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Biological Psychology xxx (2006) xxx–xxx

The effect of glucose administration on the emotional enhancement

effect in recognition memory

Karen R. Brandt *, Sandra I. Sunram-Lea, Kirsty Qualtrough

University of Lancaster, United Kingdom

Received 11 April 2005; accepted 4 April 2006

Abstract

Previous research has demonstrated that glucose administration improves memory performance. However few studies have addressed the

effects of glucose on emotional material that by nature already enjoys a memory advantage. The aim of the present research was therefore to

investigate whether the memory facilitation effect associated with glucose would emerge for emotional words. Experiment 1 demonstrated that

negative words were better recognized and remembered than positive and neutral words. Experiment 2 further explored these effects under

conditions of glucose administration and an aspartame control. The results revealed that both the aspartame and glucose groups replicated the

results from Experiment 1. The present research therefore demonstrated that the glucose facilitation effect did not emerge for material that already

benefits from a memory advantage. These results also raise the question of whether the dose response relationship previously associated with

glucose administration is applicable when the information being processed is of an emotional nature.

# 2006 Published by Elsevier B.V.

Keywords: Glucose administration; Recognition memory; Emotional enhancement effect; Subjective experiences

1. Introduction

Research investigating the effects of glucose administration

on cognitive performance has found beneficial effects in

healthy young adults (see for example Benton et al., 1994;

Kennedy and Scholey, 2000; Scholey et al., 2001; Sunram-Lea

et al., 2002a); older adults (Craft et al., 1994; Gondor-Frederick

et al., 1987) and even adults with severe cognitive pathologies

such as Alzheimers disease (Craft et al., 1992; Manning et al.,

1993). Although, the benefits in cognitive performance that

have been found occur in a range of cognitive tasks, in general,

it appears that glucose administration has a pronounced effect

on tests of declarative long-term memory (for a recent review

see Messier, 2004).

It has long been recognized that emotionally significant,

stressful or arousing events can play an important role in the

regulation of memory (for a recent review, see Packard and

Cahill, 2001). Acute emotional arousal results in activation of

* Corresponding author at: School of Psychology, Dorothy Hodgkin Building,

University of Keele, Keele, Staffordshire ST5 5BG, United Kingdom.

Tel.: +44 1782 583667; fax: +44 1782 583387.

E-mail address: k.r.brandt@psy.keele.ac.uk (K.R. Brandt).

0301-0511/$ – see front matter # 2006 Published by Elsevier B.V.

doi:10.1016/j.biopsycho.2006.04.001

two major endocrine systems, the hypothalamic-anterior

pituitary-adrenocortical axis (HPA) and the sympatho-adreno-

medullary axis (SAM axis). Activation of the HPA axis is

associated with the release of glucocorticoids from the adrenal

cortex and activation of the SAM axis leads to a release of

adrenaline from the adrenal medulla. The hormone for which

we have most evidence concerning the regulation of memory

formation is adrenaline (for a detailed account see Gold, 1992).

In considering the mechanisms by which adrenaline enhances

memory, it is important to note that circulating adrenaline is

largely excluded from the central nervous system (CNS); that

is, adrenaline does not cross the blood–brain barrier (Weil-

Malherbe et al., 1959). Since adrenaline does not appear to have

direct actions on the CNS, it is most likely that the beneficial

effect of adrenaline upon memory performance is closely

related to its actions in the periphery (Gold, 1992). It has been

suggested that the effects of adrenaline on memory may be

mediated by activation of peripheral b-adrenergic receptors,

located on vagal afferents projecting to the nucleus of the

solitary tract in the brain stem (Cahill and McGaugh, 1998).

However, another important peripheral action of adrenaline is

to produce an increase in circulating blood glucose levels (Ellis

et al., 1967; Gold, 1992). Increased plasma glucose levels

subsequent to the release of adrenaline from the adrenal

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medulla appear to be an important contributor to the processes

by which memory is normally regulated. Subsequent research

indicated that it is this increase in glucose levels subsequent to

peripheral adrenaline actions which contributes to enhance-

ment of memory storage processing, rather than the liberation

of adrenaline per se which benefits cognitive functions (Gold,

1991, 1992; Wenk, 1989; White, 1991).

In the context of memory modulation resulting from acute

emotional arousal, it is important to investigate whether

emotionally arousing stimuli are indeed associated with

increases in (i) memory performance and (ii) blood glucose

levels. Research on emotion and memory has shown the

presence of an emotional enhancement effect such that

emotional stimuli are more memorable than their more neutral

counterparts (Hamann, 2001). This emotional enhancement

effect has been demonstrated across a range of memory

measures such as recognition memory (Kensinger and Corkin,

2003; Smith et al., 2004) and recall (Talmi and Moscovitch,

2004) and has also been found using a range of stimulus

variables including both words (Dewhurst and Parry, 2000) and

pictures (Ochsner, 2000). Moreover, research has shown that

the emotional enhancement effect not only consists of a

quantitative advantage (i.e., emotional stimuli are recognized

more than neutral stimuli), but also consists of a qualitative

advantage (i.e., emotional stimuli are more likely to be

recognized on the basis of rich episodic ‘remembering’ in

comparison to neutral stimuli, Dewhurst and Parry, 2000;

Kensinger and Corkin, 2003).

Importantly, recent research has demonstrated that pre-

sentation of emotionally arousing material not only increases

subsequent memory performance, but also raises plasma

glucose levels (Blake et al., 2001; Parent et al., 1999; Scholey

et al., 2006). Blake et al. (2001) presented participants either

with emotional or neutral pictures and measured blood glucose

levels both before and after the presentation phase, which was

then followed by an incidental memory test (free recall). The

results showed that recall was significantly greater for the

emotional compared to the neutral pictures. Importantly

though, the results also revealed that blood glucose levels

had increased significantly for participants shown the emo-

tional pictures but not for those shown the neutral pictures. This

latter effect has also been found using narratives (Parent et al.,

1999) and replicated with words lists (Scholey et al., 2006).

