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Elhaj 2013
Elhaj 2013
a r t i c l e i n f o a b s t r a c t
Article history: Unlike prospective time perception paradigms, in which participants are aware that they have to esti-
Accepted 21 June 2013 mate forthcoming time, little is known about retrospective time perception in normal aging and Alz-
Available online 18 July 2013 heimer’s disease (AD). Our paper addresses this shortcoming by comparing prospective and
retrospective time estimation in younger adults, older adults, and AD patients. In four prospective
Keywords: tasks (lasting 30 s, 60 s, 90 s, or 120 s) participants were asked to read a series of numbers and to pro-
Alzheimer’s disease vide a verbal estimation of the reading time. In four other retrospective tasks, they were not informed
Mental time travel
about time judgment until they were asked to provide a verbal estimation of four elapsed time inter-
Prospective time perception
Retrospective time perception
vals (lasting 30 s, 60 s, 90 s, or 120 s). AD participants gave shorter verbal time estimations than older
adults and younger participants did, suggesting that time is perceived to pass quickly in these patients.
For all participants, the duration of the retrospective tasks was underestimated as compared to the
prospective tasks and both estimations were shorter than the real time interval. Prospective time esti-
mation was further correlated with mental time travel, as measured with the Remember/Know para-
digm. Mental time travel was even higher correlated with retrospective time estimation. Our findings
shed light on the relationship between time perception and the ability to mentally project oneself into
time, two skills contributing to human memory functioning. Finally, time perception deficits, as
observed in AD patients, can be interpreted in terms of dramatic changes occurring in frontal lobes
and hippocampus.
Ó 2013 Elsevier Inc. All rights reserved.
1. Introduction cesses: the first to timing mechanisms, the second to general cog-
nitive mechanisms not specifically related to time, such as memory
Patients with Alzheimer’s disease (AD) exhibit great deviations (Block, 2003). The common feature between retrospective timing
from true clock time, as they tend to show significant alterations in and memory may lie in mental time travel. Mental time travel,
the judgment of time intervals (Nichelli, Venneri, Molinari, Tavani, or the ability to mentally project oneself backward in time to relive
& Grafman, 1993). Several investigations have provided support for past experiences, is the mean feature of autonoetic consciousness
this idea (Carrasco, Guillem, & Redolat, 2000; Caselli, Iaboli, & Nich- characterizing episodic recall (Tulving, 2002; Wheeler, Stuss, &
elli, 2009; Nichelli et al., 1993; Papagno, Allegra, & Cardaci, 2004; Tulving, 1997). Autonoetic consciousness, or mental time travel,
Rueda & Schmitter-Edgecombe, 2009). However, all these studies is described as a sense of a subjective experience of time, and
have been concerned by one facet of time perception, namely, pro- according to Tulving’s (2002) quote ‘‘no sense of subjective time,
spective time perception. no mental time travel’’ (p. 2). According to this assumption mental
In prospective time perception measures, participants are in- time travel, allowing episodic recall, is likely to be heavily relying
structed in advance that they have to estimate time intervals. In on retrospective time perception, or the subjective experience of
retrospective measures, on the contrary, they are not. Prospective the past.
and retrospective timing are thought to be related to different pro- Research on time perception is mainly concerned by prospec-
tive timing and only a few papers have focused on retrospective
timing in normal aging (Block, Zakay, & Hancock, 1998), and this
⇑ Corresponding author. Address: Neuropsychology and Auditory Cognition,
Department of Psychology, University of Lille 3, Domaine Universitaire du Pont
absence of studies on retrospective timing is even more striking
de Bois, BP 60149, 59653 Villeneuve d’Ascq Cedex, France. Fax: +33 3 20 41 63 24. in AD. A typical measure of prospective time perception in AD
E-mail address: mohamad.elhaj@univ-lille3.fr (M. El Haj). has been described by Rueda et al. (2009). These authors asked
0278-2626/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.bandc.2013.06.008
46 M. El Haj et al. / Brain and Cognition 83 (2013) 45–51
Table 1
Neuropsychological characteristics of participants in the three study groups.
Another participants fulfilled two retrospective (60 s and 90 s) and recognition phase. In the study phase, participants were presented
two prospective tasks (30 s and 60 s), and in the second session with a list of 12 words. These words (i.e., translated from French:
she/he performed two prospective (30 s and 120 s) and two pro- vest, domino, copper, lime, judo, celery, harp, waltz, stool, phone,
spective tasks (90 s and 120 s). The session and trial orders were fork, pen) were selected according to their frequency (Content,
randomized for each participant. Mousty, & Radeau, 1990) and consisted of two or three syllables.
