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Dissociation of the acute effects of alcohol on implicit and explicit memory processes
0028-3932 91 5300+000 PergamonPrc5s plc
"irurop\,lhol,,yiu. Vol 29.No 12.pp 1205-1212. 1991 PnntedI"
DISSOCIATION IMPLICIT RICHARD
OF THE ACUTE EFFECTS AND EXPLICIT MEMORY
OF ALCOHOL PROCESSES
ON
G. LISTER, CLARICE GORENSTEIN, DEBRA RISHER-FLOWERS, HERBERT J. WEINGARTNER and MICHAEL J. ECKARDT
Laboratory of Clinical Studies, NIAAA. DICBR, NIH. Building 10 Room 3C102. 9000 Rockville Pike. Bethesda,
MD 20892, U.S.A.
(Receicud 12 July 1990;
accepted12 July 199 1)
Abstract-The effects of alcohol (0, 0.3 and 0.6 g.!kg) on learning and memory were assessed in independent groups of male student volunteers. Subjects were shown a list of words and asked to form an image of a scene involving each word 1 hr after drinking an alcohol-containing beverage. Alcohol consumption impaired the ability of subjects to explicitly remember the words in a test of free recall. However, no impairment was observed if memory for the same material was assessed implicitly using a backwards-reading or word-completion task. That is. both alcohol-and placebo-treated subjects showed similar degrees of priming. The data indicate that alcohol’s effects on memory are selective.
INTRODUCTION IT HAS BEEN known for many years that subjects who are under the influence of alcohol (ethanol) are impaired in their ability to learn and remember information [ 1, 9, I 1, 13, IS]. The goal of the present study was to examine the specificity of the impairment caused by acute alcohol intoxication. A large number of neuropsychological studies have provided substantive evidence of the differentiated nature of cognition. For example, neuropsychological evaluation of various patient populations have shown that some patients are capable of learning skills and procedures despite being severely impaired in their ability to learn and remember episodic information [4, 151. Indeed, many models of normal memory function are based upon the selective nature of the cognitive impairments observed in different patient populations. while much of this work has been performed by neuropsychologists evaluating patients with various cognitive difficulties, psychopharmacologists have also examined whether the cognitive changes caused by various drug treatments are selective. For example, benzodiazepines appear to produce a pattern of amnesia that resembles to some degree that seen in patients with Korsakoff’s disease [2]. Benzodiazepine-treated subjects have a severe impairment in their ability to learn episodic information but may not be impaired in their ability to learn skills [14]. An important advantage of acute drug studies in normal volunteers over neuropsychological studies in cognitively impaired patients is that the amnesia can be experimentally produced by drug administration and reversed either by the administration of a pharmacological antagonist or by waiting for the drug to be eliminated from the body. In contrast, in most CNS-impaired patient populations the lesions associated with the behavioral impairments are permanent. The present study examines the effects of alcohol on implicit and explicit memory 1205
1206
R. G. Lwt
K cr I//
processes. Implicit memory processes are those that arc asscsscd in tasks that do not require conscious recollection of previous experiences. In contrast explicit memory, which is assessed in traditional tests of free recall and recognition, requires the conscious recollection of previously presented information 18. 191. Two implicit memory tasks were used. They were derived from the observation that performance on word identification tasks is enhanced if subjects have previously been shown the words to be identified [7, IO, 12,233. One involved the reading of transformed text 17, 121, and the other was a word-completion task 1231. The effect of alcohol on semantic priming [3] was also examined. Two doses of alcohol were studied. the higher dose being chosen so as to give maximum blood alcohol concentrations just under 0.08 g.’100 ml.
METHODS Twentyzight healthy malt student volunteers age 21 35 ~crc rccruitcd bq advertlsment in the University of Maqland student ncwspapcr. They were social drlnkcrs. consuming between 6 and 15 drinks on avcragc per week. Thcl here all given a phyucal and psychiatric evaluation, and blood and urine tests here conducted to screen for possible drug abuse. Subjects acre not allowed to participate of their blood or urine tests wre posti\e. or If thq satialied DSM-III-R criteria for alcohol abuse ‘dependence. or a major psychiatric disorder.