These findings further support the notion that increases in

circulating and (one may argue) central glucose levels in

response to emotional arousal may reflect naturally occurring

biological mechanisms regulating the formation of memory.

If increases in blood glucose levels are an important

underlying mechanism for the emotion-induced memory

enhancement effect, the question arises as to whether glucose

administration, which has been shown to enhance memory

performance, would increase memory for emotional material

beyond the normal advantage this type of material benefits

from, or whether administration of a memory enhancing dose of

glucose would actually impair memory for emotionally

arousing material. This question has recently been explored

(Ford et al., 2002; Mohanty and Flint, 2001; Parent et al., 1999).

Parent et al. (1999) found that glucose administration prevented

the normal memory enhancing effects for an emotional

narrative. In addition, Mohanty and Flint (2001) found that

whilst glucose administration had no effect on the proportion of

errors for neutral stimuli on a spatial memory task, it

significantly increased the number of errors for the emotional

material. The authors concluded that glucose might therefore

attenuate the emotional enhancement effect. However, an effect

of glucose on emotional material was not found in Ford et al.

(2002) study in which more direct tests of memory were

employed (as opposed to just measuring the proportion of

errors). In this study, participants were either given a glucose or

a placebo drink and then presented with 20 emotional and

neutral words to memorise at study followed by tests of recall

and recognition. The results demonstrated that across drink

conditions emotional words were both recalled and recognized

to a greater extent than the neutral words. However no effect of

glucose on recall and recognition of the emotional (or indeed

the neutral) words was observed. The authors argued that the

lack of a glucose effect may have been due to glucose

facilitation generally not being present using simple memory

tests but only arising under conditions of increased cognitive

demand such as dual task conditions (Foster et al., 1998;

Sunram-Lea et al., 2001).

Given the mixed findings from previous studies, the aim of

the present research was to provide a more comprehensive

investigation of the possible effects of glucose administration

on the emotional enhancement effect. Ford et al. (2002) argued

that the lack of a glucose effect in their study was probably due

to glucose facilitation effects only occurring under more

difficult task conditions. In their study, they presented

participants with 20 words to memorise and the results

demonstrated scores averaging about 90% on the recognition

memory test. These high recognition scores reflect the ease of

the memory task and therefore, in order to make the task more

difficult, in the present research participants were presented

with 60 words at study (20 emotionally positive, 20 emotionally

negative and 20 neutral).

The present research additionally included the use of

emotionally positive as well as emotionally negative and

neutral words. Past research exploring emotional enhancement

effects in memory have mostly failed to make the distinction

between emotionally positive and emotionally negative stimuli

(e.g., Kensinger and Corkin, 2004; Talmi and Moscovitch,

2004) despite evidence showing that valence (how positive or

negative an item is) affects recognition memory (Dewhurst and

Parry, 2000; Ochsner, 2000). These studies have shown that

both emotionally positive and negative material is more likely

to be recognized than neutral items. Importantly though,

emotionally negative stimuli are recognized to a greater extent

than emotionally positive stimuli. Thus, type of valence

differentially affects recognition memory and this finding

contradicts the conclusions made by Blake et al. (2001) that the

emotional enhancement effect is not related to the pleasantness

of the stimulus material. Clearly, the size of the emotional

enhancement effect depends on whether positive or negative

stimuli are employed. A further aim of the present research was

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to therefore investigate whether any effects of glucose

administration on the emotional enhancement effect might

also be influenced by the valence of the to-be-remembered

material.

A final aim of the present research was to explore the role

that subjective experiences might play on the effects of glucose

administration on the emotional enhancement effect. Sub-

jective experiences refer to how we recognize something/

someone and according to Tulving (1985) can be based either

on ‘remembering’ or ‘knowing’. Whereas ‘remembering’ refers

to recognition that is accompanied by recollection of contextual

details, ‘knowing’ lacks this episodic richness and is based on

feelings of familiarity. Based on Tulving’s theory, Gardiner and

Java (1993) developed the remember/know paradigm to

measure the different subjective experiences that can accom-

pany recognition. This paradigm is used in recognition tests

whereby participants at test are shown a set of studied and

unstudied items and are required to decide whether each item

was presented in the study phase (old) or not (new). Following

an ‘old’ decision, participants are then further required to make

a ‘remember’, ‘know’ or ‘guess’ decision (the ‘guess’ response

category is included so that the ‘know’ response category is not

inflated by guesses, Gardiner et al., 1996). There is ample

evidence demonstrating that ‘remember’ and ‘know’ responses

can be dissociated experimentally (Brandt et al., 2003;

Dewhurst and Hitch, 1999; Gardiner and Java, 1990).

Additionally, evidence has also pointed to ‘remember’ and

‘know’ responses reflecting different patterns of brain activity,

both temporally and spatially (Eldridge et al., 2000; Mangels

et al., 2001; Rugg et al., 1998).

Although an effect of glucose administration on the

emotional enhancement effect in recognition memory was

not found in Ford et al. (2002) study, it may be the case that such

an effect would be apparent in subjective experiences. Recent

research has shown that glucose does indeed have a part to play

in subjective experiences. Specifically, the proportion of

‘remember’ responses have been found to be significantly

greater following glucose administration (Sunram-Lea,

Dewhurst and Foster, in preparation). Hence, the failure to

find a glucose effect on the recognition of emotional stimuli

(Ford et al., 2002) does not rule out the possibility that such an

effect might be present in the subjective experience of

‘remembering’.

Thus, the aim of the present research was to provide a

more comprehensive investigation of the possible effects of

glucose administration on the emotional enhancement effect

by (1) using a more difficult cognitive task coupled with a

retention interval between study and test, (2) investigating the

effect of valence by using both emotionally positive and

negative words (as well as neutral words) and finally (3)

exploring qualitative (as well as quantitative) effects using the

remember/know paradigm (Gardiner and Java, 1993).

Experiment 1 was firstly designed to explore the emotional

enhancement effect under these three criteria and the purpose

of Experiment 2 was to specifically test the effects of glucose

administration on the emotional enhancement effects found in

Experiment 1.

