Cognitive Activity in Sleep and Responsiveness to External Stimuli

Transcription

1 Sleep 11(1):61-68, Raven Press, Ltd., New Yrk 1988 Assciatin f Prfessinal Sleep Scieties Cgnitive Activity in Sleep and Respnsiveness t External Stimuli Stephen A. Burtn, Jhn R. Harsh, and *Pietr Badia Department f Psychlgy, University f Suthern Mississippi, Hattiesburg, Mississippi, U.S.A., and *Department f Psychlgy, Bwling Green State University, Bwling Green, Ohi, U.S.A. Summary: The relatinship between respnsiveness t auditry stimuli presented during sleep and cgnitive activity during sleep was assessed. Sixteen cllege-aged wmen were instructed while awake t turn ff a tne by taking a deep breath. The tne was then presented during Stage 2 and REM sleep. Subjects were awakened after select trials t assess the relatinship between respnding and reprts f nging cgnitive activity. Cnsistent with the view that cgnitive activity reduces respnsiveness, significantly fewer respnses were fund n reprt (cgnitive activity) trials relative t n-reprt (n cgnitive activity) trials in analyses invlving all trials and Stage 2 trials alne. Trained judges then rated the subjects' reprts f cgnitive activity as indicating incrpratin r nt indicating incrpratin f the tne and/r the breathing respnse. Incrpratin was assciated with a reduced likelihd f respnding relative t n incrpratin in analyses invlving all trials. N difference in respnding was fund between n-incrpratin trials and n-reprt trials, suggesting that reduced respnsiveness is assciated with cgnitive activity nly when incrpratin ccurs. These findings supprt hyptheses that the reduced respnsiveness t external stimulatin during sleep is at least in part due t nging cgnitive activity. Key Wrds: Perfrmance-Instrumental respnding-dreaming-external stimuli - Incrpratin. With apprpriate instructins and/r training, sleeping subjects respnd t bth external stimuli presented by an experimenter (1,2) and naturally ccurring internal stimuli, e.g., rapid eye mvement (REM) sleep nset (3,4). Many f the factrs related t the level f cntrl by external stimuli have been identified (5,6). Relative t wakefulness, hwever, respnsiveness during sleep is cnsiderably reduced. One factr that may be related t reduced respnsiveness is sleep mentatin. Fr example, Fulkes (7) suggested that reduced respnsiveness t external stimuli during sleep is in part due t the preccupatin f the sleeping subject with nging cgnitive activity. He hypthesized that the vivid mental activity f REM sleep results in exclusin f ther surces f stimulatin, which explains why REM sleep in terms f EEG and subjective reprts appears t be light sleep while in terms f behaviral respnsivity appears t be deep sleep. A secnd pssibility is that respnsiveness is reduced by incrpratin f ex- Accepted fr publicatin September Address crrespndence and reprint requests t Dr. Steve Burtn, Rush-Presbyterian-St. Luke's Medical Center, 1653 W. Harrisn, Department f Psychlgy, Rawsn 310, Chicag, IL 60612, U.S.A. 61

2 62 S. A. BURTON ET AL. ternal events int nging cgnitive activity. The pssibility that infrmatin presented during sleep may be incrprated int a dream was nted by Freud (8). Freud therized that ne functin f dreaming is t prtect sleep frm the intrusin f external stimuli and that it des this by disguising the meaningfulness f stimuli which might therwise prduce arusal (e.g., a passing train, an alarm clck). Currently, there are little r n data cncerning Fulkes' ntin that preccupatin with sleep mentatin interferes with respnsiveness t stimuli presented during sleep. Thus, it is nt knwn whether a sleeping subject is less likely t respnd t a stimulus in the presence as ppsed t the absence f cgnitive activity. Nr is it knwn if cgnitive activity (dreams) during REM sleep is mre "preccupying" than the thught-like activity frequently assciated with nn-rem sleep. Freud's thery has received mre experimental attentin. The data frm several studies have indicated