Sleep, 2(2):193-198
© 1979 Raven Press, New York
Sentence Memory and Sleep: A Pilot Study C. Cipolli and P. Salzarulo Istiwto di Psicologia, Facoltd di Medicina, Unil'ersitd di Bologna, Bologna, Italy, and INSERM U3, Paris, France
Summary: In four consecutive weekly sessions 12 subjects, aged 20-25 years, listened to a sentence stimulus before the onset of sleep and were asked to reproduce it after an awakening provoked during stage 2 or REM sleep of the first cycle. Recall of the sentence stimuli heard before sleep was affected by their semantic acceptability, but was unaffected by the sleep type (REM/ NREM) or by the length of waking preceding sleep. The differing retention intervals involved for the recall tests after REM and NREM sleep may, however, have masked any effect of the former on recall. Key Words: SleepMemory-Syntactic structures.
As we previously emphasized (Salzarulo and Cipolli, 1975), most of the research into the relation between sleep and memory of verbal material pertains to elementary verbal units. As far as structured verbal material is concerned, we know only that the absence of REM sleep is followed by a decrease in the recall of lexical constituents which is more marked than when these constituents are presented in isolation (Empson and Clarke, 1970). This indicates that for structured verbal material, one linguistic level (that of lex is) is particularly involved; we do not know if the syntactic level is also involved. We may ask whether only recall of lexical constituents is modified, or whether this is also true for syntactic structure. First of all, does REM sleep affect recall of syntactic structures? We can formulate various hypotheses which take into account REM sleep as opposed to NREM sleep, on the one hand, and any modification of levels of linguistic organization on the other. According to the linguistic levels which are modified, a different role may be attributed to REM sleep in the process of modifying verbal material. An increase in the recall of the lexical constituents alone in the presence of REM sleep could be due to a quantitative modification of the "interword associations" (Cartwright et aI., 1975), whereas an increase in the lexical and syntactic indices could be due to the activation of the semantic representation of the sentence (Craik and Lockhart, 1972; Kintsch, 1974). In the absence of REM versus NREM variation, we should also be able tojudge Accepted for publication November 1979. Address reprint requests to Dr. Salzarulo at INSERM U3, 91 Boulevard de I'H6pital, Paris 13, France.
193
194
C. CIPOLLI AND P. SALZARULO
the role of the type of cerebral activity following the presentation of the stimulus: we can suppose that there might be an increase in recall when sleep follows a lengthy period of waking (Bloch, 1970). Also under this hypothesis, purely lexical modification could be attributed to greater interword associations, which, as is known, may also occur during periods of waking (Rosenberg, 1966). An increase in both lexical and syntactic indices could be due to rehearsal of the sentence and/or its representation at some level. Stimulus material should therefore be of a linguistic structure which permits separation of the indices. We therefore decided (1) to study the effects of these two physiological variables (REM and NREM sleep) in the context ofa natural sleep sequence (avoiding such techniques as the selective deprivation of sleep and the comparison of different amounts of sleep stages in two distinct moments of the circadian rhythm) and (2) to use two kinds of stimulus material: (a) structured material in which the lexical indices can be modified independently of the syntactic indices, given the noncompatibility of the indices (a semantically unacceptable sentence, SEM -) and (b) structured material in which the lexical and syntactic indices must be modified together owing to the compatibility of the two indices (a semantically acceptable sentence, SEM +). We can hyp6thesize that if there is an increase in "interword associations," when a SEM - sentence is presented, there will be a more marked effect on the lexical indices, and therefore, there will be more such indices. On the other hand, if there is an activation of the semantic representation, more lexical and syntactic indices will be obtained when SEM + sentences are presented. MA TERIALS AND METHODS
Twelve male students, Italian native speakers, aged between 20 and 25 years, participated in this experiment. The 12 subjects were recruited among students who had already proved to be "good sleepers" in previous experiments of sleep mental activity. At the time of recruitment they were told that the experiment involved a recall test after awakening, on material presented before the onset of sleep. Subjects were given no specific instruction as to how to carry out the retention of the stimulus material. Electroencephalogram (EEG), electromyogram (EMG), and electroculogram (EOG) activities were recorded (using a Battaglia-Rangoni polygraph) to discriminate between waking and sleeping states. After lights-out the subjects were asked to listen carefully to one of the two stimulus sentences (SEM - or SEM +) played once only on the tape recorder and were then allowed to sleep. lithe subject had failed to hear the stimulus, he could signal this to the experimenter with a push button; the experimenter would then have replayed the stimulus and discarded the subject from the experimental group. In no case, however, did this occur. Subjects were awakened once each night, either 9 min after the appearance of the first spindle of NREM sleep (awakening A) or 9 min after the appearance of the first eye movement of REM sleep (awakening B). On awakening, subjects were asked, "Can you repeat the sentence you heard on the tape recorder before going to sleep?" The responses were tape-recorded and transcribed.