2. Experiment 1

Experiment 1 investigated the emotional enhancement effect

both in overall recognition memory and in subjective

experiences. Participants were presented with a set of

emotionally neutral, positive and negative words to memorise

at study. In a subsequent recognition test, participants were

required to make old/new judgements for each word and

following an old judgment were further required to make

remember/know/guess decisions. It was predicted that overall

recognition memory would be enhanced for the emotionally

negative words in comparison to the emotionally positive words

and the emotionally neutral words (Kensinger and Corkin,

2003; Smith et al., 2004). This same pattern of effects was

predicted to arise in the subjective experience of ‘remembering’

(Dewhurst and Parry, 2000; Ochsner, 2000).

2.1. Methods

2.1.1. Participants

Forty undergraduate students from the University of Lancaster (20 female

and 20 male) participated in the present experiment. The range of ages of the

participants was 18–25. The Ethics Committee of the Department of Psychol-

ogy, University of Lancaster approved the experimental procedure prior to the

start of the study and all procedures were carried out with written consent of the

participants.

2.1.2. Design and stimulus materials

The experiment consisted of a within-subjects design using repeated

measures with three levels of emotion (neutral versus positive versus negative).

A set of 120 words was selected from a study by Dewhurst and Parry (2000) in

which participants were required to rate the emotionality of words. Based on

these ratings, three lists of words were created varying in emotional valence,

i.e., negative, positive and neutral. For the purpose of the present study, 40

words were selected from each emotional category list, giving 120 words in

total. Two word lists (Sets A and B) were then created (please see Appendix A),

each containing 60 words of which 20 were emotionally positive (e.g., peace,

rainbow), 20 emotionally negative (e.g., corpse, mucus) and finally 20 emo-

tionally neutral (e.g., mirror, cloak). The words in the two lists did not differ

significantly on frequency [t(59) = 0.419, p = 0.625, ns], on length

[t(59) = 0.497, p = 0.621, ns], or on imagery [t(59) = 0.516, p = 0.608, ns].

In addition, no significant differences were found on imagery ratings between

the negative and positive words [t(39) = 0.095, p = 0.925, ns], the negative and

neutral words [t(39) = 0.995, p = 0.326, ns], and the neutral and positive words

[t(39) = 0.900, p = 0.374, ns]. The lists were counterbalanced such that half the

participants in the present study were given Set A as targets and Set B as

distractors and the other half were given Set B as targets and Set A as distractors.

2.1.3. Procedure

Participants were randomly and sequentially presented with words on a

computer screen for 2 s with a 1 s inter-stimulus interval. They were informed

that they should try to remember these words as their memory for them would be

tested at a later stage. After the study phase participants were given a 10-min

distractor task which involved multiplication problems. Following the distractor

task, participants were given a recognition test. In this test, participants were

presented with the 60 target words and an additional 60 distractor words and

were required to make old/new decisions for each word by means of a key press.

Following an old response, participants were further required to make a

remember/know/guess decision. The instructions for the remember/know

responses were closely modelled from those by Rajaram (1993). Participants

were told that a ‘remember’ response meant that they could consciously

recollect the experience of having seen the word before. A ‘know’ response

meant that they could not consciously recollect the experience of having seen

the word before but simply just knew they had been presented with it.

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Participants were instructed to use the ‘guess’ option if they felt the word was

old but could not attribute either a ‘remember’ or a ‘know’ response to the word.

On completion of the recognition memory task, participants were debriefed,

thanked for their participation and dismissed.

2.2. Results

2.2.1. Overall recognition

Overall correct recognition hits were submitted to a three

(emotion: neutral versus positive versus negative) repeated

measures ANOVA. The analysis demonstrated a significant

effect of emotion [F(2,78) = 12.49, p < 0.01]. Pair-wise

comparisons were then carried out on this effect using a

Bonferroni correction to control the family-wise error rate at

the p < 0.05 level. This revealed that negative words were

recognized significantly more than both neutral and positive

words. No significant differences were found between the

neutral and positive words. In addition, the A-prime sensitivity

index was calculated on the recognition memory data (see

Pollack and Norman, 1964). A-prime varies from 0 to 1

whereby 0 indicates no discrimination (low sensitivity)

between hits and false alarms and 1 indicates perfect

discrimination (high sensitivity). A-prime scores were sub-

mitted to a three (emotion: neutral versus positive versus

negative) repeated measures ANOVA. The analysis demon-

strated a significant effect of emotion [F(2,78) = 10.53,

p < 0.001]. Pair-wise comparisons were then carried out on

this effect using a Bonferroni correction to control the family-

wise error rate at the p < 0.05 level. This revealed that

participant’s discrimination was significantly greater for the

positive than the neutral words (respective M: 0.85 versus 0.82).

In addition, discrimination was significantly higher for the

negative in comparison to the neutral words (respective M: 0.88

versus 0.82) (see Table 1 for all treatment means).

2.2.2. Subjective experience

Correct ‘remember’, ‘know’ and ‘guess’ responses were

then each submitted to separate three (emotion: neutral versus

positive versus negative) repeated measures ANOVAs. The

analysis on ‘remember’ responses revealed a significant effect

of emotion [F(2,78) = 13.60, p < 0.01]. Pair-wise comparisons

were then carried out on this effect using a Bonferroni

correction to control the family-wise error rate at the p < 0.05

level. This revealed that negative words (M = 0.56) elicited

significantly more ‘remember’ responses than either neutral

Table 1

Recognition performance (Hits) and false alarms (FA) as a function of word valen

Word valence

Neutral Positive

Hits FA Hits

Overall 0.66 (0.20) 0.12 (0.10) 0.72 (0.

Remember 0.42 (0.21) 0.01 (0.02) 0.45 (0.

Know 0.17 (0.11) 0.07 (0.08) 0.23 (0.

Guess 0.06 (0.07) 0.04 (0.05) 0.04 (0.

