Psychological Bulletin1987, VoflOa, No. 2,234-

Copyright 1987 by the American Psychological Association, Inc.0033.2909/87/J00.75

Carbohydrates, Tryptophan, and Behavior: A Methodological Review

Bonnie Spring, June Chiodo, and Deborah J. BowenTexas Tech University

In this methodological review, we examine the behavioral effects of carbohydrates and tryptophan

and conclude that high-carbohydrate foods do not provoke hyperactivity, contrary to popular beliefs.Unbalanced carbohydrate meals, however, often induce fatigue and can impair performance amongboth children and adults. Although tryptophan hastens sleep onset, dulls pain sensitivity, and may

reduce aggressiveness, it is unclear whether similar effects can be obtained through carbohydrate

ingestion. We provide support for the hypothesis that carbohydrates and tryptophan function sim-ilarly and like drugs that modify brain biochemistry and accompanying mood and behavior. We also

examine implications for clinical populations who selectively crave carbohydrates.

Despite professional skepticism, both anecdotal and empiri-

cal evidence continue to suggest that foods affect behavior. The

empirical literature has now grown sufficiently to evaluate the

validity of beliefs about one nutrient category, carbohydrates.

Claims about the psychological effects of carbohydrates, espe-

cially sugar, are multiple. They range from the assumption that

sugar enhances activity and aggression, to the premise that

sugar has an energizing effect on behavior, to the assertion that

sugar induces an anxious or depressed mood. Scientific evalua-

tion and dissemination of accurate information about diet-be-

havior relations may lead to beneficial applications. They may

also help to dispel folk wisdoms that can justify ineffective or

even harmful health practices.

Recent clinical research suggests that certain population sub-

groups selectively crave carbohydrates, usually as snack foods.

Examples include some proportion of individuals with obesity

(Hopkinson & Bland, 1982; Wurtmanetal., 1985), postpartum

depression (Dalton, 1980), seasonal affective disorder (Rosen-

thai et al., 1984) and nicotine withdrawal (Grunberg, 1982). It

is possible that these individuals are unwittingly practicing self-

medication, using carbohydrates to induce desired effects on

mood and behavior. To evaluate this possibility, one must define

the effects of carbohydrates on mood and behavior.

To provide a rationale and interpretive framework for the em-

pirical literature, we first examine possible mechanisms to ex-

plain the acute behavioral effects of carbohydrates. In the sec-

ond section, we review findings from empirical studies of chil-

dren, in which hyperactivity and associated performance

impairments have been the most studied dependent variables.

In the third section, we focus on studies of adults, including the

effects of carbohydrate or tryptophan on mood, performance,

pain, and sleep. We evaluate results with reference to method-

ological factors that could contribute to discrepant conclusions.

These factors include research design, sample characteristics,

Deborah J. Bowen is now at the Fred Hutchinson Cancer Research

Center in Seattle, Washington.Correspondence concerning this article should be addressed to Bon-

nie Spring, Department of Psychology, Texas Tech University, Lubbock,Texas 79409.

nutrient composition, time of day, measurement of target be-

haviors, and the interval between food intake and behavioral

testing.

Possible Mechanisms Underlying Carbohydrate Effectson Behavior

One reason for professional skepticism about the existence of

nutrient effects on behavior has been ignorance of a plausible

mechanism whereby foods could influence behavior. Three

mechanisms have been proposed: expectancy effects, hypogly-

cemia, and brain neurotransmitter precursors.

Expectancy Effects

Behavioral change that spuriously appears to be nutrient in-

duced could arise if food-related expectations influence behav-

ior in a way that creates self-fulfilling prophecies (Rosenthal &

Jacobson, 1968). As such, behavioral change following carbohy-

drate ingestion would be unrelated to nutrients per se but would

represent a placebo effect.

Cognitive expectations constitute a complex problem in

studies of diet-behavior relations. Expectations can be con-

trolled by means of double-blind placebo-controlled trials.

Double-blind studies that use pure nutrients disguised in pill

form, however, may manipulate only part of the carbohydrate-

behavior relation. Omitted from this picture are the varying

sensory and gastric parameters that accompany meals differing

in nutrient composition and volume. The problem of selecting

a placebo that lacks behavioral effects is also a thorny one (Rip-

pere, 1983). For example, valine or leucine placebos can block

the brain uptake of both tryptophan and tyrosine. Aspartame

elevates brain tyrosine in rats (Ybkogoshi, Roberts, Caballero,

& Wurtman, 1984) and lowers it in humans. Hence, it remains

possible that some placebos can produce acute behavioral

change. Nonetheless, double-blind studies are necessary, espe-

cially at a later stage in research, for testing whether diet-behav-

ior relations persist when expectations are controlled.

Although several investigators have warned of the potentially

powerful role of expectancies in diet-behavior research (Con-

ners, 1984; Sprague, 1981), two points of evidence question this

234

CARBOHYDRATES AND BEHAVIOR 235

position. First, food-related expectancy effects may be difficultto induce. Christensen, White, and Krietsch (1985) found thatneither preexisting nor experimentally induced expectationsabout the behavioral effects of sugar engendered consistentsymptom reports following sugar or placebo. Results indicatedthat subjects do not necessarily bold personal expectanciesabout the effects of food constituents, such as sugar andcaffeine. Instead, they expect others to be more strongly affectedthan themselves. Second, if placebo effects do operate, then onewould expect the major research findings to parallel popularstereotypes about sugar's effects on behavior. As the rest of thisreview indicates, few data, however, demonstrate that sugarheightens activity, energy, or depression.

It is not clear that expectations play a major role in generatingdiet-behavior relations under ordinary circumstances. How-ever, because placebo effects operate most powerfully in the con-text of a client-therapist relationship (Shapiro, 1971), onewould expect placebo effects to play a greater role when dietaryinterventions constitute a formal treatment program. In dailylife or under laboratory conditions, expectations about theeffects of carbohydrates may be neither sufficiently uniform norsufficiently personal to engender systematic behavioral change.The crucial test is whether effects observed with actual foodspersist or vanish in double-blind controlled trials of nutrients.

Hypoglycemia

When given exogenously, as in the treatment of diabetes, in-sulin can profoundly lower plasma glucose to a degree at whichbrain glucose supplies are affected. Hypoglycemia triggers thesecretion of epinephrine, which in turn causes glycogen to bebroken down into glucose so that the brain's supply of glucose isnot jeopardized. Epinephrine secretion is associated clinicallywith trembling, sweating, heart palpitations, hunger, and weak-ness, providing what has been the primary rationale for re-search testing whether sugar induces symptoms of hyperactiv-ity, anxiety, and depression.

Because exogenous insulin induces hypoglycemia and its as-sociated symptoms, it has been suggested that endogenous insu-lin, triggered by carbohydrate intake, can also induce hypogly-cemia. This is unlikely, however, because carbohydrates elevateglucose to such a degree that plasma glucose levels can remainhigher than fasting levels even 4 to 5 hr after eating (Spring etal., 1986). Consequently, absolute fluctuations in plasma glu-cose and insulin appear unlikely to simply explain the behaviorchanges that normal subjects exhibit 2 hr after eating carbohy-drates.

A possible exception may occur among individuals whosuffer from functional reactive hypoglycemia (Harris, 1924). Inthis population, blood glucose levels fall to abnormally low lev-els (30-40 mg/100 ml) 2.3 to 5 hr after a carbohydrate-richmeal (Porte & Halter, 1981). It has been suggested that reactivehypoglycemia, associated with increased production of epi-nephrine, could produce restlessness in hyperactive childrenwho eat sugar. Langseth and Dowd (1978) claimed that 75%of 265 hyperactive 7- to 9-year-olds showed abnormal glucosetolerance curves. The study lacked a normal control group,however, and Langseth and Dowd used norms that are at vari-

ance with other data for normal children (Josefsberg et al.,1976).

Although intriguing, reactive hypoglycemia is a rare condi-tion characterizing only a small minority of the population.Known cases are explicitly excluded from many studies of car-bohydrate effects on behavior. Additionally, plasma glucose lev-els after a glucose challenge fell to similarly low levels in manyindividuals who do not report symptoms of physiological orpsychological distress. Further, in patients who do report symp-toms, their timing is not clearly related to the rate of descent ofthe glucose level or to the level of glucose at the time of thesymptoms (Johnson, Dorr, Swenson, & Service, 1980). Finally,DeFronzo, Hendler, and Christensen (1980) demonstrated thatin normal humans, a decline in plasma glucose within the nor-mal range fails to trigger the epinephrine secretion that presum-ably induces hypoglycemic symptoms. For all these reasons, itis unlikely that reactive hypoglycemia is a major mechanismresponsible for carbohydrate-behavior relations.

