REVIEW ARTICLE

REVIEW ARTICLE

Memory suppression in Alzheimer’s disease

Mohamad El Haj1

Received: 5 October 2015 / Accepted: 9 December 2015 / Published online: 23 December 2015

� Springer-Verlag Italia 2015

Abstract An important challenge for memory is the

competition between appropriate and inappropriate infor-

mation during retrieval. This competition is normally

reduced thanks to controlled inhibitory processes that

suppress irrelevant memories. In Alzheimer’s disease

(AD), compromise of suppression ability may result in

strong competition between relevant and irrelevant mem-

ories during retrieval. The present review highlights this

issue by examining studies using the directed forgetting

method in AD. This method in which participants are

typically instructed to forget no longer relevant information

is argued to reflect suppression in memory. Studies using

the directed forgetting method suggest that AD participants

experience difficulties when they are asked to suppress no

longer relevant information in working, autobiographical,

source and destination memory. Difficulties in suppressing

irrelevant information, as may be observed in AD, may

hamper memory retrieval by activating irrelevant memo-

ries at the expense of relevant ones.

Keywords Alzheimer’s disease � Directed forgetting � Inhibition � Memory � Suppression

Suppressing interference in memory

The brain’s ability to store an unlimited amount of infor-

mation creates the problem of remembering the relevant

information from a large pool of interfering memories [1,

2]. This difficulty can be exacerbated by similarity between

the interfered memories since similarity between memories

induces strong competition during retrieval, leading to

difficulties in remembering the relevant memory [3]. For

example, when trying to remember what occurred during

one’s commute back home from work, difficulties with

recall are exacerbated if the journey regularly takes place at

the same time and on the same itinerary. On the other hand,

better recall can be expected if the targeted journey

involved an unusual event such as taking the subway rather

than driving.

An important challenge for memory retrieval is the

competition between appropriate and inappropriate infor-

mation, especially when such information is bound by

common contextual, semantic or emotional features.

Without effective control mechanisms that reduce this

competition, one may fail to remember the targeted episode

as the irrelevant information is likely to be retrieved.

Thanks to inhibitory mechanisms, such failure can be

avoided since these mechanisms are in charge of sup-

pressing competition during memory retrieval [4].

Retrieval inhibition, or the ability to suppress irrelevant

information during recall, is found to be compromised in

aging. According to May and Hasher [5], older adults

experience difficulties in suppressing the activation of

irrelevant thoughts and stimuli. As a result, their memory

becomes overloaded with task-irrelevant information,

which leaves few resources for processing task-relevant

information and induces cognitive decline. This account

has been supported by studies showing that older adults are

& Mohamad El Haj el.haj@hotmail.fr

1 Univ. Lille, CNRS, CHU Lille, UMR 9193 – SCALab –

Sciences Cognitives et Sciences Affectives, Lille F-59000,

France

123

Neurol Sci (2016) 37:337–343

DOI 10.1007/s10072-015-2441-5

 

 

prone to interference in verbal working memory, visu-

ospatial working memory, and even implicit memory [5].

As for episodic memory, older adults tend to maintain

information from tasks in the past even when that infor-

mation is no longer relevant for the current task [5]. This

sustained access to prior irrelevant information has been

attributed to reduced inhibitory mechanisms, which should

optimally operate to delete old, irrelevant information. In

this view, compromised inhibitory ability as observed in

aging may disrupt memory retrieval by introducing com-

petition between relevant and irrelevant responses.

Retrieval inhibition has also been found to be compro-

mised in Alzheimer’s disease (AD) and, as this review

suggests, this compromise may result in reduced ability to

suppress irrelevant information during memory retrieval in

AD. To illustrate this issue, the main cognitive character-

istics of AD, namely, memory and inhibitory compromise,

are discussed first.

AD, memory and inhibitory compromise

AD is a neurodegenerative disease characterized by accu-

mulation of b-amyloid peptides in the gray matter of the brain, an accumulation that forms b-amyloid peptide deposits and neurofibrillary tangles composed of hyper-

phosphorylated Tau protein [6]. On a cognitive level, the

main hallmark of AD is memory decline, i.e. an impaired

ability to acquire and remember new episodic information

[6]. This impairment is thought to be mediated by neu-

ropathology in the default mode network, a network that

includes nodes at the medial and lateral prefrontal cortex,

the posteromedial parietal lobe, angular gyrus, as well as

the medial temporal lobes [7]. AD-related memory decline

is mainly observed for episodic memory or the ability to

relive specific personal events that occurred at a particular

time and place. Individuals with AD experience difficulty

in retrieving the context in which a specific episode has

occurred, a difficulty that has been attributed to decline in

source memory or the ability to remember the conditions or

features in which a memory was acquired [8–10] (for a

review, see [11]). Similar to source memory decline,

research shows difficulties in destination memory in AD

[12–16]. Destination memory, a component of the episodic

system, refers to the ability to remember the destination to

remember to whom information has previously been

imparted (e.g. ‘‘did I tell you about the promotion?’’) (for a

review, see [17]). Another feature of episodic memory

decline in AD is impaired ability to relive past events

mentally [18, 19], a decline that has been attributed to

difficulties in retrieving contextual information [12, 20].