that stimulus events may be incrprated int nging dreams (9,10) and a reprt by Bradley and Meddis (11) prvided evidence that stimulus incrpratin reduces respnsiveness. Under the prcedure used by Bradley and Meddis, a stimulus was presented during REM sleep which gradually increased in ludness until subjects clsed a handheld switch. The subjects were then asked t reprt their dreams. It was fund that lnger respnse latencies were assciated with dream reprts that evidenced stimulus incrpratin. Nt all studies, hwever, have prvided evidence f this effect. Fr example, in a study cmparing arusal threshld during Stage 2 and REM sleep, Rechtschaffen et al. (12) fund little evidence that nnrespnding was assciated with stimulus incrpratin. That is, subjects were awakened when n respnse ccurred t the experimental stimulus, and "bvius" stimulus incrpratin was fund n nly abut 6% f the trials. It shuld be nted, hwever, that ne pssible explanatin f the lw level f incrpratin is that the investigatrs purpsefully selected a stimulus presentatin prcedure (methd f cnstant stimuli) that they believed wuld minimize incrpratin. The purpse f the current study was t prvide further infrmatin abut the relatin between cgnitive activity during sleep and respnsiveness t external stimulatin. One gal f the study was t evaluate Fulkes' suggestin (7) that nging cgnitive activity during sleep will reduce respnsiveness t external stimuli. Tward this end, signal tnes were presented t sleeping subjects, and cmparisns were made f the prbability f a prearranged respnse (taking a deep breath) n trials with and withut subject reprts f nging cgnitive activity. The cgnitive activity-behaviral respnse relatin was examined during bth Stage 2 and REM sleep. A secnd related gal f the study was t replicate and extend the findings f Bradley and Meddis (11) that stimulus incrpratin during REM sleep reduces respnsiveness. A stimulus presentatin prcedure similar t that f Bradley and Meddis was used, i.e., the stimulus was presented at a lw level and, in the absence f a respnse, the db level was increased. Judges rated subject reprts fr evidence f incrpratin. Stage 2 presentatins, in additin t the REM presentatins, permitted determining whether stimulus incrpratin wuld be related t reduced respnsiveness in bth Stage 2 and REM. MATERIALS AND METHODS Subjects Subjects were 16 female vlunteers wh ranged frm 18 t 25 years ld, with n significant health-related r sleep prblems and n sleep labratry histry. Twelve f Sleep, Vl. 11, N. I, 1988

3 SLEEP RESPONSIVENESS TO EXTERNAL STIMULI 63 the subjects spent tw nights in the sleep labratry. Due t equipment prblems, tw subjects were tested a third night. Tw subjects withdrew frm the study after the first night. Subjects were paid $5 per night and a $5 bnus if they cmpleted the experiment. Apparatus Subjects slept n a twin-sized bed in an 8' by 8' sleep chamber; all experimental equipment was lcated in an adjacent rm. A Grass Mdel 78 plygraph was used fr recrding sleep variables. Slid-state mdular cntrl equipment, a Cybrg mdel 91 A analgue/digital (A/D) cmputer interface, and an Apple lie micrprcessr were used fr the cntrl f stimuli and the recrding f breathing respnses. The signal stimulus was a 1,OOO-Hz beeping tne (0.5 sec n/ff) presented via a speaker munted apprximately 3 feet abve the subject's head. Plysmngraphic variables were recrded fllwing standard prcedures (13). Respiratin (chest expansin) was measured by a Grass Mdel PRTB pneumatic respiratin transducer secured arund the subject's chest. The respiratin signal was recrded using a Mdel 7PF preamplifier and the A/D cmputer interface during and 60 s prir t tne trials. During the 60-s pretne interval, a baseline was calculated by averaging the change in the respiratry signal assciated with each inspiratry effrt. A 50% increase ver the baseline was established as the criterin respnse fr the trial (5). All baseline and criterin respnse determinatins were