Ingestion and emotional health.

INGESTION A N D EMOTIONAL HEALTH Nancy K. Dess Occidental College

Evidence abounds of a close relation between ingestive and affective processes in rats and in humans. Emotional distress alters food intake and body weight; conversely, alterations in eating and weight influence emotional health. Thorough experimental analysis of the ingestionaffect relation may clarify the mechanisms of anxiety and depression. A strategy is proposed for examination of environmental and dispositional

determinants of ingestive processes, emotionality, and responses to stress. KEY WORDS" Taste; Ingestion; Body weight; Stress; Depression; Anxiety; Rats; Humans

Kreshover (1976) opens Taste and Development: The Genesis of Sweet Preference by proclaiming, "The m o u t h is a complex organ system essential for life, and, upon it, physical and mental well being depend to a far greater extent than is generally recognized" (1976:xv). Surely whether or not people are happy depends on more than their eating habits. But how much can be learned about emotional health by studying the variables that control appetite, eating, and body weight? Quite a lot, according to research on emotionally healthy vs distressed (depressed, anxious) humans and laboratory rats. This paper describes a conceptual and empirical framework linking ingestion to emotional functioning in both species Received February 26, 1991; accepted March 11, 1991. Address correspondence to Nancy K. Dess, Department of Psychology, Occldental College, 1600 Campus Road, Los Angeles, CA 90041.

Copyright 9 1991 by Walter de Gruyter, Inc. New York Human Nature, Vol. 2, No. 3, pp. 235--269. 235

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and then discusses ways in which the framework could be profitably elaborated. INGESTION IS CLOSELY RELATED TO AFFECTIVE PROCESSES

Covariation Between Depression and Disordered Eating Changes in appetite and weight are prominent features of clinical depression (e.g., Beck 1967; Casper et al. 1985; Paykel 1977). These changes are more reliable characteristics across depressive episodes than is the "endogenous character" or severity of the depression (Stunkard et al. 1990). In addition, depression is unusually common among people with the clinical eating, disorders, bulimia and anorexia (Piran et al. 1985). Family history studies also attest to a strong relationship between ingestion and affective disorder. Leckman et al. (1984) studied 133 depressed subjects, 82 nondepressed subjects, and more than 1300 of the subjects' relatives. Subjects were evaluated on 12 scales of psychological (e.g., guilt, loss of interest) and vegetative (e.g., appetite and sleep problems) functioning. The ability of subjects' scores on each scale to predict depression in their relatives was determined. Appetite disturbance was the best predictor of depression in a subject's relatives, from which the authors reasoned "the neurochemical and neurophysiologic mechanisms that regulate appetite may be closely linked to some forms of depression" (Leckman et al. 1984:843). Family history studies of affective and eating disorders support this reasoning. The prevalence of depression is greater among the relatives of bulimic and anorexic patients than among relatives of various control groups (Hudson et al. 1982; Strober et al. 1982; Winokur et al. 1980). A review of the literature led Swift et al. (1986:297) to "the incontrovertible conclusion that affective disorder and eating disorders are related phenomena."

Human Experimental Work Descriptive and family history studies show that ingestion and emotional health are related, but they do not show whether ingestion influences emotion or emotion influences ingestion, or both, or whether other variables modulate emotion as well as ingestion. Experimental work suggests that all of these causal relationships exist. In a classic experiment, Keys et al. (1950) starved healthy male volunteers for sever-

Ingestion and Emotional Health

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al months and monitored their physical and psychological functioning. Virtually every subject became depressed, complaining of dysphoric mood and feelings of inadequacy. The authors noted the striking resemblance of the starved men to victims of "natural" starvation experiments of famine and civil war. The results of the Keys et al. study are reminiscent of the dieting depression that sometimes accompanies rapid weight loss by obese people on low-calorie diets, despite their desire to lose weight (Stunkard and Rush 1974). The emotional risks of dieting are not unique to obese people. Polivy and Herman (1985) review evidence that dieting produces anxiety, tension, and irritability in normal-weight dieters. In a similar vein, Rozin (1989:377) argues that overvigilant eating habits cause "anxiety, dysphoria, and the despoiling of one of the great pleasures of life." All of these phenomena imply that eating good food is important to emotional health. There is also evidence of the converse causal relationship: Dysphoric moods influence eating. For example, Schachter et al. (1968) measured the number of crackers eaten by normal-weight, nondieting college students with and without anxiety (fear of receiving an electric shock). Anxiety suppressed eating. Others have obtained similar results for comparable subjects (e.g., Herman and Polivy 1975; Mehrabian 1987:95-102). Although experimental manipulation of mood enables researchers to make causal inferences, severe anxiety or depression cannot be induced in humans for ethical reasons. Thu~, the relevance of induced-mood effects to severe emotional distress is debatable. On the other hand, the ability of mood-induction to alter eating shows that effects of mood on eating are not exclusive to extreme mood states or to people with affective or eating disorders.

Stress: Linking Affect to Ingestion Across Species Humans. Not every depressed person experiences a change in appetite and weight, and not every dieter or eating-disorder patient is depressed. Though causal relationships exist between ingestion and emotional distress, other factors must be involved. One potential common modulator is stress. In individuals at risk for depression, stress increases the likelihood of a depressive episode (Anisman and Zacharko 1982; Smith and Nemeroff 1988) and appears to produce greater-than-normal fluctuations in appetite and weight (Harris et al. 1984). Less is known about the role of stress in eating disorders, but as with depression, stress seems to promote the onset or maintenance of eating disorders in

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combination with other risk factors (see Striegel-Moore et al. 1986; Swift et al. 1986).

