||Comments by Robert L. Isaacson
Department of Psychology, State University of New York at Binghamton, Binghamton, New York 13901
Are we ready to localize motivational systems? In his target article Dr. Adams undertakes to provide a basis for understanding varieties of behaviors related to aggression, flight, and "submission." What makes his analysis unusual is that its basis is hypothetical neural circuitry. In his theory the presumed neural circuitry ties actions together into meaningful patterns. At least, this is the ultimate goal of his work.
Adams deserves credit for his concern with the ethological significance of behavioral sequences or acts. Too frequently, neuroscientists study behaviors without regard to their role in an animal's life patterns. We need to be concerned with the role of behavioral acts. Many times similar motor patterns in one species or in different species are considered to be "the same" when, in fact, they may be components of behaviors with different significance to the animal. A rat standing on its hind legs could be engaging in behaviors that may be related to aggression, defense, or exploration. The standing erect of a great ape on its hind feet is an entirely different matter.
The article is in the tradition of the distinguished group that was assembled at Yale in the 1950s (i.e. John Flynn, Jose Delgado [qv], and Paul Maclean) These men invented a new approach to the study of the central nervous mechanisms responsible for behaviors - one that was sufficiently broad for the neurobehavioral data they were collecting. Subsequent research has been directed at an increasingly fine-grained analysis of related neural and behavioral systems. Adams's large-scope theory may be too general to encompass the specific physiological, anatomical, and behavioral evidence now available.
He analyzes three types of "motivational systems": offense, defense, and submission. In connection with the last two, a "consociate modulator" is proposed that determines which of the two will occur at any moment in time. This is necessary because both types of systems are thought to share portions of the same neural system: the central gray of the midbrain. This modulator acts to facilitate submissive acts if an intruder is familiar. The intruder need not be an animal of the same species. The consociate modulator is thought to be the ventromedial nucleus of the hypothalamus. As mentioned, both the defense and the submission behavioral systems are thought to be located in the central gray, although separate neuronal pools are associated with each. The modulator selects one or the other for expression. The neural mechanisms responsible for offense reactions are not specified, but they are also thought to lie in the midbrain. All systems receive influences from forebrain regions and are regulated by hormonal influences as well.
The motivational systems are said to be made up of "homogeneous" neurons. The actions of these homogeneous neurons determine the motivational state of the organism. It is not clear what "homogeneous" means. Should the neurons be thought ot as identical in terms of anatomical structure, in terms of input or output relationships, or in their biochemical nature or their responsiveness to circulating neuromodulators?
In this theory the motor systems ultimately responsible for all behavioral as executed by an animal are located in the brain stem and the spinal cord, Few would object to this. Specific facilitation of any particular act is thought to occur when motor mechanisms are "activated" by "simultaneous" input from motivational mechanisms and from "sensory filters responsive to releasing and directing stimuli specific to that motor pattern." The entire complex of specific motivational stimuli, sensory filters, and motor mechanisms is also referred to as a specific motivational system. This seems to add confusion to an already complex theoretical structure.
Stimuli can have motivational or directional functions. They function in one or the other capacity, depending on how the information they convey is processed by the central nervous system - that is, on the reactions they induce. All that we know, however, is thaI stimuli can serve both types of function.
An intruder can elicit aggressive reactions related to defensive or submissive responses. Adams believes that laboratory animals are more prone to exhibit submissive reactions than are their wild brethren, but even they can exhibit defensive reactions that will occur in a particular situation. Stimuli, especially olfactory ones in the rat, activate the "consociate" motivator. This mechanism biases responsiveness toward submission instead of aggressive defense.
While there may be a bias toward submissive acts in laboratory rodents and tame cats, the evidence is less than convincing. Indeed, it is rather difficult to imagine just what sort of evidence might be convincing. Every species undoubtedly has rather special releasing stimuli for such behaviors whose efficacy, both absolute and relative, may not be known. Consequently, how could legitimate comparisons be made? Further, are all submissions the same within a species or across them? There is no question but that most species have a range of behaviors that are associated with defense and submission. They can be observed in free-roaming and laboratory-bred and-reared animals. They can occur in response to a variety of threats or environmental events. The issue is whether "tame" animals or strains selectively bred for docility show enhanced amounts of submission compared to wilder members of their species.
How stable are the defensive, submissive, and offensive reactions? Are they really hard-wired? It is curious that submissive behaviors tend to be ones appropriate to young animals, or those with sexual significance.
However, the real issue is whether there is scientific value in associating defense and submission reactions to specific regions of the central nervous system in certain species with implied generality to other mammals or in the notion of a "consociate modulator."
Both the defensive and submissive reactions are assigned locations in the central gray of the midbrain, although each is said to reside in different subpopulations of the region. Therefore, each of the behavioral patterns has a location in the brain stem - defense in A, submission in B Under some conditions the diencephalic "consociate modulator" selectively facilitates neural region B at the expense of A. But it can't be concluded that these are the only areas involved with motivational systems, since Adams indicates that these must include sensory "filters" and the lower motor mechanisms as well. Even if these centers are not "motivational," some component of them must facilitate the appropriate motor pattern, and others must influence sensory systems. If this is correct, how can these areas be "homogeneous?"
In Adams's theory various forebrain regions, especially those of the limbic system, are thought to funnel their influences via tracts passing in lateral hypothalamic areas to the midbrain centers. These include the septal area, the amygdala, the cingulate cortex, and so forth. A number of lesion and stimulation studies in cats and rats are cited to show their relevance to the motivational states. Many of these are classics of the literature, but there are rather difficult problems of interpretation. Lesion studies cannot be interpreted as reflecting the effect of loss of tissue per se. The effects of any lesion are partly the effects of secondary alterations in remaining neural tissues. These effects change over time. Furthermore, those effects produced by a lesion depend on the genetic background of the animals, the prelesion experiences of the animal, the post- lesion environment, and the testing procedures used. Many of these same considerations apply to electrical stimulation studies as well, but, in addition, factors relating to frequency, current density. amount of current, spread of current, and the like must be considered as important determinants of effects.
At our present state of knowledge about the brain and behavioral patterns, it seems premature to localize motivational systems in particular regions of the central nervous system. What is needed is more understanding about how motivational systems, localized or diffuse, exert their influences to govern behavior, and not where they are.