A proposal that warrants further investigation is the possibil-ity that individuals who habitually practice high carbohydrateintake may lower the threshold for hypoglycemia. It is knownthat in rats, chronic hyperglycemia decreases the transport ofglucose across the blood-brain barrier (McCall, Millington, &Wurtman, 1982). Consequently, hypoglycemia can occur atnormal absolute values of plasma glucose, because brain glu-cose transport is reduced. In individuals who become hypergly-cemic because of chronic, high intake of sugars, a temporarynormalization of plasma glucose, produced by a balanced dietor by fasting, could significantly reduce glucose transport intothe brain (Gjedde & Crone, 1981; Kanarek & Marks-Kaufman,1979) and engender symptoms of hypoglycemia. Analogously,hypoglycemic reactions are known to occur in hyperglycemicdiabetics at normal or high plasma glucose concentrations be-cause of an upward resetting of the glucostat at which counter-regulatory hormones are released (DeFronzo et al., 1980).

Hence, hypoglycemia might provide a potentially useful ex-planation of central nervous system (CNS) symptoms accom-panying a normalization of plasma glucose after a chronic high-carbohydrate diet. In contrast, for populations maintained onnormal dietary regimens, reactive hypoglycemia is probablytoo rare to fully account for the acute effects of carbohydrates.

Brain Neurotransmitter Precursors

A third possible mechanism to explain carbohydrate effectson behavior stems from the observation that certain food con-stituents that are neurotransmitter precursors can alter the syn-thesis and release of brain neurotransmitters (Fernstrom &Wurtman, 1971, 1972; Wurtman, Hefti, & Melamed, 1981).These findings raise the possibility that carbohydrates or otherfoods might produce changes in behavior, not by means of pla-cebo effects or hypoglycemia but rather by altering the levels ofbrain neurotransmitters that are associated with various psy-chological functions.

Synthesis of the monoamine neurotransmitter serotonin hasbeen shown to be influenced by the availability of its amino acidprecursor, tryptophan, in the diet. Precursor control has alsobeen demonstrated, under certain conditions, for the catechol-

236 B. SPRING, J. CHIODO, AND D. BOWEN

amine neurotransmitters norepinephrine and dopamine andfor acetylcholine, histamine, and glycine.

The essential amino acid, tryptophan, cannot be synthesizedby humans or other mammals. Because the body's entire supplyof tryptophan is obtained from dietary protein, it might seemthat a protein meal would elevate brain tryptophan or seroto-nin. However, the opposite occurs. Brain tryptophan and sero-tonin decline after a protein-rich meal. This paradox occursbecause protein contains very little tryptophan (1-1.6%), incomparison with the other large neutral amino acids—leucine,isoleucine, valine, tyrosine, and phenylalanine (25%). Becauseall the large neutral amino acids compete for access to the samecarrier molecules for transport across the blood-brain barrier,the brain influx of tryptophan declines relative to its competi-tors after a high-protein meal.

Paradoxically, a meal lacking protein but rich in carbohy-drate increases brain tryptophan and serotonin synthesis, eventhough such a meal contains no tryptophan. In organisms thathave been fasting, a carbohydrate-rich, protein-poor mealbrings about a rise in the ratio of plasma tryptophan to the otherlarge neutral amino acids. The change in this ratio comes aboutbecause the carbohydrate meal triggers insulin secretion, whichcauses most of the amino acids other than tryptophan to leavethe bloodstream and be taken up into muscle. In animals thathave fasted overnight, the insulin secretion triggered by carbo-hydrates causes a 40% to 60% fall in plasma leucine, isoleucine,and valine and a 15% to 30% fall in plasma tyrosine. Plasmatryptophan levels do not fall because tryptophan binds to albu-min molecules as insulin strips away the free fatty acids that areusually albumin bound. In humans who fast after breakfast andeat a carbohydrate test meal for lunch, the plasma tryptophanratio rises regardless of whether the test meal consists primarilyof sucrose or starch (Lieberman, Spring, & Garfield, 1986).Carbohydrate-rich meals not only increase the brain influx oftryptophan; they also enhance the synthesis and release of brainserotonin, insofar as the latter are assessed by cerebrospinalfluid 5-hydroxyindoleacetic acid (5-HIAA; Fernstrom & Wurt-man, 1971, 1972).

For a test meal to reliably elevate brain serotonin, it must benot only carbohydrate rich but also protein poor. A meal needonly contain some protein to impede the brain influx of trypto-phan. However, the minimum proportion of protein needed tooffset the effects of carbohydrates on brain tryptophan in hu-mans remains to be established.

In the remainder of this article, we review studies on the be-havioral effects of carbohydrates. If alterations in the brain in-flux of tryptophan constitute a mechanism whereby these foodsaffect brain neurochemistry, the effects of consuming carbohy-drates should be similar to those following ingestion of the foodconstituent tryptophan. For comparison, therefore, we includestudies on the behavioral effects of tryptophan.

Effects of Carbohydrates on the Behavior of Children

Activity and Aggression.- Overview

The majority of research on sugar and childhood hyperactiv-ity has been guided by one of the following two hypotheses: (a)Sugar induces hypoglycemia, or (b) hyperactivity results from

an allergy to sugar or other food constituents (the Feingold,1976, hypothesis). Evidence bearing on the relation betweencarbohydrate intake and activity levels stems from threesources: trials of the Feingold diet, animal studies of activity,and experimental and clinical observations of aggression.

Feingold (1976) diet. Although the Feingold diet, intendedto restrict food additives and salicylates, is believed by manyparents to control hyperactivity, its efficacy remains controver-sial (Conners, 1980; Harley et al., 1978; Weiss et al., 1980). Inaddition to its intended restrictions, the Feingold diet also inad-vertently reduces carbohydrates, including up to 86% of prod-ucts high in sucrose (Prinz, Roberts, & Hantman. 1980). Conse-quently, it remains possible that reductions in dietary carbohy-drates are partly responsible for decreases in hyperactivity.However, although parents frequently nominate sugar as a trig-ger for unmanageable behavior (Crook, 1975), double-blind tri-als often fail to confirm this speculation (Benar, Rapoport, Ad-ams, Berg, & Cornblath, 1984; Egger, Carter, Graham, Gumley,&Soothill, 1985).

Animal studies of activity. Whereas practitioners of the Fein-gold (1976) diet expect sugar to exacerbate hyperactivity, datafrom animal studies using acute serotonin precursor adminis-tration yield the opposite prediction. The serotonin precursorsL-tryptophan and 5-hydroxytryptophan (5-HTP) usuallyacutely decrease motor activity in rats (Modigh, 1972, 1973;Taylor, 1976; Warbritton, Stewart, & Baldessarini, 1978). Oneapparent exception is that when given with agents that increaseCNS serotonin availability (e.g., monoamine oxidase inhibitorsand reuptake blockers), serotonin precursors can induce auto-nomic activation and skeletal muscle hyperactivity (e.g., myo-clonus; Grahame-Smith, 1971; Sloviter, Drust, & Conner,1978). Locomotor activity is not increased, however, despitethese other indexes of activation (Warbritton et al., 1978).

It is possible that carbohydrates exert different effects on ac-tivity and work by another mechanism when given chronicallyrather than acutely. Chiel and Wurtman (1981) found that ratsfed a diet involving increasing ratios of carbohydrate to proteinshowed increased nocturnal activity levels. Findings were inde-pendent of fat content, caloric intake, and weight gain. Sim-ilarly, rats fed solutions containing 20% sucrose were signifi-cantly more active than those not fed sucrose (Buckalew &Hickey, 1983).

As mentioned earlier, fats maintained on a high-glucose dietshow reduced brain influx of glucose. These hyperglycemic ratsmay, therefore, be especially prone to become deficient in brainglucose when food intake is discontinued during sleep or fast-ing. It may be that the restlessness these animals exhibit afterawakening is related to CNS hypoglycemia, although this expla-nation remains speculative.

Experimental and clinical observations of aggression. A ma-jority of findings indicate that muricide (mouse killing) can beinduced in rats by reducing serotoninergic function (Gibbons,Ban, Bridger, & Leibowitz, 1979; Grant, Coscina, Grossman,& Freedman, 1973; Sheard, 1969). Aggression can be reversedby tryptophan administration, and similar effects would be pre-dicted for carbohydrates. In humans as well, considerable clini-cal evidence connects serotoninergic hypofunction, activity,and aggression (cf. Brown, Goodwin, Ballenger, Goyer, & Ma-jor, 1979; Linnoilaet al., 1983; Morand, Young, & Ervin, 1983;

CARBOHYDRATES AND BEHAVIOR 237

Sheard, 1975). Kruesi, Linnoila, Rapoport, Brown, and Peter-

son (1985) recently described a conduct-disordered child mani-

festing impulsivity, inattentiveness, low 5-HIAA, and carbohy-

drate craving.