Rats. This section consists of a discussion of the usefulness of rats in the study of emotional distress and ingestion, followed by a brief overview of the effects of stress on ingestion in rats. Validity of rat models. A review of the clinical and ethological validity of stress, anxiety, and depression models is beyond the scope of this paper (for examples see Gray 1982; Pare and Glavin 1986; Willner 1985). Instead, one paradigm will be used to illustrate how exposing a nonhuman species to seemingly "arbitrary" stress can speak to the issue of human emotional distress (Overmier 1991). In the helplessness paradigm, exposure to a series of inescapable, unpredictable shocks is used to study the effects of naturally occuring stress on animals (Seligman et al. 1971). Species studied in this manner include dogs (Overmier and Seligman 1967), cats (Seward and Humphrey 1967), gerbils (Brown and Dixon 1983), mice (Braud et al. 1969), chickens (Job 1987), and goldfish (Padilla et al. 1970). Laboratory rats (Rattus norvegicus) are the most popular subjects (e.g., Seligman and Beagley 1975; Williams and Maier 1977). To the casual observer, rats behave quite normally soon after shock, but a closer look reveals profound changes in vegetative, cognitive, and motor processes (Weiss and Simson 1989; Zacharko and Anisman 1989). These effects parallel anxiety and depression in humans, including sensitivity to psychosocial variables and mood-elevating drugs. Thus, the helplessness paradigm is used as a model of affective disorders (Overmier and Helhammer 1988; Petty 1986; Willner 1986). Recently, the helplessness paradigm has been viewed from an ethological perspective (Minor et al. 1991; Williams 1989). Shock is usually delivered to the base of the tail or the back of the neck, primary biting targets in fights (Barnett 1963; Calhoun 1962). A shock models an attack by another rat and repeated, inescapable shocks model resounding defeat. Indeed, shock and defeat share m a n y consequences, including impaired escape behavior (the helplessness effect; Seligman and Beagley 1975; Williams and Lierle 1988), reduced social competitiveness (Rapaport and Maier 1978; Williams 1982), and increased defensive posturing (Seligman and Beagley 1975; Williams 1987). Shock and defeat both increase submissiveness. This interpretation of the helplessness paradigm sets it in the context of the dominance hierarchy, a social structure found in rats and m a n y primates (Sapolsky 1991). Henry (1982) argues that loss of status can take many forms, but the core emotional experience and its neural mechanisms are shared by social mammals:


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The prime meaning of dejection is being lowered in rank or circumstances. The loss of status and power to control one's circumstances is found in the rejected consort or the lost infant monkey or the immobilized rat . . . . The same |imbic [brain] mechanisms transform social perceptions into neurohormonal responses in mouse and man (Henry 1982: 372, 378). Mehrabian and colleagues (reviewed in Mehrabian 1987) have asserted that most human subjective experiences are fundamentally emotional. Experience is supposed to arise from three primitive, psychobiological dimensions: pleasure-displeasure, dominance-submissiveness, and arousal-nonarousal. In this scheme, displeasure and submissiveness underly both anxiety and sadness, and arousal distinguishes between them. The present paper is not the place to debate the strengths or weaknesses of these two theories. They are presented here to show that emotional health and distress can be conceptualized in terms appropriate to rats and humans. Phenomena such as negative affect, fear, defeat, submission, and even separation (Ehlers et al. 1989) bind together emotionally distressed rats and humans. Rats are excellent experimental models of humans with respect to ingestion. Both species are predators (Carlson 1986:481) and have eclectic diets (Beck et al. 1988). Indeed, rats share human habitats around the world in part because they readily exploit human food processing, storage, and disposal facilities. In rats and humans, food preferences and aversions are shaped by individual as well as social experience (Galef 1990; Rozin and Zellner 1985). The similarity of the behavioral and physiological regulation of ingestion in rats and humans has spawned dozens of rat models of obesity, diabetes, and eating disorders (Booth 1972; Sclafani 1984; Smith 1989). Rats are not humans, of course. The species encounter different stresses and feeding opportunities--rats do not lose their jobs or make chicken soup. And each species has unique adaptations relevant to social and emotional functioning and ingestion (e.g., language in humans, inability to regurgitate in rats). The substantial continuity between rats and humans with respect to emotional distress and ingestion does, however, suggest that parallel studies of the stress-ingestion relationship in the two species are worthwhile. Stress and ingestion in rats. If the helplessness paradigm models affective disorders, then eating and b o d y weight should be altered by inescapable, unpredictable shock. Reduced food intake and b o d y weight have been reported in the helplessness paradigm (e.g., Dess, Raizer, Chapman, and Garcia 1988; Dess et al. 1989; Weiss 1968). Simulating the stress with infusion of the stress neurohormone corticotropin-releasing

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factor (CRF) into the brain also suppresses food intake and weight gain (Krahn et al. 1986; Levine et al. 1983; Rivest et al. 1989). Conversely, food deprivation is routinely used as an experimental stress (e.g., Curzon et al. 1972; Katz 1982; Vaswani et al. 1983). It may retard recovery from shock's effects. Shock-induced impairment of avoidance or escape performance normally is alleviated by antianxiety or antidepressant drugs (Petty 1986); however, food deprivation prior to shock reduces the therapeutic effectiveness of antidepressant drugs (Soubri6 et al. 1989). These and other studies (e.g., Curzon et al. 1972; Krieger 1974; Ritter et al. 1978; Smotherman and Levine 1978) document the substantial overlap between the mechanisms engaged by stress and ingestion in rats. TASTE: PERIPHERAL OUTPOST OF THE PSYCHE Coevolution of Taste and Hedonic Processes