Sleep, Vol. 2, No.2, 1979
195
SENTENCE MEMORY AND SLEEP
In the experimental procedure (a 2 x 2 repeated measures design), there were two factors, namely, (1) type of sleep (REM vs NREM) and (2) type of sentence stimulus (SEM + vs SEM -). Each of the 12 subjects was run in four consecutive sessions, with an interval of a week between one session and the next. The order of the four possible combinations of the levels of the two factors was counterbalanced across subjects and across sessions. We attempted to exclude the learning effect by presenting the same stimulus sentence after 2 weeks had passed and by not telling subjects that there would, in fact, be a second presentation. The sentence stimuli heard were: "Verdi idee galoppano dormendo furiosamente e do po la nomina leggono francobolli isterici" (Green ideas gallop sleeping furiously and after their appointment they read hysterical stamps) (SEM -), composed of 12 lexical constituents and derived through 14 syntactic transformations, and "La spada viene estratta dalla roccia e il masso si stacca dalla sommita del monte" (The sword is pulled out of the stone and a rock breaks loose from the top of the mountain) (SEM +), composed of 15 lexical constituents and derived through 10 syntactic transformations. The lexical constituents and the transformations were defined according to the criteria of generative transformational grammar (Chomsky, 1957, 1965; Salzarulo and Cipolli, 1974). The measures of the dependent variables (respectively called lexical and syntactic indices) were determined by the percentages of lexical constituents and syntactic transformations correctly reproduced in the material recalled. RESULTS The presence of REM sleep had no effect either on the recall of lexical indices [analysis of variance, F(l,l1) = 0.519, n.s.] or on the recall of syntactic indices [F(1,l1) = 0.1251, n.s.] (Table 1). On the other hand, the recall of lexical indices was greater for the SEM + sentence than for the SEM - sentence [F(1, 11) = 13.4612, p < 0.01], as was that of syntactic indices [F(l,l1) = 5.6853, p < 0.05]. The interaction between the type of sleep and the type of sentence produced almost negligible effects [F(1,l1) = 0.0032, n.s., for lexical indices; F(1,l1) = 0.0871, n.s., for syntactic indices]. Comparisons of recall in the first session and the mean of the three following sessions did not show significant differences for lexical indices [56.57 ± 33.47 vs 61.17 ± 16.18%; t for paired data (d.t. = 11) = 0.4671, n.s.] or syntactic indices [58.92 ± 29.07 vs 70.93 ± 21.58%; t for paired data (d.f. = 11) = 0.9226, n.s.]. This implies the absence of any learning effect. There was no significant variation for lexical or syntactic indices in either senTABLE 1. Linguistic indices of recall Lexical
SEMSEM+
Syntactic
NREM
REM
NREM
REM
43.18:t 16.81 77.21:t 23.15
42.42:t 15.63 77.27:t 23.15
61.86:t 21.85 77.50:t 19.88
56.52 ± 27.41 75.83 ± 31.35
Sleep. Vol. 2, No.2, 1979
C. CIPOLLI AND P. SALZARULO
196
TABLE 2. Effects of awake time on recall
SEMSEM+
Awake time
Lexical indices
Syntactic indices
24 min and 19 sec ± 17 min and 32 sec 24 min and 26 sec ± 17 min and 28 sec
-0.07 -0.14
0.06 0.09
Factors: x, recall fidelity (= % of indices exactly recalled); y, awake time (= continuous alpha rhythm before sleep onset); z. sleep time (= amount of sleep before awakening).