In sum, on the basis of popular beliefs and chronic animal

studies, one might expect carbohydrates to increase activity lev-

els and aggression. In contrast, on the basis of animal studies

acutely manipulating serotoninergic function and clinical stud-

ies associating aggression and serotoninergic hypofunction, one

would expect carbohydrates to acutely lower activity levels. We

now review correlational and experimental evidence concern-

ing how carbohydrates affect activity and aggression in chil-

dren. Table 1 provides methodological details.

Activity and Aggression: Correlational Studies

Prinz et al. (1980) asked mothers of hyperactive and normal

children to maintain food-intake records for their children dur-

ing the week prior to laboratory testing. Children were then vid-

eotaped in a playroom and rated for destruction-aggression,

restlessness, and movements across quadrants on the floor by

raters who did not know their diagnostic and dietary character-

istics. Hyperactive children did not differ significantly from

control subjects in patterns of food intake. Among hyperactive

children, however; sugar consumption was positively correlated

with destruction-aggression (r = .45) and restlessness (r = .33).

Among control subjects, sugar consumption was significantly

correlated with quadrant changes (r = .59).

Wolraich, Stumbo, Milich, Chenard, and Schultz (1986) at-

tempted to replicate Prinz et al.'s (1980) findings in a second

correlational study. Mothers of hyperactive and control boys

completed 3-day diet records and food-frequency interviews.

The hyperactive group was of lower socioeconomic status than

was the control group, and a significantly greater proportion

of hyperactive children were on sugar-restricted diets. Sugar-

restricted children did not, however, actually differ from nonre-

stricted children in dietary content, with the result that there

were no significant dietary differences between hyperactive and

control children. Partial correlations (controlling for age) be-

tween total sugar intake and 37 behavioral and cognitive vari-

ables failed to detect any significant correlations within the hy-

peractive group (the only group for which behavioral data were

available). The ratio of sugar to total calories consumed, how-

ever, correlated positively (r = .39 to .50) with free-play activity

levels (measured by floor grid crossings and ankle actometer),

off-task behaviors, and attention shifts (both rated by observ-

ers). Results can be considered to represent only a weak replica-

tion of Prinz et al.'s findings because of the lack of significant

correlations between total sugar intake and behavior Moreover,

as Wolraich et al. (1986) pointed out, the few significant find-

ings could have emerged by chance alone, given the large num-

ber of correlations computed.

In the third correlational study, Prinz and Riddle (1986) ex-

amined food-intake records for healthy Caucasian boys to se-

lect the highest and lowest sucrose consumers with intake ad-

justed for body weight. At the end of the week of food-intake

recording, they administered a version of the Continuous Per-

formance Test (CPT) of vigilance. The children who were in the

habit of eating large quantities of sucrose (averaging 6.65 g/kg

per day) showed vigilance deficits similar to those observed in

hyperactive children with attention deficit disorder. When com-

pared on other variables, the children who usually ate much

sucrose habitually consumed 30% more carbohydrates than did

low-sucrose consumers but did not differ in protein or fat in-

take. That the two groups failed to differ in body weight is strik-

ing, because the high-sucrose children consumed a highly sig-

nificant (p = .001) excess of calories.

Although Prinz et al. (1980) hypothesized that sucrose might

provoke agitated or aggressive behavior in hyperactive children

with attention deficits, they acknowledged that this conclusion

cannot validly be drawn from correlational data. Because no

information is available about what children ate shortly before

testing, it is unclear what foods were acutely influencing their

activity levels and vigilance test performance. If food intake was

limited in the hours before testing, it is even possible that the

children who usually eat much sucrose were in a state ofhypo-

glycemia when they were tested, with this factor explaining their

restlessness and poor performance.

Although correlational data cannot delineate the effects of

sugar on behavior, they can help describe the characteristics of

individuals who selectively eat large amounts of sugar. Findings

suggest that restless, aggressive children who have difficulties

sustaining vigilant attention are prone to eat large quantities of

sugar. The most pressing question now is why? Three possible

explanations present themselves.

First, a subgroup of hyperactive children may display alter-

ations of tryptophan metabolism such that insufficient plasma

tryptophan is available for brain uptake (Irwin, Belendiuk, Mc-

Closkey, & Freedman, 1981), but this hypothesis remains con-

troversial (Coleman, 1971; Rapoport, Quinn, Scribanu, & Mur-

phy, 1974; Wender, 1969). For this subgroup of highly active

and aggressive hyperactive children, dietary preference for

sugar could be an adaptive means of elevating brain tryptophan

to help modulate high levels of unmanageable behavior. Such

children may even have acquired their dietary preferences by

learning that sugar produces a calming effect on behavior.

The second interpretation of the correlational findings attri-

butes both the increased activity levels and the increased carbo-

hydrate intake to a third variable, heightened metabolic rate.

Perhaps highly active or aggressive children consume excess

carbohydrates and calories because of a metabolic need for en-

ergy. The absence of a weight difference between high- and low-

sucrose-consuming children is consistent with the hypothesis of

an increased metabolic rate in hyperactive children.

The third and least convincing explanation is that mothers of

highly active children foster their children's high sugar intake

by setting few limits on children's access to foods (Prinz & Rid-

dle, 1986). Contrary to this proposal, Wolraich et al. (1986)

found that a majority (59%) of mothers of hyperactive children

claimed to restrict their children's sugar intake, in comparison

with a small minority (8%) of mothers of control children. The

more fundamental question concerns whether self-reported pa-

rental behaviors reflect actual parental behavior and whether

either bears a relation to what children in fact eat. Parents who

allege to practice sugar restriction appear to have difficulty im-

plementing this policy, because Wolraich et al. (1986) found

that only 47% are able to restrict their children's daily sugar

intake to below 50 g. Moreover, hyperactive children may un-

238 B. SPRING, J. CH1ODO, AND D. BOWEN

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dermine their parents' dietary regimens, because children

claim to consume more sugar than their parents know about

(Wolraichetal., 1986).

Correlational research has generated interesting ideas about

the relation between sugar and children's behavior. The positive

correlation between activity levels and carbohydrate consump-

tion appears to be reliable but sheds no light on the direction of

causality. Although often interpreted to imply that sugar exac-

erbates hyperactivity, this conclusion is at variance with results

from most experimental research. Two alternative interpre-

tations warrant further investigation. The first is that highly ac-

tive children have heightened cravings for sugar because of its

normalizing effect on brain chemistry and behavior. The second

is that both hyperactivity and high sugar intake reflect a height-

ened metabolic rate.

Activity and Aggression: Experimental Studies

Behar et al. (1984) identified boys whose parents responded

to a newspaper advertisement seeking children with adverse be-

havioral reactions to sugar. Of the 21 responding children, 9

met criteria for attention deficit disorder with hyperactivity, and

4 others presented mixed or past symptoms. Subjects were med-

ication free for 1 week before the study and were maintained on

a high-carbohydrate diet for 3 days prior to testing. On 3 days

a minimum of 48 hr apart, children fasted overnight. The next

morning in double-blind fashion they received drinks contain-

ing a saccharin placebo, sucrose, or glucose. From 30 min to 5

hr after the challenge substances, Behar et al. measured motor

activity by means of an actometer and behavioral ratings.

When examined singly, neither sugar produced differences in

activity, compared with the placebo. When the data from both

sugars were combined, however, the actometer registered a sig-

nificantly greater decline in movements for sugar, compared

with the placebo 3 hr after ingestion. The observer rating scale

failed to detect this phenomenon, suggesting that the decline in

activity was quite subtle.

Ferguson, Stoddart, and Simeon (1986) performed two sugar-

challenge studies. In the first, they challenged children three

times with sucrose at different dosages and three times with

aspartame. Even though these children were selected because

their parents believed them to show adverse reactions to sugar,

Ferguson et al. found no differences between the two challenges'

effects on activity levels, observer behavior ratings, or cognitive

measures. In the second study, they administered aspartame

and sucrose to preschoolers. Again, they detected no differences

in actometer measures, behavioral observations, or cognitive

measures, although three boys performed slightly worse on

drawings following the sugar challenges.