The stimuli used in the study wcrc 3X semantically and phoncmlcallq unrelated seven-letter words. Their frcqucncies ranged from one to more than 100 occurrences per million words L22]. They were dlwdcd mto foul group5 (A. B. <‘ and D). matched for frequenq. of 12words each. For wmc of the st~bjccts (approx. I 3 111 eachdrutl t~catmcnt group) list A v,ordb wrre u\ed 1n the imaging task. list B words in the backwards-reading tahk. 1151c \vords 1n both the Imaging and back\~ards-reading tasks. and list D words were only in the Nerd-completion txk. Similarl! for approximatel! another I 4 ofthe subjects the li\t A ~\ords ncrc used oni) in the word-completion task. list B words in the lrnaglng task. hat c‘ words in the hack\*nrda-reading task. and the list D words In both the imaging and bach\~urd\-re;ldlnp t&s. Half the words from each IISI were used i:l the word-completion tush. In summary. the stimulus list\ were counterbalanced across test condition\.
Alcohol dose W;I\ baxd on each wbject’a body ucipht and ~a\ mlxcd vvlth tonic water (to diaguiae total iolumc of400 ml. Suhjccts drank the mixture through a strau from a beaker ~IIII a Ild In which alcohol had been placed. Thi\ meant that olfactory cues provided by the alcohol could not be used determine N hether or not the> wcrc rccclung an active treatment. They wcrc given I5 min to consume
the taste) to ;I a few drop\ 01 hq sub~ccts to the lxxcragc.
sub~cct~ ucrc KlndOmly assigned to 0111‘ of Ihrec groups rccci\ illg either phccbo (II = Y 1 or one of INo doses 01 alcohol (0.3 g kg. t1= IO. or 0.6 g hp. II = Y). The mean ages of the subjects In each group wcrc 23.7. 2.1 4 and 24.0. rcspccti\cly. On the experimental da!. suhJect\ arrlvcd in the laboratory at approx X a m ‘Thar breath was checked for alcohol wng an Alto-sensor III meter (Into‘tlmeters. St. Louis. MO). The) had been Informed that if alcohol \+a detected thq would not bc pcrmittcd to contintx \lith the study. This did not occur in any ofthe subyxts. Thcj were then giLen :Llowfat brcakf,L\t followed by ;t lwerage containlnp thclr trcatmcnt drink. as described above. One hour after nlcohol :~dmimstration. each \ubjcct W;IS \huun ;t IISI of 23 words, one at ;I time on 4 in. x 6 111. cards. Each \\urd compriacd xvcn lcttcrs typed 1n upper cast. The subject uab asked to rend each word and then imagine a scene involving the word and to rate on ;Lthree-point scale how easy it LVXSto do this. After the In51 ofthe words had been presented. the s~~blect \\a\; ashcd to count backwards by threes from 200 for 2 min. After this. he v,as asked to freely recall II\ many of ;hc words a\ possible.
After the test of free recall. subjects L\Lcrcpre\ented with cards on which uorda had heen typed hack~~ard\. 111 Iowcr-case characler\ (e.g. ragen,\ ). The suhjoct U;L\ asked to read each word so that It made scnx. and the time II took to read each lord uorrcctl! was recorded. I-arty words \+erc used. There wcrc I2 words that the suh~ects had prc! iou\l) been ;&cd to ~magc. I2 aorda that the auhjcct had not praiouslq lmagcd and tight pair\ ofscmanticall> related words le_g. tnedut\. > rarhll: dnomaid. dlarcmcl. The semantically r&ted wc>rds \\crc all of wvcn Icttcrs. and had frequencies that ranged Irom tv,o to greater rhan 100 pet- million [ 221.The uord\ were presented 111a random
EFFECTS OF ALCOHOL
Table
ON MEMORY
1. Experimental
PLACEBO or AUXHOL
oal
1207
PROCESSES
design
(0.3 or 0.6 &kg)
I:00
IMAGE WORDS
I:05
FREE RECALL
DISTRACTOR
BACKWARDS
I:10
READING
NEWS
I 30
I
NEW WORDS
WORDS
WORD COMPL.ETION
I
IMAGED WORDS
I
WORDS READ BACKWARDS
I
WORDS IMAGED ANE READ BACKWARDS
order except that the two members of each semantic pair were preaented in sequence. Semantic priming would be reflected by an increased speed of identifying the second word of each pair as a result of exposure to the first. The presentation of the semantically related pairs was balanced across subjects so that approximately half the subjects read “student” before “library” and the other half read these words in the opposite order.
After the backwards-reading test. subjects were presented with a series of cards on which words with seven letters had been typed, in upper case. In each word. however, three of the characters had been replaced by dashes (e.g. P A I T). The subject was asked to complete the word with the first solution that came to mind (e.g. PIANIST). Twenty-four words were used. There weie six words that the subjects had imaged before. six words that the subjects had read backwards (but not imaged), six words that the subjects had both imaged and read backwards, and six new words. The words were presented 15 min after the backwards-reading task, and the subjects were allowed 45 set to complete each word. The proportion of words from each group that were successfully completed was scored.
