Abstract.
Search activity concept provides a new classification of the behavior which distinguishes search activity (activity in the uncertain situation with the constant feedback between behavior and its outcome), stereotyped behavior with a definite probability forecast, panic (activity without feedback between activity and its outcome) and renunciation of search. Only search activity which includes fight, flight, orienting behavior and creativity raises the body's resistance to stress, to natural and experimentally induced pathology whereas renunciation of search which display itself in freezing, helplessness and depression forms a nonspecific predisposition to somatic disturbances (e.g. psychosomatic diseases) . Dreams in REM sleep are regarded as a specific form of search activity aimed at compensating for the lack of search in waking. REM sleep deprivation on a small as well as on rotating platform raises the requirement in REM sleep by frustrating search activity. It is suggested that in wakefulness characterized by the prominent search activity the inhibitory alpha-2-adrenoreceptors became less sensitive to stimulation and consequently in this state the activity of the brain monoamine neurons is less limited by the level of brain monoamines. During renunciation of search brain monoamine synthesis is not stimulated by monoamine exhaustion. In REM sleep the critical level of brain monoamines for search activity to start is lower than in wakefulness and alpha-2-adrenoreceptors are less sensitive than in the state of renunciation of search although more sensitive than during search behavior in waking. REM sleep indirectly contributes to memory consolidation by carrying out its main function – restoration of search activity. A functionally sufficient REM sleep contains search activity in dreams (subject is active in his/her own dream scenario) while in functionally insufficient REM sleep dreams are characterized by subject's passive position and feeling of helplessness. REM sleep insufficiency is an obligate condition for mental and somatic disorders to appear. The difference between normal (adaptive) and pathological (maladaptive) emotional tension is determined by the presence or absence of search activity in the structure of emotional tension. Repression of the unacceptable motive causing neurotic anxiety is a human variant of renunciation of search. Hypochondriac symptoms are in negative relationships with psychosomatic disorders and they, as well as positive symptoms in schizophrenia and anorectic behavior in anorexia nervosa, represent a pathological misdirected search activity.
Key words: search activity; brain monoamines; REM sleep; psychosomatic diseases; neurosis; schizophrenia; anorexia; anxiety;
SEARCH ACTIVITY CONCEPT: RELATIONSHIP BETWEEN BEHAVIOR, HEALTH AND BRAIN FUNCTIONS.
V. S. Rotenberg, MD, PhD, DSc.
INTRODUCTION.
Stress theory of Selye (1974) integrated data of physiological and clinical investigations related to the level of subject's health in front of life challenges. According to this theory, an intensive and/or long lasting stress (distress) is considered to be one of the main factors predisposing subject to mental and psychosomatic disorders. This theory was confirmed in many investigations on animals and supported by numerous clinical cases.
However, this theory contains some serious contradictions and fails to explain a substantial part of clinical data. Thus, there are no relevant methods and even no theoretical approaches for the preliminary distinction of stress with positive outcome (eustress) from stress with negative outcome (distress). It is difficult to explain why different stressors cause initially the increase of body resistance (in comparison to the neutral state without stress) while being continued in the same frame they are almost inevitably leading to the tremendous decrease of body resistance (stage of exhaustion). Actually, it is hard to imagine how the same condition without any qualitative alterations is changing subject's state to the opposite one.
It is worth to emphasize that psychosomatic disorders may also appear when stressful situation has a successful outcome accompanied by positive emotional state ("diseases of achievement"). Such diseases appear not during the fight by itself, no matter for how long this fight is going on, but only after a desired goal is already achieved.
This phenomenon is difficult to explain using the concept of exhaustion because a new goal or the unexpected prolongation of stress usually prevents psychosomatic disorders.
On the other hand, even a very long and intensive stress may increase body resistance instead of decreasing it. For example during the Second World War participants in military operations or individuals who did hard work in the rear showed a drop in the rate of diseases compared to the pre-war period. (Natelson, 1983). Furthermore, while many concentration camp prisoners have died due to the development of psychosomatic disorders, those prisoners who survived until their release often exhibited the disappearance of the symptoms of their pre-camp psychosomatic diseases, and these diseases come back soon after the release. However, if the same stress may cause either exacerbation or disappearance of the diseases it means that it is necessary to search for additional factors explaining the difference in stress outcome.
