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Physiology & Behavior, Vol. 67, No. 1, pp.

69–74, 1999
© 1999 Elsevier Science Inc.
Printed in the USA. All rights reserved
0031-9384/99/$–see front matter
PII S0031-9384(99)00040-2

The Influence of a Glucose Drink on a


Demanding Working Memory Task

PEARL Y. MARTIN AND DAVID BENTON1

Department of Psychology, University of Wales–Swansea, Swansea SA2 8PP, Wales, UK

Received 23 September 1998; Accepted 11 February 1999

MARTIN, P. Y. AND D. BENTON. The influence of a glucose drink on a demanding working memory task. PHYSIOL
BEHAV 67(1) 69–74, 1999.—A group of young adult females, who had or had not eaten breakfast, drank either a glucose
drink or a placebo. Fasting was associated with poorer performance on the Brown–Petersen task, a test of memory. A glucose
drink improved the memory of those who had fasted, although it did not influence those who had eaten breakfast. In those
who had fasted, the glucose drink resulted in memory comparable to those who had consumed breakfast. Those with higher
levels of blood glucose upon arrival in the laboratory had better memories. In those taking a glucose drink, after an initial
rise, rapidly falling levels of blood glucose were associated with better memory. © 1999 Elsevier Science Inc.

Blood glucose control Breakfast Brown–Peterson task Glucose Memory

RAISING the level of blood glucose has been found to im- stated that it places great demands on the central executive of
prove memory in healthy young adults (4,5,13,19,30,32). There Working Memory. [A preliminary version of some of the data
are also reports that in those whose blood glucose levels re- in this article has been published previously (6).]
mained higher cognitive performance was poorer, an observa-
tion made in the normal elderly (13), those suffering with MATERIALS AND METHODS
Alzheimer’s disease (9,10), diabetics (14), elderly rats (36),
and young humans (4,18). Subjects
Only recently have laboratory methods been used to ex- Eighty female undergraduates, with a mean age of 22.6
amine the influence of breakfast on cognition. A consistent years, who were each paid 6 pounds, acted as subjects. Only
picture is emerging—memory is adversely influenced by miss- females were studied, as previous research has reported that
ing breakfast (6,12,34,35). In contrast, other measures of cog- similar responses have been found in both sexes (4,11). No di-
nitive functioning tend not to be influenced by missing break- etary restrictions were enforced, and subjects from choice had
fast. Because following a meal the levels of glucose in the fasted or eaten their normal breakfast. On the basis of a meal
blood increase, one question that is addressed in the present record, and standard portion sizes, the energy content of the
study is the role played by blood glucose in breakfast-induced breakfast was calculated from food tables (32). A mean of
memory improvement. Benton and Sargent (8) reported that 1049 6 767 kJ were consumed by those in the breakfast
those who missed breakfast had a poorer memory later in the groups, made up of 42.6 6 30.3 g carbohydrate, 7.2 6 5.5 g
morning and that those with higher levels of blood glucose protein, and 6.8 6 8.4 g fat. In the majority of cases breakfast
had better memory. However, as this finding was simply a consisted of breakfast cereal and milk and/or toasted bread
correlation, there is a need to systematically vary the level of with butter or margarine and preserve.
blood glucose. Four groups of subjects were compared, those who had: 1)
It has been hypothesized that more cognitively demanding eaten breakfast and consumed a drink that contained 50 g
tasks are particularly susceptible to changes in blood glucose glucose, n 5 28; 2) eaten breakfast and consumed a placebo
(11,31). Therefore, the present study has extended the exami- drink, n 5 25; 3) fasted and consumed a drink containing 50 g
nation of the influence of the control of blood glucose levels glucose, n 5 12; and 4) fasted and consumed a placebo drink,
by considering the Brown–Peterson task (33) as Baddeley (1) n 5 15.

