Stress-induced eating: Fact, fiction or misunderstanding?

Appetite 1980, 1, 103-133

Stress-induced Eating: Fact, Fiction or Misunderstanding? T. W. ROBBINS and P. J. FRAY The Psychological Laboratory, University of Cambridge

The commonly-held view that stress can elicit eating, and that this eating is an attempt by the organism to reduceanxiety, is criticallyexamined. It is shown that a variety of factors, other than food-deprivation and palatability, can elicit eating in animalsand man. Many of theseelicitorsdo not have obviousaversive correlates. It is argued, by analogy with avoidance learning, that the eating cannot produce a reduction in the aversiveness of the eliciting stimulus, since the eating behaviour would not be strengthened and maintained. It is suggestedthat the eliciting stimuli simply activate the organism, making it more responsive to external, food-related stimuli, which direct behaviour towards eating. These stimuli elicit metabolic responses associatedwith eating,whichserveto increaseactivation,and strengthen the eating response further. "A stomach full offood also soothes by draining the blood away from a disgruntled and maladaptive brain" (Selye, 1956). Substitute the word "stress" for "blood" and we have the opinion of many clinicians and popular psychologists of an important aetiological factor in human obesity. The organism eats in order to reduce the stress produced by the anticipation or presence ofa noxious event. Such theorists consider obesity syndromes as being analogous to obsessive-compulsive behaviour, where the performance of a "ritual" eating response is instrumental in reducing anxiety. However, just as others have questioned the role of anxiety-reduction in maintaining obsessive-compulsive neurosis (Beech, 1974; Haslam, 1965; Walker & Beech, 1969; Walton, 1960), we also question its role in maintaining compulsive over-eating. The problem can be attacked by asking two main questions: (1) Can factors other than deprivation or food palatability elicit (over-) eating? If they can, we define these elicitors as exerting non-specific motivational influences upon eating. (2) By what behavioural mechanism are the effects of those non-specific elicitors mediated? One possible mechanism could be the reduction of aversive properties of the eliciting stimulus. We must then assume (a) that the elicitor has aversive correlates, (b) that these aversive correlates (or "anxiety") are reduced by eating, / and (c) that this sort of process can explain not only the acquisition, but also the maintenance of compulsive eating behaviour. This set of assumptions hinges upon the crucial one that stressful situations (or the "elicitors") are aversive. Stress is a vague concept, and difficult to define, but one of the better attempts at definition encapsulates the problem: "... a state when the 'adaptive' mechanisms (of an organism) aretaxed The invaluable comments of J. E. Blundell, D. A. Booth and B. J. Sahakian are gratefully acknowledged. Correspondence and requests for reprints should be addressed to T. W. Robbins, University of Cambridge, The Psychological Laboratory, Downing Street, Cambridge CB2 3EB, U.K. 0195-6663/80/020103 + 31$02-00/0

© 1980 Academic Press Inc. (London) Limited

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beyond their normal range offunctioning either because of the intensity or duration of the response required" (Valenstein, 1976, p. 113). This definition does not include reference to the affective qualities of stressors, but these are often assumed to be aversive or noxious. However, if one ignores the emotional valence of the stressor or elicitor, and emphasizes instead the intensity of the eliciting stimulus, then the need for assumptions about the hedonic properties of stressors are obviated. After reviewing evidence that non-specific stimuli (i.e. stimuli other than fooddeprivation) can indeed elicit eating behaviour, we shall argue instead that many motivational states, including "hunger", "stress" and "anxiety", have in common interoceptive stimulus-changes which are sufficiently similar to be indiscriminable to the response selection mechanism, and which can, therefore, elicit responses apparently irrelevant to the particular motivational state actually present. These interoceptive stimulus-changes provide the substrate for what Killeen, Hanson and Osbourne (1978) call "motivational excitement", or "arousal", and what we shall call activation. Activation is inferred from the rate or vigour of behavioural output. A distinction therefore is drawn between arousal and activation, since the former is often measured as electrocortical desynchrony, and dissociations can be found between electrocortical activity and behavioural output (Feldman & Waller, 1962).Factors determining which responses are elicited by the "non-specific" interoceptive cues include biassing by previous experience of the organism, and by present circumstances. It is very difficult to attribute to these "non-specific" stimuli properties of definite hedonic valence such as pleasure or distress. There is a good deal of evidence ranging from human experimental social psychology to operant behaviour of animals, that these traditional notions of polarity of motivation may be too simple. For example, Schachter and Singer's (1962) experiments on the different interpretations of interoceptive stimuli induced by adrenaline (including both euphoria-and aggression) in human subjects exposed to different contexts are well known, although the results of Maslach (1979)and others must be taken into account. Morse and Kelleher (1977) have recently reviewed work with animals suggesting that stimuli such as electric shock, food or drugs can have both positive or negative properties depending on the context in which they are presented, and the experience of the organism. Perhaps the most dramatic demonstration of this lack of absolute hedonic value of stimuli is the selfadministration of (painful) electric shocks by squirrel monkeys under certain conditions. Such phenomena are difficult to explain in terms ofthe instrumental reduction of a stressful or anxious state, and may stand as remarkable demonstrations of environmental control over compulsive-like behaviour in animals. Moreover, the proposition that an organism can never be said to be "avoiding" one stimulus without also "approaching" another one questions the necessity ofa reduction in anxiety. Thus, to argue that behaviour is instrumental in avoiding or escaping stimuli (the correlates of the aversive event) neglects the possibility that there might be other factors supporting approach to another set of stimuli, making the avoidance response incidental to the elicited approach behaviour. We shall expand this argument in some detail later in the article. However, for the moment, it is sufficient to point out that compulsive eaters often do not feel "relieved" by their eating binges. Rather, these binges can exacerbate, or produce, anxiety states (Leon & Roth, 1977). These phenomenological reports are not explicable in terms of a hypothesis suggesting that the eating binges reduce anxiety. However, they are compatible with the view that eating can be elicited by non-specific stimuli.

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NON-SPECIFIC INFLUENCES ON FEEDING. A. ANIMAL LITERATURE

1. Noises and Other Stimuli Drew (1937) was perhaps the first investigator to realise how eating could be elicited by many apparently "irrelevant" stimuli including incidental noises and lights presented to rats. Drew found initially that satiated rats placed in a wire cage to which the animals had been familiarised, with pieces of bread, did not eat in response to buzzers or lights. However, complex stimuli such as the sound of rapid jets ofwater, or the buzzer in combination with the light produced eating, after an interval ofabout 1,52·5 min. It is worth quoting Drew's description of the eating behaviour: "The success of a sensory stimulus in arousing eating depends on its arousing a state of great activity. Without this activity there is no eating. The normal course of the recurrence ofeating is a sudden jump at the onset of the stimulus followed by a period of great activity, chiefly exploratory in nature, during which the animal explores the cage thoroughly and pays particular attention to the light, but showing no particular interest in the direction of the sound, Then, after this exploratory period, the rat seizes the food and eats. Eating when it takes place is very rapid in nature." Further descriptions suggest that the eating had abnormal characteristics, and was unpredictable, appearing only on about 70% of trials, after which it extinguished altogether. These interesting observations could not be replicated with hungry animals, for which the presentation of buzzers or lights often inhibited their eating behaviour. These latter results are puzzling when considered with a little-known letter to Nature by Kupferman (1964). This paper claimed that noise could elicit a complex chain of behaviour, including chewing, approach to food and eating, in rabbits, guinea pigs and rats. To demonstrate this phenomenon, Kupferman starved rats for two days, put them in a box, and subjected the rats to clicks, hand-claps, whistles, lights, etc. Most ofthe animals "explored", sniffed the food, but did not eat it on the first test day. On the second day, all rats exhibited sound-induced eating, with some animals only eating during the sound stimulus. Kupferman reported that a sound of60dB elicited chewing, 70dB approach and 80 dB active eating. He further claimed that the vigorous rate of eating shown was related to the intensity and duration of the stimulation. Satiation did not inhibit eating in all of the animals, and when deprived of water alone, the animals drank instead. These phenomena clearly deserve further attention, although Fray and Robbins (unpubl. observations) have found it difficult to repeat many of them in pilot studies. 2. Handling, Miscellaneous Disturbance, etc. Anecdotes are rife of animals eating in response to handling (e.g. Wesley, 1978) or injection. However, there are few experimental observations available. Booth and Campbell (1975) reported that saline injections during the day reduced the latency to feed in rats housed in isolation. However, the meal taken was short, and the latency for a second meal was actually lengthened. Some of the most detailed relevant observations again come from the work of Drew (1937). In one set of experiments, satiated rats were placed in cages of varying familiarity either prior to or following the introduction offood. When offered food after the rat had been placed into a familiar cage, the animal would frequently "retrieve" the food, without necessarily eating it. A degree of incongruity was apparently an important determinant for both retrieving and eating to occur. Thus, food placed immediately in front of a familiar home-cage would be retrieved, but not eaten