A-prime 0.81 (0.09) 0.85 (0.

Note: Standard deviations in parentheses.

(M = 0.42) or positive words (M = 0.45). No significant

differences were found between the neutral and positive

words. The analysis on ‘know’ responses revealed no effects

[F(2,76) = 2.46, p = 0.92, ns]. A similar lack of effects was

found in the analysis on ‘guess’ responses [F(2,78) = 1.31,

p = 0.27, ns] (see Table 1 for all treatment means).

The results of Experiment 1 revealed that both overall

correct recognition and the proportion of remember responses

was significantly greater for negative words in comparison to

both neutral and positive words. The effects of glucose

administration on this emotional enhancement effect was

investigated in Experiment 2.

3. Experiment 2

The aim of Experiment 2 was to address the role of glucose

on the emotional enhancement effects found in Experiment 1.

Whilst some research has shown that glucose administration

reduces memory accuracy for emotional material (Mohanty and

Flint, 2001; Parent et al., 1999), other research has found that

glucose has no effect on memory for emotional items (Ford

et al., 2002). However, research has shown that unless the

cognitive task is demanding, then glucose administration will

have no effect on cognitive performance (Scholey et al., 2001;

Sunram-Lea et al., 2002a,b). In Ford et al. (2002) study,

participants were given only 20 words to memorise leading to

average recognition scores of around 90% and it is possible that

the ease of this task is the reason behind the lack of a glucose

effect in their study. The results of Experiment 1 showed

average recognition scores of 72% using triple the number of

words to memorise and importantly the emotional enhancement

effect was still demonstrated. Using the same methodology as

Experiment 1, the aim of Experiment 2 was therefore designed

to investigate the effect of glucose administration on the

emotional enhancement effect under more difficult task

conditions.

3.1. Methods

3.1.1. Participants

Forty undergraduate students (14 males, 26 females) from the University of

Lancaster who had not taken part in Experiment 1 participated in the present

experiment for which they were paid £5. The range of ages of participants was

18–36 years (mean age = 22 years). Participants were not diabetic and had a

mean BMI of 22.5 kg/m2. The Ethics Committee of the Department of

ce and subjective experience (Experiment 1)

Negative

FA Hits FA

18) 0.24 (0.14) 0.78 (0.14) 0.16 (0.12)

21) 0.06 (0.07) 0.56 (0.20) 0.04 (0.06)

16) 0.11 (0.09) 0.18 (0.13) 0.08 (0.08)

06) 0.07 (0.08) 0.04 (0.06) 0.04 (0.06)

07) 0.88 (0.08)

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Table 2

Blood glucose levels (mmol/l) as a function of condition and time (Experiment

2)

Condition Time

T0 T25 T45

Glucose 4.93 (0.51) 6.80 (1.36) 7.37 (1.42)

Aspartame 5.21 (0.69) 5.58 (0.92) 5.45 (0.77)

Note: Standard deviations in parentheses.

Psychology, University of Lancaster approved the experimental procedure prior

to the start of the study and all procedures were carried out with written consent

of the participants.

3.1.2. Treatment

Participants received either 25 g of glucose or five tablets of aspartame

dissolved in 300 ml of water. Glucose was used in a dose of 25 g, as previous

studies in this and other laboratories have shown this dose to be effective for

memory enhancement (Foster et al., 1998; Kennedy and Scholey, 2000;

Sunram-Lea et al., 2001, 2002a,b, 2004). Five tablets of aspartame were used

since, when dissolved in 300 ml of water, the resulting sweetness was rated as

equivalent to that of the glucose solution.

3.1.3. Design and stimulus materials

The experiment had a double blind, placebo-controlled, between-subjects 2

(condition: aspartame versus glucose) � 3 (emotion: neutral versus positive

versus negative) mixed factorial design with repeated measures on the second

factor. The stimulus materials were identical to those used in Experiment 1. In

addition to the stimulus materials being counterbalanced across participants (as

in Experiment 1), the word lists were also counterbalanced across condition.

Participants were randomly allocated to the different experimental conditions as

they entered the laboratory. A between-subjetcs placebo-controlled design with

20 participants per treatment group was used, as past experience indicates that

this represents a suitable sample size to provide appropriate statistical power

and reveal the effect of glucose administration on declarative memory (Sunram-

Lea et al., 2001, 2002a,b, 2004). In addition, previous studies investigating the

relationship of emotional memory, glucose administration and/or blood glucose

levels using a between-subjects design have used similar sample sizes [for

example, N = 17 per condition, Blake et al. (2001); N = 10–14 per condition,

Mohanty and Flint (2001); N = 10 per condition, Parent et al. (1999)].

3.1.4. Procedure

Participants arrived at the laboratory and were randomly assigned to either

the aspartame or the glucose group. A double blind procedure was adopted so

that neither the participants nor the experimenter were aware of which condition

each person was allocated to. Each participant attended one test session that

lasted approximately 45 min. Participants were informed that they should not

eat or drink anything (except water) for 2 h before arriving in the laboratory. A

2-h fasting period was chosen as previous research has shown that this time

interval is sufficient to demonstrate the glucose memory facilitation effect

(Sunram-Lea et al., 2001, 2002a,b, 2004). Testing was carried out between

09:00 and 13:00 h. This time frame was chosen for convenience, as a previous

study demonstrated that circadian rhythms in glucose tolerance do not influence

glucose-mediated facilitation of cognitive performance, and that glucose-

related memory facilitation can be observed after 2 h of fasting throughout

the day (Sunram-Lea et al., 2001). All participants were informed that they

would undergo cognitive testing related to human memory performance, and

that they were required to consume a non-harmful, non-intoxicating drink.

Participants were asked to give information about their age, weight, and height.