tence according to the length of the awake time before the onset of sleep. The partial correlation coefficients (Kendall's range test) are all, in fact, very low (Table 2). DISCUSSION The principal aim of the research was to test the effect of the natural sequence of sleep stages on the retention in memory of structured verbal materials, and, before passing to the interpretation of the results, it is worth making two points about the experimental design. On the one hand, no immediate recall test was incorporated; on the other, no control group was employed to measure the effect of elapsed time on memory. The former decision undoubtedly led to a cruder measure of effective retention, as this was calculated on the basis of the difference between the material actually presented and the material recalled, rather than of that between the material actually learned and that recalled. Nevertheless, we considered it preferable to avoid the risk of disturbing the processes of the sentence stimulus or of disturbing sleep onset with a test a few minutes later. The second decision concerned the risk that any effect of REM sleep on memory could be masked by the larger retention interval for materials recalled after REM sleep. The data on the relation between recall scores and duration of NREM sleep (92 min and 10 sec ± 28 min and 33 sec) preceding REM sleep showed virtually nil correlations (Kendall's range test): sentence SEM+, -0.06 for syntactic indices, +0.09 for lexical indices; sentence SEM -, +0.08 for syntactic indices, +0.03 for lexical indices. These data, however, do not exclude the possibility that the progressive decay of the linguistic indices in memory during NREM sleep was counterbalanced by a positive action of REM sleep. Such an action might be due to spontaneous recovery (Ekstrand et al., 1971) or to covert rehearsal, as suggested by the Programming and Restructuring Hypotheses (see Empson and Clarke, 1970). Evidence for the action of REM sleep could probably be obtained if subjects were awakened in REM sleep and after an equivalent interval of NREM sleep before the onset of REM sleep; but, given the intra-individual variability in the duration ofthe first cycle of night sleep, such an experiment would not be easy to realize. In our study, given the impossibility of counterbalancing the length of the retention intervals for the two sleep types (the sleep sequence not being manipulable), it was not felt that an awake control group could provide useful
Sleep, Vol. 2. No.2, 1979
SENTENCE MEMORY AND SLEEP
197
indications for the measurement of any effect produced by elapsed sleep time. A waking interval equivalent to the sleep interval would, in fact, have inevitably led to different results in view of the mental operations thereby made possible (rehearsal of the stimulus material or a continuous interfering task to prevent such rehearsal) . Having clarified these points, we pass to the conclusions it appears may be drawn from the results. These, in fact, failed to demonstrate the expected main effect, i.e., greater importance of REM as opposed to NREM sleep in facilitating memory processing of structured verbal material. No appreciable difference was found in recall of syntactic indices, as would have been expected if REM sleep had played an important role in restructuring the level of syntactic organization. There was no evidence of greater recall of lexical indices in the presence of REM sleep, as was found by Empson and Clarke (1970) for sentences and prose paragraphs, and by Cartwright et al. (1975) for word lists. Further, in reference to our original hypothesis, there appeared to be no noticeable increase in interword associations for structured verbal material. Differences in the lexical indices from Empson and Clarke's data may be due to the method used, i.e., REM deprivation as opposed to awakening after REM sleep. Our choice of awakening during REM sleep derived from the need to find if the presence of such a physiological variable as REM sleep in the context of the "natural" organization of sleep led to restructuring of syntactically structured material not evident in NREM sleep. The differences with Cartwright et al. 