Breathalyser readings were taken every 30 min throughout Intoximeter Inc.. St. Louis. MO. Subjects were not allowed concentration was belo\\ 20 mg,,dl.
the study usmg a portable Alto Sensor to be transported home until the blood
II from alcohol
Data were analysed using analysis of variance procedures with drug treatment as the independent factor. For the backwards-reading test, a repeated measures analysis was performed using the median times to read familiar and unfamiliar words for each subject. Since the data appeared to have a skewed distribution a second analysis was performed following a rank transformation [S]. A similar analysis was performed on the median times to read the pairs of semantically related words. For the word-completion task, a repeated measures analysis of variance was performed with prior exposure to words in the backwards-reading and imaging tasks as the two within subject factors.
RESULTS The mean blood alcohol concentrations of the subjects are plotted as a function of time after drug administration in Fig. 1. Alcohol significantly reduced the number of words that
120x
subjects freely recalled [r (2, 25)=4.7. 0.6 g.:kg dose.
K. (i. IJSII
P
K 1’1
Cl/
see Fig. 2. This was due to the effect of the
In the backwards-reading test, words were read faster if they had been imaged previously [I; (I. 15) = 6.5. PC 0.021. There was no etrect of alcohol consumption on the speed of reading (i.e. there was no main effect of alcohol [F (2, 25) = 1.2, P> 0.2]), and alcohol did not reduce priming (i.c. thcrc was no alcohol x familiarity interaction [F (2. 25)= I .45, P>O.2]. Similarly, following the rank transf~~rmation, the mean rank of the words that had been imaged previously was significantly lower than that of the novel words [F (I. 25) = 21.4. PO.2] and no alcohol x familiarity interaction [F(2. 25)=0.04. P>O.2], see Fig. 3.
1209
:
SO
Cl H
40
T
lc
30
2 2
20
10
2
i
i
0
NEWWORDS FAMILIAR WORDS
0
l-
0.3
ALCOHOL
0
SO
n
0.6
(G/KG)
FIRSTWORD SECOND WORD
I
ICC i
0
0.3
0.6
ALCOHOL(G/KG)
Fig. 3. The mean rank of rank. the faster the word prior exposure to material of pairs
the reading speed for words in the backwards-reading task. The lower the was read (see text for details). The top half of the figure shows the effect of in the imaging task. The lower half of the figure shows the speed of reading of semantically related words. Values are means+SEM.
The mean rank of the second member of the semantic pairs was lower than that of the first [F (I, 25)=9.5, P-cO.0051. Again there was no main effect of alcohol on speed of reading [F (2, 25)=0.2. P>O.2] and alcohol did not reduce the degree of priming (i.e. there was no alcohol x order interaction [F (2. 25)=0.3, P>O.2], see Fig. 3. In the word-completion task, there was a significant interaction between reading backwards and imaging [F (1,25) = 16.7, PO.2].Further. alcohol did not alter the
ft. G. LIST1 R (‘I I//
0
0.3
0.6
eff‘ects of having previously imaged the words. or having read the words backwards on improving word-completion performance (i.c. there was no alcohol x imaging [F-(2, 25)- 0.41 or al&ho1 x backwards-reading [I;‘ (2, 25) =O.Ol] interactions. P> 0.2 ).