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immediately, whereas food encountered in novel locations distant from the home-cage would be both retrieved and eaten. In addition, the amount of food eaten depended inversely upon the amount encountered. Therefore, small crumbs of food were eaten where they were found, without being retrieved. Although those early experiments on the balance between hoarding and feeding can perhaps be regarded as examples of "optimal foraging", it is evident that control over satiation is complex, and can depend on such factors as the surprise engendered by food delivery. In other experiments, Drew found that satiated rats would eat if offered food through the bars of their home cage such that effort was required to bite off small pieces of it. This finding has been repeated by our own unpublished informal observations on occasion of similar examples of elicited eating, which are often accompanied by considerable excitement in the rats. In both of the last two cases, the surprise or motivational excitement engendered by incongruity of food delivery, or by the effort required to obtain the food, may be considered to increase arousal or activation. We shall soon consider in more detail similar effects of motivational excitement produced apparently by conflicting or thwarted drive, or by novelty per se. 3. Social Influences Social influences upon eating may reasonably be thought to exist, but experimental work on this factor has produced apparently confusing results. Social isolation has been reported to produce both reductions and increases in food intake in many species. However, social facilitation of eating has also been widely reported. The confusion probably results in part from a confounding between the permanent housing and more transient conditions under which the animals are tested, including both housing and deprivation state. (i) Social Facilitation Bayer (1929) was perhaps the first to demonstrate social facilitation effects, finding that the intake of a satiated hen placed with a hungry hen increased by 25-30%. Placement with three satiated hens increased the intake by 33-67%. He was also able to induce feeding in the satiated hen merely by sweeping the food and replacing it, a result similar to that of Drew's with rats. Since Bayer's time, social facilitation effects have been claimed for the rat (Harlow, 1932), dog (Ross & Ross, 1949), ewe (Tribe, 1950), and monkey (Harlow & Yudin, 1933). However, there have been plenty of results apparently in the opposite direction ("social inhibition") too, e.g. Cooper and Levine (1973). (ii) Social Isolation Isolation-rearing often makes rats gain weight and eat more than normal during ad lib. access (Morgan, 1973; Sahakian, 1976; Shelley, 1965). They tend to eat more during the day than group-reared controls, with no real discrepancy with the social facilitation literature, inasmuch that most demonstrations of social facilitation depend on a deprivation state. Isolation-reared rats also exhibit enhanced gnawing responses to tail-pinch stimulation, are more active, and more reactive to novel stimuli in general (Morgan, 1973; Sahakian & Robbins, 1977; Sahakian, Robbins & Iversen, 1977). The specific cause of enhanced intake in the isolates is less clear than in the other examples; it has been suggested to arise from a thermoregulatory need, from a reduction in competing social behaviour or from increased stress or arousal.

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4. Novelty and Variety Although both situational novelty and novel foods can inhibit eating, these effects probably depend markedly upon the degree of novelty involved. For example, there have been suggestions that variety can stimulate appetite, typically in the context of experimental models of 0 besity in animals involving "cafeteria" feeding(Sclafani, 1978). Analysis of the variety effect has generally been confined to short-term situations. Le Magnen (1956a) found that a repeated change of odour associated with food can cause over-eating, and suggested also that even the change in intensity of single odour could produce this effect (e.g. Le Magnen, 1956b). In pilot work following up these results, Booth (1972) has investigated the psychological mechanisms underlying the novelty-enhancement effect (see Table 1). After prolonged familiarisation of rats to the test odours, he showed that the facilitating effect on intake produced by a change in odour seemed to depend on the nonassociative effects offamiliarisation with the first odour, but were independent of prior exposure to the second odour. That is to say, the elevation of intake was mainly due to the previous experience of the first odour, regardless of its association with food. However, the controlling factors in this phenomenon may need further clarification, since replication of the results has proven difficult (D. A. Booth, pers. comm., 1979). Rolls (1979) has reported further research on the variety effect in both rats and in human subjects. For rats, isocaloric foods were provided of different taste and texture. Hungry rats were tested with each of four foods alone, and with all four foods in succession over four, 30-min periods. A variety effect of over-eating was evident in the second, third and fourth period when there was a change in food. Parallel experiments with human subjects revealed a similar effect.Further work on the variety effect should perhaps focus on the question as to whether the results are due to contrast effects resulting from differential baseline preferences between the two foods, or whether the effect is still present with changes among equally-preferred foods. TABLE 1 Food eaten (g in 30 min) after change of odour (Booth, 1976)

Odour 2 Odour 1

(a)

(b)

(c)

(a) Un familiarised (b) Familiarised, food present (c) Familiarised, food absent

2·0 5·5 5·1

2·5 4·9 5·0

2·3 3-8 4·9

5. Pharmacological Elicitation of Eating (i) Neurotransmitters and Eating

Interest in the neurochemical substrates of feeding was sparked off by Grossman's (1962) discovery that noradrenaline or adrenaline, when injected into the hypothalamus could induce eating in the rat, but did not reliably increase drinking, whereas carbachol, a cholinergic drug, produced strong drinking, but suppression of foodintake. This is a striking dissociation between two different motivational states, but the behavioural specificity of the effects perhaps needs further analysis, considering other motivational states. For example, carbachol injected into certain brain areas such as substantia nigra in the rat can elicit strong eating (Winn & Redgrave, 1979) and

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so the possible neurochemical specificity of the earlier results are probably considerably constrained by neuroanatomical considerations. It is also salient, for example, that tail-pinch apparently provides a similar dissociation (Antelman, Rowland & Fisher, 1976a) and it seems most unlikely that this stimulus could be uniquely involved with feeding-motivation. Nevertheless, technical refinements have revealed that noradrenaline (NA) administered intracerebrally can produce meal patterns that closely resemble those of normal eating (Leibowitz, 1975). In addition, NA (but not dopamine) release has been observed from dorsomedial and perifornical regions in the hypothalamus during feeding, but not during the performance of other activities such as drinking or grooming (Slangen & van der Gugten, 1977; van der Gugten, 1977). In this latter study, NA release from the medial hypothalamus was enhanced by 16 h of food-deprivation. A detailed review of noradrenaline-elicited eating is beyond the scope of the present article. However, although NA release seems to be tied to hunger-motivation in some way, the demonstration of correlation does not provide a psychological or physiological account of the processes determining meal patterning, which may be no less specific than some of the cases we have discussed. Tailpinch, for example, produces increased noradrenaline turnover in the forebrain (Antelman, Szechtman, Chin & Fisher, 1975). Dopamine has been accorded a far less specific role in the induction of eating. Ungerstedt (1971) demonstrated that dopamine depletion ofthe nigrostriatal pathway could mimic many of the behavioural effects of aphagia and adipsia that electrolytic lesions of the lateral hypothamus produce. The depletion also seemed to produce a general motivational state of sensorimotor neglect that was not solely restricted to food-related stimuli (Marshall, Richardson & Teitelbaum, 1974). Intriguing evidence of a possible general activating role for DA release has been provided by subsequent demonstrations of reversal of the aphagia by such stimuli as tail-pinch (Antelman et al.; 1976b), immersion in cold water (Marshall, Levitan & Stricker, 1976)and injection with catecholamine agonists such as d-amphetamine (Teitelbaum & Wolgin, 1975). These surprising demonstrations strengthen our argument that eating can be elicited by rather non-specific stimuli. It must not be thought that research into neurochemical control of eating has concentrated solely upon the catecholamines. Virtually every other putative neurotransmitter has been implicated in feeding, of which perhaps GABA (see Hoebel, 1977), serotonin (Blundell, 1977) and the peptide hormones (e.g. Margules, Moisset, Lewis, Shibuya & Pert, 1978) are the most salient examples. Furthermore, the consensus would be that no neurotransmitter system can be considered in isolation because of multiple dynamic and topographic interactions. These too are beyond our scope, but the effects of drugs on eating that we summarize below may ultimately be precisely linked with their neurochemical actions. (ii) Drugs and Eating Almost exhaustive reviews have been provided by Hoebel (1977) and Blundell and Latham (1978). A diversity of drugs can elicit eating possibly by mimicking underlying neurochemical substrates for eating, but there are also grounds for believing that some of these agents may work in an indirect fashion. Benzodiazepines and Barbiturates. Anti-anxiety drugs such as chlordiazepoxide (CDP) and diazepam (DP) can produce eating in both deprived (Poschel, 1971) and satiated (Wise & Dawson, 1974) animals. There is controversy as to whether the