Wolraich, Milich, Stumbo, and Schultz (1985) conducted

two studies of hyperactive boys admitted to a clinical research

center and maintained on a sucrose-free diet for 3 days of test-

ing. After a day of baseline testing, children were challenged in

double-blind fashion with a beverage containing either aspar-

tame or sucrose. In the first study, challenges were given 1 hr

after lunch. In the second, drinks were given in the morning

after an overnight fast. For 3 hr after the challenges, children

were assessed with actometer and observer ratings of playroom

activity; with tests of learning, vigilance, and memory; and with

measures of impulsivity. Wolraich et al. (1985) found no sig-

nificant differences between sucrose and aspartame on any

measure in either study.

Results of these challenge studies have been impressively con-

sistent in demonstrating either no effect in comparison with a

placebo or a slight reduction of activity when children consume

sugar. In another series of studies, Conners and his associates

(Conners & Blouin, 1983; Conners et al, in press) have ob-

served much more variable effects of sugar on the behavior of

more severely disturbed psychiatric inpatient children.

In the first report, Conners and Blouin (1983) studied chil-

dren hospitalized for severe behavior disorders, anxiety, and at-

tention deficits. After a high-protein breakfast, children were

challenged with sucrose, fructose, or orange juice on alternate

days in counterbalanced order. The intervals between breakfast

and challenge and between challenge and testing were unspeci-

fied. The children were not unaware of treatment conditions,

although observers and staff were. Children were also permitted

to eat other foods during the protocol. When compared with

juice, both sugars increased observer ratings of total movement

and decreased ratings of appropriate behaviors based on 15-s

samplings of behavior in a classroom. Teachers and nurses,

however, were unable to detect these changes. Conners and

Blouin discouraged generalizing from these results because of

three methodologic problems: Dietary control was not main-

tained; all challenge substances were high in carbohydrates; and

subjects were not unaware of experimental conditions.

In the second study, children who were psychiatric inpatients

received sucrose, fructose, or the taste equivalent of aspartame

(Conners et al., in press). All subjects received the three treat-

ments in counterbalanced order following breakfast for a week,

for periods ranging from 1 to 21 weeks. Conners et al. main-

tained double-blind conditions and assessed but did not control

daily food intake. The intervals between breakfast and chal-

lenge and between challenge and testing were unspecified, and

subjects could apparently eat other snacks during these times.

Consistent with Behar et al.'s (1984) findings, the sucrose chal-

lenge lowered minor motor activity and had no effect on gross

motor activity, according to observer ratings of classroom be-

havior. Fructose lowered gross motor activity without affecting

minor motor activity. A hierarchical regression analysis, per-

formed to control for the effects of age, baseline behavior rates,

and nutrients eaten for breakfast, indicated that protein and

carbohydrate intake at breakfast explained a greater proportion

of the variance in behavior than did the challenge substances.

In fact, when age, baseline behaviors, and breakfast foods (ap-

parently not including snacks) were held constant statistically,

the sugar challenge appeared to increase rather than decrease

deviant behaviors. This effect was blocked, at least statistically,

by a breakfast meal of mixed nutrients, including protein.

The Conners et al. (in press) findings demonstrate the need

to control the intake of other foods when examining the behav-

ioral consequences of carbohydrate challenges or snacks. Statis-

tical control provides preliminary information but requires

confirmation by experimental manipulation. Evaluating the

Conners et al.'s specific findings about carbohydrate effects on

behavior is difficult because of three uncontrolled sources of

variability: the amount of food eaten by the children for break-

fast and snacks, its nutrient composition, and the interval be-

CARBOHYDRATES AND BEHAVIOR 241

tween eating and behavioral assessment. Because subjects werepermitted to choose their own meals and snacks and becausenonchallenge nutrient intake explained the greatest amount ofvariance in behavior, one probably should regard the Connerset al. results as correlational rather than experimental.

In sum, in contrast to correlational evidence, the majority ofexperimental studies of sugar's effects on children's behaviorhave suggested no change or a decrease in activity after sugarconsumption. The only exception is a series of studies by Con-ners and associates (Conners & Blouin, 1983; Conners et al.,in press), in which they found both decreases and increases inactivity after carbohydrate consumption. These conflicting re-sults may be due in part to other foods that the children atebefore and during behavioral testing, because subjects were al-lowed to choose what they ate for breakfast and snacks prior tochallenge. Another difference that may help explain the discrep-ancy is that the Conners et al. sample was presumably moreseverely disturbed: They were psychiatric inpatients, and manymet criteria for pica (eating nonfood substances).

Whereas activity has been one important dependent variablein studies of children, performance on cognitive tests has beenanother. Both types of measures help to answer the question ofwhether diet affects childrens' performance in the classroom.Methodological details for the studies of performance appear inTable 2.

Correlational and Experimental Studies of Performance

Some studies already reviewed included tests of performance.In their correlational study, Prinz and Riddle (1986) comparedthe responses of high- and low-sucrose-consuming children onthe CPT of vigilance. This test assesses the type of attentionalimpairment known to characterize many hyperactive children.Prinz and Riddle asked children to press a lever in response toa slide of a duck shown for 500 ms and to refrain from respond-ing to slides of other animals. Although the high-sucrose-con-suming children responded to significantly fewer targets thandid the children who usually ate lower amounts of sugar, theydid not overrespond to a related nontarget stimulus (an eagle).Consequently, differences reflect lowered sensitivity to targetsrather than impulsive responding to nontargets among childrenwho usually ate much sugar. These correlational data do notpermit the conclusion that sugar causes vigilance impairments.An equally plausible interpretation is that children with atten-tion deficits manifest cravings for sugar.

Two double-blind experimental studies failed to detect effectsof a sugar challenge on children's performance. Behar et al.(1984) detected no effects of sucrose or glucose on vigilanceperformance or memory. Similarly, Wolraich et al. (1985) failedto find effects of sucrose on vigilance, paired-associate learning,nonsense-word spelling, the Matching Familiar Figures Test(Kagan, Rosman, Day, Albert, & Phillips, 1964), or drawing.

Opposite effects of carbohydrates on childrens' performanceemerged in two studies reported by Conners et al. (in press). Inthe first study, children hospitalized as psychiatric inpatientsate a breakfast of their own choosing, and afterwards, on differ-ent days in counterbalanced order received challenges of rela-tively low dosages of sucrose, fructose, oraspartame. Comparedwith aspartame, sucrose reduced errors of omission on the CPT

of vigilance when the test was administered 30 min but not asmuch as 3 hr after challenge. The sucrose challenge also facili-tated reaction time for the earlier but not the later test. Connerset al. suggested that results may indicate a facilitating effect ofsmall dosages of sugar on performance, at least against the back-ground of a normal breakfast that probably contained mixednutrients. Sample sizes were too small, however, for actually ex-amining the effects of breakfast nutrients on performance.

To our knowledge, Conners et al.'s (in press) Study 1 is theonly study to report facilitating effects of sucrose on perfor-mance outside of the case in which carbohydrates end a pro-longed period of caloric deprivation. Because breakfast nutri-ents were uncontrolled, it is possible that some children failedto eat breakfast and that the sugar challenge did terminate aprolonged fast for these subjects. The facilitating effects of su-crose emerged, in comparison with the effects of aspartame. Inhuman subjects, aspartame may decrease brain catecholaminesynthesis because phenylalanine competes with the catechol-amine precursor, tyrosine, for brain uptake. Aspartame also in-hibits tyrosine hydroxylase, which catalyzes the conversion ofphenylalanine to tyrosine and tyrosine to DOPA. Consequently,it is possible that the aspartame placebo actually impaired per-formance by lowering brain catecholamines. Sample character-istics may also have contributed to discrepant results, becausethe children were psychiatric inpatients.

In Study 2, which was more carefully controlled, Conners etal. (in press) reported what is apparently the first comparisonof carbohydrate and protein breakfasts on childrens' behavior.In a cross-sectional design, they randomly assigned normal andhyperactive children to fasting, a high-carbohydrate breakfast,or a high-protein breakfast. Immediately after the breakfast,children were challenged with a relatively high dosage of su-crose or aspartame. From .5 to 3.75 hr after breakfast plus chal-lenge, the carbohydrate breakfast engendered greater vigilanceimpairments than did the protein breakfast or fasting. More-over, when ingested after the carbohydrate breakfast or afterfasting, the sugar challenge produced a detrimental effect onevoked potential measures of attentiveness. When ingested afterthe high-protein breakfast, the sugar challenge did not producea detrimental effect.