DISCUSSION Consumption of 0.6 g/kg alcohol impaired the ability of subjects to freely rccali information presented to them in an intoxicated state. Similar findings have been reported in numerous other studies and attributed to an impairment in acquisition rather than retrieval processes [I, 1I]. That is, subjects’ free recall of information presented to them in an intoxicated state is not improved by allowing them to sober up. It may be noted, howcvcr. that alcohol in some circumstances has been shown to affect retrieval processes [ 161. While our subjects’ explicit memory was impaired (as assessed by free recall). their memory for the same material appeared intact when tested implicitly both in the backwards-reading and word-completion tests. Both the placebo- and alcohol-treated groups read words that had been typed backwards faster if they had previously been exposed to them in an imaging task. Similarly. both groups were more likely to successfully complete a word if they had imaged it or read it backwards previously. The order of the tests was fixed across subjects, and in the groups that received alcohol, the blood alcohol concentrations declined in the period over which the tests were administered. Thus, blood alcohol concentrations were highest during the explicit tests and lowest during the implicit tests. However, as noted above, previous studies indicate that explicit memory would not have improved by allowing subjects to recall at lower blood alcohol levels [I. 111. A distinction has been made between perceptual and conceptual priming (see e.g. Ref. [24]). It may be noted that in the imaging task. the words were presented in a large, uppercase font, and in the backwards-reading task they were presented in a smaller, lower-case font. Therefore, the priming mechanism would appear not to be purely perceptual. although it may not require high level semantic processing. In the word-completion task. letters wcrc presented in the same case and font-sire as in the imaging task. The increased probability of
tFFECTS OF ALCOHOL 0s MEMORYPKOCESSES
1211
successfully completing words that had previously been imaged, therefore, may reflect purely perceptual priming. However, subjects also successfully completed more words if they had been exposed to them earlier in the backwards-reading task (in the smaller, lower-case font), again suggesting the involvement of some higher level processing in the priming mechanism. Although the exact mechanisms underlying the various types of repetition priming are somewhat unclear, alcohol, at the doses used in the present study, showed no indication of impairing any of them. Neither did alcohol impair priming in the test of short-term semantic priming. In a previous study, HASHTROUDI ef al. [9] reported that alcohol impaired free recall of words, but failed to impair priming in a perceptual identification task. In their study, however, HASHTROUDI et al. found an overall impairment in the ability of intoxicated subjects to correctly identify degraded words regardless of whether they were new or primed. This change in baseline complicates the interpretation of their data. In contrast, in the present study there were no differences between the two groups in their ability to read the new words in the backwards-reading test, or to successfully complete words not shown previously. There are some parallels between the deficits observed in normal volunteers under the influence of alcohol, and those observed in patient populations with a history of long-term alcohol abuse [ 181. For example patients with Korsakoff’s disease are markedly impaired in tests of explicit memory but may be unimpaired if memory is tested implicitly using methods similar to those of the present study. In conclusion, the results of studies in normal subjects as well as in various patient populations have provided good evidence that implicit memory for information (as assessed by tests of priming) is distinct from explicit memory for the same material [S, 19-21,241. The current study provides further support for this suggestion using a pharmacological probe (alcohol) in normal student volunteers. Similar data have come from studies using drugs with different mechanisms of action such as anticholinergics [ 171 and benzodiazepines [6, 141. A~k,loM/edyements~We
are grateful
to Ann Granger
and Mary Rosner for excellent technical
assistance
REFERENCES 1. BIKNBAUM,I. M.. PAKKEK, E. S., HARTLEY. J. T. and NOBLE, E. P. Alcohol and memory: retrieval processes. J. w-h. Lrum. rrrh. Brhar. 17, 325-335, 1978. 2. BROWN. J.. LEWIS, V., BROWN, M., HORN, G. and BOWES, J. B. A comparison between transient amnesias induced by two drugs (diazepam and lorazepam) and amnesia of organic origin. Neuropsychologia 20, 55-70.
1982. 3. CARR. T. H., MCCAULEY, C.. SPERBER, R. D. and PARMELEE,C. M. Words. pictures and priming: on semantic conscious identification. and the automaticity of information processing. J. rsp. Psycho/.: Hum. Per/&n. 8, 757-777, 1982. COHEN, N. J. and SQUIKE, L. R. Preserved learning and retention of pattern-analysing skill in amnesia: dissociation of knowing how and knowing that. Science 210, 207-210, 1980. COKOVER. W. and IMAN. R. Rank transformations as a bridge between parametric and nonparametric statistics. Am. Stufist. 35, 124--129, 1981. DANION. J.-M., ZIMMEKMANN. M.-A., WILLARD-SCHROEOER, D., GRANGER, D. and SINGER, L. Diazepam induces a dissociation between explicit and implicit memory. Ps_whophurmacology 99, 238-243, 1989. GKAF, P. and LEVY. B. A. Reading and remembering: conceptual and perceptual processing involved in reading rotated passages. J. w-h. Learn. wrh. Brhav. 23, 405 424, 1984. GRAF, P. and SCHACTER, D. L. Implicit and explicit memory for new associations in normal and amnesic subjects. J. cup. P.~ychol.: Learn. Mem. Cognit. 11, 501 508, 1985. HASHTROCDI, S., PARKER. E. S., DELISI, L. E., WYATT. R. J. and MUTTER, S. A. Intact retention in acute alcohol amnesia. J. uup. Psycho/.: Learn. Mem. Cognit. IO, 156-163, 1984. activation, Perc~ept.
4. 5. 6. 7. 8.
9.