's data may be due to the presence of syntactic relations between lexical constituents in our stimulus material. These relations, which function as connectors between lexical chunks, may favor the retention of longer verbal units (Miller, 1962) and, therefore, inhibit interword associations (which are essentially substitutions of one word for another or combinations with another word frequently link' d with it), thus limiting any greater recall of single lexical constituents. Although such an effect (of the structured verbal material limiting interword associations) was not evident in this case, we feel that in the study of REM sleep effect on verbal recall, syntactically structured material is preferable to word lists, in that the latter are rarely encountered during waking life. Moreover, the absence of any notably greater recall of syntactic rather than lexical indices after REM sleep makes it seem improbable that semantic representations of sentences are activated during REM sleep. We would rather stress that after REM and NREM sleep, as in waking (Epstein, 1961; O'Connell, 1970), the recall of structured verbal material seems to be influenced by semantic acceptability. Concerning the effect of the length of the waking preceding sleep, our data clearly differ from that of Portnoff et al. (1966). It may be that our stimulus materials (syntactically correct sentences) are not sensitive to variations in cerebral activity. But it may also be that the disagreement is a consequence of the experimental situations employed. Portnoff et al. 's subjects had been sleeping before the stimulus was presented; we know that this might have some effect on memory (Ekstrand et aI., 1977). The problem of waking time following stimulus presentation calls for a discussion of the problem of rehearsal. During the period of awake time before sleep, the
Sleep, Vol, 2, No, 2, 1979
198
C. CIPOLLI AND P. SALZARULO
subject may, in fact, rehearse the stimulus, thus modifying the recall potential. Unfortunately, we do not know the major type of rehearsal employed (maintenance rehearsal or elaborative operations: Craik and Watkins, 1973) or how much there is of it. Study of these aspects would only be possible by manipulating the task to obtain overt rehearsal, while at the same time estimating the quantity and major type of rehearsal on the basis of waking time elapsed before sleep. Neither procedure falls within this area of research, and moreover, neither seems easily realizable. Aside from these, we point out that rehearsal could be one of the factors which accounts for divergent results obtained in research on sleep and memory. This experiment, based on the study of syntactically structured verbal material (the most frequently perceived and memorized during waking life), reveals the absence of any effects of sleep patterns on memory that would be consistent with those described in other experiments (for the literature, see Salzarulo and Cipolli, 1975). This uncertainty as to the role of sleep and its various patterns on memory has also been discussed, in its theoretical aspects, by Ekstrand et al. (1977). ACKNOWLEDGMENT The authors thank Dr. I Fagioli for his help. This work was supported in part by C.N.R. C.C. is a Lecturer at the University of Trento. P.S. is a Charge de Recherche, INSERM. REFERENCES Bloch V. Facts and hypothesis concerning memory consolidation processes. Brain Res 24:561-575, 1970. Cartwright RD, Lloyd S, Butters F, Weiner L, McCarthy L, and Hancock J. Effects of REM time on what is recalled. Psychophysiology 12:561-568, 1975. Chomsky N. Syntactic Structures. Mouton, The Hague, 1957, pp 61-84. Chomsky N. Aspects of the Theory of Syntax. MIT Press, Cambridge, Mass., 1965, pp 128-147. Craik FIM and Lockhart RS. Levels of processing: A framework for memory research. J Verb Learn 1l:671-684, 1972. Craik FIM and Watkins MJ. The role of rehearsal in short-term memory. J Verb Learn 12:599-607, 1973. Ekstrand B, Barrett T, West J, and Maier W. The effect of sleep on human long-term memory. In: RR Drucker-Colin and JL McGaugh (Eds), Neurobiology of Sleep and Memory, Academic Press, New York, 1977, pp 419-438. Ekstrand BR, Sullivan MJ, Parker DF, and West IN. Spontaneous recovery and sleep. J Exp Psychol 88: 142-144, 1971. Empson J and Clarke P. Rapid eye movements and remembering. Nature 227:287-288, 1970. Epstein W. The influence of syntactical structure on learning. Am J Psychol 74:80-85, 1961. Kintsch W. The Representation of Meaning in Memory. Lawrence Erlbaum Associates, Hillsdale, N.J., 1974, pp 137-151. Miller GA. Some psychological studies of grammar. Am Psychol 17:748-762, 1962. O'Connell D. Facilitation of recall by linguistic structure in nonsense strings. Psychol Bull 74:441-452, 1970. Portnoff G, Baekeland F, Goodenough DR, Karacan I, and Shapiro A. Retention of verbal material perceived immediately prior to onset of non-REM sleep. Percept Mot Skills 22:751-758. 1966. Rosenberg S. Recall of sentences as a function of syntactic and associative habit. J Verb Learn 5:392-396, 1966. Salzarulo P and Cipolli C. Spontaneously recalled verbal material and its linguistic organization in relation to different stages of sleep. Bioi Psychol 2:45-57, 1974. Salzarulo P and Cipolli C. Verbal memory in relation to sleep. In: P Levin and WP Koella (Eds), Sleep 1974, Karger, Basel, 1975, pp 145-149.