Each retrospective task consisted of a different activity: decid- Their presentation was randomized in the study and the recogni-
ing whether words were abstract or concrete (30 s), filling con- tion phase. They were printed in a black, 48 Time New Roman font.
nected squares (60 s), deciding whether words were animal or and presented separately in the center of a white A4 paper sheet.
object names (90 s), or reading a text about mushroom picking Each word was presented during approximately 5 s. Participants
(120 s). All tasks were paper-and-pencil-based. Prior to each task, had to read the words aloud and try to memorize them. After an
the experimenter explained the lure purpose of the procedure interval of approximately 5 min, filled with executive/timing tasks,
(e.g., categorizing words as representing abstract or concrete a recognition task was administered. Subjects were presented the
things). He then asked the participants if they were ready to per- 12 formerly-exposed words added to 12 unrelated foils, in the
form the task. When the answer was affirmative, he gave the signal same way as in the study phase. For each word, the participants
‘‘Go’’. At the end of the corresponding time interval (30 s, 60 s, 90 s, had to decide whether it was old or new. If judged to be old, par-
or 120 s), he gave a ‘‘Stop’’ signal and immediately asked the par- ticipants gave a ‘‘Remember’’ response if they could consciously
ticipants ‘‘How many seconds did the task last?’’. recollect details about the word presentation, or they gave a
At the start of the ‘‘Go’’ signal, the experimenter activated a lap- ‘‘Know’’ response if they did not recollect specific details about
top stopwatch. At ‘Stop’’ the stopwatch was deactivated. The its presentation. When participants were not sure about their deci-
screen of the laptop was hidden from the participants’ view so that sion, they were asked to give a ‘‘Guess’’ response (for a similar pro-
she/he was not aware of timing. For the same purpose, the exper- cedures, see, Clarys, Bugaiska, Tapia, & Baudouin, 2009). There was
imenter was careful to give the ‘‘Go’’ signal and to keep working on no time limit for responses.
the laptop during all the study tasks. During the retrospective con- Prior to this task, and in order to ensure that participants under-
dition, all the participants had the same mindset. Namely, they stood the difference between the Remember and Know responses,
were instructed that their task was to complete the assignments the experimenter explained: ‘‘Imagine you recognize a person you
as accurately as possible. Another precaution that was taken to encounter. If you can remember information about him (e.g., his
minimize guessing for the real purpose of these tasks was inter- name, where and when you have met him before) then you
mixing them with neuropsychological tests, in which participants ‘‘remember’’ him. On the contrary, if you cannot remember such
were not asked to provide time estimation. information, than you ‘‘know’’ him. The same can be said about
The procedures of the retrospective condition were the same the words that you will see. If you recognize an earlier-exposed
but for four other prospective tasks (lasting 30 s, 60 s, 90 s, or word (e.g., gift) and you remember that, during its presentation,
120 s). However, here the participants were explicitly instructed you thought about a gift that you have already received, you can
that the task consisted of reading a series of numbers and to esti- provide a ‘‘Remember’’ response. If you only know that this word
mate the duration of reading. Numbers randomly ranged between was in the list without remembering more information, than we
3 and 5 digits, in view of the fact that reading numbers with less expect a ‘‘Know’’ response from you. However, if you are not sure
than 3 digits can be done in 1 s which may bias time estimation. whether you remember or know the word than you can give a
On the other hand, reading more than 5 digit numbers can be chal- ‘‘Guess’’ response. To further familiarize participants with these
lenging for AD patients. In order to prevent subvocal counting, par- instructions, they went through this procedure with four training
ticipants were asked to read numbers aloud. words (two targets, two lures) in the same way as in the later
Performance on time perception was represented by two vari- Remember/Know paradigm.
ables: mean time estimate and absolute error value. The first mea- Recognition scores for the ‘‘Remember’’ responses were calcu-
sure designates the raw score registered for each time interval. The lated as the number of correct recognition (hits/targets) minus
second measure refers to the difference between the mean time the proportion of false alarms (false alarms/lures) (for a similar
interval and the real interval, regardless of the sign (Hicks, Miller, procedure, see, Clarys et al., 2009). For instance, if a participant
& Kinsbourne, 1976). The absolute error measure was used because provided 6 ‘‘Remember’’ responses to 12 former exposed words,
Rueda et al. (2009) signal it as a sensitive indicator of time percep- his hit rate was 6/12 = .50. If the same participant provided 4
tion deficits in AD. ‘‘Remember’’ responses to the 12 lure words, hits false alarms rates
was 4/12 = .33. The recognition ‘‘Remember’’ score for this partici-
2.2.2. Remember/Know paradigm pant was .50 .33 = .17.
Mental time travel was assessed with the Remember/Know par- The same procedure was adopted for calculating the perfor-
adigm (Gardiner, 2001). This paradigm consists of a study and a mance for the ‘‘Know’’ responses. The ‘‘Guess’’ responses were
48 M. El Haj et al. / Brain and Cognition 83 (2013) 45–51
not taken into account because they were only used to enhance the Table 2
quality of the ‘‘Know’’ responses. Means and standard deviations (in parentheses) for mean time estimates and
absolute errors values in the four prospective and the four retrospective timing tasks.