An Adaptational Rationale. Taste is an enticing entr6e to the ingestionaffect relationship. An intimate association between the sense of taste and affect must have begun very early in mammalian evolution (Garcia and Hankins 1977; Garcia et al. 1984). Substances in the mouth can easily enter the body. Early taste systems were under tremendous pressure to evaluate the substances as good or bad and to provoke, respectively, swallowing or ejection. Rapid evaluation of a few tastes would have been advantageous. For example, sugars contain easy-to-use calories, so a positive evaluation of their taste (sweet) would have been beneficial; alkaloids are toxic, so a negative evaluation of their taste (bitter) would have been beneficial (Garcia and Hankins 1975). The adaptive default evaluation would have been negative: If in doubt, spit it out or consume only a small bit (Beck et al. 1988; Domjan 1977). Most foragers also encounter foods that defy simple categorization. Many foods are complexly flavored. Those that contain storable fats and trace nutrients should be exploited; those containing nonbitter toxins should be avoided. Therefore, the ability to analyze complex flavors and to learn about foods' nutritional or toxic properties would also have been advantageous. Yet from the very beginning, flavor-analysis and learning mechanisms would have had to modulate food acceptance and rejection to confer any adaptive advantage (Aboitiz 1989): Primitive hedonic mechanisms were probably co-opted in the evolution of flavor analysis and conditioning (Garcia and Hankins 1975; Rozin and Zellner 1985). Other mammalian senses can also provoke emotional responses. For example, intense sounds elicit startle (Davis 1984), and fear can come


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under the control of otherwise neutral stimuli (e.g., Levis 1989; Mineka et al. 1984). But relative to taste, other senses are subjected to a great deal of hedonically neutral information. Telereceptors (eyes, ears) scan the environment, detecting clearly unimportant as well as potentially important events. An efficient telereceptive system would sort unimportant events from important ones, so only the latter would gain access to hedonic and behavioral resources. Touch, like taste, requires direct contact, yet only some aspects of touch are phylogenetically old and closely linked to affect and action (e.g., pain; Zimmerman 1978:51-57). Olfaction (smell) comes closest to taste in relatedness to affect. In mammalian evolution, taste and smell were once a single sense, and they still work together in flavor perception. Some mammals have olfactory organs that require direct contact with an odor source; these organs retain close ties to emotion and motivation (Carlson 1986:386387). In most mammals, conditioning can lead to robust emotional responses to odors (Bartoshuk 1989; Minor and LoLordo 1984; Williams 1989). Yet noses also survey distant odor sources. They inevitably detect neutral as well as hedonically loaded odors, which may or may not be related to feeding. Olfaction's functional diversification left taste unrivaled among the senses in hedonic richness and relatedness to ingestion. The Evidence. This simple story of selection for taste hedonics is probably more accurate for some species than for others (Grill et al. 1987:153-154). Nonetheless, there is a fair amount of truth in it, e s p e cially for the two species emphasized in this paper. An illustrative empirical test was conducted by Richter and Clisby (1941). Rats and humans tasted solutions made with the substance phenylthiocarbamide (PTC). PTC is lethal in small doses and is described by humans as bitter. The concentration of PTC at which the rats' drinking was first suppressed was the same as the humans' PTC detection and recognition thresholds. Furthermore, 95.5% of the rats never drank a lethal dose of PTC solution. Detection of the bitter taste did not differ between rats and humans and, in the case of rats, saved lives. The adaptational rationale is also consistent with the psychobiology of taste. Stereotyped expressions elicited by simple tastes develop early and vary little among individuals, at least in rats and humans. Adult rats with or without a functional forebrain and rat pups all show speciestypical orofacial rejection of quinine and acceptance of sucrose (Grill and Berridge 1985; Hall and Bryan 1981; Pelchat and Brake 1987). H u m a n infants with or without a forebrain also show similar reactions to quinine and sucrose (Steiner 1977). Thus, hedonic evaluations of simple taste qualities occur in the phylogenetically old and precocial circuitry of the hindbrain.

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Though the hindbrain is sufficient for hedonic evaluation of tastes, the relationship between taste and affect does not stop there in mammals. Taste signals from the hindbrain directly or indirectly reach the limbic system, the forebrain seat of learning, emotion, and motivation (Panksepp 1982). The limbic system projects back to hindbrain tasteprocessing sites. Thus, routes exist through which learning and emotion can influence and can be influenced by taste hedonics (Norgren et al. 1989; Scott and Yaxley 1989). The evolutionary path to human taste neuroanatomy is interesting. Projection of taste signals to the forebrain became more direct (i.e., dropped a synapse) when mammals diverged from their progenitors (Barnard 1936). At some point, rodent and primate evolution diverged: in rodents, taste signals from the hindbrain project directly to the limbic system, whereas in primates hindbrain taste signals detour through sensory-analysis centers in the thalamus and cortex before reaching the limbic system (Scott and Yaxley 1989). Despite this "encephalization" of taste processing in primates, the limbic destinations of taste and their projections back to the hindbrain suggest that taste has retained close ties to emotion. Very little is known about the functions of these central taste pathways in humans, so we can only speculate about the neural bases of taste-affect relations. Some case studies hint that simple taste qualities and their hedonic value are maintained at high levels. Anderson (1887) asked a temporal lobe epilepsy patient to describe his pre-seizure "ictal" state: he replied that he knew about a minute before by "a sensation in his mouth," "a rough bitter sensation," which lasted during the attack. He generally had an attack after any excitement (1887:385). Similar descriptions were given 100 years later by patients about to have electrically induced seizures (Hausser-Hauw and Bancaud 1987). Ictal tastes were described "in general terms such as 'bitter,' 'unpleasant' or 'a t a s t e ' . . . [and] the gustatory hallucinations were usually unpleasant" (Hausser-Hauw and Bancard 1987:350). During h u m a n evolution, taste's essentially hedonic tone seems to have been preserved as its pathways were elaborated in the forebrain.