At the beginning of each session (i.e., before drink ingestion), baseline

blood glucose levels were measured. All participants agreed to have their blood

glucose levels monitored. They were reassured that they were permitted to

withdraw without prejudice during the experiment if they were not willing to

have small samples of blood taken. Blood glucose readings were obtained using

the ExacTech blood glucose monitoring equipment (supplied by MediSense

Britain Ltd., 16/17 The Courtyard, Gorsey Lane, Coleshill, Birmingham B46

1JA), following the manufacturer’s recommended procedure. All participants

then received either a glucose- or an aspartame-containing drink depending on

the group they had been allocated to and asked to consume the drink as quickly

as possible. There was a 15-min delay between participants finishing their drink

and the start of the study phase.

The study phase in Experiment 2 was identical to that of Experiment 1.

Participants were randomly presented with a set of emotionally neutral, positive

and negative words and asked to memorise them as their memory for these

words would be tested. Following the study phase, all participants gave a second

blood glucose sample and then completed some multiplication problems as a

distractor phase for 10 min. They were then given the recognition test in which

they had to make old/new as well as remember/know/guess judgements.

Following the completion of the recognition test, participants gave their third

and final blood sample and then were thanked, debriefed, paid and dismissed.

3.2. Results

3.2.1. Glycaemic response

Blood glucose levels were submitted to a 2 (drink: glucose

versus placebo) � 3 (time: i.e., at what point blood glucose was

measured; T0 = baseline blood glucose levels, T25 = 25 min

post ingestion, T45 = 45 min post ingestion) mixed factorial

ANOVA (see Table 2 for all treatment means). The analysis

revealed a main effect of drink [F(1,38) = 15.01, p < 0.01], a

main effect of time [F(2,76) = 34.13, p < 0.01], and a significant

drink � time interaction [F(2,76) = 21.01, p < 0.01]. Simple

main effects analyses on this interaction (supplemented with a

Bonferroni correction) revealed a significant effect of time on the

glucose group [F(2,38) = 33.32, p < 0.01] whereby blood

glucose levels were significantly greater both at T25 and T45

in comparison to T0. Although there was a strong tendency for

blood glucose levels to be higher at T25 and T45 compared to T0

in the aspartame group, the simple main effects analysis just

failed to reach significance [F(2,38) = 3.04, p = 0.05]. The

analyses also revealed that whilst there were no differences

between the aspartame and glucose groups at T0, blood glucose

levels were significantly greater in the glucose compared to the

aspartame group both at T25 [F(1,38) = 10.96, p < 0.01] and

T45 [F(1,38) = 28.37, p < 0.01].

3.2.2. Overall recognition

Overall correct recognition hits were submitted to a 3

(emotion: neutral versus positive versus negative) � 2 (condi-

tion: aspartame versus glucose) mixed factorial ANOVA. The

analysis revealed a main effect of emotion [F(2,76) = 6.78,

p = 0.01]. Pair-wise comparisons were then carried out on this

effect using a Bonferroni correction to control the family-wise

error rate at the p < 0.05 level. This revealed that recognition of

negative words (M = 0.79) was significantly greater than that of

either neutral or positive words (respective M: 0.72 versus 0.73).

No significant differences were found between the neutral and

positive words. The effect of condition was not significant

[F(2,76) = 0.07, p = 0.78, ns], nor was the emotion � condition

interaction [F(2,76) = 2.02, p = 0.14, ns]. A-prime scores were

then submitted to a 3 (emotion: neutral versus positive versus

negative) � 2 (condition: aspartame versus glucose) mixed

factorial ANOVA. The analysis demonstrated a significant effect

of emotion [F(2,76) = 11.19, p < 0.001]. Pair-wise comparisons

were then carried out on this effect using a Bonferroni correction

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Table 3

Recognition performance (Hits) and false alarms (FA) as a function of condition, word valence and subjective experience (Experiment 2)

Condition Word valence

Neutral Positive Negative

Hits FA Hits FA Hits FA

Aspartame

Overall 0.72 (0.20) 0.10 (0.09) 0.76 (0.16) 0.21 (0.16) 0.78 (0.19) 0.15 (0.12)

Remember 0.49 (0.27) 0.02 (0.03) 0.49 (0.25) 0.04 (0.05) 0.55 (0.26) 0.02 (0.04)

Know 0.21 (0.14) 0.06 (0.06) 0.23 (0.17) 0.12 (0.11) 0.20 (0.21) 0.08 (0.08)

Guess 0.02 (0.05) 0.02 (0.04) 0.04 (0.07) 0.05 (0.10) 0.03 (0.05) 0.05 (0.05)

A-prime 0.88 (0.06) 0.86 (0.06) 0.89 (0.06)

Glucose

Overall 0.72 (0.17) 0.10 (0.11) 0.70 (0.19) 0.26 (0.15) 0.80 (0.11) 0.18 (0.12)

Remember 0.45 (0.19) 0.01 (0.04) 0.39 (0.18) 0.06 (0.07) 0.54 (0.19) 0.05 (0.04)

Know 0.21 (0.20) 0.04 (0.06) 0.24 (0.18) 0.13 (0.10) 0.21 (0.19) 0.09 (0.08)

Guess 0.06 (0.08) 0.05 (0.05) 0.07 (0.07) 0.07 (0.09) 0.05 (0.07) 0.04 (0.04)

A-prime 0.88 (0.07) 0.80 (0.10) 0.88 (0.06)

Note: Standard deviations in parentheses.

to control the family-wise error rate at the p < 0.05 level. This

revealed that participant’s discrimination was significantly

greater for the neutral than the positive words [respective M:

0.88 versus 0.83]. In addition, discrimination was significantly

higher for the negative in comparison to the positive words

(respective M: 0.88 versus 0.83). The effect of condition was

not significant [F(1,38) = 1.96, p = 0.16, ns], nor was the

emotion � condition interaction [F(2,76) = 2.74, p = 0.07, ns]

(see Table 3 for all treatment means).