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facilitatory effect is directly upon appetite, or is mediated via an indirect effect of reducing "emotionality" that can sometimes inhibit food-intake. For example, the stimulant effect upon appetite might arise from the attenuation of "emotional" responses either in reaction to novel food or to a novel environment containing food. There is clear evidence that CDP increases intake of novel food (e.g. Poschel, 1971). However, Wise and Dawson (1974) have presented persuasive evidence ofthe similarity of effects between manipulation of food deprivation and benzodiazepine treatment. Similarly, Cooper and Posadas-Andrews (in press) have shown the similarity of effects of CDP and food deprivation in enhancing the time spent eating familiar chow following familiarisation tests in an open-field with several alternative foods. Cooper and Crummy (1978) also found that CDP increased time spent eating familiar food, whilst not changing the time spent eating novel foods. Hence, these findings favour the hypothesis that the benzodiazepines, at least at certain doses, may enhance eating by a more direct action than upon reduction of "emotionality". On the other hand there is evidence that CDP can increase tail-pinch-induced eating at doses not affecting eating in the open-field in satiated animals immediately preceding the tail-pinch trials (Robbins, Phillips & Sahakian, 1977), and Tye, Nicholas and Morgan (1975) have found evidence for reduction of neophobia in a situation producing "responding in the presence of free food". Clearly, work remains to be done to clarify further the mechanism underlying the facilitation of eating by benzodiazepines. An obvious possibility is that these drugs exert both "specific" and "non-specific" influences on eating that are separately mediated by elements of the diversive neurochemical actions of these drugs. These remarks may also apply to the facilitation of feeding by barbiturates in satiated rats (Jacobs & Farel, 1971; Watson & Cox, 1976), which has thus far been analysed less. Amphetamine and Apomorphine. Amphetamines are classic anorectic drugs (Hoebel, 1977) and so it is perhaps surprising to note that these drugs can apparently stimulate eating in some sense, under particular conditions. The induction of eating in aphagic cats by d-amphetamine (Teitelbaum & Wolgin, 1975) was mentioned earlier. Holtzman (1974) reported a definite mild stimulation of food-intake in rats by low (0,3 mg/kg) doses of d-amphetamine. Since then, Blundell and Latham (1978) have observed similar results, but have formed a detailed analysis of meals which takes into account frequency, duration, and rate of eating. Their results show that certain doses of amphetamine enhance the rate of eating, even when the total intake is reduced because the drugged animals spend less time eating. This is good evidence for behavioural competition as a process underlying stimulation of behaviour by amphetamine (Lyon & Robbins, 1975), and suggests that possible facilitating effects upon appetite may be masked by this competition and also perhaps by a genuine anorectic effect also. The nauseous and anorectic effects of apomorphine, a dopamine agonist, are perhaps surprising when considered in the context of the earlier discussion of the facilitatory role of DA in feeding. To escape the paradox that DA activity can apparently both elicit and inhibit eating, many theorists invoke the ubiquitous inverted U -shaped function which relates .the curvilinear effects of arousal or activation to efficiency of behavioural performance (Yerkes & Dodson, 1908). That is, high levels of activity disrupt efficiency because of "over-activation", whereas low levels disrupt efficiency because of the converse effect. Lyon and Robbins (1975) have proposed more specifically that behavioural sequencing, which is probably crucial in controlling eating

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responses, is disrupted by increasing rates of behavioural output. Evidence for these notions is not easy to obtain, but a recent report of Eichler and Antelman (1977) is germane. They found that apomorphine, in low doses (0'05-0' 30 mg/kg), stimulated eating in rats "pre-sated" with sweet mash, but the same doses reduced eating in fooddeprived rats. As these authors state, the findings are consonant with an inverted-U model of the involvement of DA in behaviour. According to their idea, activation produced by food-deprivation may summate with apomorphine to inhibit eating, but in "sated animals" apomorphine produces an "activation of DA receptor activity within the limits appropriate to stimulate feeding" (Eichler & Antelman, 1977, p. 538). An alternative interpretation is that the stimulant effect of low doses of apomorphine results from inhibition ofDA neurones by preferential stimulation of presynaptic DA receptors. However, this possible action must still be dependent on the behavioural state of the organism. Neuroleptics. Drugs which are commonly used in treatment of psychosis can stimulate intake in both rat and man. This effect is well-documented for the phenothiazine, chlorpromazine (e.g. Robinson, McHugh & Bloom, 1975; Stolerman, 1970), but the underlying neurochemical mediation remains obscure, and may even depend upon inhibition of insulin release (see Robinson et al., 1975). Clozapine, a dibenzodiazepine, can also elicit eating in the rat, when injected by either intragastric or intraventricular routes (Antelman, Black & Rowland, 1977), and can also apparently stimulate tail-pinch-induced feeding (Antelman & Szechtman, unpubl. observations). The mechanisms underlying these effects again are obscure. Antelman et al. argue for an anti-adrenergic action, but another possibility may be the relatively specific DA receptor blocking action in structures such as the nucleus accumbens and olfactory tubercle. Depletion of DA from these regions by the neurotoxin 6-hydroxydopamine can produce small increases in feeding in some contexts, possibly because of the removal of competing locomotor activity (Koob, Riley, Smith & Robbins, 1978). 6. Irrelevant Drive

Again, there have been several anecdotal reports of eating in situations with alternative dominant drives to that of hunger. Barnett (1958) has described bouts of eating in wild rats during brief interludes during copulation and there are several reports of eating in birds during boundary disputes (e.g. Hinde, 1952; Pickwell, 1931; Tinbergen, 1937).Such behaviour is often termed "displacement activity" (Tinbergen, 1952). Later we shall describe how vigorous eating could be induced following thwarting of eating when sticklebacks were hungry (Tugendhat, 1962).However, in this section, we wish to discuss examples of vigorous behaviour occurring during the period of thwarting of a dominant drive. "Adjunctive behaviour" serves as an excellent laboratory analogue of displacement activity. Typically; if hungry rats are presented with single 45-mg food pellets, with inter-pellet intervals of about 30-120 sec, drinking may occur which is excessive and which cannot be explained in physiological terms, nor as an example of "superstitious" behaviour (Falk, 1971). A possible explanation of this drinking is that motivational excitement outlasts the consumption of the food-pellet and can elicit alternative behaviours, such as drinking, activity or aggression, which are high in the animal's repertoire (Killeen et al., 1978). The obvious question then arises, can increased eating be generated in satiated animals when presented with incentives related to another deprivation state? Thus far, although adjunctive eating has been observed in the

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intervals between the presentation of small volumes ofwater in water-deprived rats, the eating is not excessive, and could hardly be expected to lead to obesity (see Wetherington & Brownstein, 1979). 7. Electric Shock ("Fear")

Fear inhibits gastric motility and causes release of sugar into the blood (Cannon, 1915; Carlson, 1916). Consequently we might expect fear caused by noxious stimuli to inhibit the physiological contribution to hunger. Indeed, a standard anxiety-test invented by Estes and Skinner (1941) depends upon a stimulus paired with shock inhibiting operant behaviour for food (conditioned suppression). However, even here things are not completely clear-cut; the use oflow baselines of responding can result, in certain circumstances, in increases in responding during the CS which question the effect of anxiety on hunger motivation (Blackman, 1968). Therefore, the apparent incompatibility of instrumental responding for food with "anxiety" or "fear states" may depend on response incompatibility rather than on some opponent motivational process where "fear" inhibits hunger. Anecdotal observations support this view; Kelley (1973) reports that chewing of food-pellets by monkeys exposed to an "aversive" CS was observed in the study by Brady, Kelley and Plumlee (1969). Kupferman (1964) similarly describes chewing and eating movements made by restrained rabbits in an aversive conditioning procedure, both during and immediately after an electric shock, although the shock had never been paired with eating. Thus it appears that consummatory and instrumental elements in feeding chains may be differentially affected by shock (or "fear" or "anxiety"). There have been several studies on the effects of "fear" induced by electric shock on eating in animals. All of these have shown that eating can be increased by shock in certain circumstances. Two of the earliest studies of the effects of electric shock on eating were by Ullman (1951,1952). In the first of these, female rats were trained to eat small food-pellets in four, 20-min sessions. In subsequent sessions electric foot-shocks (24'5 /lamp) were then introduced for 5 sec of each minute. These shocks reduced eating for the first two days, followed by increases in eating mainly during the 5-sec periods when the shock was on. As the intensity of the shock was subsequently slowly increased to 32/lamp, so the eating also increased. Although preloading with food reduced eating, much of the remaining eating was in the shock periods. These results were generally replicated in a second study (Ullman, 1952), when a parametric design showed that shock-induced eating was maximised by high levels of hunger (80% of free-feeding weight), relatively high levels of shock, and only short (i.e. 20 min) durations of training to eat in the test situation prior to the introduction of shocks. The major criticisms ofthis study, the lack of comparable control groups receiving no electric shocks, was met in a later study by Sterritt (1962).Rats were deprived to 80% offree-feeding weight, followed by one 5-min pre-exposure to a test apparatus containing food-pellets, but with no shocks presented. There were then two phases: (1) On days 1-4 following pre-exposure, rats were placed in the apparatus for 21 min, with shock (either 0·5 or l-Omamp, for different groups) being turned on during the first 5 sec of each minute of the test, following the first minute. Gathering or eating food-pellets did not affect the schedule of shocks. A control group received no shocks. (2) Following day 4, the rats were "sated" by pre-exposure to wet-mash, and the same procedure was used for days 5-8. The main measure was the number of food-pellets eaten and the main results ofthe experiment are shown in Table 2.

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T. W. ROBBINS AND P. J. FRAY TABLE 2 Effect of electric shock on eating iSterriit, 1962)

High shock Deprived

Low shock

No shock

Satiated

Deprived

Satiated

Deprived

Satiated

785

297

830

200

569

177

In 20min

3658

515

5358

751

6500

2171

% Pellets eaten during first 5 sec"

21-4

57-7

15·5

26·6

8·8

8·1

Number of pellets (4-day total)

In first 5 sec

a g.3% is the expected value if eating in first 5 sec is at the same rate as the rest of the test period. Copyright (1962) by the American Psychological Association. Reprinted by permission.