IO. JAC.OBY.L. L. and D,\I.I AS, M. On the relationship between autobiographical memory und pcrccptual learmng. J. r’\-p_ P.sw/w/.. Gal. 3, 306 340, 19X I. II. JONES. B. M. Memory impairment on the ascending and dewending limbs ofthc blood alcohol curve. .I. ohnorrr~. P\~ChOl. 82, ‘4-32. 1973. Lewx. ,2!ev1. 2, 554 565. 1976. I?. Kort~s. P. A. Reading a year lutcr. J. vyp. P.s~c~/Io/.; /lw. H. Ethanol intoxication and memory. In Rrwr~r 13. LISTT.K, R. G., ECKAKIIT. M. J. and WFIYG,~KT~K. Drrc~/optmv~rv !?I .4/co/di.w~. M. GALAIGTTK(Editor). Vol. 5. pp. I I I 126. Plenum Press, New Yorh, 19X7 amnesia. P.s~chopl~ur/t~trc~o/o~/~ 83, I X3 187. 14. LISTFK, R. G. and FILL.. S. E. The nature of lorazepam-induced 19X4. 15. MILVLK. B. Amnesia following operation on the temporal lobes. In .~mwsitr. C. M W Wtun-Y and 0. I. Z.\UG~ILL (Editors). Butterworth. London. 16. NELSON. T 0.. M~~SPAIXX~. M.. FKOMI~~.. K. and M~KIAT~-. G. A. Effects of alcohol intoxication on metamemory and rctrie\al from long-term memory. J. cup. P.\~&o/.: Guts. 115. 747 254. 1986. dissociation of memory aq’temr, 17. NISSEN, M. J.. K”;OP&IAN. D. S. and S~H~C’TIK. D. L. Ncurochemtcal n’~wolo(/~ 37. 7X9 794. 1987. IX. RYLIA~. R. S. The continuum and specificity of the efl&t\ of alcohol on memory. Q. .I Stlr~i. .4/~oho/ 32, 90s 1016. 1971. I Y. 10. SHIMAI1L!K\. A. P. Priming cl&Is in amnesia: ebidencc for a dlssociable memory function. Q. .i. c\-[I. /‘.\!,c/I~/. %.A, 619 644. 1986. f’. Strength and duration ofprimlng elrects Ln normal subJccts and 21. SQI IKI., L. R.. SHIMAN KA, A P. and c;KAI amnesic patients. h’r,~r~~~pr~~rh~~/r~~iu 25. I95 210. 1987. 72. THOKNDIKL. E. L. and L.OKCI. I The teacher‘s word hook of 30.000 words. Teachers College, C‘olumhla Uni\crsit). 1944. 23. TV LYING;.E., SC HA< 71 K. D. L. and ST 4K6. H. A. Priming e&cts in word fragment completion arc independent of recognltlon memor!. J. op. P.\I~c/w/.: Lc~rrr~ Alrm Cmqnit. 8. 336 342. 1982. 74. T~‘I \ I\(,. F. and %II~~C it K. D. I.: Priming and humnn mcmor) system\. .S~~itw~,247, -301 306. lY90.
"irurop\,lhol,,yiu. Vol 29.No 12.pp 1205-1212. 1991 PnntedI"
DISSOCIATION IMPLICIT RICHARD
OF THE ACUTE EFFECTS AND EXPLICIT MEMORY
OF ALCOHOL PROCESSES
ON
G. LISTER, CLARICE GORENSTEIN, DEBRA RISHER-FLOWERS, HERBERT J. WEINGARTNER and MICHAEL J. ECKARDT
Laboratory of Clinical Studies, NIAAA. DICBR, NIH. Building 10 Room 3C102. 9000 Rockville Pike. Bethesda,
MD 20892, U.S.A.
(Receicud 12 July 1990;
accepted12 July 199 1)
Abstract-The effects of alcohol (0, 0.3 and 0.6 g.!kg) on learning and memory were assessed in independent groups of male student volunteers. Subjects were shown a list of words and asked to form an image of a scene involving each word 1 hr after drinking an alcohol-containing beverage. Alcohol consumption impaired the ability of subjects to explicitly remember the words in a test of free recall. However, no impairment was observed if memory for the same material was assessed implicitly using a backwards-reading or word-completion task. That is. both alcohol-and placebo-treated subjects showed similar degrees of priming. The data indicate that alcohol’s effects on memory are selective.