According to some authors (Laudenslager et al., 1983; De Boer et al., 1990; Rodin, 1986; Mason et al., 1990; Levine & Ursin, 1991) a controllability and loss of control are crucial factors determining stress outcome. Real or perceived control prevents somatic disorders in stressful conditions while loss of control predisposes subject to these disorders. Nevertheless, it was shown in some investigations performed on animals (Seligman 1982) and on humans (Brosschot et al., 1992) that strong efforts, even being unsuccessful and being performed by subjects without any illusions according to their controllability might increase body resistance and immune activity. However, in other investigations unsuccessful efforts are often leading to learned helplessness (Seligman, 1975) accompanied by somatic disorders.
The concept of coping as a mediator of stress outcome is central in the modern stress theory. According to this concept, subject's overt and covert behavior in front of stressful life events determines the stress outcome in the domain of the psychological and somatic health. However, different authors proposed different lists of coping mechanisms (see Folkman & Lazarus, 1988) and it is still unknown whether some of them have definite advantages in comparison to others, and whether they are qualitatively different.
The goal of this paper is to propose a special psycho-behavioral mechanism crucial for health protection vs. health disturbance
in stressful and non-stressful conditions and to discuss the application of this mechanism to physiology, psychology and medicine.
SEARCH ACTIVITY CONCEPT: AN EXPERIMENTAL BACKGROUND.
Search activity concept arose from an analysis of the results of our own investigations and their comparison with literary data in different fields. Basic experimental investigations have been performed in collaboration with V.V. Arshavsky. In the 1974-1978 period we have studied the influence of different types of behavior and emotional states on the course of experimental pathologic processes and sleep (Arshavsky & Rotenberg, 1976; Rotenberg & Arshavsky, 1979). The subjects were rats and rabbits with lacquer-insulated bipolar nichrome electrodes 100 microns in diameter (the inter-electrode distance was 0.8 millimeter) implanted in the lateral and ventromedial parts of the hypothalamus. Three or four days after the operation we tested the reaction that follows stimulation of the hypothalamic structures by one-second square pulse bursts each lasting a millisecond. They had a frequency of 60-80 hz and an amplitude (with minimal current) of 100-180 microampers (mcA) in the case of the reaction of self-stimulation and 40-80 mcA in that of the reaction of avoidance. The experiments were conducted under conditions of free behavior. Stimulation of the lateral hypothalamus in rats, as a rule, provoked the beginning of self-stimulation with a frequency of 40 to 80 pedal pushes a minute. Stimulation of the ventromedial hypothalamus in both rats and rabbits evoked two types of behavior: 1) active defense reaction of the fight-flight type: flight, fury, jumps, nibbling at various objects to be found in the chamber, and 2) passive fear of the freezing type: the animals hid in one of the corners of the cage without trying to get out of it, pressed themselves to the floor and froze with tensed muscles, exhibited frequent piloerection and dyspnea, constant defecation and urination. Freezing behavior was often although not always accompanied by an increase in heart rate and arterial pressure. The thresholds of electric stimulation for elucidation freezing were, as a rule, higher than those exhibited in the case of active-defense behavior.
In order to check the effect of the different emotional states and different types of behavior on the body resistance to somatic disorders, we have studied the dynamics of different forms of experimentally induced pathology. We have used the following models: anaphylactoid edema in the case of the intra-abdominal injection of 1.5 milliliters of protein of a hen egg; arrythmia of cardiac contractions in the case of a parenteral injection of sub-lethal doses of aconitine; epileptic focus (application through a chronically implanted cannula of some metal cobalt powder to the sensori-motor region of the cortex); extrapyramidal disturbances (rise of muscular tension, constraint, tremor with a frequency of 3-4 hz and an amplitude of 5-10 angular degrees) with intramuscular injection of neuroleptics (aminazine, 2 milligrams per kilogram); "proclivityґto the use of alcohol.
The dynamics of these forms of artificial pathology were studied in control animals, which were not exposed either to self-stimulation or to stimulation of hypothalamic structures. In the experimental animals 10 to 15 minutes of stimulation of these structures induced the aforementioned types of behavior. Through the implanted electrodes an electroencephalograph registered the biopotentials of the hypothalamic structures and hippocampus. The experiments were followed by the examination of the electrode localization on the brain's serial sections.