The major findings were: (a) shocks increased eating during the 5 sec shock periods in the deprived phase; (b) there was more eating in shock than in no-shock periods, this effect being greater in the "sated" phase; (c) eating was inhibited in no-shock intervals in the shock compared to the no-shock groups; (d) overall, there was greater eating in the no-shock group. Thus, there appears to be a sharp division in the incidence of eating during and immediately after a shock period. However, Fentress (1976) has discussed how anticipation or recovery from intense forms of stimulation may facilitate broad categories of behaviour, and so one might expect the activation produced by electric shock sometimes to out-last the presentation ofthe shock stimulus, and perhaps, in the longer term, facilitate eating. Indeed, the anecdotal instances of eating during aversive conditioning procedures mentioned above adds credence to this view. In experimental studies, Strongman (1965) and colleagues (Strongman, Coles, Remington & Wookey, 1970) have demonstrated enhanced intake in rats as an aftermath of experience of electric shocks. In the 1965experiment, three groups offive rats, (all deprived offood for 23 h) were subjected to low (3 sec), medium (30 sec) or high (300 sec) periods of footshock (2'6 mal in a shock compartment. A fourth (n = 15)served as unshocked controls. After this experience, the rats were transported back to their home-cages and given access to their normal diet for 1h. Rats given low duration of shock showed 80% increases in normal dietary intake, whereas the medium and highshock groups showed a slight reduction in intake, relative to the unshocked controls. Parallel groups of rats (each n= 10),also receiving low, medium or high durations of shock were exposed to a quinine-adulterated diet upon return to their home-cages, and uniformly showed reduced eating compared with unshocked controls. Therefore, the post-shock state evidently interacts with the palatability of the food in producing changes in intake. This latter effect obviously deserved further investigation, since the reduced intake may have been due to an interaction with either the novel or the unpalatable features of the quinine-adulterated diet. Strongman et al. (1970)repeated the earlier study with the exception that the different groups received adulteration of food with a novel, but palatable substance, sucrose. The duration of shock (3 or 30 sec),intensity offoot-shock (0, 0'5, 1'5, 2,5, 3·5mal, and level of adulteration by sucrose (0%, 10%, 25%) were all varied in a parametric 2 x 5 x 3 design, using 150, 23-h food-deprived rats. The main results were that, as before, a 3-sec shock generally enhanced intake, whereas a 30-sec shock generally suppressed it. However, there was no systematic variation in food-

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intake with shock intensity, and no interaction of shock intensity with the level of sucrose adulteration, although 10%generally increased intake, whereas 25% decreased it. It seems likely that normal factors contributing to food palatability will influence intake in the aftermath of an intense stimulus such as shock but we see no reason for believing that a special interaction will occur, although this possibility obviously requires further study. Regretfully, there has to date been little detailed analysis of behavioural sequences of eating during or following electric shock. However, one classic study, by Tugendhat (1960) has provided a lead. Sticklebacks have a characteristic feeding sequence comprising visual fixation of the prey (generally Tubifex) and grasping of the prey immediately followed by ingestion. Defining fixation as the initiation of a feeding sequence, and grasping as completion, Tugendhat measured total time engaged in feeding and the ratio of initiation/completion as indices of "hunger drive", in several conditions. Satiation was varied simply by observing behaviour over successive IS-min periods of the session. Conflictinvolved the presentation of shocks upon entering the feeding area, on the first two occasions, or for each 10 or 20 "grasps" of the prey. There were four main subconditions in the conflict condition, involving no shock, lowintensity shock, medium shock or high shock. Thwarting was studied by denying the stickleback access to the prey. Each of these main conditions was investigated after one, two or three days of food-deprivation. The major results were: (1)increasing durations of deprivation did not change total feeding time, but reduced the initiation/completion ratio, thus resulting in more frequent completion of eating sequences; (2) satiation reduced total feeding time and increased the initiation/completion ratio; (3) conflict (i.e. shock) reduced total feeding time, and reduced the initiation/completion ratio; and (4) prior thwarting increased total feeding time, but increased the initiation/completion ratio. Thus, although in terms of duration of feeding, behaviour was reduced by electric shock, when feeding did occur, it resembled that of very hungry fish. A possible interpretation of this result is that the non-specific cues produced by the shock resemble some of those produced by intense deprivation, so eliciting strong eating. However, since shock also elicits behaviour incompatible with eating, such as withdrawal, there will be fewer opportunities for the fish to come into contact with food, thus reducing the time spent feeding. The interoceptive cues produced by thwarting, however, perhaps because of their lessened intensity, increased the propensity towards feeding either in terms of feeding-time or in terms of the number of feeding sequences "initiated". 8. Electrical Stimulation of the Brain (ESB) It seems superfluous to say that it is well known that electrical stimulation of

various sites in the brain, notably the lateral hypothalamus, produces eating. At first sight, it might seem easy to prove that the stimulation is generating a state akin to that offood-deprivation, but this turns out to be quite hard. We suggest that the stimulation does not directly mimic the cues offood-deprivation, but rather, produces a set of nonspecific cues, which under certain conditions the animal learns to interpret as cues of hunger. In fact, the state induced by the stimulation may become indistinguishable from hunger, not because it activates an eating system, but because eating itself may likewise be a response that the animal has learned by a lifetime of Pavlovian association of the activational cues of deprivation and food with eating behaviour. A great deal of evidence suggests that electrically-induced eating is qualitatively similar to deprivation-induced eating. Electrically-induced eating is not simply

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stereotyped mouth movements, as might be expected if the stimulation were directly activating a motor pathway; in the absence of food, animals respond by exploring the environment (Smith, 1972). Electrical stimulation of the brain (ESB) interacts with external sensory factors in a similar way to deprivation; quinine inhibits eating induced by both states (Tenen & Miller, 1964), and preferred tastes facilitate them both (Smith, 1972). Furthermore, Wise and Albin (1973) have demonstrated that an artificially induced taste-aversion disrupts electrically-induced eating of food with the conditioned taste. Finally, super-satiation, by prolonged stimulus-bound eating, increases the eating threshold, leaving the drinking threshold unchanged (Devor, Wise, Milgram & Hoebel, 1970), and food-deprivation facilitates stimulus-bound eating. These facts may all seem consonant with the hypothesis that electrical stimulation of the brain evokes natural hunger. However, ifit is being argued that the motivational states (of hunger) are similar in the two instances, it is also of importance to show that these states can support the learning of similar sequences of behaviour leading to food (such as operant lever-pressing), and that transfer of such learning can occur between the states. Mendelson and Chorover (1965) demonstrated that rats would learn a Tmaze for food during ESB, and Coons, Levak and Miller (1965) showed that rats could be trained.to press one of two levers for food during ESB, and would respond on the other lever if the contingency was changed. The rats were then food-deprived and replaced in the apparatus without ESB under extinction conditions (lever-pressing did not produce food-pellets), The rats continued to respond on the lever previously yielding food-pellets and gradually extinguished. Transfer of a learned habit in this way from one state to another is very strong evidence that the two states are functionally equivalent. Miller (1957) had previously reported transfer the other way; deprived rats trained to lever-press for food were satiated and transferred to a schedule in which ESB was applied for alternating periods of2 min on, 2 min off. The rats pressed the lever for food only during the on periods. These data have been used to support the hypothesis that ESB is activating a site in the brain concerned specifically with the control offood-intake. However, it can also be argued that rather than providing evidence in favour of the specificity of ESB, the results can be used in the opposite way to demonstrate that hunger itself may be largely non-specific. Valenstein and his colleagues have been foremost in suggesting that ESB may indeed be acting non-specifically. The first demonstration (Valenstein, Cox & Kakolewski, 1968b) was that rats given a choice of activities during ESB, e.g. eating, drinking or gnawing wood, would form a marked preference for one of the activities, usually eating. If the food was removed, a second response, drinking or gnawing, would eventually emerge with the stimulation parameters unchanged. Re-introduction of the preferred goal-object resulted in elicitation of eating as frequently as the second response of choice. The authors suggested that the stimulation was inducing a general activational state which could elicit a variety of consummatory activities depending upon the goal-objects present, and the previous experience with those goal-objects. In support ofthis idea, Caggiula (1969) found that the emergence of a second response was retarded by extended experience with the preferred goal-object. Wise (1968, 1969) observed that, in naive animals, considerable experience was necessary with the stimulation before even the first response appeared, and that the threshold decreased with experience. This suggests that the rats have to learn to eat in response to the stimulation, although Wise originally interpreted the results in terms of the stimulation simply altering the sensitivity of the neurones at the electrode tip with repeated testing. However, Valenstein et al. (1970) reported that rats that had gradually acquired a