INTRODUCTION IT HAS BEEN known for many years that subjects who are under the influence of alcohol (ethanol) are impaired in their ability to learn and remember information [ 1, 9, I 1, 13, IS]. The goal of the present study was to examine the specificity of the impairment caused by acute alcohol intoxication. A large number of neuropsychological studies have provided substantive evidence of the differentiated nature of cognition. For example, neuropsychological evaluation of various patient populations have shown that some patients are capable of learning skills and procedures despite being severely impaired in their ability to learn and remember episodic information [4, 151. Indeed, many models of normal memory function are based upon the selective nature of the cognitive impairments observed in different patient populations. while much of this work has been performed by neuropsychologists evaluating patients with various cognitive difficulties, psychopharmacologists have also examined whether the cognitive changes caused by various drug treatments are selective. For example, benzodiazepines appear to produce a pattern of amnesia that resembles to some degree that seen in patients with Korsakoff’s disease [2]. Benzodiazepine-treated subjects have a severe impairment in their ability to learn episodic information but may not be impaired in their ability to learn skills [14]. An important advantage of acute drug studies in normal volunteers over neuropsychological studies in cognitively impaired patients is that the amnesia can be experimentally produced by drug administration and reversed either by the administration of a pharmacological antagonist or by waiting for the drug to be eliminated from the body. In contrast, in most CNS-impaired patient populations the lesions associated with the behavioral impairments are permanent. The present study examines the effects of alcohol on implicit and explicit memory 1205
1206
R. G. Lwt
K cr I//
processes. Implicit memory processes are those that arc asscsscd in tasks that do not require conscious recollection of previous experiences. In contrast explicit memory, which is assessed in traditional tests of free recall and recognition, requires the conscious recollection of previously presented information 18. 191. Two implicit memory tasks were used. They were derived from the observation that performance on word identification tasks is enhanced if subjects have previously been shown the words to be identified [7, IO, 12,233. One involved the reading of transformed text 17, 121, and the other was a word-completion task 1231. The effect of alcohol on semantic priming [3] was also examined. Two doses of alcohol were studied. the higher dose being chosen so as to give maximum blood alcohol concentrations just under 0.08 g.’100 ml.
METHODS Twentyzight healthy malt student volunteers age 21 35 ~crc rccruitcd bq advertlsment in the University of Maqland student ncwspapcr. They were social drlnkcrs. consuming between 6 and 15 drinks on avcragc per week. Thcl here all given a phyucal and psychiatric evaluation, and blood and urine tests here conducted to screen for possible drug abuse. Subjects acre not allowed to participate of their blood or urine tests wre posti\e. or If thq satialied DSM-III-R criteria for alcohol abuse ‘dependence. or a major psychiatric disorder.
The stimuli used in the study wcrc 3X semantically and phoncmlcallq unrelated seven-letter words. Their frcqucncies ranged from one to more than 100 occurrences per million words L22]. They were dlwdcd mto foul group5 (A. B. <‘ and D). matched for frequenq. of 12words each. For wmc of the st~bjccts (approx. I 3 111 eachdrutl t~catmcnt group) list A v,ordb wrre u\ed 1n the imaging task. list B words in the backwards-reading tahk. 1151c \vords 1n both the Imaging and back\~ards-reading tasks. and list D words were only in the Nerd-completion txk. Similarl! for approximatel! another I 4 ofthe subjects the li\t A ~\ords ncrc used oni) in the word-completion task. list B words in the lrnaglng task. hat c‘ words in the hack\*nrda-reading task. and the list D words In both the imaging and bach\~urd\-re;ldlnp t&s. Half the words from each IISI were used i:l the word-completion tush. In summary. the stimulus list\ were counterbalanced across test condition\.
Alcohol dose W;I\ baxd on each wbject’a body ucipht and ~a\ mlxcd vvlth tonic water (to diaguiae total iolumc of400 ml. Suhjccts drank the mixture through a strau from a beaker ~IIII a Ild In which alcohol had been placed. Thi\ meant that olfactory cues provided by the alcohol could not be used determine N hether or not the> wcrc rccclung an active treatment. They wcrc given I5 min to consume
the taste) to ;I a few drop\ 01 hq sub~ccts to the lxxcragc.
sub~cct~ ucrc KlndOmly assigned to 0111‘ of Ihrec groups rccci\ illg either phccbo (II = Y 1 or one of INo doses 01 alcohol (0.3 g kg. t1= IO. or 0.6 g hp. II = Y). The mean ages of the subjects In each group wcrc 23.7. 2.1 4 and 24.0. rcspccti\cly. On the experimental da!. suhJect\ arrlvcd in the laboratory at approx X a m ‘Thar breath was checked for alcohol wng an Alto-sensor III meter (Into‘tlmeters. St. Louis. MO). The) had been Informed that if alcohol \+a detected thq would not bc pcrmittcd to contintx \lith the study. This did not occur in any ofthe subyxts. Thcj were then giLen :Llowfat brcakf,L\t followed by ;t lwerage containlnp thclr trcatmcnt drink. as described above. One hour after nlcohol :~dmimstration. each \ubjcct W;IS \huun ;t IISI of 23 words, one at ;I time on 4 in. x 6 111. cards. Each \\urd compriacd xvcn lcttcrs typed 1n upper cast. The subject uab asked to rend each word and then imagine a scene involving the word and to rate on ;Lthree-point scale how easy it LVXSto do this. After the In51 ofthe words had been presented. the s~~blect \\a\; ashcd to count backwards by threes from 200 for 2 min. After this. he v,as asked to freely recall II\ many of ;hc words a\ possible.