3.2.3. Subjective experience

Correct ‘remember’, ‘know’ and ‘guess’ responses were

then each submitted to separate 3 (emotion: neutral versus

positive versus negative) � 2 (condition: aspartame versus

glucose) mixed factorial ANOVAs. The analysis on ‘remember’

responses revealed a main effect of emotion [F(2,76) = 7.65,

p < 0.01]. Pair-wise comparisons were then carried out on this

effect using a Bonferroni correction to control the family-wise

error rate at the p < 0.05 level. This revealed that ‘remember’

responses for negative words (M = 0.54) were significantly

greater than that of either neutral or positive words (respective

M: 0.46 versus 0.44). No significant differences were found

between the neutral and positive words. The effect of condition

was not significant [F(2,76) = 0.66, p = 0.42, ns], nor was the

emotion � condition interaction [F(2,76) = 1.08, p = 0.34, ns].

No effects were found in the analyses on either ‘know’ or

‘guess’ responses (see Table 3 for all treatment means).

A further series of analyses in the form of correlations were

carried out in order to test (i) whether there was a relationship

between blood glucose levels at 25 and 45 min and recognition

memory performance and (ii) whether individual differences in

the glycaemic response to a glucose drink had any effects on

recognition memory.

3.2.4. Relationship between blood glucose level and

memory

Analysis of the Pearson’s product moment correlation

coefficient (two-tailed) across drink conditions showed a

significant negative correlation between blood glucose levels at

T45 and number of correct recognition hits for positive items

(r = �0.42; p < 0.01). Further analysis of the subjective

experiences revealed a significant negative correlation between

blood glucose levels at T45 and number of correct ‘remember’

responses for positive items (r = �0.35; p < 0.05). Moreover,

there was a significant negative correlation between blood

glucose levels at T45 and number of false alarms for neutral

items (r = �0.39; p < 0.01). No significant correlation between

blood glucose levels at T25 and memory performance (correct

and false alarms) was observed.

3.2.5. Glucoregulation indices and emotional memory

Previous research has suggested that individual differences

in the ability to regulate blood glucose levels following a

glucose drink influences the degree to which glucose

administration affects memory performance (Messier et al.,

1999). As the effect of glucose administration on emotional

memory may also be moderated by glucoregulatory control we

decided to examine the relationship between the ability to

regulate glucose levels and memory performance following

administration of a glucose drink. In order to assess the degree

of glycaemic control we used two glucoregulation indices, that

is (i) recovery from evoked glucose levels which is defined as

the difference between evoked glucose levels 45 min post

glucose administration and fasting glucose levels (previously

used by Awad et al., 2002; Craft et al., 1994; Donohoe and

Benton, 2000; Meikle et al., 2004; Messier et al., 1997, 1999),

and (ii) area under the curve of evoked glucose levels (see for

example Awad et al., 2002). It is important to note, that

although a high correlation was observed between both indices

(r = 0.82; p < 0.01) they differed in terms of their relationship

with memory performance. In terms of recovery and memory

performance, a significant negative correlation for recognition

of negative items (r = �0.47; p < 0.05), and false alarms for

both neutral (r = �0.54; p < 0.05) and positive items

(r = �0.05; p < 0.05) was observed. There was no significant

correlation between area under the curve and correct

K.R. Brandt et al. / Biological Psychology xxx (2006) xxx–xxx 7

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recognition memory, but a significant negative correlation

between area under the curve and false alarms for positive items

(r = �0.51; p < 0.05).

4. General discussion

The aim of the present research was to provide a more

comprehensive investigation than has been previously offered

into the effects of glucose administration on the emotional

enhancement effect (Ford et al., 2002; Mohanty and Flint, 2001).

Experiment 1 was designed to establish the effects of emotional

words on memory by investigating valence (how positive or

negative an item is), by measuring the qualitative nature of the

emotional enhancement effect (i.e., subjective experiences) as

well as looking at quantitative measures. Experiment 2 was then

designed to specifically explore the effects of glucose admin-

istration on the emotion effects found in Experiment 1.

The results of Experiment 1 revealed that negative words were

better recognized and remembered compared to both positive

and neutral words, thereby replicating results found using mixed

lists (neutral, positive, negative) of pictorial material (Ochsner,

2000) and extending these effects to verbal material. The present

results did not however find that positive words were recognized

or ‘remembered’ more than neutral words, an effect that has been

previously demonstrated using both pictures and words

(Dewhurst and Parry, 2000; Ochsner, 2000). Although Dewhurst

and Parry (2000) demonstrated an emotional enhancement effect

using positive words, this effect was found using lists which

included neutral words only. In light of the present results, it

therefore appears that the memory advantage associated with

positive words may only emerge when these words are presented

in the context of neutral words alone. Hence the presence of

negative words appears to reduce the salience of and therefore the

memory advantage for positive words. The lack of a memory

advantage for positive words in the present research coupled with

the presence of such an effect for positive pictures in the Ochsner

(2000) study, is most likely due to the finding that the effects of

emotion are significantly more enhanced when using pictures

than words (Hamann, 2001). Taken together, this suggests that

the emotional enhancement effect is much stronger for negative

than positive stimuli as the presence of an effect of positive

material appears to be dependent on using pictures or on the use

of lists that do not contain negative words. In light of previous

research, the present results therefore suggest that negative

valence seems to be the main factor driving the emotional

enhancement effect in recognition memory.

However, it is important to note that the stronger emotional

enhancement effect observed for negative stimuli might also be

due to arousal. It has been shown that emotional stimuli can be

defined in terms of valence (i.e., the degree to which an item is

negative, neutral or positive), and in terms of arousal (i.e., the

degree to which an item leads to physiological and/or

psychological arousal; Lang et al., 1993; Russell, 1980). In

addition, both factors appear to contribute independently to the

emotional enhancement effect of memory performance via

distinct neural and cognitive mechanisms (for a recent review

see Kensinger, 2004). As level of arousal elicited by positive

and negative words was not assessed in the present study it is

not possible to determine whether the negative stimuli led to

greater levels of arousal than the positive stimuli, which in turn

resulted in enhanced memory for these items. One task for

future research should be to carefully control for the relative

contribution of arousal and valence to the memory enhance-

ment effect.

