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University of Lübeck, Department of Neuroendocrinology, D-23538 Lübeck, Germany
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ABSTRACT |
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 TOP ABSTRACT ResultsDiscussionMethodsREFERENCES |
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;
Rugg and Yonelinas 2003). One
refers to a conscious or explicit process of recollection, where the person
initially searches for qualitative information about the context in which the
event to be remembered took place. The other process refers to the experience
of familiarity, induced automatically or implicitly at a reoccurrence of an
event, and can emerge in the absence of any conscious knowledge about the
context in which the event originally occurred. The two forms of memory
involved in recognition can be separated and show different sensitivity to
experimental manipulations. For example, elaborated encoding of stimuli and
their context facilitates explicit recollection, but leaves judgments of
familiarity at later recognition tasks rather unaffected
(Yonelinas 2002). Explicit
recollection and familiarity-based implicit processes of recognition are
probably supported by distinct neuronal systems. Studies in brain-lesioned
patients indicate that the hippocampus is critical for conscious recollection,
whereas this seems not to be the case for familiarity-based judgments
(Manns and Squire 2001;
Yonelinas et al. 2002).
Correspondingly, studies using functional magnetic-resonance imaging have
shown that the hippocampus is more active when recognition is based on
recollection rather than on familiarity
(Cansino et al. 2002;
Dobbins et al. 2003). Here, we
were interested in whether these two forms of recognition memory are
differentially affected by sleep.
Sleep is considered to be a brain state, optimizing the consolidation of
memories (Maquet 2001;
Stickgold et al. 2001).
Further, the consolidation of different types of memory seems to be tied to
different sleep stages (Born and Gais
2003). In humans, sleep in the early part of the night, dominated
by extensive epochs of slow wave sleep (SWS), has been found to enhance, in
particular, declarative memories, which refer to episodic and semantic memory
and essentially rely on the hippocampal formation
(Fowler et al. 1973; Plihal
and Born 1997,
1999). This effect has been
related to a higher proportion of SWS as compared with rapid eye movement
(REM) sleep during early sleep, as well as to accompanying low levels of
cholinergic activity in the hippocampus
(Hasselmo 1999;
Gais and Born 2004). On the
other hand, for nondeclarative forms of memory, such as priming, which is
considered an implicit form of memory and procedural memory that refers to
sensory motor skills, and among others, strongly relies on cortico-striatal
circuitry, a greater benefit has been found after periods of late nocturnal
sleep (Plihal and Born 1997,
1999;
Wagner et al. 2003). This late
period of nocturnal sleep is characterized by high amounts of REM sleep, and
contains little SWS. While not independent of SWS, procedural memory thus
appears to be particularly strengthened by REM sleep-related mechanisms
(Gais et al. 2000;
Stickgold et al. 2000;
Fischer et al. 2002).
So far, most of the studies examining the effects of sleep on memory
consolidation in different memory systems used different tasks for this
comparison. During the acquisition of task stimuli, both explicit and implicit
memories are developed in parallel
(Tulving et al. 1999;
Willingham and Goedert-Eschmann
1999). In order to separate these two forms of memory at later
retrieval testing, a number of recognition tasks have been developed that
offer the opportunity to access the two memory systems in the framework of the
same task. The process-dissociation procedure by Jacoby
(1991) is one such approach
that separates explicit recollection from implicit familiarity-based use of
memory during recognition. The procedure provides a mathematical approach for
the calculation of estimates of explicit and implicit memory in recognition
tasks. The contribution of explicit recollection to recognition is estimated
primarily on the basis of the subject's responses, indicating that he/she
correctly identifies where and when a previously encountered stimulus occurred
(e.g., a word is correctly classified as belonging to a certain study list).
The use of familiarity-based implicit memory is estimated as the conditional
probability of correctly recognizing an item as one that has been previously
seen, given it was not recollected (see Methods for a detailed description).