The basic findings can be summed up as follows. Both active self-stimulation and active defense behavior of the fight-flight type reduced the distinctness of pathologic manifestations or even completely prevented their emergence. Passive self-stimulation of the lateral hypothalamus (when a rat simply lay down on the pedal thus closing the circuit and sending rare pulse bursts to the brain) did not influence the course of the pathologic process. In contrast, freezing predictably speeds the progress of the pathologic process, rendering its course more difficult. For example, the duration of epileptic seizures (cobalt epilepsy) in the "mirror" focus equaled 1.3+0.08 seconds in the control series, 0.98+0.08 seconds in that of active preliminary self-stimulation, 0.96+0.08 seconds in that of active defense behavior and 2.4+0.3 seconds in that of passive behavior of the freezing type (p<0.05). The manifestation of anaphylactoid edema was measured by the change in the shadow's width on a contact print. In control the edema equaled 3.25+0.16 millimeters, after self-stimulation it was weakly expressed (1.04+0.12 millimeters) , freezing made the latent period of edema emergence almost twice as short and edema by itself was equal to that observed in control animals. At the same time, active defense reaction reduced the degree of edema (2.2+0.1 millimeter) in comparison to the control state and freezing. The injections of librium changed the character of animal's self-stimulation; animal was not "playing" with the pedal but instead lay down on the pedal and closed the circuit sending pulse bursts to the positive rewarding brain structures. In this case the development of edema was not blocked and it equaled 3.27+0.21 millimeters. Other experimental models, including model of artificial myocardiac infarction (Simonov, 1981) gave similar results.
The main question raised by these data was the following: what is the common basis of the protective effect of active self-stimulation and active-defense behavior? What brings together these two behavioral forms making them opposite to freezing and passive self-stimulation? We have performed a substantial analysis of this topic (Rotenberg, 1984)
Apparently, neither the positive nor the negative sign of the dominant emotion is crucial: in the case of self-stimulation, behavior is determined by positive reinforcement whereas the reaction of the fight-flight type, as well as freezing, signifies the domination of negative emotions. At the same time, passive self-stimulation exercises an effect similar to that of freezing although these behavioral forms are accompanied by emotions of the opposite sign. The differentiation of behavioral types based on the "approach" and "avoidance" principle also fails to furnish the clue to the problem: freezing and flight are classed with avoidance behavior but exert the opposite influence on the body's resistance. At the same time, flight and self-stimulation according to this criterion are the opposite behavioral types but exercise a similar effect on the course of pathological processes. Apparently, the character of autonomic reactions is not basic to the problem either. It is true that in all types of behavior blocking the development of pathologic processes the activity of the sympathetic system is the dominant factor. However, in the case of the behavior furthering the development of pathological processes, sympathetic system is often also very active. In freezing, defecation and urination as signs of the parasympathetic activity were frequently accompanied by piloerection, mydriasis, tachycardia and high blood pressure (see also Anderson and Jingling, 1978). Thus, the animal exhibits, as it were, the anxious expectation of catastrophe. Furthermore, it has been demonstrated (Valdman, Kozlovskaya and Medvedev, 1979) that whereas in the case of active defense avoidance the blood pressure rapidly normalizes after the completion of a stressful situation, in the case of freezing it persists for a prolonged period at a relatively high level.
Finally, it could be assumed that the basic factor influencing the course of experimental pathology is motor activity: whereas in self-stimulation and the fight-flight behavior it is at its peak, in freezing and in passive self-stimulation it is almost completely absent. However, many studies in the literature contradict this assumption. Thus, when animals were trained to inhibit motor activity arbitrarily in order to avoid electric shock (passive avoidance), the successful “learners” had less gastrointestinal lesions than those animals that failed to inhibit motor behavior (Goesling, Buchholz, Carreira, 1974). On the other hand, when animal is exposed to unavoidable electric shock it cannot prevent by coping behavior, ulceration of the gastrointestinal tract correlates with the intensity of motor activity (Weiss, 1977). Weiss emphasizes the absence of cause-and-effect relationships in these investigations: it is not the motor that accounts for the exacerbation of the ulcerous process. However, both indices increase in parallel, indicating that motor activity does not prevent the development of somatic pathology. It is also known that a non-purposeful motor activity, which predictably manifests itself at initial stages of the development of learned helplessness, does not prevent the development of this state, which is accompanied by disturbances of different somatic systems (Miller, Rosellini and Seligman, 1977; ). Apparently, it is not motor activity that forms the basic protective factor in cases of different behavior types.