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response during stimulation of one side of the brain would eat immediately they were stimulated for the first time on the other side of the brain, even when the electrode was not in the same part of the lateral hypothalamus. Wise (1974) admits that this is indisputable evidence that the emergence of stimulus-bound eating reflects learning. This conclusion is strongly supported by the finding of Watson, Short and Hartman (1979), that rats, trained to eat one food during ESB, took time to switch to another food, even though they had been familiarised with it under food-deprivation. If, then, lateral hypothalamic stimulation is non-specific, it may seem somewhat surprising that the observed behaviour is so rigid and compulsive. Rather than switching between different goal-objects during the stimulation, rats develop a strong preference for one goal-object and spend their time almost exclusively with this. Furthermore, Valenstein et al. found some puzzling properties of the rats' choice behaviour, which, on the surface, are not consistent with the idea that the stimulation is making the rats hungry. Given the choice of food-pellets, the same pellets in powdered form, and water, they initially selected food-pellets, but when these were removed, they .switched to water rather than to the powdered food, as might be predicted if the stimulation was making them hungry (Valenstein et al.; 1968c).Similarly, rats given the choice of a familiar water-dish, which they preferred over a water-bottle when waterdeprived, chose the bottle during ESB and did not eat much. When the bottle was removed, they changed to eating rather than drinking from the dish (Valenstein, Kakolewski & Cox, 1968a). Valenstein and Phillips (1970) found that rats reared on a liquid diet, without contact with solid objects, preferred to eat food-pellets when stimulated, although they had never experienced the pellets before. One possible explanation of both the rigidity of the behaviour observed during ESB and the rather unexpected results of Valenstein et al. is that the stimulation at anyone site has mixed effects, both appetitive and aversive, and the aversive component partially antagonises the eating induced by the appetitive component. Evidence of mixed effectsofESB comes from a study by Soper and Wise (1971), demonstrating that the tranquillizer diazepam (Valium) increases stimulus-bound eating, and can induce previously unresponsive rats to eat during the stimulation. The anxiolytic effect of the drug presumably reduces the effect of the aversive component of the stimulation, unmasking the appetitive component, which is expressed by increased eating. Wise and Erdmann (1973) have suggested that this aversive component, by making the animals "emotional" will also make their behaviour more rigid. As a test of this hypothesis, they studied the eating behaviour of two groups of deprived rats (without electrodes) when given the choices of goal-objects used by Valenstein et al. One group of rats was wellhandled and habituated to the test apparatus before the experiment, whereas the other group was unhandled and unhabituated and therefore could be expected to be more "emotional" in the test apparatus. The handled, habituated rats switched readily between different foods, whereas the "emotional" rats did not. Furthermore, the "emotional" rats were more likely to switch to water rather than to a second food when the preferred food was removed, and preferred novel, solid food to a familiar liquid diet, which was the choice of the other group. Thus, manipulations which should make the rats more "emotional", that is exposing them to a novel test-chamber and not handling them, produced the rigidity of the behaviour characteristic of that seen during ESB. This suggests that ESB does indeed have mixed effects, and the rigidity of the behaviour is produced by very high levels of activation or arousal similar to emotional stress. In all of Valenstein et al.'s experiments the rats preferred to indulge in behaviour involving an intense licking or

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biting response, even when this meant changing to a novel goal-object; this compulsive desire to bite something may be a reflection of the high state of arousal produced by the stimulation. 9. Tail-pinch

Tail-pinch is a largely non-specific stimulus of eating that has received a great deal of attention recently; in particular, comparisons have been drawn with ESB, since if it can be shown that tail-pinch has similar properties to ESB, the case for a non-specific action ofESB is supported. Antelman and Szechtman (1975) reported that a sustained, mild pinch to the tail could induce eating, gnawing and licking in nearly every rat tested. The pressure ofthe pinch could be adjusted so that the rats would eat vigorously without vocalising or showing other signs of distress. Rowland and Antelman (1976) have demonstrated hyperphagia and obesity in rats drinking milk during a 10- to 15min pinch every 4 h for up to five days. Other features of tail-pinch-induced behaviour encourage a comparison with behaviour produced by electrical stimulation of the brain. For example, Antelman et al. (1976a) have shown that preloading the stomach with milk reduced tail-pinch-induced milk drinking; isotonic saline was ineffective. They were able to produce a taste aversion to saccharin-flavoured food-pellets induced by lithium; unflavoured pellets were consumed normally. They also showed that diazepam would facilitate a switch to a novel food. Robbins et al. (1977) have also demonstrated that chlordiazepoxide (Librium) increases tail-pinch-induced eating at doses which have no effect on eating during control trials with no pinch. As with ESB, the eating behaviour takes some time to appear. On the first trial, rats usually run around the test arena, showing evidence of a high level of activation; they bite at protruding parts of the apparatus and lick their tails and the floor. When they come across food-pellets, they give them an occasional bite, but with repeated experience, the eating behaviour becomes stronger and, by the fifth trial or so, most of the competing responses are replaced by eating (Koob, Fray & Iversen, 1976). At first-sight, it might appear that tail-pinch is a purely aversive stimulus, rather like an electric shock, and the animals' reactions are merely coping responses which reduce the aversiveness of the pinch. This is a difficult hypothesis to test. However, the results with diazepam and Librium suggest the same analysis put forward for ESB; the pinch has mixed effects, and the inhibitory effect is reduced by the tranquillizers allowing unmasking of the appetitive component. As with ESB, it was important to show that tail-pinch is having a genuine motivational effect,and so it was demonstrated that rats with their tails pinched would learn a T-maze for the opportunity to gnaw on wood (Koob et al., 1976), and food (Fray, Koob & Iversen, 1978).The finding that the rats would readily reverse the maze (Koob et al.; 1976) suggests that the principal motivation was not simply to have the pinch removed, since this could be achieved in either goal-box. Rather, the wood-chips had gained some positively reinforcing value of their own, and it was this that the rats were running for. This conclusion was supported by a further experiment (Fray et al., 1980),in which the same rats were required to reverse the maze again, but this time the tail-pinch was removed when they reached either goal-box. The rats successfully reversed the maze, running towards the wood-chips, but not gnawing them, since the pinch was removed as soon as they reached them. Naive rats, which had no experience of gnawing wood under the influence of tail-pinch, did not learn the maze under these conditions. Thus, the wood-chips had acquired reinforcing properties, as a result of pairing with tail-pinch, sufficient to change a learned habit in the absence of a consummatory response.

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If the reinforcing value of a particular activity has to be learned during tail-pinch, we can ask to what extent this reinforcement is similar to that experienced during natural, deprivation-induced eating. This calls for some kind of transfer experiment, in which rats, trained on a task for food reinforcement under conditions of fooddeprivation, are then tested on the same task, satiated and under tail-pinch. If the transfer oflearning is flawless, it can be argued that the rats regard the two motivational states (deprivation and tail-pinch) as sufficiently similar to be indistinguishable functionally. However, transfer is rarely flawless, and so a control group is called for, with which to make a comparison. Such a control group might be given a different task under deprivation, and given the same task as the experimental group when transferred to tail-pinch. This task would be new to them, and so if the experimental group were to do better than the control group during the transfer phase, this might provide evidence of a transfer of information in the experimental group. Unfortunately it can be argued that the difference in performance is not due to the experimentals doing better but the controls doing worse, because they have experienced a change in both motivational state and task, and are therefore prone to greater non-specific disruption. Thus the control group should have identical experience to the experimental group; if this is the case, they cannot be controls! The solution (Fray, Koob & Iversen Note 1) was to make the change at the transfer stage. One large group of rats was given experience of eating under the influence of tailpinch, and then trained on a spatial discrimination in a T-maze for food reinforcement under food-deprivation. The rats were then divided into two groups, balanced for performance on the T-maze task. They were all returned to ad lib. feeding and then tested in the T.-maze under tail-pinch, with one group required to continue the same spatial discrimination (FC group: pre-exposed to Food under tail-pinch; trained in the maze under deprivation; and required to Continue the same discrimination under tailpinch), and the other group required to reverse (FR group: pre-exposed to Food under tail-pinch; trained in the maze under deprivation; and required to Reverse under tailpinch). If the rats remembered nothing of their previous experience in the maze under deprivation the two groups should have performed equally badly during transfer, but if they did remember there would be a difference. This was found to be the case. However, it is not necessarily a correspondence between the motivational states that results in transfer. The difference between the groups might well be 'due to cues from the maze reminding the rats what to do. If the difference in performance is indeed due to the fact that the rats had learned to associate tail-pinch with eating, and this association produced a state similar to that experienced during hunger, then rats preexposed to wood, rather than food, under tail-pinch, trained in the maze for food under deprivation as were the other two groups, and then tested in the maze for food under tail-pinch on the same discrimination (a WC group) should do worse than the FC group, since they have never learned to associate tail-pinch with eating. Also, a WR group, in which the rats are pre-exposed to wood under tail-pinch, trained in the maze under food-deprivation and then required to reverse the maze for food under tail-pinch would provide a measure of the transfer due to maze-cues when compared to the WC group. The results showed that the FC group took fewer trials to return to criterion than the WC group during the transfer test, indicating that tail-pinch was sufficiently similar to food-deprivation for learned information to be transferred between the two motivational states, and that this transfer was critically dependent on pre-exposure to

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food under tail-pinch; the similarity was learned. The we group performed better than the WR group, but not significantly so, indicating no real effect of reminder by the maze-cues. The WR group did as badly as the FR group; since a first reversal usually takes as long as initial acquisition, this was to be expected. The fact that tail-pinch can acquire a functional similarity to hunger with experience suggests that not only the tail-pinch and ESB have their effects in a nonspecific way, but so does food-deprivation itself. Animals may have to learn the significance of hunger with respect to eating behaviour in the first place, and all the nonspecific influences on eating may be a re-enactment of the original learning. Despite strong parallels between tail-pinch induced behaviour, ESB-induced behaviour and behaviour induced by natural motivational states, there are some discrepancies which compromise attempts at synthesis. For example, it has proven difficult to elicit drinking with tail-pinch in contrast to ESB (Antelman et al., 1976a). Although tail-pinched rats will not drink water, they will take milk and saline (Marques, Fisher, Okrutny & Rowland, 1979), which is consistent with the view that tail-pinch enhances reactivity to salient external stimuli.