Table 3 kay, 1996; Zakay & Block, 1996). According to this view, prospec-
Means and standard deviations (in parentheses) for recognition scores for ‘‘Remem- tive timing requires an attentional gate controlling pulses that
ber’’ and ‘‘Know’’ responses.
are emitted by a pacemaker. When attentional resources are solic-
Younger Older Alzheimer ited for timing, the gate allows more pulses to head to an accumu-
Remember .37 (.21) .21 (.20) .08 (.11) lator. The main function of the accumulator is to count the number
Know .17 (.19) .16 (.18) .21 (.24) of pulses, referring to the duration of an interval. When a target
interval must be reproduced, the numbers of ongoing pulses that
are counted into the accumulator are compared with previous
pulses counts, who are stored in working memory and long-term
‘‘Remember’’ responses or the ability to mentally project oneself to memory. Interesting in this account, is that the dependency of time
relive past events. perception on memory is high, both working memory and long-
Disorders of temporal processing have been extensively investi- term memory are constantly compared when producing target
gated in normal aging and, to some extent, in AD. However, few intervals. In this sense, the attentional gate model might be consid-
experiments have been carried out on retrospective time percep- ered as a theoretical cornerstone emphasizing how time percep-
tion with older adults (Block et al., 1998) and AD patients. Fried- tion and memory are overlapping. This being said, it is
man et al. (2010) recently addressed this shortcoming by interesting to illustrate the link between time perception and the
assessing prospective and retrospective time estimation with a core episodic memory component, that is, mental time travel. Next
large cohort of younger and older adults who were asked to report we will disentangle this issue.
their subjective experience of forthcoming (e.g., how fast do you Time is physically irreversible. This law can however be violated
expect the next hour to pass?) and elapsed time (e.g., how fast by mental time travel. Traveling back into the past is the hallmark
did the previous week pass for you?). Most participants reported of human being. According to Tulving (2002), the most distinguish-
experiencing time as passing quickly. Elapsed time was perceived ing feature of human memory is mental time travel, or the state of
as quicker than forthcoming time and forthcoming time was per- autonoetic consciousness permitting the episodic reliving of past
ceived as quicker than actual time. The feeling that time passes experiences. Mental time travel is further considered by Tulving
quickly did not differ between younger and older adults, except (2002) as allowing the feeling of subjective time in which events
for very long past intervals (e.g., how fast did the previous 10 years happened. By inducing the feeling of subjective time, mental time
pass for you?). The findings of Friedman et al. (2010) fit with our travel is likely to be heavily related to time perception, which may
own results, showing more underestimation of the duration of ret- explain why in our paper the ‘‘Remember’’ responses, reflecting
rospective than prospective tasks. Our findings further replicate autonoetic reliving, were significantly correlated with the perfor-
those of Friedman et al. (2010) on short time intervals (<120 s). mance on time perception. It is worth noting that no significant
In line with papers investigating time perception in AD (Carras- correlations were found between the latter performance and
co et al., 2000; Caselli et al., 2009; Nichelli et al., 1993; Papagno ‘‘Know’’ responses, reflecting a discrepancy between time percep-
et al., 2004; Rueda et al., 2009), our data point to a considerable tion and noetic consciousness, or a failure to achieve mental time
perturbation in time estimation in these patients. Our AD partici- travel.
pants gave shorter verbal time estimations than older adults and With regard to AD patients, time perception perturbations in
younger participants did, suggesting that time is perceived to pass these patients can be related to their failure to mentally travel back
quickly in AD patients. According to existing literature, the pertur- in time to relive past events. Studies of retrospective time percep-
bation of time perception in AD can be attributed to several factors, tion have shown that intervals are underestimated if fewer events
such as executive/attentional functions (Carrasco et al., 2000; Pap- are remembered (Block, 1989). Therefore, it is likely that the diffi-
agno et al., 2004) and distortions in the internal clock (Caselli et al., culty of recollecting many events from a certain interval of time
2009). Even though suggesting different explanations, this litera- leads to the impression that this interval is shorter than actual time
ture highlights the common link between the perturbation in time (for a similar suggestion, see, Friedman et al., 2010). Hence, we
estimation and memory disorders in AD. We would like to push the suggest that by leaving fewer events to be remembered, episodic
latter account a bit further, as our findings show reliable correla- decline, or mental time travel failure in AD patients, induces the
tions between time perception and the ‘‘Remember’’ reports, refer- feeling of ‘‘empty’’ time interval, and thus, the underestimation
ring to mental time travel. In the following, we will discuss the link of elapsed time.
between time perception and mental time travel, but first we Beside the cognitive processes that may underlie time percep-
would like to emphasize, at a general level, the relationship be- tion deficits in AD patients, it would be of interest to shed light
tween time perception and memory. on the neural bases of such deficits. Our correlation analyses link
The relationship between time perception and memory can be executive function to time perception, suggesting frontal involve-
understood by referring to the attentional gate model (Block & Za- ment in the latter ability. Not surprisingly, the literature suggests
Table 4
Correlation matrix for prospective/retrospective timing, Remember/Know responses, and executive measures.