Sleep, Vol. 2, No.2, 1979
© 1979 Raven Press, New York
Sentence Memory and Sleep: A Pilot Study C. Cipolli and P. Salzarulo Istiwto di Psicologia, Facoltd di Medicina, Unil'ersitd di Bologna, Bologna, Italy, and INSERM U3, Paris, France
Summary: In four consecutive weekly sessions 12 subjects, aged 20-25 years, listened to a sentence stimulus before the onset of sleep and were asked to reproduce it after an awakening provoked during stage 2 or REM sleep of the first cycle. Recall of the sentence stimuli heard before sleep was affected by their semantic acceptability, but was unaffected by the sleep type (REM/ NREM) or by the length of waking preceding sleep. The differing retention intervals involved for the recall tests after REM and NREM sleep may, however, have masked any effect of the former on recall. Key Words: SleepMemory-Syntactic structures.
As we previously emphasized (Salzarulo and Cipolli, 1975), most of the research into the relation between sleep and memory of verbal material pertains to elementary verbal units. As far as structured verbal material is concerned, we know only that the absence of REM sleep is followed by a decrease in the recall of lexical constituents which is more marked than when these constituents are presented in isolation (Empson and Clarke, 1970). This indicates that for structured verbal material, one linguistic level (that of lex is) is particularly involved; we do not know if the syntactic level is also involved. We may ask whether only recall of lexical constituents is modified, or whether this is also true for syntactic structure. First of all, does REM sleep affect recall of syntactic structures? We can formulate various hypotheses which take into account REM sleep as opposed to NREM sleep, on the one hand, and any modification of levels of linguistic organization on the other. According to the linguistic levels which are modified, a different role may be attributed to REM sleep in the process of modifying verbal material. An increase in the recall of the lexical constituents alone in the presence of REM sleep could be due to a quantitative modification of the "interword associations" (Cartwright et aI., 1975), whereas an increase in the lexical and syntactic indices could be due to the activation of the semantic representation of the sentence (Craik and Lockhart, 1972; Kintsch, 1974). In the absence of REM versus NREM variation, we should also be able tojudge Accepted for publication November 1979. Address reprint requests to Dr. Salzarulo at INSERM U3, 91 Boulevard de I'H6pital, Paris 13, France.
193
194
C. CIPOLLI AND P. SALZARULO
the role of the type of cerebral activity following the presentation of the stimulus: we can suppose that there might be an increase in recall when sleep follows a lengthy period of waking (Bloch, 1970). Also under this hypothesis, purely lexical modification could be attributed to greater interword associations, which, as is known, may also occur during periods of waking (Rosenberg, 1966). An increase in both lexical and syntactic indices could be due to rehearsal of the sentence and/or its representation at some level. Stimulus material should therefore be of a linguistic structure which permits separation of the indices. We therefore decided (1) to study the effects of these two physiological variables (REM and NREM sleep) in the context ofa natural sleep sequence (avoiding such techniques as the selective deprivation of sleep and the comparison of different amounts of sleep stages in two distinct moments of the circadian rhythm) and (2) to use two kinds of stimulus material: (a) structured material in which the lexical indices can be modified independently of the syntactic indices, given the noncompatibility of the indices (a semantically unacceptable sentence, SEM -) and (b) structured material in which the lexical and syntactic indices must be modified together owing to the compatibility of the two indices (a semantically acceptable sentence, SEM +). We can hyp6thesize that if there is an increase in "interword associations," when a SEM - sentence is presented, there will be a more marked effect on the lexical indices, and therefore, there will be more such indices. On the other hand, if there is an activation of the semantic representation, more lexical and syntactic indices will be obtained when SEM + sentences are presented. MA TERIALS AND METHODS
Twelve male students, Italian native speakers, aged between 20 and 25 years, participated in this experiment. The 12 subjects were recruited among students who had already proved to be "good sleepers" in previous experiments of sleep mental activity. At the time of recruitment they were told that the experiment involved a recall test after awakening, on material presented before the onset of sleep. Subjects were given no specific instruction as to how to carry out the retention of the stimulus material. Electroencephalogram (EEG), electromyogram (EMG), and electroculogram (EOG) activities were recorded (using a Battaglia-Rangoni polygraph) to discriminate between waking and sleeping states. After lights-out the subjects were asked to listen carefully to one of the two stimulus sentences (SEM - or SEM +) played once only on the tape recorder and were then allowed to sleep. lithe subject had failed to hear the stimulus, he could signal this to the experimenter with a push button; the experimenter would then have replayed the stimulus and discarded the subject from the experimental group. In no case, however, did this occur. Subjects were awakened once each night, either 9 min after the appearance of the first spindle of NREM sleep (awakening A) or 9 min after the appearance of the first eye movement of REM sleep (awakening B). On awakening, subjects were asked, "Can you repeat the sentence you heard on the tape recorder before going to sleep?" The responses were tape-recorded and transcribed.