Taken together, episodic memory decline in AD hampers

retrieval of specific personal events.

Even though episodic memory decline has been con-

sidered as the main cognitive hallmark of AD, inhibitory

decline is also common in the disease. Studies suggest

that, in comparison to older adults, individuals with AD

systematically demonstrate a large interference effect as

assessed by the Stroop task (for a review, see, [21, 22]).

This effect refers to the increase in response time that

occurs when word meaning and stimulus do not match

(e.g., the word green presented in the color blue) relative

to when they correspond. As with the Stroop effect, AD-

related inhibitory decline can be observed on tasks

requiring controlled suppression, such as the Hayling task

in which participants are required to generate an appro-

priate word as quickly as possible to complete a sentence

[23, 24]. Another feature of AD-related inhibitory decline

is the negative priming effect [21], i.e. the increased

reaction time to respond to a stimulus that had been

recently inhibited. However, unlike their performance on

tasks requiring controlled inhibition, individuals with AD

tend to show some preservation on tasks requiring auto-

matic inhibition, the latter preservation can be observed

on inhibition of return paradigms, in which AD partici-

pants and controls tend to show similar reaction times to

detect a target if it appears in a location where it was

previously shown (for a review, see [21]). Dissociation

between controlled and automatic inhibitory performance

in AD fits with the theoretical model of Harnishfeger [25]

who made a distinction between effortful inhibitory con-

trol, which corresponds to suppression of the information

considered as irrelevant for the ongoing task, and auto-

matic interference from distracting. Besides being

observed in AD, compromise of controlled inhibition has

been observed in individuals with mild cognitive

impairment on the Stroop task [26, 27], the Hayling task

[28], and the Flanker task (a task on which participants

have to respond to a central target flanked by distractors)

[29]. Besides being associated with impaired frontal

activation, inhibitory compromise in mild cognitive

impairment are considered as a risk factor for the devel-

opment of AD [30]. In a related vein, Belanger et al. [27]

suggested that inhibitory compromise, as observed in mild

cognitive impairment, may develop well before cognitive

symptoms reach significant levels in AD.

Altogether, there is evidence to suggest a decline in

controlled inhibition or mechanisms allowing voluntary

suppression of irrelevant information in AD. This decline

can also be extended to controlled inhibition in memory, an

assumption that is supported by findings from studies using

the directed forgetting task.

338 Neurol Sci (2016) 37:337–343

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AD and suppression in memory, the directed

forgetting task

Resistance to interference in memory can be assessed with

the directed forgetting task. In its conventional configura-

tion, this task requires the processing of two lists of words

(i.e., List 1 ? List 2) [4]. Subjects are typically instructed

to retain the words in List 1, after which they are asked

either to continue remembering or to forget the words in it.

Subsequently, they are instructed to retain the words in List

2. Finally, in a recall test, they are asked to remember all of

the words in both lists, regardless of the intermediary forget

or remember instructions. One main effect of the directed

forgetting method is the observation that participants with

the forget instruction tend to show poorer memory for the

items in List 1 than the remember participants. This effect

has been attributed to retrieval inhibition, whereby the

forget instruction induces a suppression of the List 1 words,

making them less accessible during retrieval [4]. The forget

instruction also reduces the proactive interference of these

words in List 2, thereby improving retrieval of List 2 in the

‘‘forget’’ participants [4]. More precisely, the suppression

effect of the forget instruction reduces the accessibility of

information for retrieval by deactivating the retrieval route

between the irrelevant information and the current cue

[31]. In other words, the suppression effect reflects route

deactivation rather than deletion of the irrelevant infor-

mation, an assumption supported by research showing that

recognition tests can reactivate to-be-forgotten items [4,

32].

A variant of the directed forgetting method is the

‘‘word’’ procedure in which the forget or remember

instruction is provided after the presentation of each word

rather than after List 1. However, both the list and word

procedures are thought to reflect intentional forgetting in

which the accessibility of irrelevant out-of-date informa-

tion is reduced and retrieval of relevant information is

selectively enhanced [33]. Both the list and word methods

have also been used in research assessing ability of

individuals with AD to suppress irrelevant information in

memory. In this area of research, one study administered a

directed forgetting working memory task by exposing AD

participants to two trigrams of three consonants each [24].

A ‘‘to be forgotten’’ indication followed the second tri-

gram, prompting participants to forget the trigram as they

would not be required to recall it later. Immediately after

the presentation of the trigrams, an interpolated activity

took place, consisting of reading strings of numbers aloud.

Afterwards, participants were asked to remember the

three letters of the trigrams, regardless of the ‘‘forget’’

instruction. Results showed difficulties in AD participants

to suppress the to-be-forgotten items from working

memory.