What then is there in common between self-stimulation and the fight-flight behavior, and what criterion makes them opposite to freezing in our investigations? I assumed that this criterion is search activity (Fig. 1).
By search activity is understood activity designed to change the situation or the subject's attitude to it in the absence
of a definite forecast of the results of such activity, but with constant monitoring of the results at all stages of activity.
Without an appropriate monitoring it would be impossible to change a direction of search in the case of its inefficiency.
This definition makes it clear that certain behavioral categories cannot be classed with search behavior.
This primarily applies to all forms of stereotyped behavior having a quite definite forecast of results.
The role of activity in anticipating and confronting stressful situations was emphasized by Gal and Lazarus (1975)
however they do not propose the notion of search activity and do not discriminate search activity from any other forms of subject's activity.
On the other hand, panicky behavior at first glance may seem to imitate search behavior but differ from
it by the disturbance of the feedback between the outcome of activity and its regulation. Really,
during panic the results of the activity are not considered at any stage and cannot be used for the correction of behavior.
No line of activity can be traced to its conclusion and panicky behavior easily becomes imitative, approaching stereotyped behavior.
Finally, the antipode of search behavior is the state of renunciation of search, which in animals may assume the form of freezing.
(Fig. 2) Learned helplessness in animals and humans as an outcome
of regular failures (Seligman, 1975) is also a typical example of renunciation of search.
In the Introduction I have stressed that the controllability vs. loss of control are considered by some authors to be crucial for stress outcome. Loss of control or lack of the sense of control are the main notions of the learned helplessness theory (Peterson et al., 1993). By control is understood a relationship between action and outcome. An inescapably shocked rat can be immunized against helplessness if it was trained before to escape shock by using a particular behavior. Thus, according to Peterson at al., 1993, the previous experience of control eliminates the learned helplessness effect. However, is it really a sense of control that prevents learned helplessness? And is it really an absence of the sense of control determining the development of learned helplessness? Peterson et al., emphasized that learned helplessness is going to ensue even if the uncontrollable event is positive or neutral, but independent on the animal's behavior. According to these authors, animals exposed to positive events independently of their behavior should learn that these events are uncontrollable. Due to this uncontrollability, animals became vulnerable to the development of learned helplessness.
However, if the outcome of any action and any response is positive, or if the outcome is positive even without any special response, from my point of view, animal receives a quite opposite experience - an experience of omnipotent control, because every action causes a positive outcome. If subject achieves goals in any case what can be a real basis for the subjective conclusion that control is absent? It is only the conclusion of the investigators. Although humans are more sophisticated than animals it is true also for humans, especially by taking into consideration the tendency of healthy subjects to create positive illusions (Taylor & Brown, 1994) and to believe that they can control things more than is actually the case. When subjects are solving easy intellectual tasks and are successful in 100% (Jones et al., 1977), it is very doubtful that they come to the conclusion that they are unable to control the situation. I suppose, in this condition they have a sense of a very high control. However, it does not immunize them to learned helplessness when they subsequently confront with regular failures. Quite opposite, they became more predisposed to learned helplessness in comparison to subjects who received difficult tasks and were able to solve only 50% of these tasks. According to the search activity concept, it happens because subjects achieved their 100% success without additional efforts, without search, on the basis of stereotyped behavior. This experiment shows that not the controllability by itself, but only efforts to achieve control (search activity) immunize subject to learned helplessness.
Perceived control may relate to two different conditions:
A definite forecast of the outcome of the objective situation. Such estimation of the situation usually causes stereotyped behavior. It can facilitate adaptation only in very particular (often artificial) conditions.
Subject feels himself to be able to control the situation without definite probability forecast of the outcome of the situation by itself. In this condition perceived control is actually a potential control and relates not to the situation but to the implicit evaluation of subject’s ability to cope with the unpredictable situation. This ability is based on search activity.