10. Lesions of the Ventromedial Hypothalamus (VMH)

Obesity and over-eating produced by lesions of the VMH have been the subject of a great deal of research, which cannot be fully reviewed here. We will mention briefly a few studies which suggest that the lesion produces a general hyper-reactivity to environmental stimuli; a modified theory along these lines has recently been proposed by Powley (1977), which, we believe, gives an excellent account of the data. Grossman (1966)reported that VMH lesions produced increased irritability in rats during handling, and that the rats were improved in the acquisition of an active avoidance response, suggesting that they were generally over-reactive to the negative aspects of a situation; this would explain their finickiness, and over-reactivity to the positive aspects offood would explain their hyperphagia. Marshall (1975)showed that rats with unilateral VMH lesions spent more time feeding from a food-cup on the contralateral side, and were hyper-responsive to visual, olfactory and tactile stimulation on the contralateral side, in a manner that is complementary to the contralateral sensory neglect produced by unilateral hypothalamic lesions. Thus the obesity may result indirectly from this heightened sensitivity. However, the lesion also produces metabolic effects(e.g. hyperinsulinaemia), and so it is possible that this is the primary result of the lesion, leading to behavioural hyperreactivity as a secondary effect. Equally, the metabolic effects could be a direct result of the increased food-intake generated by the hyper-reactivity. Or thirdly, the hyperinsulinaemia could be one expression of a general autonomic reactivity displayed towards all stimuli, particularly food-related ones. In trying to tease apart cause from effect concerning over-eating and metabolism, it is significant that there is a great deal of evidence that the metabolic disturbance does not result from increase in total daily food-intake. For instance, Han (1968)found that VMH rats became obese compared to controls when both groups were fed a fixed amount of food. All rats were kept in restraining cages so that no significant differences in activity could have contributed to the result. Thus, over-eating per se cannot account for the metabolic effectsof the lesion (Friedman & Stricker, 1976).However, it is not clear how a metabolic disturbance can account for hyper-reactivity to a wide variety of environmental stimuli on one side of the body after a unilateral lesion, and unilateral over-eating (Marshall, 1975).

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To resolve this paradox, Powley (1977) has proposed an ingenious mechanism centred around the cephalic reflexes. He suggests that the lesion produces an exaggerated sensory reaction to stimuli, and as a consequence, exaggerated foodrelated reflexes, such as release 0 f insulin. These responses make the animal hungrier than it really is, and so more food is eaten. Even when over-eating is prevented, the increased insulin release will nevertheless lead to the increased deposition of fat. Evidence in favour of this idea comes from studies showing increased food-associated insulin release in VMH animals immediately after the lesion (e.g. Steffens, 1970). In addition, Weingarten and Powley (in Powley, 1977) measured gastric acid secretion during an 18min CS, during the last 3 min of which a high-fat food was given. A conditioned increase in gastric acid release developed, and then the animals were given VMH lesions. Immediately after the lesion, measurements were taken of gastric acid secretion every day for 12days during the 15min oftheCS prior to food delivery. Only those rats which had good VMH lesions showed an enhanced conditioned acid secretion immediately after the lesion. These rats were also shown to be hyperphagic when allowed free access to the high-fat diet. Thus increased gastric acid secretion is a good predictor of hyperphagia; since the enhanced secretion was seen during the CS before food was delivered, the effectof the lesion must have been due to an over-reaction to the stimuli predicting food.

I.

NON-SPECIFIC INFLUENCES ON FEEDING.

B.

HUMAN LITERATURE

There have been rather few studies on the effect of stressors on food intake. Mostly, they have been concerned with two major hypotheses, which apparently are in some conflict. (i) Externality Hypothesis (Schachter)

Overweight individuals are "over-controlled" by food-related cues, while their eating is relatively unaffected by internal hunger and emotional states (e.g. Schachter and Rodin, 1974). (ii) Psychosomatic Hypothesis (Various Authors)

Implied in the writing of many theorists is that over-eating is a mechanism to reduce anxiety generated by internal emotion states (see Leon & Roth, 1977for review; Bruch, 1973; Kaplan & Kaplan, 1957). Bruch's view is more eclectic and original than most in considering eating habits of obese subjects, e.g.: "During eating binges they feel driven to eat against their wish not to gain more weight, and even consume food they ordinarily dislike. They experience neither hunger nor pleasure or satiation during this kind of eating. They may find temporary relief from the anxious and depressive feelings that have been mistakenly experienced as 'need to eat', but it is short-lived and the cycle of 'not feeling right' and unsatisfying eating is endlessly repeated" (Bruch, 1973, p. 45). But Bruch's complete view is definitely more subtle than this, and it is her other notions that we wish to pursue, since they provide a bridge between the "externality" and "psychosomatic" accounts. Specifically, Bruch has proposed that hunger cues can be "confused" with cues from emotional states, and that this lack of discrimination can produce "inappropriate" eating. She thus emphasises the importance of early experience and learning in abstracting from the total stimulus input that pattern of cues

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which is eventually labelled as "hunger" and leads to eating behaviour. This second set of ideas can be readily distinguished from the "anxiety-reduction" account, and so it is possible to reject the anxiety-reduction hypothesis but retain the emphasis of learning as an important mechanism in the development of hunger (cf. also Hebb, 1949).For the moment, however, we consider experiments in which "anxiety" has been manipulated in attempts to study such non-specific influence on intake in both normal and obese subjects. Before reviewing this literature, it is important to note that most of these studies are performed on restricted populations of mildly-obese college students, and hence generalisation to other populations should be guarded. In addition, the measures of eating are generally made in contrived circumstances designed to mislead the subjects from believing that they are actually participating in an experiment on eating. Indeed, some ofthis eating, often of cashew nuts or crackers, might almost be described as "adjunctive" or "displacement" eating. 1. Non-specific Influences on Human Feeding: Results

One ofthefirst studies conducted as a test of the psychosomatic hypothesis was that of Schachter, Goldman and Gordon, (1968) in which subjects were threatened with severe or mild shock (high and low fear) and eating measured directly in a "taste test". The results were that normals ate more when calm than when frightened. The obese ate the same amount of food in high and low fear conditions, and did not report any subjective reduction offear contingent upon eating. Rather naturally, these results were interpreted as evidence against the psychosomatic hypothesis, that the obese are overcontrolled by interoceptive cues resulting from the aversive emotional state. Instead, the results are consistent with Schachter's externality hypothesis. Similarly, McKenna (1972) found no evidence to support the psychosomatic position. Subjects received "physiological" procedures designed to produce anxiety and one group only received reassurance that the procedures were not harmful. Eating of both "good" and unappetising food was measured. In this study, the normal subjects ate more when calm than when aroused because oflack ofre-assurance. The obese ate slightly more good food in the "aroused" than in the "calm" state, but this result only achieved significance at the p < 0·10 level. The obese subjects did not apparently experience "reduction of arousal" during eating, as measured by report of anxiety. Both the Schachter et al. and the McKenna studies have been criticised because they manipulated "objective fear" rather than "neurotic anxiety" which the psychosomatic theorists postulate affects eating. Therefore, Abramson and Wunderlich (1972) threatened obese subjects with shock (i.e. objective fear) or made predictions of later social failure of the subjects (i.e. neurotic anxiety). The obese ate the same amount in all of the conditions, although data from questionnaires collected in the study suggested that the experimenter had been successful in generating different emotional states. Hence, the psychosomatic position again lacks support. Despite these rather disappointing results, Slochower (1976)has recently performed a major experiment which has clarified many of the issues. She criticised the assumption of Abramson and Wunderlich that neurotic anxiety was in fact generated by the prediction of social failure, maintaining that the "arousal" induced would have been too specific and easily identifiable to be interpreted by the subjects as "anxiety". Therefore, she varied the degree to which subjects would be able to attribute high levels of arousal to an external cause. The absence of such possibilities of "rationalisation" of a high arousal state is held to induce anxiety. To achieve this, Siochower arranged an experiment that was apparently concerned with the "psychophysiology of thought".

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Subjects were led to believe that their heart-rate was being monitored with auditory feedback; in fact they were being fed either low or high heart-rates as auditory feedback. These two conditions are assumed to generate relatively low or high arousal. One subgroup of obese or normal subjects with high-rate feedback was given a good reason why their heart-rate was apparently high (i.e. an artefact of the sound characteristic of the room). This was the "labelled arousal" condition. In the other sub-group, subjects were not given a good reason for their apparently rapid heart-rate. This was the condition of "unlabelled arousal". Eating of cashew nuts was then measured in a 3-min period with the usual "covert" procedures. The results showed a striking dissociation. Obese subjects showed large increases in intake in the high arousal, unlabelled condition compared with the normal-weight subjects who actually showed reduction in intake. That is, high unlabelled arousal ("anxiety") produced effects on eating in opposite directions depending on whether the subjects were of normal-weight or obese. On the basis of this evidence, together with other data on subjective report, Slochower finds in favour of a role for anxiety in eliciting food-intake, although she does not reach any firm conclusion as to whether there is also anxiety-reduction as a result of eating. Leon and Chamberlain (1973) tackled the same questions by simply asking both normal and obese subjects to monitor concurrently food-intake and subjective mood in everyday life over three days. The normal subjects did suggest that they felt better when eating was associated with a negative emotional state. However, most significantly, subjects with a weight problem either reported no change or reportedfeeling worse. These subjective data, which obviously require corroboration, are an important element in our hypothesis which maintains that the obese do not eat in order to reduce anxiety. Two other studies support the general position that activation or stress can elicit eating although they do not bear particularly on the psychological underpinnings of the phenomena. Meyer and Pudel (1972) used a food dispenser which disguised the visual feedback of intake received by the subjects. They established baselines of eating over about seven sessions in about 100 subjects. They then introduced stressors (noise, flickering lights, insoluble anagrams) over three sessions. In some subjects, these conditions produced hyperphagia, and in others hypophagia (see Table 3). Mature, obese women showed the greatest hyperphagic effects, and children and the aged the smallest. It is interesting that the hyperphagics scored highest on a neuroticism questionnaire. TABLE 3 Percentage ofsubjects showing significant change in food-intake (Mayer & Pudel, 1972, 1977)

Hyperphagia Hypophagia

Standard conditions

Noise

Light flicker

Insoluble anagrams

2

13

26

30

7

3

10

Jung (1973) reported that the stress of removing toys from children reduced their intake, whereas (Jung, 1976) suspense-films seemed to enhance "oral responsiveness", "psychic activation" and eating in four to six year-old children. The largest effects in the later experiment were in overweight, older girls.