cntrlled by the micrprcessr system. Prcedure The subjects were requested nt t ingest alchl r nnprescriptin drugs during the 24-h perid preceding each test night. Test nights were separated by at least three nntest nights. Lights-ut fr each subject was 2300 and lights-n was at Prir t lights-ut, subjects were given 10 practice trials. The prcedure fr presenting stimulus trials and btaining ncturnal reprts was adapted frm Helscher et al. (14). The stimulus trials were presented n a variable-interval 45-min schedule, which ranged frm 30 t 90 min, and began 2.5 h after lights-ut. Ten minutes prir t each scheduled awakening, the plygraph was turned n and the stage f sleep was determined using a standard sleep staging prcedure (13). Trials were initiated nly if the subject was in unambiguus Stage 2 r REM sleep. Prir t sleep, each subject was instructed t take a deep breath (a minimum 50% increase frm inspiratry baseline) in respnse t a tne, which wuld be presented during the night. The tne began at 40 db (the decibel level was measured at the pillw) and increased 10 db in intensity if there was n breathing respnse within 8 s. After 16 s (at a maximum intensity f 50 db) the tne autmatically terminated if a subject failed t respnd. Selectin f the parameters fr this stimulus presentatin prcedure was based n a pilt study investigating prcedures that wuld result in respnding n apprximately 50% f the trial presentatins. The micrprcessr system prvided the experimenter with instantaneus feedback regarding the initiatin f a trial and either the subject's successful cmpletin f the behaviral respnse r failure t respnd. Ten practice trials were given prir t lights-ut. During sleep, the subjects were awakened t btain verbal reprts 30 s after signal nset fr bth respnse and n-respnse trials. These reprts were recrded n auditape and later transcribed fr scring. All subjects were briefed n the imprtance f limiting their remarks t the cgnitins ccurring befre the experimental awakening. They were als infrmed that they might have perids in which they were nt thinking r dreaming. Each night resulted in a minimum f fur and a maximum f seven experimental awakenings. Verbal reprts Sleep. Vl. 11, N

4 64 S. A. BURTON ET AL. were btained frm fur trial cnditins: trials n which a breathing respnse ccurred and thse n which n breathing respnse ccurred, during REM and during Stage 2 sleep. T minimize time-f-night effects, data were cllected frm alternating respnse and nnrespnse trials when pssible. On 21.8% f the tne trials, it was nt pssible t cllect data frm trials alternating in this fashin. Data were never cllected, hwever, frm mre than tw cnsecutive respnse r nnrespnse trials. The subjects were awakened by the principal investigatr entering their sleep chamber and calling their name. Subjects were then prmpted with the statement, "Tell me what was n yur mind." Fllwing cmpletin f the subject's reply, a secnd prmpt was issued, "Can yu tell me anymre?" Each subject was then allwed t return t sleep. Scring A cgnitive reprt was defined as any verbal respnse t the experimenter's prmpt that was indicative f sleep mentatin (e.g., dreaming, thinking, imaging). Tw judges, aware f the experimental hyptheses but blind as t the trial cnditins, rated the verbal reprts fr evidence f incrpratin. Evidence included (a) a reprt invlving the actual tne and/r respnse; (b) a reprt invlving any discrete signal stimulus and/r respiratry act; r (c) a reprt in which unusual nise r breathing was described r culd be inferred. Only thse reprts indicating sleep mentatin were included, i.e., reprts limited t such cmments as "I was awakened by the tne" r "I heard that tne again" were excluded. There was 100% agreement between the judges n which reprts t exclude. The judges were trained in the use f the scring criteria via grup training sessins using verbal reprts frm a pilt study as training exercises. All f the reprts were independently scred by each judge t determine