Sleep, Vol. 2, No.2, 1979
195
SENTENCE MEMORY AND SLEEP
In the experimental procedure (a 2 x 2 repeated measures design), there were two factors, namely, (1) type of sleep (REM vs NREM) and (2) type of sentence stimulus (SEM + vs SEM -). Each of the 12 subjects was run in four consecutive sessions, with an interval of a week between one session and the next. The order of the four possible combinations of the levels of the two factors was counterbalanced across subjects and across sessions. We attempted to exclude the learning effect by presenting the same stimulus sentence after 2 weeks had passed and by not telling subjects that there would, in fact, be a second presentation. The sentence stimuli heard were: "Verdi idee galoppano dormendo furiosamente e do po la nomina leggono francobolli isterici" (Green ideas gallop sleeping furiously and after their appointment they read hysterical stamps) (SEM -), composed of 12 lexical constituents and derived through 14 syntactic transformations, and "La spada viene estratta dalla roccia e il masso si stacca dalla sommita del monte" (The sword is pulled out of the stone and a rock breaks loose from the top of the mountain) (SEM +), composed of 15 lexical constituents and derived through 10 syntactic transformations. The lexical constituents and the transformations were defined according to the criteria of generative transformational grammar (Chomsky, 1957, 1965; Salzarulo and Cipolli, 1974). The measures of the dependent variables (respectively called lexical and syntactic indices) were determined by the percentages of lexical constituents and syntactic transformations correctly reproduced in the material recalled. RESULTS The presence of REM sleep had no effect either on the recall of lexical indices [analysis of variance, F(l,l1) = 0.519, n.s.] or on the recall of syntactic indices [F(1,l1) = 0.1251, n.s.] (Table 1). On the other hand, the recall of lexical indices was greater for the SEM + sentence than for the SEM - sentence [F(1, 11) = 13.4612, p < 0.01], as was that of syntactic indices [F(l,l1) = 5.6853, p < 0.05]. The interaction between the type of sleep and the type of sentence produced almost negligible effects [F(1,l1) = 0.0032, n.s., for lexical indices; F(1,l1) = 0.0871, n.s., for syntactic indices]. Comparisons of recall in the first session and the mean of the three following sessions did not show significant differences for lexical indices [56.57 ± 33.47 vs 61.17 ± 16.18%; t for paired data (d.t. = 11) = 0.4671, n.s.] or syntactic indices [58.92 ± 29.07 vs 70.93 ± 21.58%; t for paired data (d.f. = 11) = 0.9226, n.s.]. This implies the absence of any learning effect. There was no significant variation for lexical or syntactic indices in either senTABLE 1. Linguistic indices of recall Lexical
SEMSEM+
Syntactic
NREM
REM
NREM
REM
43.18:t 16.81 77.21:t 23.15
42.42:t 15.63 77.27:t 23.15
61.86:t 21.85 77.50:t 19.88
56.52 ± 27.41 75.83 ± 31.35
Sleep. Vol. 2, No.2, 1979
C. CIPOLLI AND P. SALZARULO
196
TABLE 2. Effects of awake time on recall
SEMSEM+
Awake time
Lexical indices
Syntactic indices
24 min and 19 sec ± 17 min and 32 sec 24 min and 26 sec ± 17 min and 28 sec
-0.07 -0.14
0.06 0.09
Factors: x, recall fidelity (= % of indices exactly recalled); y, awake time (= continuous alpha rhythm before sleep onset); z. sleep time (= amount of sleep before awakening).