The results of Experiment 2 demonstrated that compared to

the aspartame group, circulating blood glucose levels were

significantly higher in the glucose group after glucose

administration. Interestingly, there was a nearly statistically

significant increase in blood glucose levels in the aspartame

group following presentation of the study material compared to

baseline measures. This finding is consistent with the results

from Blake et al. (2001) who found that studying emotional

pictures significantly increased circulating blood glucose levels

in the aspartame group (see also Ford et al., 2002; Parent et al.,

1999). The results from the aspartame group also replicated the

results found in Experiment 1 in demonstrating increased

recognition and greater ‘remembering’ for negative words in

comparison to both positive and neutral words. Importantly, the

present results demonstrated that glucose administration had no

effect on memory performance compared to the aspartame

group, hence the glucose group also demonstrated greater

recognition and ‘remembering’ for negative compared to both

positive and neutral words.

One possible explanation as to the lack of a glucose effect

may be due to the nature of the material to be encoded. Blake

et al. (2001) found that encoding emotional material led to an

increase in circulating blood glucose levels in comparison to

neutral stimuli. The authors concluded that the emotional

enhancement effect was therefore due to emotional stimuli

increasing blood glucose levels which in turn improved

memory performance. This conclusion is reflected by the view

that emotionally significant or stressful events lead to a release

of adrenaline from the adrenal medulla which is then followed

by an increase in plasma glucose levels through hepatic glucose

release. A number of findings suggest that this increase in

glucose levels subsequent to peripheral adrenaline actions

contribute to enhancement of memory storage processing

(Gold, 1991; Wenk, 1989). However the memory enhancing

effect of glucose follows an inverted U-shaped curve such that

there is a cut-off point at which increasing glucose levels will no

longer benefit memory and further increasing glucose levels

will in fact begin to impair memory performance (Gold et al.,

1986). Replicating previous research by Parent et al. (1999), the

results of the present research demonstrated that whilst glucose

ingestion before viewing emotional material further increased

circulating blood glucose levels compared to the aspartame

group, there was no additional memory benefit.

Thus, the presence of glucose effects on memory for

emotional material may be dependent on the dose of glucose

administered. In a recent review Messier (2004) suggested that

for young human adults lower dosages of glucose (25 g)

appeared to be more effective in improving memory performance

(for neutral items) whereas for aged human adults higher dosages

(50–75 g) were needed in order to reliably improve memory.

K.R. Brandt et al. / Biological Psychology xxx (2006) xxx–xxx8

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Consequently, the lack of a glucose effect observed in the present

study does not appear to be due to the fact that the dosage used

does not improve memory performance per se. What this finding

suggests is that the dosage used is not the optimal dose for

memory enhancement of emotional stimuli. Previous research

has demonstrated that administration of 50 g of glucose impaired

memory for emotional material (Mohanty and Flint, 2001; Parent

et al., 1999), whereas research using 25 g of glucose has shown

no effect of glucose and hence the emotional enhancement effect

remains (Ford et al., 2002; the present study). These findings

suggest that the additive effect of glucose ingestion and a rise in

glucose levels due to the emotional nature of the stimuli shifts the

previously observed dose–response curve. That is to say, whereas

memory for neutral events benefits from the administration of a

25-g dose of glucose (for example Sunram-Lea et al., 2001,

2002a,b), no such effect is observed for emotional material (Ford

et al., 2002, present research). A second possibility is that the

effects of glucose on emotional memory may follow a downward

linear trend. It may be the case that glucose administration will

never further enhance emotional memory beyond that obtained in

normal control conditions. Hence, at a dose of 25 g, glucose has

no effect but increasing doses will impair performance gradually

(as they certainly do at 50 g).

In the present study, high blood glucose levels were associated

with improved memory performance for neutral material

(in terms of number of false alarms) and poorer memory for

positive items (irrespective of drink). These findings tentatively

support the notion that high blood glucose levels may indeed

impair memory performance for emotional items, but improve

memory for neutral items and suggest that memory for emotional

material which in itself may lead to a rise in blood glucose levels,

may not be facilitated by additional glucose administration.

Previous research has demonstrated that presentation of

emotional stimuli results in an increase in blood glucose levels

which in turn leads to memory facilitation for such items

compared to neutral items (Blake et al., 2001; Parent et al., 1999;

Scholey et al., 2006). This research investigated the effect of

emotional stimuli on blood glucose levels using ‘pure’ stimulus

lists (i.e., word lists containing emotional items only). In the

present study the use of mixed word lists might have prevented

clear facilitation of memory for neutral items (in the glucose

condition) as presentation of emotional items (which raised

blood glucose levels) in conjunction with glucose administration

might have resulted in a sub-optimal glycaemic response for

memory facilitation. This might therefore explain the failure to

observe any memory facilitation for neutral items in the present

study. One important task for future research will be to determine

the dose–response relationship for the effects of glucose

administration on emotional memory for ‘pure’ (emotional

versus neutral) and mixed sets of stimuli.

It is also possible that the presence of glucose effects on

memory for emotional material is dependent on inter-individual

differences in glucoregulation mechanism. Past research has

suggested that differences in an individual’s ability to regulate

blood glucose levels following a glucose drink may influence

the degree to which glucose administration affects memory

performance (Messier et al., 1999). The findings of the present

study suggest, if only tentatively, that this may also be the case

for memory of emotional material. Following administration of

a glucose drink, individuals whose blood glucose levels

returned quickly to baseline following glucose ingestion had

better recognition memory for negative items, but also made

more errors when recognizing neutral or positive items.

Moreover, larger evoked glycaemic responses (area under the

curve) following glucose ingestion was associated with better

memory for positive items (fewer errors). Individuals’ blood

glucose regulation might affect the degree to which they are

susceptible to the effects of glucose administration on

emotional memory and this in turn might affect the degree

to which additional glucose administration affects memory for

emotional material. Consequently, inter-individual glycaemic

response variability to glucose administration needs to be taken

into account when investigating the dose–response relationship

for the effects of glucose administration on emotional memory.