After the test of free recall. subjects L\Lcrcpre\ented with cards on which uorda had heen typed hack~~ard\. 111 Iowcr-case characler\ (e.g. ragen,\ ). The suhjoct U;L\ asked to read each word so that It made scnx. and the time II took to read each lord uorrcctl! was recorded. I-arty words \+erc used. There wcrc I2 words that the suh~ects had prc! iou\l) been ;&cd to ~magc. I2 aorda that the auhjcct had not praiouslq lmagcd and tight pair\ ofscmanticall> related words le_g. tnedut\. > rarhll: dnomaid. dlarcmcl. The semantically r&ted wc>rds \\crc all of wvcn Icttcrs. and had frequencies that ranged Irom tv,o to greater rhan 100 pet- million [ 221.The uord\ were presented 111a random
EFFECTS OF ALCOHOL
Table
ON MEMORY
1. Experimental
PLACEBO or AUXHOL
oal
1207
PROCESSES
design
(0.3 or 0.6 &kg)
I:00
IMAGE WORDS
I:05
FREE RECALL
DISTRACTOR
BACKWARDS
I:10
READING
NEWS
I 30
I
NEW WORDS
WORDS
WORD COMPL.ETION
I
IMAGED WORDS
I
WORDS READ BACKWARDS
I
WORDS IMAGED ANE READ BACKWARDS
order except that the two members of each semantic pair were preaented in sequence. Semantic priming would be reflected by an increased speed of identifying the second word of each pair as a result of exposure to the first. The presentation of the semantically related pairs was balanced across subjects so that approximately half the subjects read “student” before “library” and the other half read these words in the opposite order.
After the backwards-reading test. subjects were presented with a series of cards on which words with seven letters had been typed, in upper case. In each word. however, three of the characters had been replaced by dashes (e.g. P A I T). The subject was asked to complete the word with the first solution that came to mind (e.g. PIANIST). Twenty-four words were used. There weie six words that the subjects had imaged before. six words that the subjects had read backwards (but not imaged), six words that the subjects had both imaged and read backwards, and six new words. The words were presented 15 min after the backwards-reading task, and the subjects were allowed 45 set to complete each word. The proportion of words from each group that were successfully completed was scored.
Breathalyser readings were taken every 30 min throughout Intoximeter Inc.. St. Louis. MO. Subjects were not allowed concentration was belo\\ 20 mg,,dl.
the study usmg a portable Alto Sensor to be transported home until the blood
II from alcohol
Data were analysed using analysis of variance procedures with drug treatment as the independent factor. For the backwards-reading test, a repeated measures analysis was performed using the median times to read familiar and unfamiliar words for each subject. Since the data appeared to have a skewed distribution a second analysis was performed following a rank transformation [S]. A similar analysis was performed on the median times to read the pairs of semantically related words. For the word-completion task, a repeated measures analysis of variance was performed with prior exposure to words in the backwards-reading and imaging tasks as the two within subject factors.
RESULTS The mean blood alcohol concentrations of the subjects are plotted as a function of time after drug administration in Fig. 1. Alcohol significantly reduced the number of words that
120x
subjects freely recalled [r (2, 25)=4.7. 0.6 g.:kg dose.
K. (i. IJSII
P
K 1’1
Cl/
see Fig. 2. This was due to the effect of the
In the backwards-reading test, words were read faster if they had been imaged previously [I; (I. 15) = 6.5. PC 0.021. There was no etrect of alcohol consumption on the speed of reading (i.e. there was no main effect of alcohol [F (2, 25) = 1.2, P> 0.2]), and alcohol did not reduce priming (i.c. thcrc was no alcohol x familiarity interaction [F (2. 25)= I .45, P>O.2]. Similarly, following the rank transf~~rmation, the mean rank of the words that had been imaged previously was significantly lower than that of the novel words [F (I. 25) = 21.4. P
1209
:
SO
Cl H
40
T
lc
30
2 2
20
10
2
i
i
0
NEWWORDS FAMILIAR WORDS
0
l-
0.3
ALCOHOL
0
SO
n
0.6
(G/KG)
FIRSTWORD SECOND WORD
I
ICC i
0
0.3
0.6
ALCOHOL(G/KG)
Fig. 3. The mean rank of rank. the faster the word prior exposure to material of pairs
the reading speed for words in the backwards-reading task. The lower the was read (see text for details). The top half of the figure shows the effect of in the imaging task. The lower half of the figure shows the speed of reading of semantically related words. Values are means+SEM.