tence according to the length of the awake time before the onset of sleep. The partial correlation coefficients (Kendall's range test) are all, in fact, very low (Table 2). DISCUSSION The principal aim of the research was to test the effect of the natural sequence of sleep stages on the retention in memory of structured verbal materials, and, before passing to the interpretation of the results, it is worth making two points about the experimental design. On the one hand, no immediate recall test was incorporated; on the other, no control group was employed to measure the effect of elapsed time on memory. The former decision undoubtedly led to a cruder measure of effective retention, as this was calculated on the basis of the difference between the material actually presented and the material recalled, rather than of that between the material actually learned and that recalled. Nevertheless, we considered it preferable to avoid the risk of disturbing the processes of the sentence stimulus or of disturbing sleep onset with a test a few minutes later. The second decision concerned the risk that any effect of REM sleep on memory could be masked by the larger retention interval for materials recalled after REM sleep. The data on the relation between recall scores and duration of NREM sleep (92 min and 10 sec ± 28 min and 33 sec) preceding REM sleep showed virtually nil correlations (Kendall's range test): sentence SEM+, -0.06 for syntactic indices, +0.09 for lexical indices; sentence SEM -, +0.08 for syntactic indices, +0.03 for lexical indices. These data, however, do not exclude the possibility that the progressive decay of the linguistic indices in memory during NREM sleep was counterbalanced by a positive action of REM sleep. Such an action might be due to spontaneous recovery (Ekstrand et al., 1971) or to covert rehearsal, as suggested by the Programming and Restructuring Hypotheses (see Empson and Clarke, 1970). Evidence for the action of REM sleep could probably be obtained if subjects were awakened in REM sleep and after an equivalent interval of NREM sleep before the onset of REM sleep; but, given the intra-individual variability in the duration ofthe first cycle of night sleep, such an experiment would not be easy to realize. In our study, given the impossibility of counterbalancing the length of the retention intervals for the two sleep types (the sleep sequence not being manipulable), it was not felt that an awake control group could provide useful
Sleep, Vol. 2. No.2, 1979
SENTENCE MEMORY AND SLEEP
197
indications for the measurement of any effect produced by elapsed sleep time. A waking interval equivalent to the sleep interval would, in fact, have inevitably led to different results in view of the mental operations thereby made possible (rehearsal of the stimulus material or a continuous interfering task to prevent such rehearsal) . Having clarified these points, we pass to the conclusions it appears may be drawn from the results. These, in fact, failed to demonstrate the expected main effect, i.e., greater importance of REM as opposed to NREM sleep in facilitating memory processing of structured verbal material. No appreciable difference was found in recall of syntactic indices, as would have been expected if REM sleep had played an important role in restructuring the level of syntactic organization. There was no evidence of greater recall of lexical indices in the presence of REM sleep, as was found by Empson and Clarke (1970) for sentences and prose paragraphs, and by Cartwright et al. (1975) for word lists. Further, in reference to our original hypothesis, there appeared to be no noticeable increase in interword associations for structured verbal material. Differences in the lexical indices from Empson and Clarke's data may be due to the method used, i.e., REM deprivation as opposed to awakening after REM sleep. Our choice of awakening during REM sleep derived from the need to find if the presence of such a physiological variable as REM sleep in the context of the "natural" organization of sleep led to restructuring of syntactically structured material not evident in NREM sleep. The differences with Cartwright et al. 