I suppose that it is necessary to discriminate two forms of learned helplessness (LH) (Rotenberg, 1996). If animal learns that punishments (footshocks) are limited in time and space, a conditioned LH appears tied only to specific conditions. The animal remains active in all other situations (Abramson et al., 1978). Such restricted LH does not contribute to renunciation of search as a global state. The difference between conditioned and generalized LH may explain different outcomes of chronic stress (Yehuda et al., 1993 ). Chronic stress can cause the physiological exhaustion if combined with generalized helplessness (renunciation of search). Being combined with conditioned helplessness, stress causes attenuation of hormonal response however the latter can be displaced by the increased response in front of novel, acute stressor that stimulates search activity.
Search activity can be absent not only due to the renunciation of search in stressful conditions. It can be absent if subject is completely satisfied with the situation and if search, with its unpredictable outcome, is threatening. In cases such as these, appearing mostly in artificial conditions, the animal is motivated to give up search behavior. However, some of the specimens even in these cases, too, exhibit a tendency toward search behavior even if the latter involves risks and fear. When rats were placed in comfortable conditions, in which they had sex partners and a sufficient food, some of them shortly attempted to enter the unexplored neighboring premise although these attempts were accompanied by pronounced emotional tension. This manifested itself in an increased heart rate and in defecation (Simonov, 1975).
Thus, it would be incorrect to assume that search activity in all cases is merely a "servant" of some irrelevant requirements, although the latter happens very often. If the organism only follows the course of a continuously changing world with the aim to adapt to it, it may lose time and initiative. It cannot be excluded that, alongside certain biologic requirements, there is one in search, which is anti-homeostatic. Exploratory activity without any pragmatic necessity reflects a high level of search requirement, as does creativity in humans.
Search behavior in animals is categorized as all types of active defense behavior (both aggression and active avoidance) as well as the active self-stimulation of the brain zones of positive reinforcement. Such self-stimulation is a complex multi-component behavior, which includes appetence, aversion, and search activity proper (Grastyan, 1976). It has been shown that self-stimulation is obtainable from the same brain structures whose forcible stimulation creates orienting-exploratory (search) behavior; the duration of self-stimulation correlates with the manifestation of the general exploratory reaction of the animal being stimulated (Schiff, Rusak and Block, 1971); self-stimulation is in competitive relations with stereotyped behavior (Wauquier, 1980).
In many mammals (cats, rats etc.) the electrophysiological correlate of search behavior is synchronous high-amplitude theta-rhythm in the hippocampus. None of the existing hypotheses pertaining to the functional relevance of this rhythm contradicts the above mentioned assumption: search activity plays a great role in learning, in directed attention, in behavior planning, in the organization of arbitrary motor acts, and in the selective memorizing of information (Rotenberg, 1984). At the same time, stereotyped behavior with the definite forecast of the results of actions which promotes satisfaction of requirements ( for instance, during consummatory behavior) is unaccompanied by hippocampal theta-rhythm (Kramis and Routtenberg, 1977).
The brain system related to search activity (to orienting response, novelty detection etc.) is a widely distributed network involving hippocampus, cingulate and limbic areas, and prefrontal and posterior association cortex (Knight, 1996). It was shown recently (Procyk et al., 2000) that it is a group of anterior cingulate neurons being more active during search behavior, whereas another group is more active during the routine behavior. Search related neuron activities are specific to a situation requiring flexibility of behavioral responses and evaluation of the outcomes.
The identification of purely behavioral criteria of search presents certain difficulties.
As we have already mentioned above, an identification of search behavior with motor behavior may lead to serious errors.
Search can proceed without any manifestations in the motor sphere if the movements pose a threat or, according to the natural or experimental conditions,
involve a punishment. The temporary inhibition of overt behavior at the encounter with a new,
surprising, or emotionally significant situation is a very well tested phenomenon (Gray, 1982; Morrison, 1982).
During such inhibition intense reappraisal of the situation proceeds; that is, search behavior. Passive avoidance works.
It is not a renunciation of search. For example, in the Porsolt Test intense search activity
characterizes the rats that find the shallowest place in the pool sooner than others,
where they can maintain immobility resting on their tail. Conversely,
less adapted rats inclined to panicky behavior spend a much longer time performing exhaustive movements around the pool (Hawkins et al., 1980).
This unproductive chaotic behavior appears to be inversely correlated with search activity.
An exclusive orientation to motor activity without consideration of the entire context of
the situation and without registration of the activity of hippocampus frequently leads
to the erroneous identification of such salutary passive avoidance with the reaction of surrender (renunciation of search) of the freezing type.
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