A second possible explanation as to the lack of a glucose

effect may be related to the cognitive demand of the memory

task. Ford et al. (2002) argued that the lack of a glucose effect in

their study was probably due to the often reported finding that

the effects of glucose tend to be restricted to more cognitively

demanding tasks (Scholey et al., 2001; Sunram-Lea et al.,

2002b). In order to address this issue, the present research

provided a more cognitively demanding task by a 3-fold

increase in the study list as well as the inclusion of a retention

interval. The lower means in the present results in comparison

to the results by Ford et al. (2002) demonstrate that our task was

indeed more cognitively demanding, yet the present research

still failed to demonstrate an effect of glucose.

A further task for future research will be to explore the effects

of glucose administration on emotion using even more

cognitively difficult task conditions, such as tests of recall or

even using dual task conditions. It is important to note that robust

glucose facilitation of memory has usually been observed in

studies in which a concurrent task was carried out during

encoding, suggesting that the possible ‘‘depletion’’ of episodic

memory capacity and/or glucose-mediated resources in the brain

due to performing a concomitant task might be crucial to the

demonstration of a glucose facilitation effect (Sunram-Lea et al.,

2002b). In fact, recent research has investigated the effects of

dual task conditions on both glucose levels and emotional

memory in the absence of glucose administration. Scholey et al.

(2006) found that circulating blood glucose levels were

significantly reduced under dual task compared to low effort

conditions. The results showed that under dual task conditions

overall memory performance decreased. Moreover, no memory

advantage for emotional material was found, either under dual

task or in low effort conditions. The authors argued that the lack

of an emotion effect in their study could be due to the use of pure

lists of emotional or neutral words, which is consistent with

previous research showing null effects of emotion under these

circumstances (Dewhurst and Parry, 2000).

Hence, whilst the inclusion of dual task conditions is often

necessary in order to produce an effect of glucose, at present it is

still unclear how such conditions will affect the emotional

enhancement effect in memory. A further task for future research

K.R. Brandt et al. / Biological Psychology xxx (2006) xxx–xxx 9

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will be to explore whether the depletion in circulating blood

glucose levels that occur under dual task conditions is sufficient

to eliminate the emotional enhancement effect found under

normal low effort conditions (as demonstrated in Experiment 1).

Additionally, the use of pictures rather than words would be

beneficial as these produce stronger and more robust effects in

emotion (Hamann, 2001). These studies will provide further

clarification of whether glucose does indeed have a role to play in

the emotional enhancement effect.

Future research should also attempt to further our under-

standing about the underlying mechanisms and brain areas

implicated in the glucose enhancement effect. Glucose facilita-

tion appears to be most pronounced on measures of memory

performance pertaining to hippocampal function (Craft et al.,

1994; Korol and Gold, 1998; Messier and Gagnon, 1996). The

hippocampus is the brain region most strongly implicated in

declarative long-term memory performance, with the left

hippocampal region generally thought to mediate memory of

verbal materials and the right hippocampal region thought to

mediate memory for non-verbal (e.g., spatial) materials (for a

recent review see Aggleton and Brown, 1999). By contrast, it has

been suggested that memory for emotional events is amygdala-

dependent, as emotionally influenced memory is impaired in

patients with lesions of the amygdala (Cahill et al., 1995;

Adolphs et al., 1997). Animal data suggest that emotional arousal

activates the amygdala and that such activation results in the

modulation of memory storage occurring in other brain regions

(McGaugh et al., 1996). In the case of episodic memory,

engagement of the amygdala by emotional stimuli is thought to

up-regulate responses in the hippocampus, resulting in memory

enhancement (McGaugh et al., 1996). More specifically, it has

been suggested that enhanced emotional memory is associated

with a beta-adrenergic-dependent modulation of amygdala–

hippocampal interactions (Strange and Dolan, 2004). It has long

been recognized that the effects of adrenaline on memory

performance are blocked by peripheral administration of

adrenergic antagonists (Gold and Sternberg, 1978). Importantly

however the effects of glucose administration on memory are still

observable in the presence of alpha- or beta-adrenergic receptor

blockers (Gold et al., 1986). Taken together these results

highlight the importance in further investigating the role that

glucose plays in the suggested amygdala–hippocampal interac-

tion generated by beta-adrenergic-dependent activation.

5. Conclusions

Past research has found mixed results in terms of whether

glucose has a part to play in the emotional enhancement effect.

The results of the present research have demonstrated that at

lower doses of glucose, the emotional enhancement effect

remains intact. Coupled with the finding that higher levels of

glucose impair memory for emotional material, the present

research suggests that presentation of emotional stimuli shifts

the previously observed dose–response curve for neutral

material. One important task for future research will be to

determine the dose–response relationship for the effects of

glucose administration on emotional memory.

Appendix A. Word lists as a function of study set and

valence

Set A

Set B

Neutral

Positive Negative Neutral Positive Negative

Academy

Baby Ashamed Admiral Angel Agony

Baron

Blossom Blame Apron Beach Beast

Botany

Cheerful Blood Buckle Charity Grief

Choir

Desire Cancer Carpet Comedy Coffin

Account

Feast Corpse Agency Joke Lonely

Average

Friend Burden Collar Fantasy Evil

Cloak

Calm Disease Comet Fortune Failure

Costume

Harmony Damage Duchess Laugh Filth

Hammer

Holiday Despair Envelope Freedom Gutter

Hockey

Humour Grave Fork Fun Hatred

Horse

Joy Gloom Herd Heaven Loss

Leaflet

Loyalty Manure Inch Hobby Misery

Logic

Luxury Mucus Journal Honesty Murder

Match

Peace Odour Iron Honour Pathetic

Mirror

Eager Poison Plate Kiss Poverty

Context

Happy Reptile Library Kitten Punish

Ounce

Rainbow Scream Ruler Love Shame

Ribbon

Relax Guilt Scroll Smile Slime

Shield

Romance Spider Stripe Miracle Solemn

Symbol

Saint Hurt Thumb Safety Toilet

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