1To whom requests for reprints should be addressed. E-mail: d.benton@swansea.ac.uk

69
70 MARTIN AND BENTON

Trigrams (mean 10.86 mmol, n 5 14), were distinguished. After the


glucose drink, those whose levels fell or rose no higher than
Forty consonant trigrams were constructed (e.g., QCN or
1.80 mmol/L (mean 1 1.27 mmol/L, n 5 14), or rose by 2.7
KSF), with association values between 17 and 33% (38), ac-
mmol/L or more (mean 1 3.28 mmol/L, n 5 14), were con-
cording to the following criteria. A consonant appeared as the
trasted.
first letter of a syllable no more than twice within a list, or no
Change in blood glucose during the task. Changes in blood
more than once in any three consecutive syllables. Alphabeti-
glucose while performing the task were considered by subtracting
cal sequences were avoided.
the second blood glucose measure from the final one. Subjects in
the placebo condition whose blood glucose fell by at least 20.60
Glucose and Placebo Drinks
mmol/L (mean 21.23 mmol/L, n 5 14), were distinguished from
The glucose drinks contained 50 g of glucose dissolved in a those whose blood glucose that stayed the same or rose (mean 1
mixture of 250 mL water and two tablespoons of sugar-free 0.36 mmol/L, n 5 14). Subjects in the glucose condition whose
Robinsons Whole Orange Squash. Two teaspoons of lemon blood glucose levels fell by at least 21.39 mmol/L (mean 22.04
juice were added to decrease sweetness. Placebo drinks con- mmol/L, n 5 14), or fell no more than 20.3 mmol/L or rose
tained the same ingredients, with the exception of the glucose (mean 1 0.40 mmol/L, n 5 14), were compared.
powder, and the addition of 2 g of Sweetex, a low-calorie The percentage of trigrams correctly recalled was analysed
sweetener that contains aspartame and saccharin (Crookes using a three-way analysis of variance; blood glucose level
Health Care Limited). (high/low or rise/fall) 3 blocks (blocks 1–4, blocks 5–8) 3 in-
terval (3, 6, 9, 12, or 18 s), with the last two factors as repeated
Blood Glucose measures. The effect of drink on blood glucose levels was ex-
amined using a two-way analysis of variance; drink (placebo/
An ExacTech sensor (Medisense Britain Limited) enabled
glucose) 3 time (0, 20, or 60 min), with the latter as a re-
blood glucose to be measured accurately, using an enzymic
peated-measure factor.
method coupled with microelectronic measurement (23).
To save space and gain clarity interactions that do not in-
clude blood glucose are not reported. Where higher order in-
PROCEDURE
teractions are not mentioned it should be assumed that they
Subjects gave their written informed consent, and their are nonsignificant.
blood glucose was measured for the first time. Randomly and
under a double-blind procedure the subjects consumed either RESULTS
a glucose or placebo drink. The subjects sat quietly for 20 min,
and, after a second blood glucose measure, testing began. A When the effects of drink and breakfast on blood glucose
trigram was spelt out and a three-digit number was given. The levels were examined, the interactions drink 3 time, F(2, 152) 5
subject counted backwards in threes from this number, at the 42.84, p , 0.001, and meal 3 time, F(2, 152) 5 4.11, p , 0.018,
rate of one calculation every 2 s. When a signal light flashed, reached significance, although the three way interaction was