With the exception of the Conners et al. (in press) Study 1, inwhich breakfast nutrients were uncontrolled, no other pub-lished study known to us has reported a facilitating effect of asugar challenge on childrens' performance. Effects of sugar havebeen either nonexistent or debilitating. In Conners et al's Study2, which systematically varied breakfast composition, the ad-verse effects of a carbohydrate-rich breakfast on performancewere sustained for almost 4 hr after the meal. These findingshighlight the importance of controlling and experimentallyvarying the nutrient composition of test meals.

Effects of Carbohydrates on the Behavior of Adults

Unlike the empirical literature on children, many studies ofadults have been guided by the hypothesis that carbohydratesaffect behavior by altering brain serotonin synthesis. Much re-search has involved controlled trials of the amino acid trypto-phan, sometimes accompanied by carbohydrates to augment itseffects on behavior. Because brain scrotoninergic neurons are

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CARBOHYDRATES AND BEHAVIOR 245

believed to play a role in the regulation of pain, sleep, and

mood, these behaviors have been examined in adults. Their ne-

glect in children constitutes an important gap and a fruitful di-

rection for studies that could reveal useful clinical applications.

Aggression and performance have been examined in both chil-

dren and adults, enabling comparison of the effects of carbohy-

drates in the two populations.

Aggression

In light of evidence that violent individuals show low levels

of the serotonin metabolite 5-HIAA (Brown, Goodwin, et al.,

1979; Linnoila et al., 1983) and may profit from treatment with

tryptophan (Sheard, 1975), Young (1986) examined the effects

of tryptophan depletion on aggression in normal adults. After

an overnight fast, normal men consumed tryptophan-free, tryp-

toptian-balanced, or tryptophan-supplemented amino acid

mixtures at 8:00 a.m. Young assessed hostility 5 hr later by us-

ing a self-report measure of mood and by using a laboratory

test of aggression first introduced by Buss (1961). Subjects were

deceived to believe that they were to be tested for auditory per-

ception and reaction time and that they had a partner who was

to be tested for pain sensitivity by rating electric shocks. Each

subject heard tones supposedly selected by the partner. Some of

the tones that the partner apparently chose to inflict on the sub-

ject were uncomfortably loud. In response to each tone, the sub-

ject was to rapidly choose from buttons that allegedly delivered

the partner different intensities of shock. Hence, the subject had

an opportunity to retaliate for the unnecessarily loud noise. The

dependent variables were the duration and intensity of shocks

intended for the partner.

Consistent with the absence of evidence that carbohydrates

alter activity and aggression in children, in Young's (1986) study

of adults, neither self-reported hostility nor the Buss (1961) ag-

gression paradigm detected changes following the amino acid

mixtures. Ingesting the amino acid mixtures induced nausea,

but it is unclear how the feeling of nausea affected the results.

Pain

Results of animal studies suggest serotoninergic involvement

in pain sensitivity. Rats fed a tryptophan-poor corn diet display

reduced brain serotonin and lowered tolerance to painful stim-

ulation (Lytle, Messing, Fisher, & Phebus, 1975). An injection

of tryptophan reverses these effects. In humans also, tryptophan

can reduce pain sensitivity and increase pain tolerance. The evi-

dence is reviewed in Table 3.

Two groups of authors have examined healthy adults. Seltzer,

Stoch, Marcus, and Jackson (1982) were able to increase pain

tolerance by feeding subjects 2 g of tryptophan combined with

a high-carbohydrate, low-protein, low-fat diet. Lieberman, Cor-

kin, Spring, Growdon, and Wurtman (1983) used signal detec-

tion methodology to study the acute effects of tryptophan on

thermal and pain perception in normal men. The morning after

an overnight fast, male subjects received tryptophan, tyrosine,

or a placebo in a double-blind crossover design. Nearly 2 hr

later, Lieberman et al. (1983) tested subjects for their ability to

discriminate among intensities of thermal stimuli delivered by

means of a Hardy- Wolff-Goodell dolorimeter. They made sepa-

rate assessments for the subjects' sensitivity in discriminating

each stimulus intensity and for the subjects' response bias to-

ward describing stimuli as more or less intense. Of five paired

stimulus comparisons, tryptophan reduced discriminability for

stimuli rated painful or very painful. Two additional findings

are noteworthy. First, tryptophan did not alter discriminability

between the most painful stimuli or among nonpainful thermal

stimuli. Second, tryptophan did not affect response bias for any

stimulus comparison. In discussing these findings, Lieberman

et al. (1983) pointed out that morphine and diazepam also fail

to reduce discriminability among intensely painful stimuli.

However, unlike tryptophan, these drugs affect the attitudinal

or response-bias aspect of pain perception, in addition to sensi-

tivity. Taken together, these findings suggest a partial but not

total overlap in the mechanisms by which tryptophan and the

opiates and benzodiazepines affect pain responsivity.

In three studies, researchers have examined tryptophan's

effects on patients suffering from chronic pain. Studying five

patients whose pain had returned following rhizotomy and

chordotomy, King (1980) found that tryptophan alleviated self-

reported pain and restored analgesia to pinprick stimulation.

More recently, Seltzer, Dewart, Pollack, and Jackson (1983)

studied patients with chronic maxillofacial pain who were as-

signed on a double-blind basis to daily receive either cellulose

placebo or tryptophan. They combined both treatments with a

high-carbohydrate, low-protein, low-fat diet. At baseline, Week

1 and Week 4 of treatment, they assessed subjects for pain per-

ception and tolerance to tooth-pulp stimulation. They also

rated average pain, depression, and anxiety. By the end of the

treatment month, average pain had decreased to a greater ex-

tent with tryptophan (32-point decrease) than with placebo (11-

point decrease). The degree to which the decline in pain ratings

for the placebo group was attributable to their high-carbohy-

drate diet is unclear. Pain tolerance also increased to a signifi-

cantly greater degree with tryptophan than with the placebo.

Although anxiety and depression also decreased significantly

over the 1-month period, tryptophan and placebo did not differ

in their effect on mood. This finding suggests that dysphoric

mood states may not be sensitive to serotoninergic interven-

tions in all individuals.

In an early study, Sternbach, Janowsky, Huey, and Segal

(1976) studied five male patients with chronic pain. They failed

to find evidence that tryptophan or 5-HTP decreased tolerance

to ischemic pain caused by a tourniquet and noted that isch-

emic pain may actually be increased by peripheral serotonin.

Sternbach et al. suggested that serotonin precursors might have

increased pain tolerance if they had been given with an agent to

block their peripheral effects on ischemic pain.

The findings reviewed above indicate that tryptophan, partic-

ularly in combination with a carbohydrate-rich and protein-

poor meal, is usually advantageous in the treatment of chronic

pain. The avenue by which benefits come about, particularly

the interplay with psychological distress, remains to be clearly

unraveled.

Sleep

In several comprehensive reviews, authors have described

more than 43 investigations of tryptophan's effect on sleep

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CARBOHYDRATES AND BEHAVIOR 247

(Cole, Hartmann, & Brigham, 1980; Hartmann, 1981; Hart-mann & Greenwald, 1984). A majority of studies indicate thattryptophan shortens the time taken to fall asleep. Sleep onsetcan be facilitated during daytime as well as evening hours (Spin-weber, Ursin, Hilbert, & Hilderbrand, 1983). Moreover, an in-fant formula containing tryptophan, compared with a feedingof valine and a low carbohydrate level (Yogman, Zeisel, & Rob-erts, 1983), reduces sleep latencies in newborns.

A few have failed to find sleep-enhancing effects (e.g., Adam& Oswald, 1979; Nicholson & Stone, 1979). In part, the incon-sistent results may reflect differences in dosage. Soporific effectsappear to be unreliable with 1 g or less of tryptophan. AlthoughHartmann (1981) originally found a sleepiness-inducing effectof 1 g of tryptophan, Adam and Oswald failed to replicate thisresult. More recently, Hartmann, Lindsley, and Spinweber(1983) failed to find evidence that tryptophan surpassed a pla-cebo in decreasing subjectively reported sleep latencies. In thisstudy, separate groups of insomniac subjects received either 1 gof tryptophan, 100 mg of secobarbital, 30 mg of flurazepam, orplacebo 30 min before bedtime for 7 nights. For a 1-day drug-free baseline period, a 7-day treatment period, and a 6-day with-drawal period, subjects estimated time to fall asleep initiallyand after nighttime awakenings. Neither tryptophan nor seco-barbital, in comparison with a placebo, lessened subjectivelyreported insomnia, a surprising result because secobarbital isusually an effective hypnotic. Results may call into question thevalidity of self-report measures of sleep latency and quality. Anunexpected finding was that sleep latencies continued toshorten during the withdrawal period for subjects who had re-ceived tryptophan but not for any other group. Consequently,by the end of the withdrawal phase, sleep latencies were signifi-cantly shorter than pretreatment latencies for subjects in thetryptophan group. In discussing the possible "continuingeffect" of tryptophan, Hartmann et al. (1983) pointed to similartrends in several other studies. They suggested that alterationsin serotonin receptors or other receptors might occur with long-term administration of tryptophan.