Partial Autonomy of the Taste--Affect Relationship From hindbrain to forebrain, the interactions between taste and affect could pertain exclusively to feeding behavior. This does not appear to be

the case. In 1872, Darwin made the point eloquently:


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Laughter seems primarily to be the expression of mere joy. . . . The laughter of the gods is described by Homer as "the exuberance of their celestial joy after their daily banquet." . . . Disgust is a sensation rather more distinct in its nature, and refers to something revolting, primarily in relation to the sense of t a s t e . . , and secondarily to anything which causes a similar feeling (1965:196). Affectively rich taste metaphors abound: "a sweet disposition," "he's a sourpuss," "bitter disappointment." Heckhausen et al. (1989) asked their subjects to rate the desirability of more than 300 positive and negative h u m a n traits. The most wretched of all traits was "bitter." The earliest association between taste and affect probably arose to regulate feeding. The neural circuits that were shaped by this association, and some of the behaviors they control, eventually assumed experiential and expressive roles unrelated to feeding (Steiner 1977:I86). Studying the taste-affect relation in mammals may reveal as much about affect per se as it does about ingestion. Taste After Stress

It follows from the logic developed above that emotional distress will be systematically related to taste. Several experiments demonstrating effects of stress on taste are described below. The discussion then turns to the theoretical analysis of the phenomena, which quickly reveals the inadequacy of any simple view of taste hedonics and ingestion or their relation to affective disorders.

Stress Enhances Rejection of Quinine. In the following studies we exposed rats to inescapable, unpredictable shock and compared their consumption of quinine-adulterated water or food to that of nonshocked controls. Drinking bitter water after stress. Shocked rats drank less of a weak quinine solution than did nonshocked controls (Dess and C h a p m a n 1990; Dess, Chapman, and Minor 1988). Suppressed drinking was specific to adulterated water and lasted at least 24 hours. Eating bitter food after stress. Adulteration of food with quinine suppressed eating and body weight gain in rats (Peck 1978; Sclafani et al. 1976). Given the rejection of bitter water after shock, shock might be expected to potentiate the suppressive effect of quinine-adulteration of food on eating and body weight. We exposed rats to shock or no shock and gave half of each group quinine-adulterated food for 5 days (Dess et al. 1989). The other half of each group received unadulterated food. In addition, all rats were exposed to daily mild stress, a procedure that slows recovery from more severe stress (Anisman and Sklar 1979; Minor

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et al. 1988). Normal-fed shocked rats ate less than did nonshocked controls for one or two test days. In contrast, quinine-fed shocked rats ate less and lost more weight throughout testing than did all other groups. In another experiment, all rats received quinine-adulterated food. Shocks were escapable for some rats and inescapable for others. An escape response terminated shock for both the escaping rat and an inescapably shocked "partner," so shock durations were matched in the two conditions; owing to the escape contingency, however, shocks were much briefer than in the preceding experiment (average ,-~1 second vs 5 seconds). Escapably shocked rats were expected to eat more and lose less weight than inescapably shocked rats (Minor et al. 1991; Seligman et al. 1971). In contrast to the preceding experiment, shock had no effect on food intake, presumably owing to the relatively mild shock experienced. Despite equal food intake, shocked groups lost more weight than did nonshocked controls, and inescapably shocked rats lost more weight than did their escapably shocked counterparts. Diet palatability modulates the impact of shock on eating, drinking, and body weight. Shock can, however, cause weight loss in the absence of any effect on ingestion. Therefore, the effects of shock on food intake and body weight must be mediated by partially independent mechanisms. The separability of food intake and body weight is a point to which we will return later.

Stress and Sweet Solutions. Consumption of sweet fluids has been examined in two other models of depression using rats (Katz 1982; Willner et al. 1987). In both studies, chronically stressed rats drank less saccharin or sucrose solution than did nonstressed controls. Theoretical interpretation. Katz (1982) and Willner et al. (1987) interpret their results in terms of anhedonia. Hypothetically, anhedonia is the inability to experience pleasure in humans or, in comparative terms, a reduction in the reward value of positive incentives (Klein 1974; Wise 1982). If the anhedonia construct were revised to include increased negativity of aversive events (e.g., Berridge et al. 1989; McDowall 1984; Parker and Lopez 1990), it could accommodate enhanced rejection of quinine: Good tastes don't taste as good, and bad tastes taste worse. This interpretation appears to support the suggestion that chronic stress can be used as a model of depression because anhedonia is a clinically useful feature of depression. Indeed, anhedonia is the hallmark of the putative endogenous subtype (Klein 1974; Koob 1989), which Katz (1982) and Willner et al. (1987) suggest is most faithfully reproduced in their paradigms. Anhedonia would seem a promising link between taste, food intake, and body weight in stressed rats and be-


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tween the general lack of interest and pleasure, and anorexia and weight loss, in depressed humans. Problems with "anhedonia.'" The anhedonia interpretation of reduced sweet-fluid intake does not bear up well under closer scrutiny. To begin with, the suppression of drinking in Katz's and Willner et al.'s studies was not specific. Sweet-fluid intake was suppressed by stress, but so was drinking per se (water or total fluid intake; also see Par6 1965). Thus, it is not clear whether suppressed intake of sweet fluids was directly related to their hedonic value. Indeed, experimental models of anhedonia do not support a hedonic interpretation of decreased intake of sweets. These models consist of disrupting the presumed neural basis of reward with neuropharmacologically selective drugs (e.g., pimozide) or neurotoxins (e.g., 6-hydroxydopamine). When hedonic value is inferred from amount consumed or instrumental behavior, pimozide appears to reduce sucrose's hedonic value (Bailey et al. 1986; Towell et al. 1987; Xenakis and Sclafani 1981). Orofacial hedonic reactions to sucrose are not affected by pimozide (Parker and Lopez 1990) or by neurotoxin lesions, however, even in the presence of the anorexia to which anhedonia supposedly contributes (Berridge et al. 1989). Effects on reactions to quinine in these two studies were contradictory. Thus, manipulations of the putative mechanisms of anhedonia do impair generative, motivational processes, but their effects on evaluative, hedonic processes are debatable. The anhedonia-anorexia link in rats has fallen victim to increasingly sophisticated behavioral analyses (see commentaries by Koob, Milgram, Neill, and Panksepp in Wise 1982). The theoretical underpinnings of the anhedonia construct are also rapidly becoming obsolete. The construct rests on the assumption of a single essentially hedonic "reward" mechanism that mediates such diverse activities as intracranial self-stimulation, eating, drinking, sex, and recreational activities (Olds 1956; Wise 1982). The notion of a single reward pathway, even for one behavioral system (e.g., Hoebel 1976), has fallen on hard times (Berridge and Valenstein 1991; Frutiger 1986) and has yielded to more complex views (Olds and Fobes 1981). Anhedonia is having problems in the clinical literature, too. Anhedonia, anorexia, and weight loss seem to make a logical triad and, as noted above, are clustered together in the putative endogenous depressive subtype. The existence of an endogenous subtype has been questioned, however, especially with respect to appetite and weight change (e.g., Harris et al. 1984; Kendall 1976; Leckman et al. 1984). The case for anhedonia in depression models is as weak as the clinical entity to which the models look for validation.