The mean rank of the second member of the semantic pairs was lower than that of the first [F (I, 25)=9.5, P-cO.0051. Again there was no main effect of alcohol on speed of reading [F (2, 25)=0.2. P>O.2] and alcohol did not reduce the degree of priming (i.e. there was no alcohol x order interaction [F (2. 25)=0.3, P>O.2], see Fig. 3. In the word-completion task, there was a significant interaction between reading backwards and imaging [F (1,25) = 16.7, P
ft. G. LIST1 R (‘I I//
0
0.3
0.6
eff‘ects of having previously imaged the words. or having read the words backwards on improving word-completion performance (i.c. there was no alcohol x imaging [F-(2, 25)- 0.41 or al&ho1 x backwards-reading [I;‘ (2, 25) =O.Ol] interactions. P> 0.2 ).
DISCUSSION Consumption of 0.6 g/kg alcohol impaired the ability of subjects to freely rccali information presented to them in an intoxicated state. Similar findings have been reported in numerous other studies and attributed to an impairment in acquisition rather than retrieval processes [I, 1I]. That is, subjects’ free recall of information presented to them in an intoxicated state is not improved by allowing them to sober up. It may be noted, howcvcr. that alcohol in some circumstances has been shown to affect retrieval processes [ 161. While our subjects’ explicit memory was impaired (as assessed by free recall). their memory for the same material appeared intact when tested implicitly both in the backwards-reading and word-completion tests. Both the placebo- and alcohol-treated groups read words that had been typed backwards faster if they had previously been exposed to them in an imaging task. Similarly. both groups were more likely to successfully complete a word if they had imaged it or read it backwards previously. The order of the tests was fixed across subjects, and in the groups that received alcohol, the blood alcohol concentrations declined in the period over which the tests were administered. Thus, blood alcohol concentrations were highest during the explicit tests and lowest during the implicit tests. However, as noted above, previous studies indicate that explicit memory would not have improved by allowing subjects to recall at lower blood alcohol levels [I. 111. A distinction has been made between perceptual and conceptual priming (see e.g. Ref. [24]). It may be noted that in the imaging task. the words were presented in a large, uppercase font, and in the backwards-reading task they were presented in a smaller, lower-case font. Therefore, the priming mechanism would appear not to be purely perceptual. although it may not require high level semantic processing. In the word-completion task. letters wcrc presented in the same case and font-sire as in the imaging task. The increased probability of
tFFECTS OF ALCOHOL 0s MEMORYPKOCESSES
1211
successfully completing words that had previously been imaged, therefore, may reflect purely perceptual priming. However, subjects also successfully completed more words if they had been exposed to them earlier in the backwards-reading task (in the smaller, lower-case font), again suggesting the involvement of some higher level processing in the priming mechanism. Although the exact mechanisms underlying the various types of repetition priming are somewhat unclear, alcohol, at the doses used in the present study, showed no indication of impairing any of them. Neither did alcohol impair priming in the test of short-term semantic priming. In a previous study, HASHTROUDI ef al. [9] reported that alcohol impaired free recall of words, but failed to impair priming in a perceptual identification task. In their study, however, HASHTROUDI et al. found an overall impairment in the ability of intoxicated subjects to correctly identify degraded words regardless of whether they were new or primed. This change in baseline complicates the interpretation of their data. In contrast, in the present study there were no differences between the two groups in their ability to read the new words in the backwards-reading test, or to successfully complete words not shown previously. There are some parallels between the deficits observed in normal volunteers under the influence of alcohol, and those observed in patient populations with a history of long-term alcohol abuse [ 181. For example patients with Korsakoff’s disease are markedly impaired in tests of explicit memory but may be unimpaired if memory is tested implicitly using methods similar to those of the present study. In conclusion, the results of studies in normal subjects as well as in various patient populations have provided good evidence that implicit memory for information (as assessed by tests of priming) is distinct from explicit memory for the same material [S, 19-21,241. The current study provides further support for this suggestion using a pharmacological probe (alcohol) in normal student volunteers. Similar data have come from studies using drugs with different mechanisms of action such as anticholinergics [ 171 and benzodiazepines [6, 141. A~k,loM/edyements~We
are grateful
to Ann Granger
and Mary Rosner for excellent technical
assistance
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