In trying to reconcile discrepant findings concerning trypto-phan and sleep, Hartmann and Greenwald (1984) suggestedseveral generalizations. First, effects on sleep latency are un-clear or nonexistent with less than 1 g of tryptophan. Second,because the time to sleep onset is so brief in healthy adults, re-searchers need to allow sufficient duration to observe a trypto-phan effect. For example, Nicholson and Stone (1979) adminis-tered tryptophan 20 min before bedtime, and their subjects re-quired only 10 to 12 min on a placebo to fall asleep. Thus, tobe detected, an effect of tryptophan would have to occur within30 min. Because tryptophan is not as rapidly absorbed as stan-dard hypnotic drugs, it should be taken approximately 1 hr be-fore bedtime for the effects to be detectable. Finally, severelyand chronically insomniac patients may prove refractory to theacute sleep-inducing effects of tryptophan. Such patients maybecome responsive only after repeated administrations of tryp-tophan (Spinweber, 1986).

In dosages up to 5 g, tryptophan appears to have no dramaticeffects on electroencephalogram measures of sleep stages(Brown, Horrom, & Wagman, 1979; Spinweber et al., 1983).Unlike most hypnotics, tryptophan does not reduce rapid eyemovement (REM) time or shorten Stage 3 and 4 sleep. In fact,

it slightly increases the duration of Stage 4 sleep. At quite highdosages (exceeding S g), tryptophan can reduce REM sleep, andits effects on REM latency are uncertain (Hartmann & Green-wald, 1984).

Although sleep onset is clearly hastened by tryptophan, otherquestions remain. For example, because the effective hypnoticdose of tryptophan exceeds 1 g, can carbohydrates potentiatethe action of lower doses? Further, the influence of carbohy-drates alone, not only as an adjunct to tryptophan, remains tobe studied in the treatment of insomnia. Comparing dose-re-sponse curves for carbohydrates to those for tryptophan mayprove helpful in determining whether carbohydrate foods alonecould prove helpful in treating mild insomnia.

Mood: Depression and Euphoria

Serotoninergic deficiencies are implicated in the etiology ofsome primary affective disorders. Van Praag (1980) estimatedthat approximately 40% of depressed patients have a deficit incentral serotonin metabolism, because the serotonin metabolite5-HIAA is abnormally low in the lumbar cerebrospinal fluid ofa subgroup of depressed patients (Asberg, Traskman, & Thoren,1976). Plasma-free tryptophan, in relation to the competingneutral amino acids, is also decreased in a subgroup of patientswith affective disorder (Coppen & Wood, 1978; Moller, Kirk, &Fremming, 1976).

The efficacy of tryptophan for the treatment of depression iscontroversial, yielding both positive and negative results (Coo-per, 1979). More promising evidence suggests that L-tryptc-phan can enhance the antidepressant efficacy of monoamineoxidase inhibitors (Walinder, Skott, Carlsson, Nagy, & Roos,1976), although patients must be carefully monitored becauseof the accompanying clinical risks. Studies of serotonin's im-mediate precursor, 5-HTP, have indicated somewhat greater an-tidepressant efficacy than for L-tryptophan (Van Praag, 1980).For both tryptophan and 5-HTP, antidepressant efficacy maybe greatest for patients who show biochemical evidence of serc-toninergic hypofunction. Craving for carbohydrates may be aclinical sign that differentiates these patients from nonrespon-sive individuals.

In a recent study of patients with seasonal affective disorderand carbohydrate craving, Rosenthal et al. (1986) reported thata carbohydrate lunch reduced depression to a greater extentthan did an isocalonc protein lunch. Similar findings emergedin a comparison of obese subjects who regularly select carbohy-drate foods as snacks, as compared with weight-matched sub-jects who choose snacks high in either protein or carbohydrates(Lieberman, Wurtman, & Chew, 1986). The carbohydratesnackers reported reduced depression after eating a carbohy-drate lunch, in contrast to the mixed snackers, who reportedincreased depression.

Non-carbohydrate-craving subjects failed to show an antide-pressant response to carbohydrates in the Rosenthal et al.(1986) and Lieberman, Wurtman, et al. (1986) studies. Someearly studies, however, reported that L-tryptophan induced eu-phoria in entirely normal individuals (Oswald et al., 1966;Smith & Prockop, 1962). Although these findings have not beenreplicated recently (Greenwood, Lader, Kantameneni, & Cur-zon, 1975; Lieberman et al., 1983), there are reports suggesting

248 B. SPRING, J. CHIODO, AND D. BOWEN

that 5-HTP can have a significant euphoriant effect in normal

individuals (Puhringe, Wirz-Justice, Graw, LaCoste, & Gastpar,

1976; Trimble, Chadwick, Reynolds, & Marsen, 1975).

To test the prediction that tryptophan depletion would in-

duce depression, Young, Smith, Pihl, and Ervin (1985) admin-

istered balanced, tryptophan-supplemented, or tryptophan-de-

pleted amino acid mixtures at 8:00 a.m. after an overnight fast.

By 5 hours later, the tryptophan-free mixture had produced a

depletion in plasma tryptophan. When tested at this time, sub-

jects who received the tryptophan-depleted mixture showed a

significant increase in self-reported depression, compared with

baseline scores. Moreover, depression scores for this group were

significantly greater than those for the two groups fed the other

test mixtures. Young et al. sought converging evidence of de-

pression by asking subjects to proofread and detect errors in

typed passages containing punctuation and spelling mistakes.

They did so while hearing three types of distraction played over

headphones. The low (easily ignored) distractor involved pas-

sages from a statistics textbook. The high (hard-to-ignore) dis-

tractor presented eyewitness accounts of the bombing of Hiro-

shima. The dysphoric distractor presented themes of hopeless-

ness and helplessness that should match the mental set held by

a depressed person and, hence, be difficult for such an individ-

ual to ignore. Young et al. detected no differences in proofread-

ing skill at baseline. Following the amino acids, the balanced

group scored similarly with all three distractors, and the trypto-

phan-supplemented group actually performed best with the

dysphoric distractor. The finding of greatest importance was

that the tryptophan-depleted subjects showed significantly im-

paired performance with the dysphoric, as compared with the

low, distractor. Thus, findings from both the self-report mood

scales and the proofreading task were consistent with the hy-

pothesis that tryptophan depletion can produce a rapid lower-

ing of mood in normal male subjects.

In summary, for some individuals, interventions that in-

crease serotoninergic function alleviate depression and may in-

duce euphoria. Conversely, serotonin-depleting manipulations

can produce depression. These results suggest that some indi-

viduals may learn to use eating as a way of modulating mood

states. An anxious or depressed individual with serotoninergic

hypofunction may inadvertently learn that snaeking on high-

carbohydrate, low-protein foods leads to an improvement in

mood because such snacks enhance brain tryptophan uptake

and serotonin synthesis. The induction of a positive mood state

reinforces selective intake of carbohydrate-rich foods. Con-

sumption of carbohydrate snacks may become habitual because

the snaeking behavior dissipates dysphoric mood states.

Mood: Drowsiness and Calmness

Although much interest has focused on depression, trypto-

phan's most consistent effect on normal subjects is to induce

drowsiness and reduce subjective alertness. In Table 4, we sum-

marize these findings for both tryptophan and carbohydrates.

Greenwood et al. (1975) gave adult volunteers L-tryptophan

or a placebo. When compared with the placebo, tryptophan sig-

nificantly increased self-reported drowsiness, clumsiness, muz-

ziness, and mental slowing. Effects were maximal 1 hr after in-

gestion and returned to baseline by 3 hr afterward. In another

study, using a crossover design, Hartmann, Spinweber, and

Ware (1976) gave L-tryptophan, leucine, or a placebo to normal

adults late in the evening. Sleepiness ratings taken at 15-min

intervals demonstrated that by 60 to 90 min after ingestion,

tryptophan induced significantly greater drowsiness than did

either the placebo or leucine.