Both estimates of recollection and familiarity-based memory have been found to
vary statistically independently under different experimental conditions
(Yonelinas 2002).
The purpose of the current study was to compare influences of early SWS-rich periods of retention sleep with late REM sleep-rich periods of retention sleep on estimates of explicit and implicit memory in a word-recognition paradigm, using the process-dissociation procedure. Based on previous studies showing that declarative memory (hippocampus-dependent) improves, in particular from SWS, we expected explicit recollection (also hippocampus-dependent) to benefit primarily from SWS as well. Moreover, explicit hippocampus-dependent memory was expected to benefit, particularly when recollection is based on a more elaborate use of contextual features (i.e., when a word at recognition testing is presented in the same font as at acquisition, as compared with a presentation in a different font). On the other hand, familiarity-based implicit recognition, being a nondeclarative type of memory, was expected to benefit, in particular, from REM-sleep rich periods of sleep. Participants had to learn two lists of words and they also had to memorize which list each word belonged to. The words were presented in two different fonts, which changed in half of the words at recognition testing (contextual congruency manipulation). Learning was followed by a 3-h retention interval filled with either SWS-rich sleep or REM-rich sleep, and recognition was tested 15 min after sleep. In a control group, the 3-h retention intervals were spent awake. Saliva cortisol, measured to control for possible confounding effects of glucocorticoid release on memory, was sampled before and after the retention intervals.
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Results |
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TOPABSTRACTResultsDiscussionMethodsREFERENCES |
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Table 1 summarizes polysomnographic results for the early and late-night retention intervals and associated concentrations of cortisol. Total sleep time, as well as the percentages of wakefulness, stage 1 sleep (S1), and stage 2 sleep (S2), did not differ significantly from each other [F(1,20) = 0.14, 2.52, 2.51, 1.44, respectively, P > 0.13]. Percentages of SWS and REM sleep exhibited the typical and highly robust differences, with the percentage of SWS being almost four times higher in the early than late-night retention sleep, whereas the percentage of REM sleep was almost three times higher in the late-night retention sleep [F(1,20) = 88.6, P < 0.001, and F(1,20) = 45.69, P < 0.001, respectively]. Sleep prior to learning in the late night (not included in Table 1) did not differ between the sleep and the wake group. The respective values for the sleep and wake group were as follows: total sleep time, 196.21 ± 5.49 versus 195.91 ± 5.73 min; S1, 6.96 ± 1.82 versus 6.30 ± 1.91%; S2, 41.81 ± 2.96 versus 45.28 ± 3.09%; SWS, 37.78 ± 4.19 versus 34.59 ± 4.38%; REM sleep, 10.18 ± 1.90 versus 10.67 ± 1.98%, (P > 0.15, for all comparisons).
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As expected, saliva cortisol values indicated significantly lower cortisol concentrations during the early than during late-night retention intervals [F(1,21) = 23.07, P < 0.001] (Table 1), but the levels did not differ between the sleep and wake groups, [P > 0.12, for all comparisons].
Recognition performance
Immediate recognition testing on a number of recognition tasks at learning, introduced as a control for performance differences during the learning phase, revealed an overall low performance, which, however, was clearly better than chance (P < 0.01). There were no significant differences between the early and late-night conditions, as well as between the sleep and wake groups in this control task. Explicit recollection scores at this task were 0.22 ± 0.07 for the early sleep condition, 0.24 ± 0.07 for the early wake condition, 0.24 ± 0.06 for the late sleep condition, and 0.19 ± 0.06 for the late wake condition (P > 0.60 for all comparisons). The respective values for familiarity-based judgements were 0.33 ± 0.04, 0.32 ± 0.05, 0.37 ± 0.03, and 0.35 ± 0.03 (P > 0.34 for all comparisons).