after 3, 6, 9, 12, or 18 s in a pseudorandom order, the subject nonsignificant, F(2, 152) 5 0.36, NS). The calculation of sim-
attempted to recall the trigram. The 40 consonant trigrams ple main effects showed that there was no significant differ-
were grouped into eight blocks of five. Performance on blocks ence in the blood glucose levels of placebo and glucose drink-
1–4 and 5–8 was contrasted. Testing lasted for 30–35 min, af- ers at the start of the experiment, although after 20 (,0.001)
ter which blood glucose was measured for a third time. Test- and 60 min (p , 0.001) the consumption of a glucose drink
ing took place in the morning. The procedure was approved was associated with significantly higher blood glucose levels.
by the local ethics committee. The blood glucose levels of those who had eaten breakfast did
not differ at baseline or the end of the study, but after 20 min
Statistical Analysis it was significantly higher in those who had consumed break-
fast (p , 0.01).
Drink and breakfast. The percentage of trigrams recalled The percentage of trigrams correctly recalled was higher in
correctly within the first and last four blocks were computed the second rather than in the first block of trials, F(1, 76) 5
for 3-, 6-, 9-, 12-, and 18-s intervals. The effect of drink and 20.80, p , 0.001. Recall of the trigrams decreased as the dura-
breakfast was analyzed using a four-way analysis of variance: tion of the distracter increased, F(4, 304) 5 57.93, p , 0.001.
placebo/glucose drink 3 breakfast/no breakfast 3 blocks (1– When the influence of breakfast and type of meal was consid-
4/5–8) 3 distracter interval (3, 6, 9, 12, or 18 s), with the last ered, a three-way interaction, drink 3 breakfast/no break-
two factors as repeated measures. fast 3 block, resulted, F(1, 76) 5 4.98, p , 0.03) (Fig. 1).
Those in the placebo group, who did not consume breakfast,
Criterion Groups did not significantly improve from blocks 1–4 to 5–8. In con-
Baseline blood glucose levels. To examine the effects of trast, the performance of subjects who received the glucose
extreme baseline blood glucose levels, arbitrarily, the 20% drink, but had not eaten breakfast prior to testing, signifi-
with the highest and lowest levels were contrasted. Those cantly improved from blocks 1–4 to blocks 5–8 (p , 0.01).
whose blood glucose levels were less than 4.0 mmol/L (mean Similarly, when breakfast had been eaten, performance im-
3.76 mmol/L, n 5 14) and those greater than 5.31 mmol/L proved over the blocks whether they had (p , 0.03), or had
(mean 6.07 mmol/L, n 5 14), were compared. not (p , 0.001) drunk a glucose-containing drink. Those who
Change in blood glucose prior to the task. To examine the had not eaten breakfast, but received a placebo drink, re-
effects of changes in blood glucose after the drink, and before called the trigrams to a lesser extent than the other three
the task, the baseline blood glucose level was subtracted from groups. Thus, a drink containing glucose nullified the nega-
the second blood glucose measure. Subjects taking the pla- tive consequences of not eating breakfast. In those who had
cebo, whose blood glucose levels fell by at least 20.10 mmol/L eaten breakfast an additional glucose drink was of no further
(mean 20.44 mmol, n 5 14), or rose by 0.3 mmol/L or more benefit.
GLUCOSE DRINK AND WORKING MEMORY TASK 71