In a study comparing acute and chronic effects of L-trypto-

phan on mood, Yuwiler et al. (1981) administered two dosages

of tryptophan, separated by recovery. A chronic phase followed

the acute phase and involved daily administration of a single

dose of tryptophan for 14 days. At both acute doses, subjects

reported increased drowsiness that began approximately 30

min after ingestion and lasted for several hours. More pro-

nounced drowsiness occurred at the higher acute dose. Leth-

argy was greater and more enduring with chronic administra-

tion, sometimes lasting into the evening.

Lieberman et al. (1983) conducted a similar acute study. In

the morning in counterbalanced order, they gave tryptophan,

tyrosine, and a placebo double-blind to healthy men. Com-

pared with the placebo, tryptophan significantly decreased

alertness, increased fatigue, and decreased subjective vigor. The

reduction in subjective vigor after tryptophan, compared with

placebo, intake was quite large in magnitude—a decrease of

40%. As previously reviewed, tryptophan's effectiveness as a

hypnotic demonstrates its ability to induce fatigue in evening

hours. The findings of Yuwiler et al. and Lieberman et al. (1983)

establish that tryptophan also causes drowsiness following

morning administration.

Clearly, tryptophan induces drowsiness and lowers subjective

alertness. Can a carbohydrate-rich, protein-poor meal induce

the same effect? The answer seems to be yes, although the effect

is smaller in magnitude. Hartmann, Spinweber, and Fernstrom

(1977) recorded self-rated sleepiness at 15-min intervals after

normal adults consumed six different liquid test suppers in

counterbalanced order. One set of three meals contained carbo-

hydrates and lipids but no protein. The other set was high in

protein. One meal in each set was supplemented with trypto-

phan, another with L-leuci ne, and the last with a placebo. Hart-

mann et al. (1977) collapsed data across amino acid conditions,

and found that 2 hr after eating, the carbohydrate meals pro-

duced significantly greater sleepiness than did the protein-rich

meals.

To test whether age and gender influence responsivity to nu-

trients, Spring, Mailer, Wurtman, Digman, and Cozolino

(1983) tested 184 healthy adults between the ages of 18 and 65

years. They randomly assigned subjects to eat either a carbohy-

drate-rich and protein-poor meal or a protein-rich and carbo-

hydrate-poor meal for breakfast or for lunch. Protein and car-

bohydrate meals were isocaloric. Subjects assigned to eat the

test meal for breakfast maintained an overnight fast and con-

sumed the food in the early morning. Subjects assigned to the

lunch groups ate a standard breakfast and consumed the test

meal at midday. Spring et al. (1983) assessed mood 2 hr after

meals were eaten. Women who ate the carbohydrate-rich meal

reported greater sleepiness than did women who ate the pro-

tein-rich meal. Men who ate the carbohydrate-rich meal re-

ported greater calmness than did men who ate the protein-rich

meal. The findings raise a question about whether women may

be more sensitive than men to the effects of carbohydrates, be-

CARBOHYDRATES AND BEHAVIOR 249

cause they report a more intense mood (i.e., sleepiness ratherthan calmness). Additionally, individuals 40 years or older werecalmer and less tense after a carbohydrate breakfast than theywere after a protein breakfast. Younger people did not show thisdifferential response to breakfast nutrients, suggesting an age-related sensitivity difference.

Spring et al. (1986) performed a follow-up study to test (a)whether any sweet-tasting dessert-type food would induce fa-tigue, regardless of nutrient content, and (b) whether fatigueparalleled fluctuations in glucose, insulin, or amino acids. Atweekly intervals, in a within-subjects design, female subjectsfasted overnight, ate a standard breakfast in the laboratory, and,at 12:15 p.m. and in counterbalanced order, fasted or ate a high-protein, a high-carbohydrate, or a balanced lunch. The high-carbohydrate lunch was lacking in protein, whereas the bal-anced lunch mixed carbohydrates and protein in approxi-mately a 3:1 ratio. Both the carbohydrate and balanced lunches,however, were hedonically similar sweet, cookie-like dessert-type foods. Two hours after eating, the carbohydrate lunch butnot the balanced or protein lunch produced a significant in-crease in fatigue, compared with fasting. Fatigue could not beattributed to the hedonic properties of the lunches or to changesin insulin, because the carbohydrate and balanced lunches werehedonically similar and both elevated serum insulin. Nor couldfatigue be attributed to hypoglycemia because plasma glucoseremained significantly elevated by the carbohydrate lunch,compared with fasting, at the time that fatigue occurred. Fa-tigue following the carbohydrate lunch emerged at approxi-mately the same time that this lunch and no other significantlyelevated the plasma tryptophan ratio, suggesting that drowsi-ness may parallel enhanced brain influx of tryptophan and sero-tonin synthesis.

Lieberman et al. (1986) conducted a subsequent study to ex-amine two questions: (a) Would men also show sleepiness whenfed a meal that contained a great quantity of carbohydrates, and(b) would a meal consisting chiefly of complex carbohydratesproduce effects similar to those seen after a sucrose-rich meal.Lieberman et al. (1986) used a within-subjects design, requiringsubjects to fast overnight, eat a standard breakfast, and con-sume the test meals at noon. In counterbalanced order, subjectsate a carbohydrate-rich lunch and a protein-rich lunch on 2days separated by a 1-week interval. Self-reported mood wasassessed at a premeal baseline and at hourly intervals until 5:00p.m. On both days of testing, sleepiness increased and subjec-tive vigor declined significantly over the course of the demand-ing 5-hr test battery. Visual inspection of the data suggests thata postprandial upswing in sleepiness occurred following boththe starch and protein meals in the 3 hr immediately afterlunch. Although the postprandial rise in sleepiness was some-what greater following the starch meal at 1 and 2 hr after lunch,these differences were not significant.

The patterning of means for the mood data suggests that themen in this study responded to carbohydrates in a qualitativelysimilar way to the female subjects in the Spring et al. (1983)study. That is, men became slightly, though not significantly,sleepier after a carbohydrate meal than they did after a proteinmeal. The absence of a statistically distinct mood response ofmen even to a fairly large quantity of carbohydrates may meanthat men are not very sensitive to carbohydrate-induced

changes in self-reported moods. It remains unclear whethermen fail to experience mood changes following carbohydratesor are unable or unwilling to report them. Before a reliable gen-der difference in mood responsivity to carbohydrates can be in-ferred, however, it remains necessary to replicate the findingthat carbohydrate-induced drowsiness is more pronounced inwomen than in men.

In the same paper, Lieberman et al. (1986) suggested that thetime when carbohydrates elevate the ratio of plasma tryptophanto other large neutral amino acids corresponds to the time whendrowsiness and performance deficits appear. On different days,6 adult male subjects ate one of three meals—the carbohydrateor protein meal from the previous study or an isocaloric quan-tity of sucrose. By 1 hr after lunch, the protein meal had sub-stantially decreased the tryptophan ratio. Consequently, differ-ences between the plasma tryptophan ratios generated by theprotein versus carbohydrate foods were already significant. By2 hr after lunch, both the sucrose and carbohydrate lunches hadelevated the tryptophan ratio. The increase in the tryptophanratio persisted until 5 hr after the carbohydrate lunch and until4 hr after the sucrose lunch. Consequently, for the first 4 hr afterlunch, complex carbohydrates and sugar affected the trypto-phan ratio very similarly.

Taken together, the results of these studies suggest that trypto-phan and carbohydrates induce sleepiness and fatigue. Drowsi-ness is produced after either morning or evening administra-tion. Some evidence suggests that women and older individualsmay show heightened sensitivity to these effects of carbohy-drates on mood.

To test whether food constituents produce clinically signifi-cant effects in sensitive individuals, Christensen, Krietsch,White, and Stagner (1985) challenged 3 subjects with sugar byusing a single-case experimental design. They identified adultswho reported high levels of cognitive, behavioral, and somaticsymptoms and placed them on a low-carbohydrate, high-pro-tein diet lacking sucrose and caffeine. They measured moodand symptoms before and after subjects drank a sugar chal-lenge. In 1 subject, sucrose produced no noticeable effect. Inthe other 2, however, sucrose increased fatigue and decreasedvigor. These findings suggest that the fatigue-inducing effects ofcarbohydrates, previously observed in groups of subjects, canalso be clinically significant for individuals.

Performance

As would be expected because carbohydrates cause drowsi-ness, a high-carbohydrate meal can also impair performance.These findings are included in Table 2. In an early study, Simon-son, Brozek, and Keys (1948) found worse performance on avigilance test similar to the CPT of vigilance after a carbohy-drate lunch than after a high-fat or balanced lunch. In addition,the carbohydrate meal produced the greatest deterioration insuch extrinsic eye muscle functions as adduction power and ver-tical divergence.