's data may be due to the presence of syntactic relations between lexical constituents in our stimulus material. These relations, which function as connectors between lexical chunks, may favor the retention of longer verbal units (Miller, 1962) and, therefore, inhibit interword associations (which are essentially substitutions of one word for another or combinations with another word frequently link' d with it), thus limiting any greater recall of single lexical constituents. Although such an effect (of the structured verbal material limiting interword associations) was not evident in this case, we feel that in the study of REM sleep effect on verbal recall, syntactically structured material is preferable to word lists, in that the latter are rarely encountered during waking life. Moreover, the absence of any notably greater recall of syntactic rather than lexical indices after REM sleep makes it seem improbable that semantic representations of sentences are activated during REM sleep. We would rather stress that after REM and NREM sleep, as in waking (Epstein, 1961; O'Connell, 1970), the recall of structured verbal material seems to be influenced by semantic acceptability. Concerning the effect of the length of the waking preceding sleep, our data clearly differ from that of Portnoff et al. (1966). It may be that our stimulus materials (syntactically correct sentences) are not sensitive to variations in cerebral activity. But it may also be that the disagreement is a consequence of the experimental situations employed. Portnoff et al. 's subjects had been sleeping before the stimulus was presented; we know that this might have some effect on memory (Ekstrand et aI., 1977). The problem of waking time following stimulus presentation calls for a discussion of the problem of rehearsal. During the period of awake time before sleep, the
Sleep, Vol, 2, No, 2, 1979
198
C. CIPOLLI AND P. SALZARULO
subject may, in fact, rehearse the stimulus, thus modifying the recall potential. Unfortunately, we do not know the major type of rehearsal employed (maintenance rehearsal or elaborative operations: Craik and Watkins, 1973) or how much there is of it. Study of these aspects would only be possible by manipulating the task to obtain overt rehearsal, while at the same time estimating the quantity and major type of rehearsal on the basis of waking time elapsed before sleep. Neither procedure falls within this area of research, and moreover, neither seems easily realizable. Aside from these, we point out that rehearsal could be one of the factors which accounts for divergent results obtained in research on sleep and memory. This experiment, based on the study of syntactically structured verbal material (the most frequently perceived and memorized during waking life), reveals the absence of any effects of sleep patterns on memory that would be consistent with those described in other experiments (for the literature, see Salzarulo and Cipolli, 1975). This uncertainty as to the role of sleep and its various patterns on memory has also been discussed, in its theoretical aspects, by Ekstrand et al. (1977). ACKNOWLEDGMENT The authors thank Dr. I Fagioli for his help. This work was supported in part by C.N.R. C.C. is a Lecturer at the University of Trento. P.S. is a Charge de Recherche, INSERM. REFERENCES Bloch V. Facts and hypothesis concerning memory consolidation processes. Brain Res 24:561-575, 1970. Cartwright RD, Lloyd S, Butters F, Weiner L, McCarthy L, and Hancock J. Effects of REM time on what is recalled. Psychophysiology 12:561-568, 1975. Chomsky N. Syntactic Structures. Mouton, The Hague, 1957, pp 61-84. Chomsky N. Aspects of the Theory of Syntax. MIT Press, Cambridge, Mass., 1965, pp 128-147. Craik FIM and Lockhart RS. Levels of processing: A framework for memory research. J Verb Learn 1l:671-684, 1972. Craik FIM and Watkins MJ. The role of rehearsal in short-term memory. J Verb Learn 12:599-607, 1973. Ekstrand B, Barrett T, West J, and Maier W. The effect of sleep on human long-term memory. In: RR Drucker-Colin and JL McGaugh (Eds), Neurobiology of Sleep and Memory, Academic Press, New York, 1977, pp 419-438. Ekstrand BR, Sullivan MJ, Parker DF, and West IN. Spontaneous recovery and sleep. J Exp Psychol 88: 142-144, 1971. Empson J and Clarke P. Rapid eye movements and remembering. Nature 227:287-288, 1970. Epstein W. The influence of syntactical structure on learning. Am J Psychol 74:80-85, 1961. Kintsch W. The Representation of Meaning in Memory. Lawrence Erlbaum Associates, Hillsdale, N.J., 1974, pp 137-151. Miller GA. Some psychological studies of grammar. Am Psychol 17:748-762, 1962. O'Connell D. Facilitation of recall by linguistic structure in nonsense strings. Psychol Bull 74:441-452, 1970. Portnoff G, Baekeland F, Goodenough DR, Karacan I, and Shapiro A. Retention of verbal material perceived immediately prior to onset of non-REM sleep. Percept Mot Skills 22:751-758. 1966. Rosenberg S. Recall of sentences as a function of syntactic and associative habit. J Verb Learn 5:392-396, 1966. Salzarulo P and Cipolli C. Spontaneously recalled verbal material and its linguistic organization in relation to different stages of sleep. Bioi Psychol 2:45-57, 1974. Salzarulo P and Cipolli C. Verbal memory in relation to sleep. In: P Levin and WP Koella (Eds), Sleep 1974, Karger, Basel, 1975, pp 145-149.
Sleep, Vol. 2, No.2, 1979