1 2 3 4 5 6 7 8 9
1. Prospective timing –
2. Retrospective timing .38** –
3. Remember .36* .32* –
4. Know .23 .10 –.32* –
5. Plus–Minus .45** .40** .21 .01 –
6. Two-back .40** .52** .37** .01 .40** –
7. Stroop .53** .44** .46** .04 .64** .52** –
8. Forward span .40** .32* .40** .12 .41** .51** .57** –
9. Backward span .24 .22 .44** .07 .32* .47** .44** .40** –
*
p < .05.
**
p < .01.
50 M. El Haj et al. / Brain and Cognition 83 (2013) 45–51
a key role of frontal regions in timing mechanisms (Binkofski & One may argue that the body of literature dealing with retro-
Block, 1996; Grondin, 2010; Koch et al., 2002; Wiener & Coslett, spective timing is relatively small. Indeed, retrospective paradigms
2008). As our regression analyses show, frontal participation is present a crucial methodological challenge. After providing a retro-
highly relevant for retrospective timing. This mirrors classical neu- spective judgment, the participants are likely to suspect that fur-
ropsychological observations, reporting severe difficulties in pro- ther time judgments will be asked and the paradigm thus
spective thinking in patients with frontal lobe damage becomes prospective. Our experimental procedure has addressed
(Rosenbaum et al., 2005; Tulving, 1985). Neuroimaging data also this challenge by spacing tasks one week apart and by varying
show frontal activation in the construction of future events (Addis, the nature of the retrospective tasks (e.g., text reading and words
Wong, & Schacter, 2007). The frontal lobes seem to be highly rele- categorizing). For the same aim, the participants had the same
vant for prospective processing. Our data confirm these findings on mindset. That is, they were induced to believe that it was their task
prospective time perception. Parallel to frontal intervention, hip- to complete the assignments as accurately as possible, so that they
pocampal activation is also important. Noulhiane et al. (2007) have would not be aware, as far as possible, of the timing nature of these
investigated hippocampal involvement in time perception. The tasks. In our design, another element prevented the guessing of the
authors found that patients with left medial temporal lobe lesions real purpose of retrospective tasks, namely intermixing them with
had deficits in retrospective and prospective time perception, the administration of several of neuropsychological tests.
whereas those with right medial temporal lobe lesions were only One important limitation of our experimental set-up is its pa-
impaired in prospective time perception. These results highlight per-and-pencil character. This may have influenced the accuracy
the role of the medial temporal lobe in time perception mecha- of time measurement For instance, there may have been some dis-
nisms. It should be noted that this area is the main site for amyloid crepancy (in terms of milliseconds) between the ‘‘Go’’ and ‘‘Stop’’
deposition and therefore structurally and functionally compro- signals given by the experimenter, and his stopwatch manipula-
mised in AD (McKhann et al., 2011). After suggesting a potential tion. The paper-and-pencil procedures were adopted to simulate
neuroanatomical substrate for time perception deficits in AD pa- everyday life situations and also to avoid (our) use of sophisticated
tients, we turn to the prospective aspect of mental time travel. electronic devices to AD patients. Replications of our study should
Intuitively, mental time travel can be linked to past events. address this shortcoming by using simple electronic devices.
However, this faculty also allows forward projecting in time to In summary, AD patients seem to perceive time as passing more
pre-live possible events in the future (Berntsen & Jacobsen, quickly than older or younger adults. This perturbation can be re-
2008). Recent neuroimaging studies show that both remembering lated to failures in mental time travel. As already mentioned, Tul-
the past and projecting oneself into the future activate a common ving’s (2002) ‘‘no sense of subjective time, no mental time travel’’
neural network (Addis, Sacchetti, Ally, Budson, & Schacter, 2009). (p. 2) assertion, makes us wonder whether time perception pertur-
This conclusion is corroborated by our finding, of a significant cor- bation in AD would underlie the mental time travel difficulties of
relation between mental time travel and prospective timing, both these patients, or whether the reverse might be true.
requiring the processing of forthcoming events. This correlation
however, was slightly lower than with retrospective timing, sug-
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