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2. Non-specific Influences on Human Feeding: Theory There is therefore a limited amount of evidence that non-specific stimuli (stressors) increase eating by the obese, but it is possible that the effects may be confounded by a different baseline level of emotionality in obese subjects. Thus, a generally heightened level of arousal or emotionality might be sufficient to produce increased reactivity to internal or external stimuli, and produce over-eating in some people. Another problem is the causal relationship between obesity and emotionality. A self-conscious obese person may be stressed by his own obesity, possibly produced by a purely metabolic disturbance; this stress may contribute further to the over-eating. Furthermore, increased emotionality may be caused largely by exaggerated responsiveness to stimuli, just as anxiety could give rise to increased reactivity. Since heightened emotionality can only be inferred objectively from behavioural evidence, such as increased activation (the rate of behavioural output, or reactivity), we suggest that reactivity itself may be a sufficient factor in the mechanism of production of obesity. Therefore, the question remains whether the obese over-eat in response to stress because of confusion about the internal concomitants of external events (e.g. confusing the internal reaction to an aversive event with the internal reaction to fooddeprivation), or simply because of an exaggerated behavioural response to external stimuli. We shall argue that these two possibilities are both consistent with a single underlying learning process, which does not serve to reduce anxiety. There is not space to review the literature in detail, and the reader is referred to Leon and Roth's critical 1977 review, from which the following is emphasised. Obesity has been linked to states of anxiety, depression or phobia. For example the obese show elevation on both the MMPI psychoasthenia and the depression scales, although they do not appear to have unique personality characteristics. However, some studies have failed to show any incidence of neurosis or psychosis in the obese. Most relevant for our thesis, Leon and Chamberlain (1973) found that formerly obese subjects who later regained weight reported that food-intake was associated with a variety of states of emotional arousal, whereas subjects maintaining their lost weight indicated that their eating was more specific to loneliness and boredom, "suggesting that the reqainer's greater difficulty in maintaining weight loss may be related to the large number of emotional states that are discriminative stimuli for food-intake" (our italics, Leon & Roth, 1977, p. 132). This conclusion supports Bruch's idea that, for the obese, food has become associated with a variety of internal activating events, unrelated to food-deprivation. However, Bruch (1973) suggests that the obese eat in an attempt to reduce anxiety, which is unsuccessful, a conclusion reached by Leon and Roth (1977), after considering case reports and comparative results in the clinical literature: 'Thus it appears unjustified to summarily dismiss the experience of numerous clinicians in this field and conclude that obese persons as a group, irrespective of sex, degree of obesity or whether they are in treatment, do not respond to emotional arousal with increased food-intake. The research evidence however does not support the notion that foodintake reduces anxiety, suggesting the possibility thatfood consumption may be a response that is incompatible with anxiety or a highly overlearned response initially established through positive reinforcement" (our italics, Leon & Roth, 1977, p. 119). Bruch's analysis presupposes that normals are able to identify internal cues of deprivation and use them reliably, thereby staving off obesity. However, it appears that

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normals, as well as the obese, are not good at recognizing internal signals (see Wooley et al., 1976). Thus it is difficult to conclude that obesity is due entirely to lack of discrimination of hunger cues, and the question is raised whether increased externality is itself sufficient to account for obesity. Attempts to demonstrate increased externality in the obese have recently met with some difficulty, with many of the basic findings questioned, and others not repeated. Several studies, concerned with the prominence of food-related cues have confounded salience of food with the effort required to obtain it, and self-consciousness of the experimental subjects. However, there is a convincing demonstration by Ross (1974), using obese male college students and normal-weight controls. Ross varied (1) the amount of illumination ofa table carrying a bowl of cashew nuts (visual salience), and (2) whether or not the subjects were instructed to think about the taste of the cashews (cognitive salience). In the visual salience condition only, the obese ate significantly more than when the nuts were illuminated. There were no differences between the other conditions. With regard to taste responsiveness, the consensus is that the obese show greater responsiveness to taste cues when they are pleasant, with unclear results for when the tastes are less pleasant. Many of these experiments are confounded with the obese subject's confidence in his ability to make taste discriminations. There is "some consistency" in studies investigating the effect of effort to obtain food, indicafing that the obese expend less effort than normals (Leon & Roth, 1977). Despite this evidence, it is by no means clear that the obese are generally external in orientation, and normals can also be highly responsive to external stimuli (Rodin, 1978). Rodin suggests that both internal and external factors contribute to obesity in a mutually dependent fashion, and only in a way that can be observed in normals as well as in the obese. We conclude that for both normals and the obese, internal cues of deprivation are not easily discriminable, and may playa relatively minor part in the control of foodintake. Eating habits are largely dictated by social and environmental factors; in general, we tend to eat at specific times, regardless of whether we are happy, anxious or depressed. Therefore, the nature of our emotional state cannot be a good predictor of food. Rather, eating is largely under external control, and thus learning about external events must play an essential part in the establishment and change of eating habits. We suggest that, for both normals and the obese, large stimulus changes (stressors) lead to the same internal response, which produces an increased reactivity to external events (activation). Normals-those who have learned to control their eating habits satisfactorily by a set of cues that consistently predict eating, or by cognitive controlrespond by directing their energies into other activities, possible leading to obsessions in severe cases. The obese are those who respond by turning to food, and, once attracted, home in a spiral, like a moth towards a lamp. This analysis is no more than a description: the obese are those that respond to stress by eating. The mechanism that maintains the obese on their ever-tightening spiral produces a strengthening of the eating response. Although initially produced by stress, eating cannot then reduce that stress, since the behaviour would not be strengthened, but weakened.

II. DOES OVER~EATING REDUCE STRESS? There is evidence that a wide variety of non-specific influences elicit eating. The mechanism of these effects, and their relationship with natural eating will now be discussed.

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One view would be that the so-called non-specific effects result from the organism's attempt to reduce the aversive correlates of some "anxiety-state" or stress-state. The problem inherent in any "coping-response" or "anxiety-reduction" explanation of behaviour is that if the behaviour is produced by the aversive state in the first place and also acts to reduce the aversiveness of that state, then what is maintaining and strengthening the behaviour? In fact, we can argue that, given some maintaining influence is necessary, and that this influence is in itself sufficient for performance, then a recourse to the additional motivational influence of anxiety-reduction is not required. This account can be illustrated by reference to the interpretative problems posed by avoidance-learning. After an animal has learned to avoid shock, what maintains this behaviour? Mowrer suggested that anxiety or fear becomes conditioned to the warning-stimulus or CS and that the organism tries to escape from that anxietyproducing stimulus by making a response which terminates it, and, incidentally, the shock also. Unfortunately, there are several problems with this explanation. First, since the CS is no longer paired with the shock very frequently, it presumably gradually loses its anxiety-provoking properties. This should result in a cyclical extinction-andrecovery of avoidance behaviour which is not found to be the case (Wynne & Solomon, 1955). Second, Kamin et al. (1963) performed a famous experiment showing that conditioned suppression produced by an aversive CS weakened with avoidance training, and it is well known anecdotally that rats do not show very pronounced autonomic effects late in avoidance learning. Therefore, successful avoidance of the shock seems to extinguish anxiety, and yet the animal continues responding. Recent work suggests that certain features of the situation actually become positively reinforcing. For example, safety signals, paired with successful avoidance, acquire positive incentive value and even the "aversive" CS may gain positive properties (Weisman & Litner, 1972). A direct parallel with avoidance and eating is provided by an experiment by Williams and Teitelbaum (1956) who managed to induce obesity in rats by requiring that they lick a 10% sucrose solution to postpone electric shocks. We would argue here that the sucrose diet itself acquired positive properties in these satiated animals, possibly contributing to the over-eating. Consider the parallel with tail-pinch or ESB-elicited behaviour. An anxietyreduction explanation would suggest that eating is an avoidance response which somehow occludes the aversive experience of the pinch or brain stimulation. Even ifthe initial experience of tail-pinch is aversive, the evidence suggests that the maintenance of the tail-pinch-induced behaviour is dependent on the incentive properties of the goalobject (see Section IA-9). It is worth noting that many potent positive reinforcers are initially "aversive", before their incentive properties become apparent. For example, chilli and black pepper are aversive at first, but a large proportion of the world's population is virtually addicted to them although they have no obvious compensatory mood-altering effects, as does alcohol, for instance (Rozin, 1976). Therefore, even if the effects of non-specific stimuli as tail-pinch are indeed initially aversive, maintenance of eating behaviour produced by them must be under the control of some positive incentive, and independent of any attempt to reduce the aversiveness of the activation. Furthermore, the evidence that the experience of eating under the influence of tail-pinch appears to make rats regard tail-pinch as more like fooddeprivation than when they have been given experience ofgnawing wood, suggests that tail-pinch, and thus non-specific stimuli in general, may come to produce a state that is functionally similar to natural deprivation. Therefore, natural hunger may itself have to be learned.