Recognition testing after the retention interval on the word lists revealed distinct differences, depending on the type of memory as well as on the type of retention interval (Table 2A). Explicit recollection was generally enhanced after retention intervals of sleep in comparison to wake intervals [main effect for sleep/wake manipulation, F(1,22) = 4.33, P < 0.05]. The enhancing effect of sleep on explicit memory was particularly pronounced after early-night retention sleep and especially for the context congruent words (Fig. 1A), as revealed by the significant threeway "sleep/wake" x "night-half" x "context congruency" interaction [F(1,22) = 4.29, P = 0.05]. No other effect approached significance [F(1,22) < 2.74, P > 0.12, for all comparisons]. The pattern of the three-way interaction was also confirmed in a post-hoc analysis. First, one-way ANOVAs showed that the sleep and wake group differed primarily in recollection of congruent words in the early night [F(1,11) = 7.50, P < 0.05]. In the late night, this effect failed to reach the 5% level of significance [F(1,11) = 3.18, P < 0.10]. Additionally, for the incongruent words, the difference between the sleep and wake group did not approach significance either in the early-retention interval [F(1,11) = 0.95, P > 0.34] or in the late-night retention interval [F(1,11) = 2.80, P > 0.11]. Furthermore, two-way ANOVAs performed separately for the sleep and wake group showed a significant effect for the "night-half" x "context congruency" interaction [F(1,11) = 5.09, P < 0.05] in the sleep group. The direction of this effect was further investigated by paired t-tests, which confirmed the enhanced explicit recollection of words presented in congruent context in the early-night retention sleep over both (1) the same words in the late-night retention sleep (P < 0.05), and (2) the words presented in incongruent context in the early-night retention sleep (P < 0.05, Fig. 1A). The difference between words presented in congruent and incongruent context in the late-night retention sleep, or between the incongruent words in the early and late-night retention sleep, did not approach significance (P > 0.59 for both comparisons). The analyses in the wake group showed no significant effects [F(1,11) < 0.54, P > 0.48 for all comparisons].
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For the familiarity-based recognition scores, congruent words were slightly better remembered than the incongruent words [F(1,22) = 3.10, P < 0.10] (Table 2; Fig. 1B). However, there was no general effect of sleep on familiarity-based recognition scores [F(1,22) = 0.13, P > 0.70], and these scores also did not differ between early and late-night retention intervals [F(1,22) > 2.07, P > 0.17].
A supplemental control analysis showed no effect of the "sleep/wake" or the "night-half" manipulation on the ability to identify the new words. The percentages for correctly identified new words were well above chance and did not differ from each other (sleep group in the early night 78.68 ± 5.48%, in the late night 78.20 ± 5.30%, wake group in the early night 75.66 ± 5.48%, in the late night 77.47 ± 5.30%, F(1,22) < 0.13, P > 0.70 for all comparisons). Moreover, control analyses did not indicate any significant correlations between scores of recollection and familiarity (P > 0.14). The respective coefficients were in the sleep group r = 0.06 (early retention interval—congruent words), r = -0.17 (early retention interval—incongruent words), r = -0.10 (late retention interval—congruent words), and r = 0.01 (late retention interval—incongruent words). In the wake group, the respective coefficients were r = -0.38, -0.38, -0.40, and -0.46, respectively.
Questionnaires
After having completed the word-recognition task at retrieval, subjects rated their current feelings of activation, drowsiness, tiredness, motivation, and concentration. In general, all variables, including tiredness (early sleep, 3.58 ± 0.28 vs. early wake, 3.92 ± 0.28, late sleep, 3.50 ± 0.28 vs. late wake, 4.00 ± 0.28) and subjective concentration (early sleep, 2.83 ± 0.27 vs. early wake, 2.42 ± 0.27, late sleep, 2.75 ± 0.27 vs. late wake, 2.67 ± 0.27), were closely comparable for both groups for both night intervals at retrieval testing (P > 0.13, for all comparisons). None of the participants had noticed the change in fonts in the recognition task, although some (two in the sleep group and one in the wake group) said that they thought something was "strange" with some words.
