Multiple versus Single Modulatory Targets in Motor Control Circuits

MULTIPLE VERSUS SINGLE MODULATORY TARGETS IN MOTOR CONTROL CIRCUITS JEFFREY L. RAM* Motor control circuits often have several levels of organization, ranging from central "command sites" down to "final common paths." Are there preferred sites in this circuitry at which hormonal or modulatory neuronal inputs exert their action? What properties might be expected where these influences act at several sites in the system? In this article several preparations are described in which sites of hormonal and modulatory neuronal control are under investigation, and several possible explanations for the distribution of these sites are considered. Hormones are known to interact with the brain to influence behavior. For example, androgens are required for mate calling and sexual clasping behavior in the frog [1, 2], progesterone facilitates lordosis behavior in the rat [3], and angiotensin II causes drinking in the pigeon [4]. Since the control of particular behaviors is often arranged so that one or a small group of cells, known as command cells, may ordinarily initiate or control the behavior [5], a question which may be posed is whether a hormone affecting a particular behavior does so by acting only at crucial command sites for that behavior or whether it acts at many levels in the motor control circuit, from command down to final common paths [6]. To illustrate this question more clearly, refer to figure 1, which shows a very simple motor control circuit that has been demonstrated in Aplysia californica. In this figure, cell LlO is an identified neuron which has a command function*controlling heart rate. Activation of LlO results in a coordinated excitation of heart excitors and inhibition of heart inhibitors , thus leading to an effective acceleration of heart rate [7]. Cell LlO also coordinates neurosecretion and gill movements with heart rate. Studies from the author's laboratory were supported by NIH grant NS15041. The author thanks G. Ajimal and U. Shukla for assisting in experiments and R. Palovcik for useful discussions. *Department of Physiology, Wayne State University, School of Medicine, Detroit, Michigan 48201.© 1981 by The University of Chicago. All rights reserved 003 1-5982/82/2501-0247$0 1 .00 126 I Jeffrey L. Ram · Motor Control Circuits Fig. 1.—Schematic diagram showing some of the connections of identifiable neuron LlO to its follower neurons inAplysia californica. Neuron LlO controls the activity ofheart motor neurons and coordinates them with neurosecretory and other motor activity. (This figure is based on the work of many authors, as reviewed by Kandel [7]. Reproduced from Ram [6] by permission of author and publisher.) In terms of the question posed here, if a hormone affected heart rate by interacting with this neuronal and neuromuscular circuitry, would it act solely through the command cell LlO, or would it achieve its effects by acting at many levels within the control circuit, including command, motor neurons, and even the target muscle itself? This is not the same question as asking whether hormones act at many sites in the brain to coordinate different behaviors or whether they act at many sites throughout the body to coordinate different physiological responses. Obviously, for affecting different behaviors or different organs it is efficient to have sites ofaction at each target tissue, and, indeed, hormones do act at many sites throughout the body. Rather, the question posed here concerns a motor network for a single behavior. In this case one part of the circuit exerts effective control over the other parts. It would seem on first consideration that a single site of action solely at the level ofcommand cells might make most sense: Since command cells exert strong and overriding control over the neuronal circuitry underlying particular behaviors, the command cell should be ideally suited to function as the locus of action for a hormone to influence that behavior. But do hormones in fact act only at the command cell level? Evidencefor Multiple Targets within Motor Control Circuits In most cases, data to resolve this issue are presently insufficient. For a convincing answer, data must include demonstration of the behavioral Perspectives in Biology and Medicine ¦ Autumn 1981 | 127 effect of the hormone, determination of the neuronal circuit underlying the affected behavior in order to identify the relationships of its...