the percentage f agreement amng the judges. Training cntinued until the percentage f agreement amng the judges reached 90% fr incrpratin. RESULTS Furteen subjects cmpleted the experiment. A ttal f 208 tne trials were administered, and subjects were awakened fllwing 151 f these trials t btain reprts n cgnitive activity. Apprximately the same number f awakenings ccurred during Stage 2 (mean"" 5.3) and REM (mean"" 5.0). The percentage respnding t the tne during Stage 2 and REM (68.8% and 68.4%, respectively) was als apprximately equal. Reprts f cgnitive activity were mre frequent in REM (80.6%) than in Stage 2 (55.9%). This difference was statistically significant: t(12) = 4.26; P < Cgnitive reprts and instrumental respnses Trials n which subjects reprted cgnitive activity (reprt trials) were assciated with lwer respnsivity than trials n which subjects reprted n cgnitive activity (n-reprt trials). Figure 1 presents Tukey bx graphs (15) describing the distributin f the percentage respnding bserved n reprt and n-reprt trials fr Stage 2 and REM sleep tgether (based n 14 subjects) and fr Stage 2 (based n 13 subjects) and REM sleep (based n 9 subjects) separately. The differences in the number f subjects fr these graphs was due t sme subjects nt having bservatins under all cnditins. Fr example, five subjects never failed t give a cgnitive reprt during REM. The three hrizntal lines f each "bx" prtray percentiles with p values f, frm tp t bttm, 75, 50, and 25. The hrizntal lines immediately abve and belw each bx Sleep, Vl. 11, N. I, 1988

5 SLEEP RESPONSIVENESS TO EXTERNAL STIMULI 65 REPORT REPORT REPORT REPORT REPORT REPORT r--'-..., ~ 70 C Z 60 Q. CJ) UJ 50 a: ~ 40 UJ a: 30 UJ Q ST AGE 2 AND REM STAGE 2 REM FIG. 1. The distributin f behaviral respnding by reprt and n reprt fr Stage 2 and REM tgether. Stage 2 alne. and REM alne. prtray the 90th and 10th percentiles, respectively. The circles are individual subject values that fell abve the 90th r belw the 10th percentiles. It can be seen frm Fig. 1 that fr Stage 2 and REM trials tgether, cgnitive activity was assciated with reduced behaviral respnsivity. Specifically, the median percentage f respnse was 63% n reprt trials and 88% n n-reprt trials. A Wilcxn matched-sample signed-ranks test indicated that the differences in the lcatins f the samples were statistically significant (p < 0.01). Similar differences between instrumental respnse distributins can be seen between reprt and n-reprt trials fr Stage 2 and REM trials separately. Wilcxn tests indicated significant differences between reprt and n-reprt trials fr Stage 2 (p < 0.01), but the difference was nt significant fr REM. Nte that during bth Stage 2 and REM half r mre f the subjects respnded n every trial when n reprt was btained. The lack f significance fr REM trials may have been due t the smaller number f subjects with bservatins under bth reprt and n-reprt cnditins and/r the variability under the n-reprt cnditin. Incrpratin and instrumental respnses Incrpratin was defined as a cgnitive reprt in which bth judges fund evidence f incrpratin f the stimulus and/r respnse int nging sleep mentatin. The Sleep. Vl. 1/, N. I. 1988

6 66 S. A. BURTON ET AL. judges agreed n the presence and type f incrpratin n 92% f the cgnitive reprts. T cntrl fr the stage-related differences in the iikeiihd f a cgnitive reprt, calculatin f the prprtin f trials with incrpratin was based n the trials in which a cgnitive reprt was btained. Incrpratin was evident in a mean f 40.8% (±23.5) f the REM trials and 37.4% (±37.2) f the Stage 2 trials. The differences between Stage 2 and REM sleep means were nt statistically reliable. Trials with evidence f incrpratin (incrpratin trials) were assciated with lwer levels f respnsivity than trials with n evidence f incrpratin (n-incrpratin trials). Figure 2 presents Tukey bx graphs describing the distributin f percentage respnding n incrpratin and n-incrpratin trials fr Stage 2 and REM tgether (based n 13 subjects) and Stage 2 (based n 7 subjects) and REM (based n 12 subjects) separately. It can be seen that the likelihd f an instrumental respnse fr Stage 2 and REM cmbined was lwer n incrpratin trials (50%) than n n-incrpratin trials (79%) and that the respnse distributins were similar fr Stage 2 and REM separately. Statistically significant differences were fund using the Wilcxn test fr Stage 2 and REM cmbined (p < 0.01). The differences fr Stage 2 and REM alne were nt statistically different. INCORP. INCORP. INCORP. INCORP. INCORP. INCORP ,---"'--;r <> (!) ~ 70 C Z 0 60 Q. (f) UJ 50 a:... z UJ 40 0 a: UJ 30 Q e r--' STAGE 2 AND REM STAGE 2 REM FIG. 2. The distributin f behaviral respnding by incrpratin and n incrpratin fr Stage 2 and REM tgether. Stage 2 alne, and REM alne. Sleep. Vl. II. N.1, 1988

7 SLEEP RESPONSIVENESS TO EXTERNAL STIMULI 67 Cmparisn f Figs. 1 and 2 suggests that the difference in percentage respnding n reprt and n-reprt trials was due mainly t the lwered level f respnding in assciatin with incrpratin. Fr Stage 2 and REM trials tgether, the level f respnding n reprt trials with n incrpratin (79%) was nt different (by the Wilcxn test) frm the level f respnding bserved n trials with n cgnitive reprts (88%). DISCUSSION T summarize, it was fund that (a) the likelihd f respnding t an external stimulus presented during sleep was lwer n trials with reprts f cgnitive activity (reprt trials) than n trials withut reprts f cgnitive activity (n-reprt trials); (b) respnding was less likely when the stimulus and/r respnse was incrprated int nging cgnitive activity relative t n incrpratin; and (c) respnding n n-incrpratin trials did nt differ frm respnding n n-reprt trials. These relatinships were apparent when examining Stage 2 and REM trials either in cmbinatin r separately, althugh statistical significance was cnsistently btained nly fr the cmbined trials. The finding f reduced sensitivity t external stimulatin when accmpanied by cgnitive activity is cnsistent with the hypthesis that the sleeper is fcusing attentin n inner cgnitive events such as dreaming, thinking, imaging, etc. Althugh Fulkes (7) discussed this hypthesis nly in relatin t the paradxical cccurrence during REM sleep f diminished respnsiveness and EEG activatin, the present data suggest that the same relatin may hld during nn-rem sleep. Cautin must be used, hwever, in interpreting the present data as being strngly supprtive f this hypthesis. One cncern is that there were n reliable differences in respnding between n-reprt trials and n-incrpratin trials. That is, when the reprt trials were brken dwn int trials with and trials withut evidence f incrpratin, it was fund that the level f respnsiveness when there was n evidence f incrpratin was as high as when there was n reprt f cgnitive activity. This may have been due t a measurement limitatin in that several subjects respnded t 100% f bth the n-reprt trials and the n-incrpratin trials. On the ther hand, it may be that cgnitive activity is antagnistic t respnding nly when incrpratin ccurs. The finding that incrpratin trials were assciated with reduced likelihd f respnding is cnsistent with Freud's ntin (8) that dreams serve t prtect sleep. Incrpratin may serve t rb a stimulus f its riginal meaning s that if a stimulus is successfully integrated within a dream, the sleeper is undisturbed (16). As suggested in the review by Arkin and Antrbus (9), the stimulus respnse was mst frequently represented indirectly in the verbal reprts. Althugh there were insufficient bservatins t permit frmal analysis, inspectin f the subjects' cgnitive reprts suggests that the greater the meaning f the tne was changed in incrpratin, the less likely was the subject t either respnd r aruse. Fr example, the fllwing reprt cntains direct references t the tne and was btained n a trial where the subject respnded: "I remember I was dreaming that I was hearing the tne, but it was real, real, real, real high pitched and it hurt my ears and I was crying... that's all I remember." In the next reprt, there is an apparent transfrmatin f the meaning f the signal, and the subject failed t respnd: "That man... n Fantasy Island was ringing his bell and trying t get the peple t cme tgether s they culd meet and talk abut what was ging t happen. Sleep, Vl. 11, N.1, 1988