Control experiments on retrieval function
In light of evidence that performance on tasks relying on the frontal
cortex are highly sensitive to an impairing influence of sleep deprivation
(Harrison and Horne 1998;
Drummond et al. 2000), and
since explicit recollection also involves this brain region
(Fletcher and Henson 2001),
additional experiments in two separate groups of subjects (n = 22,
age 20–35 yr) examined whether a 3-h period of early wakefulness induced
any sleep deficit that would account for the inferior explicit recollection
seen in this condition in the main study. A phonetic fluency task used to
assess fluency of word retrieval from long-term memory
(Aschenbrenner et al. 2000; a
German adaptation of a test originally developed by Christensen and Guilford
[1958]) required the subject to
write down as many words as possible within 2 min, starting with a certain
letter ("p", "m"). The task was presented before and
after 3-h periods of sleep (n = 12) and wakefulness (n = 10)
during the early night, scheduled in the same way as in the main experiments.
Also, the digit-span test (forward and backward) was presented to assess
general prefrontal-mediated working memory function. Retrieval fluency after
the 3-h periods did not differ between the sleep and wake groups
[F(1,20) < 1.40, P > 0.25 for all
comparisons], and was, on average, even slightly higher in the wake group
(Table 3). Also, digit-span
test performance was closely comparable between the groups
[F(1,20) < 1.60, P > 0.22 for relevant
comparisons] and [F(1,20) < 2.18, P > 0.16
for all comparisons] for both forward and backward, respectively
(Table 3).
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Discussion |
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TOPABSTRACTResultsDiscussionMethodsREFERENCES |
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) to separate
effects of sleep on explicit and implicit memory consolidation. Compared with
retention periods of wakefulness, sleep generally enhanced measures of
explicit recollection. This effect was particularly pronounced during early
sleep periods dominated by SWS, and when, at recognition testing, the words
were presented in the same font, as at learning before sleep. Interestingly,
familiarity-based implicit memory did not benefit from sleep. There, only a
small benefit was observed for contextual congruency (i.e., when the font of
the words was kept the same at retrieval as at learning), which, however, was
independent of sleep. As a whole, these results speak for a greater
sensitivity of explicit than implicit memory formation to the enhancing
effects of sleep that might be particularly linked to SWS. The effects of sleep observed cannot be attributed to circadian variations, since changes in memory across periods of early and late sleep were compared with periods of wakefulness in the same phase of the circadian rhythm. This is also supported by the fact that saliva cortisol concentrations were closely comparable between the sleep and wake conditions, and at the same time, showed the normal circadian variation. Likewise, self ratings of fatigue and concentration did not differ between the groups at learning and retrieval testing. In addition, although at an overall low-performance level, immediate recognition (of numbers) tested at learning did not differ either between sleep and wake groups or within each of these groups when tested in the evening or at night.
The results of our control experiment also argue against the view that the
wake periods of about 3 h during the early night induced any substantial
effects arising from sleep deprivation. This experiment was conducted on the
background of evidence that sleep deprivation (for 36 h) has an impairing
influence, particularly on prefrontal-mediated retrieval functions
(Harrison and Horne 1998;
Drummond et al. 2000). Our
results show that word retrieval from long-term memory, as well as
working-memory functions, remained unaffected by a 3-h sleep deprivation in
the early night as compared with early sleep. With regard to our finding of
enhanced explicit recollection of context congruent words after early
retention sleep, it should be emphasized that this effect was not only
significant in comparison with early wakefulness, but also in comparison with
late retention sleep (Fig.
1).
A benefit of the process-dissociation procedure is that within the same task, the effects of sleep on explicit and implicit memory can be assessed simultaneously. This is important, since earlier studies indicating a differential sensitivity to the effect of sleep and sleep stages depending on the type of memory system relied mostly on completely different tasks to assess the respective memory systems. Using the same task to test explicit and implicit memory rules out that the differential effects of sleep observed here were due to some nonspecific task characteristics not related to any of the two memory systems.
