The Tuning of the Nervous System: Physiological Foundations and Implications for Behavior

THE TUNING OF THE NERVOUS SYSTEM: PHYSIOLOGICAL FOUNDATIONS AND IMPLICATIONS FOR BEHAVIOR E. GELLHORN* Since central excitation of autonomic structures leading to changes in behavior invariably alters tone and activity ofthe striated muscles, it was thought that the study ofautonomic reflexes in their action on autonomic "centers" in the brain stem (particularly the hypothalamus) and also on various levels ofthe somatic nervous system may lead to a better understanding of autonomic-somatic integrations and behavior. Experiments showed indeed that reflexes leading to increased sympathetic or parasympathetic discharges alter the reactivity ofboth autonomic divisions and alsothestate ofthesomatic system in a predictable manner [1-3]. Thecentralnervous system seemed to be "tuned" specifically by stimuli or conditions producing changes in hypothalamic excitability and balance. With the recognition ofthe intimate relations between limbic brain and hypothalamus by MacLean, Nauta, Papez, Tokizane, and others [4-7] and in view ofthe growing comprehension ofautonomic-somatic integrations [8], the time seems ripe to investigate the validity of the concept of tuning and its laws for neurophysiological problems on a broad basis and to apply it to the study ofbehavior. I. The Tuning ofthe Hypothalamus The procedure employed in these studies is simple. The effects of a stimulus A evoking an autonomic vascular reflex (through lowering of sino-aortic pressure) and ofa stimulus B applied to the hypothalamus are recorded singly and in combination (A + B). Ifthe stimulus A increases sympathetic or parasympathetic discharges, a state of sympathetic and * Professor Emeritus ofNeurophysiology, UniversityofMinnesota. Present address: 2 Fellowship Circle, Santa Barbara, California 93105. This work was supported by grant MH 06552-06 from the National Institutes of Health. 559 parasympathetic tuning, respectively, appears which shows the following characteristics:1 In a state ofsympathetic tuning, the reactivity of the sympathetic division of the hypothalamus is enhanced and that oftheparasympathetic division is lessened. Similarly, in a state ofparasympathetic tuning, the parasympathetic responsiveness of the hypothalamus is augmented, whereas its sympathetic reactivity is lessened. Sino-aortic reflexes may be used to illustrate these statements. A. TUNING THROUGH SINO-AORTIC REFLEXES2 Lowering the blood pressure (through Mecholyl or histamine, for instance) enhances sympathetic discharges. The heart rate rises, and a contraction ofthe normal nictitating membrane may occur. At the same time, the responsiveness to hypothalamic sympathetic stimuli is augmented : the pressor effect and/or the action on the nictitating membranes (n.m.) and heart rate are greatly increased. Conversely, a rise in the sinoaortic pressure through injection ofnoradrenaline increases the responsiveness of the parasympathetic system: if during the noradrenaline-induced hypertensive phase a hypothalamic (or sciatic) stimulus of the parasympathetic type3 is applied, its parasympathetic action on the heart rate is greatly increased. That the described effects are not restricted to the tuned system is evident from experiments in which the action ofparasympathetic stimuli was tested in a sympathetically tuned state and vice versa. The reciprocal relations which exist between parasympathetic and sympathetic reactions at the hypothalamic level persist under the conditions of tuning: the sympathetic test stimulus is less effective in a state of parasympathetic tuning than under control conditions; similarly, the action of the parasympathetic test stimulus is reduced in the state ofsympathetic tuning. These observations show that hypothalamic reciprocity is not only maintained in the state of tuning but exaggerated. This quantitative change in reciprocal autonomic relation has important consequences. It 1 Later, after the validity ofthe laws ofautonomic tuning for the somatic nervous system has been established, the terms "ergotropic" and "trophotropic" tuning are substituted for sympathetic and parasympathetic tuning. 2 See [i, 2]. 3 Due to low frequency stimulation ofhypothalamus or sciatic nerve. 560 E. Gellhorn · Tuning ofNervous System Perspectives in Biology and Medicine · Summer 1967 accounts for a shift in autonomic balance as well as for new qualitative changes (reversal), to be discussed later. The quantitative changes in reactivity seen in tuning seem to be based on summation processes.Just as the excitatory processes that are evoked by two parasympathetic stimuli of hypothalamic origin or that result from the interaction of a parasympathetic hypothalamic stimulus and a parasympathetically acting sciatic reflex stimulus summate [9], so the parasympathetically increased discharges that result from a noradrenalineinduced rise ofthe blood pressure summate with a central (hypothalamic) or reflex (sciatic) parasympathetic...