8 68 S. A. BURTON ET AL. Sleep stage and incrpratin The likelihd f incrpratin was similar acrss Stage 2 and REM sieep. This is in cntrast t the findings f Helscher et al. (14), where incrpratin f stimuli int sleep mentatin was reprted t be mre likely during REM sleep. It is ntewrthy that Helsher et al. 's verall respnse rate was lw (19%) relative t ther studies and that their Stage 2 data are based n nly 17 verbal reprts. The present study may prvide a mre stable index f cgnitive respnding during Stage 2 sleep. That cgnitive activity may be similar between Stages 2 and REM is cnsistent with previus findings. Fr exampie, Antrbus (17) fund n differences between reprts frm Stage 2 and REM sleep after hlding wrd length f the verbal reprt cnstant. He cncluded that higher levels f crtical arusal during REM sleep result in mre effective strage and retrieval prcesses as cmpared with thse in Stage 2 sleep, therefre increasing reprting abilities when arused frm sleep. The results frm this study indicate that a relatinship exists between cgnitive activity and respnsivity t external stimuli during sleep. That Rechtschaffen et al. (12) did nt find this relatinship suggests that prcedural factrs (e.g., using a stimulus f increasing intensity) may be imprtant. Anther explanatin invlves the definitin f incrpratin: Rechtschaffen et al. scred nly "bvius" stimulus incpratin; hwever, a stimulus may smetimes be transpsed within the cntext f nging mentatin (9). Additinal studies f cgnitive activity and respnsiveness during sleep may prvide useful insight int the rle f cgnitin in disrders f initiating and maintaining sleep. REFERENCES I. Bnnet MH. Perfrmance during sleep. In: Webb WB, ed. Bilgical rhythms, sleep, and p:fc)f"fnance. New Yrk: Jhn Wiley & Sns. 1982: Badia P, Harsh J, Balkin T, et al. Behaviral cntrl f respiratin in sleep. Psychphysilgy 1984;21 : Salamy J. Effects f REM deprivatin and awakening n instrumental perfrmance during stage 2 and REM sleep. Bii Psychiatry 1971 ;3: Brwn IN, Cartwright RD. Lcating NREM dreaming thrugh instrumental respnses. Psychphysilgy 1978; 15: Harsh J, Badia p, O'Rurke D. Burtn S, Revis C. Factrs related t behaviral cntrl by stimuli presented during sleep. Psychphysilgy 1987:5: Williams H, Mrlck H, Mrlck J. Instrumental behavir during sleep. Psychphysilgy 1966:2: Fulkes D. The psychlgy (~f sleep. New Yrk: Scribner, Freud S. The Interpretatifl j dreams. New Yrk: Jhn Wiley & Sns (translated by J. Strachey), Arkin A, Antrbus 1. The effects f external stimuli applied prir t and during sleep n sleep experience. In: Arkin A, Antrbus J, Ellman S, eds. The mind in sleep: psychlgy and psychphysilgy. Hillsdale, NJ: Lawrence Erlbaum, 1978: Chen DB. Sleep and dreaming: rigins. nature. and junctins. New Yrk: Pergamn Press, II. Bradley C. Meddis R. Arusal threshld in dreaming sleep. Physil Psychl 1974:2: Rechtschaffen A, Hauri P, Zeitlin M. Auditry awakening threshlds in REM and NREM sleep stages. Percept Mtr Skills 1966;22: Rechtschaffen A, Kales A, eds. A maflual jstandardized termifllgy, techniques, and scring system jr sleep stages f humafl subjects (NIH Publicatin N. 204). Washingtn, DC: U.S. Gvernment Printing Office, Helscher TJ, Klinger E, Barta S. Incrpratin f cncern- and nncncern-related verbal stimuli int dream cntent. J Abnrm Psvchl 1981 :90: Tukey Jw. Explratry data ~lilalysis. Reading, MA: Addisn-Wesley Kulack D. Effects f smatsensry stimulatin n dream cntent. Arch Gen Psychiatr 1969;20: Antrbus JS. REM and NREM sleep reprts: cmparisn f wrd frequencies by cgnitive classes. Psychphysilgy 1983 ;20: Sleep, Vl. 11, N. I, 1988