Our finding of a distinctly more pronounced improvement of explicit
recollection after retention periods of early rather than late-night sleep
agree with a number of previous studies, indicating a particular benefit of
hippocampus-dependent declarative memory from just this early period of
SWS-rich sleep (Born and Gais
2003). It has been proposed that the enhancing effect of early
sleep on hippocampus-dependent memories relies on a reactivation of the newly
acquired memory representations in hippocampal neuronal populations that
occurs predominantly during SWS (Hasselmo
and Wyble 1997; Buzsáki
1998; McNaughton et al.
2003). Such processes could explain a facilitated access at later
explicit recollection of these memories. An involvement of the hippocampal
formation in the sleep-associated memory process of interest is further
supported by our finding that explicit memory enhancement during early sleep
was most robust when the words were presented in the same context as during
encoding. Several previous studies have consistently shown that one essential
hippocampal function serves to bind encoded information with contextual cues,
even in the absence of awareness for these contextual cues (Henke et al.
1999,
2003;
Stark and Squire 2001). Thus,
a contextual dependence of the explicit memory enhancement during early sleep
seems to be in agreement with the notion that this type of sleep particularly
benefits hippocampus-dependent types of memory.
Contrary to our expectation, familiarity-based measurements of implicit
memory were not enhanced by sleep, either during the early part or during the
late part of the night. While this negative finding agrees with a recent study
testing effects of early and late sleep on performance in a
"remember/know" paradigm
(Rauchs et al. 2004), it
appears to contrast with a number of foregoing studies indicating that various
forms of nondeclarative memory, such as the procedural memory for skills
(Plihal and Born 1997) and the
priming of words and faces (Plihal and
Born 1999; Wagner et al.
2003) benefit in particular from REM sleep-rich periods of sleep.
Those studies led us to suppose a generalized benefit for REM sleep-rich
periods of sleep for nondeclarative memories not depending on hippocampal
function. However, it is not unlikely that familiarity, priming and procedural
tasks, apart from relying on nonhippocampal brain regions, actually represent
different types of memory (Wagner et al.
1998; Drummond et al.
2000, Stark and Squire
2000; Rugg and Yonelinas
2003), and thus, may differ in other qualities that are crucial to
their sensitivity to the enhancing effect of sleep.
In addition, there are hints that memory based on familiarity judgments
decreases at a more rapid rate than recollection based memories
(Yonelinas and Levy 2002). It
could be that in our experiment, the time spent between encoding and retrieval
was too long for any difference in familiarity-based judgments to remain
detectable. However, this possibility seems unlikely according to the
background of evidence that when relatively long time intervals in the order
of hours (and even days) are tested as in the present study, decline rates of
familiarity were found not to be greater than those for measures of
recollection (Hockley and Consoli
1999).
The absence of effects of retention sleep on familiarity-based recognition
could have its origin also in more general conceptual implications of the
process-dissociation procedure that has not remained without criticism
(Richardson-Klavehn et al.
2002; Mintzer et al.
2003). In particular, it is still under debate whether
recollection and familiarity indeed are linked to two different memory
systems, or whether they refer to different retrieval mechanisms at recall to
gain access to the same memory trace
(Ratcliff et al. 1995). Along
this line of reasoning, the failure to find effects on familiarity-based
implicit recognition scores here may just reflect a less-efficient access to
the memory trace of interest via this type of recognition judgement. Related
to this, from the perspective of the process-dissociation procedure, the
contextual effect that we observed in our study on explicit memory was also
not expected. This is because manipulations of the perceptual features of
stimuli in general are considered to affect only implicit forms of memory such
as priming (Fleischman et al.