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Finally, the anhedonia construct has little heuristic value. If everything is less rewarding to the stressed rat or depressed human, then any incentive or activity will do as a research tool. The idea of anhedonia does not guide or organize research; it does not suggest outcomes that will be particularly revealing of the mechanisms of emotional distress. Other approaches are needed that promise to explain existing data and that point research in specific n e w directions.

The Regulatory-Shift Hypothesis Perhaps it would be useful to take a step back and view taste in a broader context: the energy-regulatory macrosystem. In this scheme, taste reflects, modulates, and is modulated by ecological and organismic factors. After an overview of the system's major components (Figure 1), the discussion turns to specific ways in which energy regulation may be affected by stress.

i

\ C'" :"') / Figure 1. A schematic of energy macroregulation. Energy intake, storage, and use interact with each other and with the animal's ecology. The mouth is a semipermeable barrier between the animal and its dietary niche. Palatability is a joint function of properties of the edibles and hedonic and motivational processes. The bidirectional link b e t w e e n foraging and food availability allows for effects of resource depletion and renewal (seasonal, forager-produced, etc.) on foraging. The line from availability to palatability is broken because few data are available on this relationship.


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Energy Balance. Energy regulation consists of three basic processes: intake (eating and absorption of food), storage (glycogen and fat deposition), and utilization (glucose and fat use, thermoregulation). These processes are constrained by each other and by the environment--by food quality and availability, ambient temperature, etc. (Fanselow et al. 1988; Friedman et al. 1986; Johnson and Collier 1987; Peck 1978; Rashotte and Henderson 1988; Richard and Rivest 1989; Sclafani 1989; Stidham et al. 1987). No single part of the system is homeostatic: as long as lifesustaining metabolic needs are continuously met, substantial changes in eating, body weight, and fuel use can be produced and sustained by changes in each other or in ecological conditions. Consider rats given a rich, high fat/high carbohydrate diet (Friedman 1991; Naim et at. 1986; also see DaUman 1984). This diet shifts energy balance towards storage of ingested fuels. Because much of the ingested fuel is stored rather than oxidized, the rats could starve metabolically if they ate a normal amount of food. But they do not starve; they eat voraciously. Eating further increases fat deposition and body weight, and vice versa. Now consider another, hypothetical manipulation that shifts energy balance towards the use of stored fuels and thus away from intake. The treated animal is mobilizing stored fat and glycogen to meet its metabolic needs. This animal should have a conservative ingestive strategy: Eat, but be choosy; exploit rich, palatable foods and reject unpalatable (nutrient-poor or potentially toxic) ones. This sort of "finickiness" occurs experimentally and does vary with body weight (Beatty and Schwartzbaum 1967; Sclafani et al. 1976). Mobilization and use of stored fuels may or may not persist. A rich, palatable, cheap food supply would shift energy balance back towards storage, promoting ingestion and weight gain (as illustrated above). Conversely, adverse feeding conditions would maintain a bias against intake and promote energy conservation, e.g., inactivity and periodic hypothermia (Peck 1978; Rashotte and Henderson 1988). Depletion of fat stores would reduce the availability of fats for oxidation; finickiness should drop along with oxidation rate. And so on. Implications for Stress Effects. Weight loss, suppressed eating, and rejection of bitter tastes after shock (Dess and Chapman 1990; Dess, Chapman, and Minor 1988; Ritter et al. 1978; Weiss 1968) are consistent with an integrated shift in energy balance, with increased stored fuel use and decreased intake. This regulatory-shift hypothesis accommodates the effects of adulterating the food supply with quinine (Dess et al. 1989): w h e n normal food was available, the shift towards utilization was transient so eating and weight gain quickly returned to normal. But the utilization bias was maintained in the face of an unpalatable food sup-

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ply; thus, weight loss and suppressed food intake continued throughout testing. Weight loss after shock without anorexia (Dess et al. 1989) implies increased use of stored fat, and possibly decreased absorption of calories from consumed food. Infusion of CRF into the brains of male rats decreases body fat reserves and suppresses the extraction of energy from food (Rivest et al. 1989). Other known metabolic responses to stress support the regulatory-shift hypothesis, (Sapolsky 1991). We obtained further behavioral support from rats that earned food pellets by pressing a lever on a number of different work schedules. In general, rats press faster when many presses are required to earn a pellet. A rat who perfectly titrated pressing rate to work requirement would eat at a constant rate. On the other hand, a rat pressing at a constant rate would eat frequently w h e n the work requirement was low but infrequently w h e n it was high. Typical performance lies in b e t w e e n these extremes, i.e., variations in work requirement are partially offset by variations in response rate. Lines representing these three relationships between response rate and eating rate are shown in Figure 2. The steeper the line, the less eating rate varies across work requirements. The preferred feeding rate is the rate at which the rat would eat if the pellets were free. Pellets are never flee, but this hypothetical value can be estimated as the x-intercept of the best-fit line (i.e., where response rate = 0). In our experiment, rats earned pellets at six work requirements ranging from 2 to 64 responses per pellet in each experimental session (Ettinger and Staddon 1983; Staddon 1980). Best-fit lines representing the performance of a group of shocked rats are shown in Figure 3. Lines generated by a group of nonshocked controls are shown for comparison. These straight lines fit the data extremely well (R2 = 93.8% and 89.8%, respectively, for shocked and nonshocked groups' test data). These data indicate very good, even improved regulation of eating and a significant reduction in preferred feeding rate shortly after shock. This finding needs to be replicated, but it encourages further use of the paradigm in tests of the regulatory-shift hypothesis. The hypothesis predicts that eating and body weight will not be suppressed by shock under conditions that counteract the mobilization of fuel stores. Specifically, availability of palatable flavors should shift energy balance back towards intake and storage. In addition, finicky rats overconsume palatable foods, so finicky, shocked rats could actually consume more and weigh more than nonshocked controls. A recent study confirmed this prediction (Dess 1991). Rats exposed to shock drank significantly more sucrose solution than did nonshocked controls. Shocked rats drank less saccharin solution than did controls; data from