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Bruch (1969), using many clinical observations, comes to a similar conclusion. One ofthe most important factors for the human neonate is the hunger-feeding cycle, which may require a degree of learning, in order to associate a particular set of internal cues with eating responses. The opportunity to eat is largely provided by the parents, and so appropriate presentation of food leads to recognition of hunger by a Pavlovian mechanism. However, if food is presented inappropriately when the child is not in a state of deprivation, but is activated by an alternative set of cues, including, for example, autonomic respondents produced by external stressors, then feeding will become conditioned to that set of cues. Therefore, in the future, feeding may be elicited by a wide variety of activating circumstances. Given the observed poor ability of normals and the obese to recognize hunger cues, we suggest that the scheme proposed by Bruch works equally well for external stimuli. Thus, a child exposed by its parents to irregular eating habits will have difficulty regulating food-intake for itself, since no stimuli are reliable predictors of food. Ifhunger is hard to recognize, it seems likely that other internal activating states are similarly difficult to identify. Anxiety itselfis usually perceived by an individual in terms of a pattern of sympathetic responses. Schachter and Singer (1962)have indicated that the subjective labelling of artificially-induced patterns of sympathetic responses carl be manipulated by instructional set. Therefore, it appears that external circumstances can dictate the emotional interpretation of activation. This might account for the elevation in both "anxiety" and "depression" on the MMPI in obese subjects (Leon & Roth, 1977, p. 134):it is simply because these states may be difficult to label and discriminate. The idea that emotional valence is not an intrinsic property of stimuli, but depends on context, is strongly supported by recent developments in the analysis of operant behaviour, concerning the phenomena of response-produced shock and foodpostponement. For example, squirrel monkeys and cats will work for painful electric shocks (Morse & Kelleher, 1977) and hungry rats and squirrel monkeys will work to postpone food-presentation (Clark & Smith, 1977). Thus, early experience of eating in response to activating circumstances may be a principal determinant in the development of compulsive eating. However, we are not resting our explanation of cernpulsive eating on events occurring solely in infancy. Eating is a response which occurs at a high frequency (several times a day), and so will occur in the enormous variety of contexts experienced during the course of adult life, involving the complete range of emotional experience. This line of reasoning depends critically on evidence that.eating is indeed subject to conditioning effects. Such evidence has been found in man and animals, and strongly suggests that hunger is learned (see Booth, 1978). Thus, the obese may be seen as that class of people that learn to eat inappropriately in response to a variety of activating events. This type of conditioning may be sufficient to explain why obese subjects in "unlabelled" activating circumstances may eat whereas normals indulge in non-eating activity (Slochower, 1976). It might also explain why the obese tend to focus their eating on certain forms of food. Finickiness may simply be rigidity of preference-that is, the result of attending to a small class offoods with compelling taste, texture and appearance, and learning to respond to these exclusively. For instance, Ross (1974) found that obese subjects eat more cashew nuts from an illuminated bowl than controls; there were no differences when the bowl was not illuminated. The apparent finickiness in the obese may be a result of developing a response to particularly salient food, rather than due to a dislike for unappealing foodstuffs.

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The result of activation at lower levels produces a general increase in response rate. If behaviour is focused on to eating (and this is likely, given the number of situations which have been paired with eating), the rate of this eating will be higher than normal, and the obese subject will start to over-eat. This view is supported by many studies of rates of eating in the obese, which are generally elevated (e.g. Hill & McCutcheon, 1976).Note also that tail-pinch-induced eating is very vigorous (Antelman & Caggiula, 1977), and local eating rates after amphetamine are increased (Blundell & Latham, 1978). We have argued that over-eating in the obese cannot be- maintained by anxiety reduction, but acquires positively rewarding properties of its own. Therefore, it might be possible to find some physiological mechanism whereby this positive feedback might be achieved. Review of the VMH lesion literature suggests that one possible mechanism of obesity is an induction of insulin secretion by hyper-reactivity to external cues, particularly those related to food-intake. Thus, instead of hyper-reactivity resulting from hyperinsulinaemia, we argue, with Powley (1977), that the causal relationship is reversed. Increased attention to food may in itself trigger enhanced metabolic reflexes, leading to increased conversion of sugar to fat, and keeping the organism hungry. This explanation can accommodate even the finding that restriction of access to food for VMH rats still produces obesity. Simply, the reactivity to food cues is enhanced, and this can produce enhanced metabolic changes, regardless of how much food the organism actually absorbs. Increased activation, whether resulting from a lesion, or from some stressful external event, produces a general increase in attention to external stimuli, of which food-related cues are amongst the most prominent. In support of this notion, there is evidence that insulin secretion in animals can be conditioned to stimuli that predict food, (e.g. Woods, Vasselli, Kaestner, Szakmary, Milburn & Vitiello, 1977). Recently, Rodin (1978) has reported preliminary data on similar experiments with humans. Overweight subjects showed enhanced secretion of insulin in response to the presentation of a steak being grilled. Furthermore, formerly obese subjects gave similar results, and subjects that were independently rated as external showed the greatest effects, regardless of current weight or basal insulin level. Therefore, increased attention to food and food-related stimuli in response to activating circumstances may well produce metabolic effects which normally prepare the organism for eating. Internal stimuli produced by these changes will further increase activation, and, in addition, may also be recognized as the stimuli that normally herald food. In this way, the state induced by activation may gradually come to be virtually indistinguishable from natural hunger. In fact, learning to eat in response to stress may be a recapitulation of the process whereby neonatal organisms learn to eat in the first place. Initially, food-deprivation is a non-specific activating stimulus, to which the neonate responds with increased behavioural output and attention to external stimuli. The specific internal cues offooddeprivation, and the associated external cues, are then paired with food. The organism learns that a particular set of stimuli, probably mostly external, predict food. Activation from internal stimuli serves to direct attention to the outside world, in which are found the cues that have been conditioned to food. These cues produce conditioned metabolic effects that augment activation, and so the eating response is strengthened. If activating events result in increased attention to food-related stimuli, the neonatal pattern oflearning to eat may be repeated. In experimental animals, this is usually achieved by specifically providing food in activating circumstances, and rats under the influence of ESB or tail-pinch usually prefer eating over other activities that

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may be available. In the human population, eating is paired with an enormous variety of internal and external stimuli, and so obsessive eating will be a highly probable result of activation. However, many other obsessions are known, such as cleaning and checking rituals; these may equally be results of activation increasing attention to stimuli to which the subject is already biased. In addition, the performance of a compulsive act may occlude other forms of behaviour by response competition, in a similar way to that suggested by Lyon and Robbins (1975) for the activating effectsof amphetamine. Note that at very high levels of activation, the performance of even preferred activities is disrupted by interference with response sequencing. Therefore, at very high levels of activation, eating will probably be reduced even in the obese. ESB, tail-pinch, drugs, shock and, probably, noise produce eating at low intensities and inhibit it at high intensities. Anxietyreduction explanations of eating, in the form of coping responses, cannot possibly account for a reduction of eating at high levels of "stress". Opponent appetitive and aversive motivational constructs are often invoked to account for this curvilinear relationship between activation and performance. It is argued that an appetitive system is activated at low intensities of external stimulation and that, in addition, an aversive system is activated at a higher threshold which competes with the appetitive system and, at high intensities, outweighs it (e.g. Berlyne, 1967). According to this notion, stress-induced eating would be a result of rewarding correlates at low intensities, and eating would be reduced by aversive effectsat high intensities. We have argued that the assumed emotional valence of activating circumstances has little to do with observed behaviour, and, since valence can only be inferred from how the organism responds, it has no predictive value. We suggest that the rate of behavioural output is linearly related to activation, and thus eating responses can only occur at levels of activation compatible with their completion; at very high levels of activation, eating is not possible. CONCLUSION

We conclude that eating is induced by stress, but the eating does not act to reduce that stress. The eating response is learned in much the same way as eating in response to' food-deprivation. The activating effects of stress produce increased attention to external stimuli, many of which are likely to be food-related. These stimuli elicit eating and also metabolic changes in anticipation of food. These metabolic changes provide further activation, which augments the eating response. The intensity of the eating response is related to the level of activation in a curvilinear fashion; low levels increase eating and high levels inhibit eating. The reason for this relationship is that the rate of behavioural output is linearly related to activation, and eating is disrupted by competing, high-frequency responses at high levels. This account of stress-induced eating may provide a model for a general theory of compulsive behaviour in response to stress, of which eating in the obese is just one example. REFERENCE NOTE

1. Fray, P. J., Koob, G. F., & Iversen, S. D. Tail-pinch elicited behavior in rats: preference,

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Received 29 February, 1980

Editorial Note--c-Appetite is open to Commentary, with opportunity for Reply, on articles appearing in the journal or elsewhere. Commentary on the above review appears in this and forthcoming issues of Appetite.