1997). Diverging from this view, our findings suggest that
nonconsciously attended information influenced explicit memory. This raises
the problem of contamination, i.e., the possibility of partial overlaps
between explicit and implicit memory
(Butler and Berry 2001), and
thus implies a violation of the independence assumption of the
process-dissociation procedure, which regards explicit recollection and
familiarity-based implicit recognition as entirely independent from each
other. Accordingly, the pattern of our results brings into question the notion
that measures of implicit and explicit memory reflect memory systems as
different and independent, as assumed by the process-dissociation procedure,
although (post-hoc) linear correlation analyses of our data assured that
scores of recollection and familiarity-based judgments were independent in a
statistical sense. Adopting a perspective beyond the framework of the
process-dissociation procedure, the present data would indicate that
recognition of old words remains uninfluenced by sleep, but that after early
sleep, the subject's ability to identify the correct list for congruent words
is enhanced. This view appears to be in line with findings from a recent study
that early SWS-rich sleep enhances memory for temporal context information in
an episodic memory task (Rauchs et al.
2004).
Our data of a selective enhancement of signs of explicit recollection by
retention sleep are in line with previous reports of a preferential
enhancement of explicitly guided memory during sleep
(Robertson et al. 2004). Those
studies were based on serial reaction time tasks (SRTT), and showed that
offline improvement in task performance that occurred selectively across
retention periods of sleep required that subjects were aware of the sequence
of the task they trained for before sleep. Recent experiments indicated that
the hippocampus and closely connected temporal lobe structures can be involved
in both explicit and implicit learning on the SRTT
(Schendan et al. 2003). Thus,
activation of prefrontal cortical circuitry, including the dorsolateral and
ventrolateral prefrontal cortex, seems to be more relevant to the distinction
between explicit and implicit processes on that task
(Fletcher and Henson 2001;
McIntosh et al. 2003), which
may apply to the recognition task used here as well. Notably, some evidence
exists that slow oscillatory EEG activity dominating human SWS reflects
processes of cortical reorganization, especially in the prefrontal cortex,
that could be linked to explicit processing (such as thinking) taking place
during the wake phase (Anderson and Horne
2003a,b;
Steriade and Timofeev 2003).
From this perspective, use-dependent changes in prefrontal cortical circuitry
during explicit processing in the wake phase could be a starting point for
plastic changes underlying memory formation during SWS-rich sleep
(Sejnowski and Destexhe 2000;
Huber et al. 2004;
Mölle et al. 2004).
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Methods |
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Twenty-four healthy, nonsmoking, drug-free subjects with no prior history of sleep disturbances participated in the main experiments and received a money reward for their participation (12 males; mean age 23.0 yr, range 19–28 yr). Subjects orally reported to habitually sleep 7–9 h per night, and not to have had any major disruption of the sleep-wake cycle during the 6 wk before experimentation. Subjects were acclimated to the experimental sleep condition by spending an adaptation night in the sleep laboratory, including the placement of electrodes. On the two experimental days, the participants were instructed to get up at 7:00 h and not to take any naps during the day. They were instructed not to ingest alcohol or (after 15.00 h) caffeine containing drinks on these days. The study was approved by the local ethics committee. All participants gave written informed consent before participation.
Design and procedure
The experiment included two groups, a sleep group and a wake control group
(six men and six women in each group). Each group was examined in an early and
a late-night retention interval, with the order of the conditions balanced
across subjects. The two experimental nights were separated by an interval of
at least 1 wk. In the early retention condition, participants reported to the
laboratory at 21:30 h. After electrodes were applied for standard
polysomnography (only in the sleep group), participants performed in the
recognition task from 22:15–23:00 h (learning phase). In the sleep
group, the participants went to bed afterward. Three hours after sleep onset,
participants were awakened as soon as S1 or S2 sleep occurred. Awakening from
SWS or REM sleep was avoided, as this can decrease subsequent retrieval
performance (Stones 1977).
Fifteen minutes after awakening, retrieval in the recognition task was tested.