FIG. 1. The effect of breakfast and a glucose drink on recall of trigrams in the Brown–
Peterson task. The data are the mean number of trigrams recalled in blocks 1–4
and 5–8.

Figure 2 shows that those subjects who had high rather breakfast was limited by the supply of glucose. A potential
than low baseline blood glucose levels recalled more trigrams, problem is that because the subjects were allowed to choose
F(1, 26) 5 5.37, p , 0.029. Baseline blood glucose did not sig- whether they ate breakfast, they were a self-selected group.
nificantly correlate with the number of trigrams recalled Are people who eat breakfast more alert in the morning, and
(Pearson correlation 5 0.04, NS). Thus, the phenomenon was for this reason remember more easily, whether or not they eat
associated with extreme levels of blood glucose. In contrast, breakfast? This explanation does not seem to explain the
there was no effect of a change in blood glucose in the 20 min data. Benton and Sargent (8) randomly allowed subjects to
prior to the task in either placebo, F(1, 26) 5 0.32, NS, or glu- eat breakfast or fast, and found irrespective of whether the
cose drinkers, F(1, 26) 5 0.54, NS. subjects normally ate breakfast, that memory improved. In
When the change in the blood glucose of glucose drinkers fact, blood glucose correlated with memory in those who had
while performing the task was examined, a significant main not eaten breakfast. In other studies, where fasting or the eat-
effect was found, F(1, 26) 5 5.86, p , 0.023). Figure 3 illus- ing of breakfast was decided randomly, the meal still bene-
trates that falling blood glucose levels during the task was as- fited memory (34,35).
sociated with better recall of the trigrams. As the change in A related question is whether the benefits associated with
blood glucose while performing the task correlated with the a greater supply of blood glucose is only a reflection of a dec-
percentage of trigrams recalled (20.52, p , 0.001), the phe- rement in performance associated with missing breakfast. Al-
nomenon was displayed throughout the range of changes in ternatively, are the benefits of an increased blood supply
blood glucose. In the placebo drinkers Fig. 4 shows that the more general? Figure 1 presents evidence that a cognitive
two-way interaction, rise/fall in blood glucose 3 block (blocks problem associated with not eating breakfast responded to a
1–4/5–8), reached significance, F(1, 26) 5 6.05, p , 0.021. Fur- glucose drink (Fig. 1), although the effect of the drink was not
ther analysis showed that those whose blood glucose levels apparent in those who had eaten breakfast. There is a series
fell during the task did not show learning/practice effects of reports that the modification of blood glucose levels influ-
from the first to the second half of the test, F(1, 26) 5 0.06, ence cognition in those who have already eaten breakfast
NS. However, those whose levels rose showed a significant (4,5,9). However, after eating breakfast, it is individual blood
improvement in percentage recall in the second half of the glucose levels, rather than simply whether a glucose or pla-
test, F(1, 26) 5 13.93, p , 0.001. In this case, the phenomenon cebo drink has been consumed, that is typically important.
was characteristic of those with extreme levels of blood glu- The impression created is that an increased provision of glu-
cose, as the change in blood glucose did not significantly cor- cose has an influence irrespective of whether you have eaten,
relate with the total trigrams recalled (0.17, NS). although its impact is greater when breakfast has not been
eaten.
The blood glucose values were subject to a series of analy-
DISCUSSION
ses with a consequent increased risk of chance statistical find-
In the present study an exogenous source of blood glucose ings. The series of analyses can be justified in two ways. First,
nullified the negative effects of not eating breakfast (Fig. 1), a blood glucose measure is a single indication of a dynamic
suggesting that the performance of those who had not eaten process; therefore, there is a need for additional analyses to
72 MARTIN AND BENTON

FIG. 3. The effect of changes in blood glucose while performing the


FIG. 2. The effect of baseline blood glucose levels on performance Brown–Peterson task after taking a glucose drink. The data are the
of the Brown–Peterson task. The data are the mean number of tri- mean number of trigrams recalled.
grams recalled.

consider changes that occur over time. Second, as discussed reflected a failure to maintain an adequate supply of glucose.
below, the presently reported findings are similar to previous Falling blood glucose levels, after a placebo drink, have also
findings, strongly suggesting that they are more than chance been reported to be associated with poorer performance of a
statistical findings. Conditional Associative Learning Task (31) and an intelli-
A high baseline blood glucose was associated with better gence test (29).
recall of the trigrams (Fig. 2). Previously, a high level of base- There are only limited data available that considered the
line blood glucose has been associated with better recall of influence of glucose provision from a psychological perspec-
word lists (4,5) and increased vigilance (5). When an associa- tive. The provision of glucose has been found to aid recall for
tion between baseline blood glucose levels and subsequent word lists (4,6,18) and a story (9,10,13,20), but also retrieval of
performance has been reported, in every instance a higher information learned 24 h previously (21). The presently used
level of blood glucose has been associated with better perfor- Brown–Peterson task has been described as a measure of
mance. As it is known that an equilibrium develops between working memory (1), but any conclusion concerning working
plasma and brain glucose (19), there is reason to suggest that memory requires studies that selectively tap the various sub-
those with initially high levels of blood glucose might have systems of the working memory model. Craft et al. (9) con-
had higher levels of brain glucose. cluded that declarative memory was primarily influenced, a
Figure 3 illustrates that after a glucose drink the ability to view supported by studies discussed in the previous para-
control blood glucose levels was associated with a better re- graph, although other aspects of memory have been relatively
call: those whose blood glucose levels fell recalled more tri- ignored. However, the view that glucose administration ex-
grams. The introduction lists a series of similar findings. clusively improves declarative memory conflicts with aspects
The pattern was different following a placebo drink where of the literature. Glucose has been reported to improve vigi-
falling blood glucose levels were associated with a poorer per- lance (2,3,5), quicken reaction times (27,28), improve mental
formance (Fig. 4). An obvious suggestion is that in those who arithmetic (27), decrease errors in a driving simulator (15),
had taken a glucose containing drink, falling blood glucose decrease the Stroop effect (5), and improve performance of
levels reflected the passage of the basic fuel to metabolically an intelligence test (7). It appears that the view that declara-
active cells. After a placebo drink there is no exogenous tive memory is influenced particularly by changes in blood
source of glucose, and falling blood glucose levels may have glucose and is relatively rather than absolutely the case. It is
GLUCOSE DRINK AND WORKING MEMORY TASK 73