More recently, Spring et al. (1983) examined performance ona dichotic shadowing test of sustained selective attention 2 hrafter subjects ate carbohydrate or protein meals. This task re-quires subjects to repeat aloud, syllable by syllable, words pre-sented to one ear over stereo earphones and to ignore distractors

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CARBOHYDRATES AND BEHAVIOR 253

intermittently presented to the other ear. Shadowing was gener-ally less accurate after carbohydrate meals than after proteinmeals, but this difference was significant only for older subjects(40 years or more) who consumed the test meals for lunch.Older people omitted more syllables after the carbohydratelunch than after the protein lunch, but they did not interjectmore distractor syllables. Their performance was no less accu-rate when distraction was present than when it was absent(Spring, 1984), an expected result because distractor and no-distractor tests were equated in difficulty. Results again suggestthat older individuals may show heightened sensitivity to theeffects of carbohydrates. For older people, a carbohydrate mealeaten for lunch promoted lapses of sustained attention withoutenhancing distractibility. In this study, a test of simple reactiontime did not detect differences due to foods.

In a study comparing the effects of complex-carbohydrateand protein lunches on the performance of young men, Lieber-man et al. (1986) administered an extensive battery of perfor-mance tests from 1 to 5 hr after test meals. A dichotic listeningtest did not detect performance deficits 3 hr after lunch in thispopulation, the same as in Spring et al.'s (1983) subgroup ofyounger subjects. A simple reaction time test, however, whenadministered 1V4 hr after lunch, revealed significantly slower re-sponses after the carbohydrate lunch than after the proteinlunch. This task involved four times as many trials and waitingintervals only half as long as did the reaction time test used bySpring et al. (1983) and may have yielded more reliable scores.The Digit-Symbol Substitution Test, a measure of motor copy-ing and concentration, revealed significantly worse perfor-mance 3'/2 hr after the carbohydrate meal, compared with theprotein meal. Results of these studies suggest primarily adverseeffects of unbalanced carbohydrate meals on performances in-volving sustained attention and speed.

The findings are consistent with Conners et al.'s (in press)results concerning childrens' performance after a high-carbohy-drate breakfast The nature of the carbohydrate-induced per-formance deficit may be very specific, and its intensity may varyamong population subgroups. Vigilant sustained attention andreaction time seem to be most adversely affected. Many otherperformance tests do not reveal differences, as Table 2 indicates.The use of tasks that are insensitive to this deficit may be partlyresponsible for the general failure to find that tryptophan im-pairs performance (for review, see Spring, 1984). Studies oftryptophan have overused tests of sensorimotor function andunderused tests of concentration.

In addition to test sensitivity, population sensitivity is an im-portant consideration. Performance impairments have gener-ally been subtle except in studies of older individuals and chil-dren. Further research is warranted on these two populationsand others who may be especially sensitive to nutrient effects.

Conclusions

The study of diet-behavior relations is a promising and grow-ing field of investigation. Well-controlled empirical researchshould optimally help dispel popular misconceptions, enhanceunderstanding of brain-behavior relations, and promote bene-ficial health practices.

Three mechanisms have been invoked to explain the influ-

ence of carbohydrates on behavior expectancy effects, hypogly-cemia, and effects on brain neurotransmission. The hypothesisthat diet-behavior relations result from a placebo effect islargely unsupported by experimental findings. Controlled in-vestigations are still needed, however, for the special case inwhich diet therapies are used as treatment for a clinical prob-lem. In normal individuals, little evidence supports and someevidence contradicts the hypothesis that carbohydrate-inducedbehavior change results from hypoglycemia. The hypothesisbest supported by empirical findings is that carbohydratesaffect behavior by enhancing the brain influx of tryptophan,precursor of the neurotransmitter serotonin.

Inspection of the studies listed in Tables 1 through 4 revealsa recently developed literature with intriguing results. Researchon children has been the most extensive, and two conclusionsappear warranted. First, despite the tenacious popular opinionthat sugar exacerbates hyperactive behavior in children, the ma-jority of well-controlled experimental studies yield evidencedisputing this premise. Most studies have failed to detect aneffect of sugar on activity levels or have even noted a slight de-crease in activity. Second, concerning the influence of an acutesugar challenge on performance, a majority of studies have de-tected no effect. In contrast to a sugar challenge, a full carbohy-drate meal apparently impairs childrens' concentration. It isunclear why a carbohydrate meal induces behavioral effects notobtained with a sugar challenge. Differences in dosage (foodquantity) represent one explanation.

In adult clinical populations, tryptophan hastens sleep onsetand reduces pain sensitivity. It has also been suggested that tryp-tophan reduces aggressive behavior, although evidence is incon-sistent. In some studies, carbohydrate meals have been used asadjuncts to tryptophan. Additional research is warranted to testwhether carbohydrate meals, given alone, can produce similareffects or can lessen the needed dosage of tryptophan supple-ments.

In healthy adults, the consumption of an unbalanced carbo-hydrate-rich, protein-poor meal tends to induce drowsiness, es-pecially in women. Performance impairments have also beennoted in both men and women and especially in the elderly.Tryptophan and carbohydrates influence mood similarly, al-though the effects of carbohydrates are subtler. Behavioraleffects include drowsiness and concentration difficulties, whichreach a maximum approximately 2 hr after carbohydrate in-take.

The emergence of controlled empirical research on diet-be-havior relations is timely and in accord with public interest. Theinterpretation of future studies will be aided by attention toseven methodological factors. First, although correlationalstudies have played a useful role in generating hypotheses, find-ings can be highly misleading when interpreted to imply cause-effect relations, as has occurred with correlational findings onsugar and childrens' activity levels. Second, careful descriptionof sample characteristics is needed, especially in light of possi-ble differential sensitivities related to psychopathology, gender,and age. Third, there is a need for more careful specification oftest nutrients and the surrounding dietary regimen. In acutestudies, researchers should specify fasting duration and nutrientdosages. They should standardize and control intake of otherfoods rather than assess them but allow them to vary. If subject

254 B. SPRING, J. CHIODO, AND D. BOWEN

samples vary markedly in body weight, nutrient dosages shouldbe weight relative rather than absolute. The selection of an ap-propriate control nutrient or placebo is a pressing concern, es-pecially in the light of a lack of knowledge about whether aspar-tame induces behavioral effects. Moreover, because evidencesuggests that any high-calorie lunch, even of mixed nutrients,produces some degree of postprandial performance decrement(Craig, 1986; Craig, Baer, & Diekmann, 1981), the inclusion ofa fasting control group is advisable. Fourth, the choice of aninterval between nutrient intake and behavioral testing maycritically influence results. Because the mood and performancechanges after carbohydrates apparently peak at 2 hr, earlier orlater testing may miss these effects. There is also a need, how-ever, to sample behavior at very short (e.g., 15-min) intervalssoon after carbohydrate intake, because some anecdotal reportsimply very rapid effects. The fifth and a related issue is the im-portance of sampling the time course of biological parameters(e.g., plasma glucose, insulin, and amino acids) and relatingthese to behavioral fluctuations, in order to shed light on under-lying mechanisms. Sixth, it is desirable for investigators to usesome common measures of behavioral variables, so that resultscan be compared across studies. Finally, there is a need to con-trol and, ultimately, to investigate such variables as cigarettesmoking and exercise, which might exert moderating effects ondiet-behavior relations.

In this article, we have reviewed evidence suggesting thattryptophan and carbohydrates can function as drugs that mod-ify brain biochemistry and accompanying mood and behavior.As individuals administer drugs to modulate behavioral symp-toms and mood, so may they learn to select and self-administerfoods to achieve the same result In normal individuals, carbo-hydrates most consistently induce fatigue and impair perfor-mance, raising a question about why carbohydrate craverswould selectively consume foods that produce such effects. Veryrecent reports suggest that individuals who selectively consumecarbohydrate snacks experience activation, lowered distress, orother positive moods rather than drowsiness. If individualdifferences in carbohydrate responsivity prove to be reliable,their origins are of interest. It is unknown whether differentialfood sensitivities result from genetic or prenatal influences ormay be produced by means of chronic self-administration ofunbalanced diets.

Several interesting clinical prospects may lie ahead. One isthe possibility of developing dietary regimens that optimize per-formance in the workplace and classroom. A second is the pros-pect that unusual nutrient sensitivities or food preferences maypermit the diagnosis of treatable functional alterations in brainneurotransmission. A third is that nutrients, alone or in combi-nation with drugs, may have clinical applications in the treat-ment of disorders of mood, sleep, and pain.

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Received February 4, 1986

Revision received November 17,1986

Accepted January 6,1987 i