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Figure 3. Regression lines representing instrumental performance for two groups of rats before (baseline) and several hours after (post-stress) exposure to shock (right) or restraint without shock (left). The shift in performance in the shocked group indicates extremely well regulated feeding behavior but a lower preferred feeding rate. Thorough testing of the regulatory-shift hypothesis is yet to come. For example, the metabolic changes supposed to accompany changes in eating and weight after inescapable, unpredictable shock have not been measured directly. Other suggestions are made below. The early evidence encourages further tests of the idea that this stress reorganizes, but does not disorganize or suppress, energy regulation.

EMOTIONAL DISTRESS AND INGESTION: QUESTIONS NOT ANSWERED, NOT ASKED

So does stress decrease or increase the intake of sweets, eating, and body weight? Are increases flukes, exceptions to the rule? A survey of paradigms other than the helplessness and chronic-stress models reveals that stress can reliably increase eating and body weight. Stress from tail-pinching increases consumption of palatable food and sucrose solution, and body weight (Antelman et al. 1976; Bertiere et al. 1984; Levine and Morley 1981; Rowland and Antelman 1976). In another study, stress brought about by forcing the rat to swim not only increased eating, but differentially increased eating of a high-fat diet (Vaswani et al. 1983).


251

These findings could be attributed to the mildness of the stresses used, but the temptation to do so may arise from assumptions about the stress-ingestion relationship rather than from knowledge about it. Mildly stressed rats are routinely given ample supplies of tasty foods (e.g., Antelman et al. 1976; Bertiere et al. 1984). Severely stressed rats are usually provided with food or drink that is bland or unpalatable (e.g., Dess et al. 1989; Par6 1965) and that is sometimes in short supply (e.g., Dess, Chapman, and Minor 1988; Dess et al. 1989; Willner et al. 1987): Conditions conducive to overeating and weight gain are conspicuously absent. We may assume that eating and body weight are stimulated by mild stress and suppressed by severe stress, but we don't really know (Shimizu et al. 1989). The dietary niche could be just as important as stress severity to the direction of changes in ingestion and body weight after stress. Recent developments concerning clinical depression should motivate us to close these gaps in the literature. Current Clinical Trends: A Call to A c t i o n

Traditional wisdom held that anorexia and weight loss typify depression and that increases in appetite and weight are rare in depressed patients (e.g., Beck 1967). Recent research, however, shows that increases in appetite and weight during depression are quite common: prevalence estimates range from 13% to 46%, compared to 30-66% for appetite and weight loss (Casper et al. 1985; Harris et al. 1984; Paykel 1977; Polivy and Herman 1976; Stunkard et al. 1990; Zielinski 1978). Why some people gain appetite and weight and others lose is not clear. The "endogenous" character or the severity of the depression does not reliably predict the direction of the changes. Gender, age, interpersonal sensitivity, hostility, and dietary restraint have some predictive value. Stunkard et al. suggest that the directionality of change may itself profitably be considered an important feature of depression and a potential marker for subtypes of depression . . . . The determinants of this important feature of depression are unknown, and their elucidation would improve our understanding of depression (1990:860). Is there a place for n o n h u m a n models of depression in this endeavor? After all, depression models have yielded anorexic underweight rats, not overeaters. These models, however, are explicitly shaped to reproduce depression not by an absolute standard but by prevailing clinical standards; their admissability as models of depression depends on h o w well they do so. From a historical point of view, then, it is not surprising that models of depression have reproduced anorexia and weight loss.

252


The recent revision in clinical thinking prompts an important question: Do current models generate a depressive syndrome unique to the subset of people who lose weight? Or does the failure of models of depression to yield bidirectional changes in appetite and weight only reflect prerevisionist clinical thinking? It is important to examine more fully the potential of the models to yield increased eating and weight gain. In so doing, the modeling enterprise may even be able to take the lead in identifying the determinants of bidirectional changes in ingestion during depression.

N e w Directions

In light of the foregoing discussion, the following topics seem worthy of further study: severity of stress, dietary niche, and individual differences in taste and emotionality.

Stress Severity. A major order of business is parametric work on stress severity. The tail-pinch method has received little attention vis vis depression because of its mildness and its stimulating effects on eating and weight gain. The role of mild stress in depression is receiving increasing attention (e.g., Kanner et al. 1981; Willner et al. 1987), however, and as noted above, appetite and weight gain often accompany depression. Systematic studies of stress severity and ingestion, with other procedural details held constant, are needed to clarify the relationship between the two variables. Bertiere et al. (1984) and Rowland and Antelman (1976) observed enhanced intake of sweet fluid during tail-pinch studies, but their rats were screened for tail-pinch-induced ingestive behavior before the experiments began. Bertiere et al. used only "good responders," defined as animals that reacted to the pinch with permanent or quasi-permanent licking of a liquid diet; Rowland and Antelman used only rats that readily ingested milk from a hand-held burette during the application of stress. Why aren't all rats "good responders"? What are the sources of individual variation in stress-induced changes in ingestive behavior, and are they also sources of variation in other stress effects? Studies of stress-induced hyperphagia in unselected groups might lead to the identification of behavioral or biological markers that predict whether stress increases or decreases eating and weight. If these markers have h u m a n counterparts (see Brown 1991 and Mehrabian 1987:103-108 for some candidates), their ability to predict the direction of appetite and weight changes during depression could be evaluated.


