from species to species, including facial gland secretion, perineal, vaginal or anal-marking, ventral-rub, chin-rub, urine-marking, and flank-rub.
Although hormones may influence exploration/marking by way of their actions upon the sensory filters of various motivating stimuli (see sites 7-9 discussed below), in addition, they may activate the motivational mechanism in the absence of any motivating stimuli (figure 1, site 2). Thus, androgen apparently can activate the "spontaneous" patrolling of males (Shillito, 1963) and estrogen apparently can activate the increased locomotion of estrous females (Finger, 1969) in the absence of motivating stimuli. Also, androgen administration can reinstate ventral-rub marking of gerbils after it has been abolished by removal of' olfactory inputs (Thiessen et al, 1970b), and by direct injection of androgen into the preoptic hypothalamus (Thiessen et aI, 1973).
Androgen activation of the exploration/marking motivational mechanism may explain why patrol behaviors are characteristic of dominant males during the breeding season, and not characteristic of subordinate males or during the non-breeding season (Brown, 1953; Crowcroft, 1955; Mackintosh, .1970; Brown, .1966). The effects of androgen have been tested directly in some cases. Locomotion is decreased by castration in males and restored to higher levels by administration of testosterone (studies reviewed by Beach, 1948). Investigatory behavior, including approach locomotion and stop-and-sniff, is decreased by castration and restored by testosterone in rats (Stern, 1970). Urine-marking is abolished or reduced in rats by castration (Price, 1975; Brown, 1977) and restored by administration of testosterone (Price, 1975). Ventral-rub in the male gerbil is also under the control of androgen (Thiessen et al, 1968).
Estrogen activation of the exploration/marking motivational mechanism may explain the enhanced locomotor and marking behavior of estrous females. The increased locomotion of estrous females is well known from early work in the rat (Wang, 1923) and has also been found in other muroid rodents including deermice (Stinson, 1952), hamsters (Richards, 1966), and gerbils (Vick and Banks, 1969). Wild rat females, on the day before estrus, show increased locomotion, approach to males, flank-rub, perineal drag, and presumed urine-marking (Calhoun, 1962a, p. 153), and a recent study indicates that female laboratory rats have higher frequencies of marking at estrus than at diestrus (Birke,1978). Similarly, female hamsters show more vaginal marking on the day before estrus (Johnston, 1977a) at which time estrogen levels are high but progestin levels are still low (Labhsetwar et al, 1973). Urine-marking and perineal drag are also more frequent during estrus in the great gerbil Rhombomys opimus (Goltzman et a1, 1977). Only in the mouse are such data negative; no correlation has been found between urine-marking and the phases of the estrous cycle (Maruniak et al, 1975).
The location of the motivational mechanism of exploration/marking is not known for certain, but may be in the medial preoptic hypothalamus Lesions of this region in rats abolish the approach locomotion that is normally enhanced by androgen in males (Singer, 1968) and by estrogen in females (King, 1979). The implantation of estrogen in this region enhances the locomotor activity of ovariectomized female rats (Wade and Zucker, 1970) and implantation of androgen Or estrogen facilitates ventral-rub in gerbils (Yahr, 1977). Also, neurons of this area respond differentially to urine odors which may normally function as motivating stimuli for exploration/marking and they may be sensitized by the administration of androgen (Pfaff and Pfaffman, 1969). Neurons in this region have also been shown to have a high uptake of radioactive estrogen and androgen (Pfaff' et a1, 1973).