The participants in the wake group remained awake during the 3-h retention
interval between initial learning and retrieval testing. During this time,
they watched movies, played (computer) games, or engaged in conversations with
the experimenter.
In the late retention condition, participants came to the lab at 22:30 h. After electrodes for sleep recordings were applied, subjects went to bed and were awakened 3 h after sleep onset, as soon as sleep S1 or S2 occurred. Fifteen minutes later, the learning phase took place (2:15–3:00 h). Thereafter, participants in the sleep group went back to bed and slept for another 3 h. Again, 15 min after awakening, retrieval was tested (6:15–7:00 h). As in the early retention condition, the participants in the wake group stayed awake for 3 h after learning.
After having performed the recognition task, participants rated their current feelings of activation, drowsiness, tiredness, motivation, and concentration on five-point rating scales. Saliva cortisol was sampled before and after the retention intervals. (Results from additional samples taken before and after testing did not add any relevant information, and hence, are not reported here). At the end of the entire experiment, the participants were asked whether they had noticed the change in fonts that had taken place in some words during the recognition task.
Task materials
The words of the recognition task were selected from the Toronto word pool and translated to German. Of the 306 words selected, 18 words were used as buffer words, the remaining 288 were divided into six lists (each 48 words) balanced for imagery, frequency, and concreteness. Three lists were used for each retention interval. Two served as study lists and one served as a novel one, the words of which were presented only during recognition. The words were presented using WespXP 1.98 (freeware from the Department of Psychology at the University of Amsterdam) on a 17-inch monitor, screen area was 1024 by 864 pixels using the 16-bit color mode, refresh rate was set on 75 Hz. Two true-type (.ttf) windows-compatible fonts (font size 48) able to express special characters were used to present the words (i.e., "tsp tonight 1.ttf" and "tsp mcis 2.ttf").
Recognition task
Two lists of words were presented at learning, each starting with three buffer words, followed by 48 study words. All words were presented randomly, one at a time, on a computer screen in front of the subject. The words were presented in white on a black background for 4.5 sec with an interval of 1 sec between each word. Half of the words were presented in one font and the other half in the other. The subjects were instructed to memorize the words and also to memorize which of the two lists each word belonged to. They were told that some words would be harder to read than others (although this was not the case) by presenting them in different fonts.
During recognition testing after the retention interval, a list of words
was presented that started with nine buffer words (three from each study list
plus three new ones), followed by 144 test words. These test words included,
in random order, all words from the two study lists and, in addition, 48 new
words. Half of the words from each study list were presented in their original
font ("congruent" word presentation), while the other half of the
words were presented in the other font, i.e., changed from "tsp mcis
2" to "tsp tonight 1" and vice versa
("incongruent" words). Subjects were asked to respond to each word
with their right hand by pressing one of four buttons on a box within 3.5 sec.
They were instructed to press button 1 or button 2 (from left to right) if
they remembered that the word belonged to either the first or the second list,
respectively. Button 3 was to be pressed when the word was new to them and
button 4 when the subject knew he/she had seen the word during acquisition,
but could not remember which list it belonged to. The 3.5-sec response
interval gave the subject ample time for the decisions, which is also
supported by the fact that the recollection scores obtained here overall
resembled those obtained under conditions of unlimited response time in
previous studies (Yonelinas and Jacoby
1996).
To control for possible differences in encoding levels during the learning phase, the presentation of the study word list was preceded by a similar recognition task using three-digit numbers as stimuli instead of words and, most important, with recognition tested immediately after acquisition. Here, each list consisted of only eight numbers with one buffer number. In the recognition test, one buffer number and eight new numbers were added, and the font did not change in this task.
Data analysis
Estimates of recollection and familiarity were derived from scores of
inclusion and exclusion, according to the process-dissociation procedure as
has been described for the word-list discrimination task
(Yonelinas and Jacoby 1996).