line is formed by choline acetyltransferase, from the


precursors’ choline and acetyl CoA; glucose is the main
source of the acetyl groups used in the formation of acetyl
CoA (26,37). After a 24-h fast brain acetylcholine levels have
been reported to be lower in rats, levels that can be restored
by either feeding or the administration of glucose (17). Mess-
ier (26) reviewed the topic and concluded that in resting con-
ditions increased glucose availability had little effect on ace-
tylcholine levels in continuously fed animals. However, when
there was a high demand for acetylcholine, a high availability
of glucose increased the rate of synthesis of the neurotrans-
mitter.
Although traditionally most physiologists have believed
that the brain was well supplied with glucose, resulting in a
uniform concentration of extracellular glucose, this view is
beginning to be challenged. The concentration of extracellu-
lar glucose varies with the strain of rat and the area of the
brain examined (25). In freely moving rats McNay and Gold
(24) showed a 25% decrease in hippocampal extracellular
glucose during a spatial working memory task. An injection
of glucose, but not a placebo, prevented this decline in glu-
cose in hippocampus. The assumption that the transport of
glucose to metabolically active sites is never rate limiting, in
those with blood glucose in the normal range, is thus begin-
ning to be questioned.
Unlike other organs the energy requirement of the brain is
met almost exclusively by aerobic glucose degradation. The
energy requirement of the brain is approximately 20% of the
whole organism at rest, although its weight is only 2% of total
body weight. Strangely, the energy stores in the brain are ex-
tremely small, and without replacement the brain would be
FIG. 4. The effect of changes in blood glucose while performing the
depleted of glucose in under 10 min (22). It has been as-
Brown–Peterson task after taking a placebo drink. The data are the sumed, traditionally, that except under exceptional conditions
mean number of trigrams recalled. homeostatic mechanisms adequately supply the brain with
glucose. The present findings add to the growing data that
question this assumption, at least to the extent that some cog-
nitive tasks, under some conditions, are influenced by the
relatively easy to influence measures of declarative memory level of blood glucose. In the present study a higher level of
compared with other measures of cognition. Although we baseline blood glucose level, which can be assumed to result
need detailed studies, it seems likely that the provision of glu- in higher levels of brain glucose (19), was associated with bet-
cose influences various stages of the memory process. ter memory (Fig. 2). In those who had not eaten breakfast a
The question arises as to the biological mechanism by glucose drink facilitated performance (Fig. 1). The finding
which an enhanced provision of glucose might facilitate mem- that the ability to rapidly remove glucose from the blood
ory. An association between acetylcholine-mediated neu- stream after a glucose drink was associated with better mem-
rotransmission and memory is well accepted (16). Acetylcho- ory (Fig. 3), confirmed previous findings.

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