253

Dietary Niche. The regulatory-shift hypothesis and the available data (Dess 1991; Vaswani et al. 1983) predict that appetite and weight changes after stress will vary with the nutritional and taste quality of food and the availability of food and water. Manipulations of pre- and post-stress food supplies would provide specific tests of this general idea. For example, scarce or costly food should shift energy balance towards stored fuel use and away from intake. Relative to appropriate controls, rats maintained under these conditions should respond to stress with increased fat utilization, suppressed food intake, and perhaps increased fuel efficiency (Dilsaver et al. 1986; Rashotte and Henderson 1988). Conversely, shocked rats should eat and weigh more than controls if fed a sweet, fatty diet either before stress (preestablished intake/storage bias) or after stress (increased palatability of sweets and shift towards intake/storage). Additional experiments could determine the relative importance of palatability, variety and macronutrient content in these effects (Naim et. al. 1986). Harris et al. (1984) suggested that changes in eating and weight during depression are exaggerated versions of the person's tendency to eat or not eat w h e n stressed. These tendencies have been discussed in cognitive terms such as dietary restraint and disinhibition (Herman and Polivy 1980). The regulatory-shift hypothesis suggests that these tendencies depend primarily on eating habits and metabolic processes. For example, individuals who normally have a high fat, high carbohydrate diet (a) will have high fat, high carbohydrate foods available and (b) will be metabolically biased toward intake and storage (i.e., fat deposition). For both reasons, they are likely to eat w h e n stressed and to eat even more if a depressive episode develops. Prospective studies of the relationship between eating habits, responses to stress, and vulnerability to depression would be informative. Individual Differences in Taste and Emotionality. Laboratory rats may look the same to the uninitiated, but they differ strikingly from one another. We have recently become interested in whether genetically based individual differences in taste and fearfulness are related (Dess and Chapman 1990). Bitter taste is especially interesting in light of its natural relationship to toxicity, danger, and negative affect (Garcia and Hankins 1975; Scott and Mark 1987). If rejection of bitter tastes was a preadaptation for negative affect in general, then the two may have remained intertwined in mammalian evolution. Fear is assumed to be a prototypical negative emotion. If our reasoning is valid, then individual differences in fearfulness should be genetically related to individual differences in reactions to bitter tastes (also see Donovick et al. 1973, 1975).

254


Our initial studies provide strong support for this idea. The first study involved two lines of rats selectively bred on an avoidance task. These lines differ markedly on the avoidance phenotype and on measures of emotionality, but not at all in sensorimotor or learning abilities. For example, the highly "emotional" line shows faster fear conditioning, more defecation in an open field, and greater submissiveness in social encounters (Brush et al. 1988, 1989). Rats from each line were subjected to mild handling stress and then were offered quinine-adulterated water to drink. As predicted, the highly emotional line rejected the adulterated water more vigorously (Brush et al. 1988, Experiment 5). The converse selective breeding study has begun. The question was whether "finicky" rats would be more emotional than nonfinicky controls. This project began serendipitously, with one male rat w h o actively avoided saccharin solution (which most rats consume avidly). Saccharin solution is sweet, and it was hard to imagine an evolutionary scenario in which rejection of sweets would be advantageous. On the other hand, saccharin solution is also bitter (Morrison and Jessup 1977): it was easy to guess w h y an aversion to saccharin's bitter quality might have survived genetically. There may be a special advantage to rejecting bitterness in combination with sweetness. In the study by Richter and Clisby (1941) on PTC tasting, rats were offered a sugar solution laced with PTC. Though nearly all of the rats had rejected simple PTC solution, half the rats drank a fatal dose of the sugar/PTC solution. The rats that rejected the solution despite its sweetness survived. In certain circumstances, then, extreme sensitivity to bitterness may be advantageous, even if it means bypassing a sweet caloric treat. In the laboratory, saccharin availability is one of those circumstances: it is toxic to rats and can be fatal, even w h e n consumed voluntarily (Strouthes 1973). Our saccharin-averse (SA) male and a male with a normal saccharin preference (SP) each fathered litters with two different females. The F1 offspring did not differ on saccharin drinking. The SA males did, however, have a significantly stronger quinine aversion than the SP males; SA and SP females did not differ. The early emergence of line differences in quinine aversion suggested that the parental differences in saccharin drinking were heritable (Nachman 1959) and were due to sensitivity to bitter tastes. We have just assessed fearfulness of the F2 males in a novel open-field apparatus (Royce 1977). Sensitivity of our test to fearfulness was enhanced by placing rats in a dark place (which rats prefer to lighted places; Allison et al. 1967; Freedman 1965) and measuring their latency to emerge into the well-lit open field (Figure 4). The latency-to-emerge data are shown in Table 1. SA rats took longer to emerge into the open field than did SP rats. When subsequently placed directly into the open


255

J 15" black walls

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field for 5 minutes, SA rats were significantly more likely to defecate than were SP rats. The two lines did not differ in general activity in this test. The SA line drank significantly less saccharin than did the SP line in later taste tests; sucrose drinking did not differ between lines. These data suggest that genetically based differences in taste are related to emotionality and, given the rapid emergence of significant line differences, that the relationship is robust. Additional work is needed to clarify the nature of the taste differences by comparing lines on measures of threshold, magnitude, and hedonic reactivity to quinine, sucrose, and other tastes. Whether the lines are differentially vulnerable to stress in the helplessness model with respect to ingestive and noningestive outcomes--is also an important question. Finally, there are good reasons for studying the relationship between taste and fearfulness in male and female rats (Ganchrow et al. 1981; Valenstein et al. 1967). We plan to do more thorough testing of both sexes in future generations. Is it possible that taste and emotionality are related in humans? The available data suggest they are. People differ markedly in their sensitivity to bitter tastes, and genes are partly responsible (Kaplan and Fischer 1965). Sensitivity to the bitter compound 6-n-propylthiouracil (PROP) is bimodally distributed, indicating control by a single gene locus. In addition to being more sensitive to PROP's bitterness, PROP

