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This paper documents two propositions on the effects of hormones in muroid rodents: (1) that hormones act upon discrete, homogeneous sets of neurons in the central nervous system that are part of the circuitry of: motivational systems; and (2) that hormones initiate and maintain, by means of their actions on neurons, a few, discrete "reproductive states" in which all of the social behaviors of muroid rodents are organized into purposive social strategies. The first proposition, that hormones act upon neurons of motivational systems, originates from two traditions, brain research and ethology. Brain research, in recent years has begun to analyze behavior in terms of the operations of specific neuronal circuitry. Ethology, in some cases, has attempted to conceptualize behavior in terms of motivational systems. My original training and perspective came from brain research. I began work by recording from individual neurons during defense behavior in cats and correlating the activity of neurons to the behavior of the animal (Adams, 1968). With many researchers in the field, I have come to share a general working assumption that behavior is organized by circuits of discrete, homogeneous sets of neurons with connections at least partly determined by instructions in the genetic code, and that these circuits are responsible for the organization of behavior under various stimulus conditions and contexts. From this assumption, it follows logically that hormones, as well as learning and imprinting, should influence behavior by changing and modifying the operations of the basic neuronal circuitry of behavior. More recently I have worked within the tradition of ethology and tried to deduce the neuronal organization of behavior by observations of behavioral sequences. From empirical observations (Lehman and Adams, 1977) and from a review of the literature on behavior of muroid rodents (Adams, submitted for publication), I have come to the conclusion that aggressive social interactions in these animals are organized in terms of four motivational systems. These four motivational systems, I have called defense, offense, submission, and exploration/marking. They are activated by four corresponding motivational mechanisms which are hypothesized to consist of discrete, homogeneous sets of neurons which activate the particular sets of motor patterns which may be observed in a given social context. Defense is activated in response to a potential predator, an unfamiliar conspecific, or (in the case of a lactating female only) any other animal; it is rarely seen in "tamed" or laboratory animals, but characterizes the behavior of wild animals or laboratory animals with certain olfactory or forebrain lesions. Offense is activated in response to unfamiliar conspecifics, other males (if the protagonist is a male), or in conditions of hunger or sexual deprivation when fighting over a piece of food or a potential mate. Submission is activated by the same stimuli as defense but only when the opponent is a familiar consociate; the motor patterns are similar to those of defense in many cases, but are less damaging and may include special submissive patterns. Ex:ploration/marking is activated in response to odors of the opposite sex or of unfamiliar conspecifics and corresponds, to a great extent, to what Beach (1976a) has called "proceptivity." In order to explain how an animal shifts from defense to submission in the presence of a familiar oonsociate opponent, I have suggested that there is a "consociate modulator" which is a brain mechanism responsive to familiar consociate stimuli and which facilitates the submission and inhibits the defense motivational mechanism. In the present paper, in order to analyze the effects of hormones on neuronal circuitry, I have widened the scope of analysis to include sexual and parental behavior. Three additional motivational mechanisms must be proposed: (1) a male sex motivational mechanism; (2) a female sex motivational mechanism; and (3) a parental motivational mechanism. To some extent, these are similar to mechanisms proposed by previous authors. The male sex motivational mechanism corresponds to what Beach (1956) called the "sexual arousal mechanism." In quoting Beach, one must note that in his more recent writings he has warned that there may be no discrete sets of neurons to be found in the brain which will correspond to motivational mechanisms (Beach, 1976b). The parental motivational mechanism corresponds to that set (or sets?) of neurons in the medial preoptic area which are "not only responsive to estrogen activation, but also essential for activation of maternal behavior by sensory stimuli from the pups" (Numan et a1, 1977). The female sex motivational mechanism corresponds to that neural substrate upon which both hormones and genital stimuli act to induce lordosis and hormonal secretions in the female. The hypothesis of "motivational mechanisms" is based upon observations and theory which have been used for many years in ethology. In particular, ethologists such as Lorenz (1970) and Tinbergen (1951) have considered that stimuli may have two very different types of effects upon the organism. One effect, which they have called a "motivating" effect, biases the organism towards the performance of a broad range of functionally related motor patterns, such as those of offense or defense or exploration/marking. The other effect, which they have called a "releasing" or "directing" effect, operates upon discrete motor patterns that may function in more than one context, such as the motor patterns of "approach locomotion" or "upright posture." In order to explain how the nervous system uses these two types of stimulus effects, I have hypothesized that motivating stimuli operate upon motivat1onal mechanisms that produce the motor patterns seen by the observer. Motor patterns, in this context, are broadly defined so as to include not only acts and postures, but also secretion of pheromones and hormones, vocalizations, and autonomic effects. Releasing stimuli and directing stimuli, unlike motivating stimuli, are hypothesized to operate directly upon discrete motor patterning mechanisms. I have used the term motivational system to denote the entire complex of sensory filters for motivating and releasing and directing stimuli and motor patterning mechanisms that are related to one particular motivational mechanism. The seven motivational systems of social behavior in muroid rodents have been illustrated in figure 1. At the center of each motivational system is a motivational mechanism. To the left are the sensory filters for motivating stimuli, and to the right are motor patterning mechanisms and sensory filters for releasing and directing stimuli. Fifteen proposed sites of hormone action are shown in the figure by circled numbers. Details of the overall diagram and the individual sites of hormonal action will be described in the first section of the paper. * * *
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Although the data derived from brain research and from ethology have been obtained by totally different techniques, there is some evidence that they each accurately reflect the true neural organization of behavior. In a recent review of the literature concerning brain mechanisms of aggression in rats and cats, I concluded that the data
derived from stimulation, lesion, and neuronal recording studies fit well with an ethological model of motivational systems (Adams, BBS 2(4) 1979).
The analyses in this paper will be confined to rodents belonging to the superfamily Muroidea (Wood, 1965). This superfamily includes most of the best studied rodents, including rats, mice, hamsters, and gerbils. The two families, Muridae and Cricetidae, which include these animals, diverged only recently in terms of geological time (Wood, 1959) and so all of the muroid rodents may be considered as closely related.
Any extension of the analysis beyond this group of animals was considered to exceed the confines of a single review.
The second main proposition of this paper states that hormones initiate and maintain a few, discrete behavioral states called "reproductive states." Whereas the first proposition may be considered as an "analytic" approach, emphasizing the complexity of discrete hormone effects, the second proposition may be considered as a "synthetic" approach, emphasizing the simple and general effects of hormones upon the life history of the organism. A more extensive introduction to the proposition of reproductive states will be given at the beginning of section three of the paper.
The paper is organized into four sections. The first and third sections correspond to the two main propositions. Also, there is a short second section which considers the hypothesis that there is an "anti-gonad system" that inhibits the pituitary-gonadal axis under conditions of overcrowding, defeat and with the onset of winter. The fourth section is a test of the theory of reproductive states; it applies the theory to a practical problem, the neural and hormonal basis for the process of domestication.
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