The inclusion score defines the amount of old words for which the subject
correctly remembered the list they belonged to (buttons 1 and 2) plus the old
words, which the subject knew he/she had seen during acquisition, but did not
remember their list membership any more (button 4). This results in: inclusion
= (true positive list1) + (true positive list2) + (true positive button 4).
Exclusion is defined as the amount of old words that were falsely remembered
to belong to a certain list, i.e., the words from list 1 that were classified
under list 2 and vice versa (buttons 1 and 2 again), plus again the old words,
of which the subject knew he/she had seen during acquisition, but did not
remember their list membership any more (button 4), resulting, respectively,
in: exclusion = (false positive list1) + (false positive list2) + (true
positive button 4). Inclusion and exclusion scores are then filled in the
known formulas for recollection and familiarity as provided by Jacoby's
process-dissociation procedure being "recollection = inclusion -
exclusion" and "familiarity = exclusion/(1 - recollection)",
respectively (Yonelinas and Jacoby
1996). False alarms, delayed responses (>3.5 sec), and buffer
words were not included in the calculations.
The procedure used here differs from the original process-dissociation
procedure used by Yonelinas and Jacoby
(1996), in that it was based
on four, rather than two different button press responses, requiring a
slightly different behavioral strategy. However, the principles of the process
dissociation in our procedure remained the same as in the original procedure.
In the original procedure, each of the two buttons are used to indicate a
combination of two different decisions. Thus, one is used to indicate that a
word is remembered to belong to one of the lists, and additionally, to
indicate that a word is "known" when the list membership cannot be
remembered. The other button is likewise used to indicate that a word is
remembered to belong to the respective other list and additionally to indicate
whether a word is "new". Because we wanted to avoid this complex
double mapping of response decisions, participants had four buttons in our
study, one for every type of response (i.e., two buttons to indicate a word's
list membership, and two for "know" and "new"
responses, respectively). The calculation of the estimates for explicit
recollection and implicit familiarity are not affected by this change, with
the inclusion score as in the original procedure reflected by the sum of old
words correctly remembered, plus the correct "know" responses and
the exclusion score reflected by the sum of false decisions regarding list
membership, plus the correct "know" decisions.
Statistical analysis was performed on the scores of recollection and
familiarity-based recognition using analysis of variance (ANOVA) including a
between subject factor "sleep/wake" and two repeated measures
factors "night-half" (early vs. late-night retention interval) and
"context congruency" (congruent vs. incongruent font). Post-hoc
product moment correlations were calculated between recollection scores and
corresponding familiarity scores to ascertain statistical independence of the
two types of scores. Additionally, the percentages of correctly identified new
words were analyzed for the "sleep/wake" and
"night-half" factors. A minimum of 33% (chance level) correctly
identified "new" words was required for a subject to be included
in the analysis. All subjects met this criterion. Pairwise comparisons were
specified with t-tests. The significance level was set to 
=
0.05.
Standard polysomnographical recordings of sleep were scored offline
according to the criteria by Rechtschaffen and Kales
(1968). For each 30-sec epoch
of recording, the sleep stage was determined (W, wake; S1–S4, sleep
stage 1–4; REM sleep). Sleep onset was defined by the occurrence of the
first epoch of S1 sleep, followed by an epoch of S2 sleep. Total sleep time
and the percentages of each sleep stage were determined, with SWS being the
sum of S3 and S4. Polysomnographic recordings from the late night of two
subjects were incomplete due to technical failure, and were therefore not
included in the sleep analysis. Saliva samples for the determination of
cortisol were stored at -20°C until assay by use of conventional
radioimmunometric assay. Cortisol secretion during each retention interval was
estimated by the mean value of the samples obtained immediately before and
after the interval. The data from one subject were incomplete as a result of
insufficient amount of saliva in some samples; therefore, this analysis
contained 11 subjects in the sleep group. Analysis of sleep and cortisol data
also relied on ANOVA.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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1 E-mail drosopoulos{at}kfg.mu-luebeck.de; fax 49-51-5003640.
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