256 Table 1.

Human Nature, Vol. 2, No. 3, 1991 Latency to Emerge into a Novel O p e n Field for F 2 Males in Selectively Bred Lines of Saccharin-averse (n = 14) a n d Saccharin-preferring (n = 12) Rats, in seconds Latency to Emerge (Maximum = 300.0 seconds) Saccharin-Averse

Saccharin-Preferring

23.4 81.8 117.5 117.1 132.9 154.3 178.6 291.7 300.0 300.0 300.0 300.0 300.0 300.0

12.2 13.9 15.7 23.6 29.5 37.0 44.7 90.4 107.1 126.0 126.2 255.4

Mean -- 207.0 Standard error of the mean = 27.0

Mean = 73.5 Standard error of the mean = 21.0

t(with 24 df) ~ 3.91, p = .0007

"tasters" rate saccharin (Bartoshuk 1979) a n d quinine (Gent and Bart o s h u k 1983) as m o r e bitter than d o individuals w h o c a n n o t taste PTC. If bitter sensitivity is similar in rats and h u m a n s , a n d bitter rejection is genetically linked to emotionality in rats, t h e n bitter sensitivity m a y be genetically linked to emotional health in h u m a n s . Relative to those w h o cannot taste PTC, PTC tasters r e p o r t m o r e a p p r e h e n s i v e n e s s , tension, a n d d e p r e s s i o n both personally and in their m o t h e r s (Mascie-Taylor et al. 1983; W h i t t e m o r e 1986; also see Miller a n d N a y l o r 1989). We also f o u n d strong relationships b e t w e e n p s y c h o p h y s i c a l r e s p o n s e s to quinine and depressive s y m p t o m a t o l o g y (Dess a n d C h a p m a n 1990). DeMet et al. (1989) e x a m i n e d the relationship b e t w e e n quinine detection and emotional health in a clinical sample. T w o g r o u p s w e r e used. O n e g r o u p consisted of panic-disorder patients (PD), a n d the o t h e r consisted of nonpsychiatric controls (a third, post-traumatic stress g r o u p was too small to p r o v i d e m u c h information). C h a n g e s in quinine detection after topical application of caffeine to the t o n g u e was assessed in all subjects. Topical caffeine increases sensitivity to tastes by altering adenosine receptor sensitivity; r e s p o n s i v e n e s s to caffeine in taste tests was p r e s u m e d to be a m a r k e r for a d e n o s i n e sensitivity in the central n e r v o u s


257

system. M a n y significant relationships b e t w e e n quinine detection a n d emotional health w e r e obtained. For example, post-caffeine q u i n i n e detection varied significantly with b o t h d e p r e s s i o n a n d anxiety in the entire sample of subjects. Relative to controls, caffeine h a d a greater impact o n quinine detection in P D patients, 40% of w h o m had a secondary diagnosis of major depression. F u r t h e r studies of taste sensitivity in this m a n n e r m a y clarify the relationship b e t w e e n anxiety a n d depression in psychiatric a n d nonpsychiatric populations. Less work has b e e n d o n e o n individual differences in sweet tastes and emotional distress. A m s t e r d a m et al. (1987) report l o w e r - t h a n - n o r m a l sucrose intensity ratings a m o n g d e p r e s s e d p e o p l e but higher-thannormal sucrose pleasantness ratings. Cravings for sweets in d e p r e s s i o n are real but vary substantially b e t w e e n p e o p l e (Fernstrom 1989; Wurtm a n and W u r t m a n 1989). G r e a t e r sucrose pleasantness a n d s w e e t cravings d u r i n g d e p r e s s i o n m a y be related to the genetically b a s e d bitter p h e n o m e n a discussed above (Gent a n d Bartoshuk 1983), or the m e c h a nisms might be entirely different (Blass et al. 1989). Taste is a promising peripheral m a r k e r for emotional health. Unfortunately, virtually n o t h i n g is k n o w n about the relationship b e t w e e n emotional health a n d simple taste qualities other t h a n bitter a n d sweet, or about complex tastes. N o r has the relationship b e t w e e n taste differences, dietary habits, and metabolic processes b e e n examined. T h e existing data suggest that variations in taste, appetite, a n d w e i g h t in emotionally distressed h u m a n s (and their Rattus brethren) d e s e r v e further attention.

Preparation of this manuscript was made possible by fellowship support from the John D. and Catherine T. MacArthur Foundation and from Occidental College, for which I am grateful. Thanks are also due John Garcia for his "gut feelings," to Dennis VanderWeele and Sara Siebel for making the selective breeding study possible, and to Jeanne Altmann for bringing Human Nature to my attention.

Nancy K. Dess is Assistant Professor of Psychology at Occidental College. She wrote this paper while she was a Fellow at the Center for Advanced Study m the Behavioral Sciences at Stanford. The central theme of her work is fear. Some of her research has been on Pavlovian fear conditioning: its associative structure, ontogeny, and measurement. Although she Is interested in fear as an organizer of defensive behavior, she also studies its darker side---chronic or intense fear, or "'stress." She has examined effects of fear and stress on learnmg, hormonal, and ingestive processes; her subject species include dogs, rats, cats, and humans. Her working hypothesis is that ingestion, broadly conceived, is a useful tool for exploring the mechanisms of anxiety and clinical affective disorders.

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