Difficulties to suppress irrelevant information from

memory in AD have also been observed for autobio-

graphical memory. This memory, or memory of personal

experiences and facts about the self, has been found to be

compromised in AD [19, 34–42]. One study assessed

autobiographical suppression by asking AD participants to

generate personal events (i.e., List 1). Then half of the

participants were told that these memories were no longer

relevant to the experiment (i.e., forget participants),

whereas the other half were asked to keep these memories

in mind (i.e., remember participants) [43]. Subsequently,

all the participants were instructed to generate other per-

sonal events (i.e., List 2) and in a subsequent recall test,

they were instructed to recall all the memories regardless of

the previously given forget or remember instructions (i.e.,

List 1 ? List 2). The results showed no effect of the forget

instruction; in other words, similar recall performances for

List 1 were observed in both the remember and the forget

AD participants. The absence of directed forgetting effect

was attributed by the authors to an impairment of autobi-

ographical memory suppression ability in AD.

Another insight into memory suppression in AD comes

from a study assessing directed forgetting in source

memory [44]. In this study, participants were instructed to

remember the source of presentation of items that were

presented by an experimenter with either a black-gloved

hand or a white-gloved hand (i.e., List 1). Afterwards, half

of the participants were asked to forget the source of List 1,

whereas the other half were asked to keep it in mind.

Subsequently, all the participants were asked to retain the

source of presentation of a second List of items (i.e., List 2)

and in a later recall test, they were asked to remember the

source of presentation of the items in List 1 and List 2,

regardless of the forget or remember instructions. These

procedures showed no effect of the forget instruction, as no

differences were observed between the remember and the

forget AD participants on retrieving the sources of List 1

items. Similar findings were observed in a study assessing

directed forgetting in destination memory [45]. In that

study, AD participants were asked to tell proverbs to

celebrities (i.e., List 1); then half of the participants were

asked to forget the destinations whereas the other half were

asked to keep them in mind. After telling other proverbs to

other celebrities (i.e., List 2), participants were asked to

remember the destinations of the List 1 and List 2,

regardless of the forget or remember instructions. These

procedures showed similar destination memory in the for-

get and remember AD participants, i.e. AD participants

showed difficulties in suppressing irrelevant information in

destination memory.

Taken together, empirical evidence suggests that AD

participants experience difficulties when they are asked to

suppress no longer relevant information in working,

Neurol Sci (2016) 37:337–343 339

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autobiographical, source, and destination memory [24, 43–

45]. The compromise of memory suppression ability in AD

can be better understood by highlighting the neural basis of

this ability.

AD and suppression in memory: neural basis

With regard to memory processing in the directed forget-

ting method, a study observed greater activity in the

anterior cingulate (BA 32), the left inferior prefrontal

cortex (BA 9), and medial superior frontal gyrus (BA 6) for

to-be-remembered than for to-be-forgotten information at

encoding [46]. The same study also observed greater

activity in the left parahippocampal gyrus and right supe-

rior parietal gyrus (BA 7) for remembered than for for-

gotten information. These findings suggest that activity in

the ventral prefrontal and superior frontal regions is asso-

ciated with encoding effort in the directed forgetting

method, whereas the medial temporal and superior parietal

areas are involved in the success of encoding. Mirroring

this assumption, a study found that successful encoding and

retrieval of to-be-remembered information engaged the

hippocampus, the entorhinal cortex, the anterior medial

prefrontal cortex, the left inferior parietal cortex, the pos-

terior cingulate cortex and the precuneus, a network that is

well known to support associative encoding and retrieval

processes in episodic memory. With regard to suppression

processes in the directed forgetting method, a body of lit-

erature supports the role of the right prefrontal cortex in

inhibition of to-be-forgotten information [47, 48].

The neural basis of memory suppression in normal aging

was assessed in a study with the directed forgetting method

[49]. This study showed an increase in the recruitment of

frontal inhibitory control regions, especially the right

superior prefrontal cortex, but high activity in the parietal

cortex during intentional forgetting in healthy older adults.

According to the authors, the parietal activity may reflect

age-related compensation in older adults who show a

reduction in frontally mediated inhibition. Since the pari-

etal lobes are affected by the neuropathology of AD [50],

these inhibitory compensation mechanisms are likely to be

compromised, leaving individuals with AD with poor

suppression ability. Altogether, decline in both the right

prefrontal cortex and parietal cortex may underlie diffi-

culties in suppressing irrelevant information in memory, as

may be observed in AD.

Discussion and conclusion

Successful memory functioning depends on the intentional

ability to encode relevant information and to forget irrel-

evant information. AD-related memory compromise has

been widely attributed to difficulties in encoding and/or

general loss of available memories. The present review

contributes to understanding memory decline in AD by

highlighting difficulties in suppression of irrelevant mem-

ories during retrieval. With age and the passage of time,

memories and personal experiences tend to be more similar

than specific [36]. This similarity is likely to exacerbate

retrieval of a tar

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