Intact Perceptual Memory in the Absence of Conscious Memory

Transcription

1 Behavoral Neurosccnce 997, Vol. Ill, No. 4, In the publc doman Intact Perceptual Memory n the Absence of Conscous Memory Stephan B. Hamann Unversty of Calforna, San Dego Larry R. Squre Unversty of Calforna, San Dego, and Veterans Affars Medcal Center, San Dego Declaratve memory enables conscous recollecton of the past and has been proposed to be dstnct from prmng, a perceptual form of memory that operates nonconscously and mproves the ablty to detect or dentfy recently presented stmul. Yet, t has been dffcult to obtan unambguous evdence for the ndependence of declaratve memory and prmng. The authors report the frst demonstraton, usng matched tests, of fully ntact perceptual memory (prmng) n a profoundly amnesc patent (E.P.), despte atchance recognton memory. The prmng and recognton tests ncluded tests that were matched wth respect to test materals, length of the study and test lsts, and the knd of cues avalable at test. Prmng appears to reflect neural changes wthn perceptual processng systems that occur before nformaton reaches the bran systems that transform vsual percepton nto conscous vsual memory. An encounter wth a vsual stmulus has several dstnct consequences. The stmulus can later be recalled or recognzed through the effort of conscous recollecton. In addton, the ablty to later detect or dentfy the same stmulus s mproved, a phenomenon known as prmng (Shmamura, 986; Tulvng & Schacter, 990). A major theme of recent work on memory has been the dea that there are multple knds of memory (Gabrel, 99; Schacter & Tulvng, 994; Squre, 992; Weskrantz, 990). For example, declaratve memory s consdered to support conscous rememberng, whereas prmng s expressed nonconscously as a change n performance. Evdence that declaratve memory and prmng are separate comes especally from studes of amnesc patents wth blateral medal temporal lobe or dencephalc lesons, who exhbt ntact prmng but severely mpared declaratve memory (Hamann, Squre, & Schacter, 995; Schacter, Chu, & Ochsner, 993; Squre, Knowlton, & Musen, 993). An alternatve vew that has been dffcult to dscount completely s that both prmng and declaratve memory depend on a sngle, underlyng memory trace (Blaxton, 989; Jerngan & Ostergaard, 993; Masson, 989; Shanks & St. John, 994) and that prmng tests are smply more senstve than declaratve memory tests at detectng whatever resdual memory remans n amnesa. Proponents of Stephan B. Hamann, Department of Psychatry, Unversty of Calforna, San Dego; Larry R. Squre, Departments of Psychatry, Neuroscences, and Psychology, Unversty of Calforna, San Dego, and Veterans Affars Medcal Center, San Dego. Stephan B. Hamann s now at the Department of Psychology, Emory Unversty. Ths work was supported by the Medcal Research Servce of the Department of Veterans Affars, Natonal Insttute of Mental Health, and the McDonnellPew Center for Cogntve Neuroscence, San Dego. We thank J. Moore, J. Zouzouns, and L. Stefanacc for assstance. Correspondence concernng ths artcle should be addressed to Larry R. Squre (6A), Veterans Affars Medcal Center, 3350 La Jolla Vllage Drve, San Dego, Calforna 926. Electronc mal may be sent va Internet to lsqure@ucsd.edu. ths vew have ponted out that the amnesc patents studed to date are only partally amnesc and have resdual declaratve memory that could support performance on prmng tests. For example, even the wellstuded, densely amnesc patent H.M. (Scovlle & Mlner, 957) has some resdual declaratve memory (Corkn, 984; Mlner, Corkn, & Teuber, 968). Concevably, normal prmng could occur n amnesc patents f the relatonshp between resdual declaratve memory and prmng were hghly nonlnear. We addressed ths ssue by assessng declaratve memory and prmng n E.P., a profoundly amnesc patent who has no detectable declaratve memory. Any prmng exhbted by E.P. cannot depend on resdual declaratve memory because he effectvely lacks the capacty for declaratve memory. A fndng of fully ntact prmng n E.P. would therefore provde strong evdence for the multplesystems vew that prmng and conscous recollecton are dstnct forms of memory. Partcpants Method Patent E.P. (Fgure ) s a 74yearold retred laboratory techncan wth 2 years of educaton, who developed profound anterograde and retrograde amnesa n 992 after herpes smplex encephalts (Squre & Knowlton, 995; Table ). Hs amnesa s so severe that after more than 40 testng sessons at hs resdence he does not recognze the examner and denes havng been tested prevously. In addton, he scored at chance on a varety of senstve recognton memory tests, ncludng tests that have detected resdual declaratve memory n patent H.M. For example, E.P. scored 48% correct (chance = 50%) on a test of pcture recognton on whch H.M. scored 78% correct (Freed, Corkn, & Cohen, 987; 40 pctures presented twce at study for 0s each followed after 0 mn by a yesno recognton test). E.P. also scored at chance (48%) on an even easer verson of ths same test (40 dfferent pctures presented sx tmes for study, 5 s each tme, followed after mn by a twoalternatve, forcedchoce recognton test). E.P.'s performance on prmng tests and on recognton tests was compared wth the performance of 7 control volunteers (2 men and 850

2 BRIEF COMMUNICATIONS 85 5 women; Mage = 72. years wth 2. years of educaton) and 3 amnesc patents wth blateral damage to the hppocampal formaton (Table ). Addtonal nformaton about these 3 patents appears elsewhere (Hamann & Squre, 995). Procedure Fgure. (A) Coronal TI weghted magnetc resonance mage of patent E.P. showng extensve blateral damage to the hppocampal formaton (arrows). Note the partcularly severe atrophy of the rght parahppocampal and nferotemporal gyr (left sde of mage). (B) Axal T2weghted mage, showng the extent of blateral medal temporal lobe damage, whch extends from the temporal pole caudally and damages the perrhnal cortex, amygdala, hppocampal formaton, and parahppocampal cortex. In other mages, small foc of damage were apparent n the rght medal and dorsal frontal cortex, and reduced volume of the nsular cortex and nferotemporal gyms was apparently blateral. R = rght; L = left. E.P., along wth the 3 other amnesc patents and the 7 controls, was gven two types of prmng tests and two types of recognton memory tests. For all partcpants, prmng was tested both by word stem completon (6 dfferent tests) and by perceptual dentfcaton for words (2 dfferent tests). Recognton memory was tested both by a yesno procedure (6 dfferent tests) and by a twoalternatve, forcedchoce procedure (6 dfferent tests). Each of these 30 tests was admnstered n an dentcal way by usng dfferent sets of words. For each test, 24 target words were frst presented for study at a 3s/tem rate, preceded and followed by 3 buffer words (2 n the case of perceptual dentfcaton). At study, partcpants smply read each word aloud. Fve mnutes later, a prmng or recognton test was gven. For word stem completon prmng, each test conssted of 48 threeletter word stems (e.g., MOT) presented at a rate of 5 s/tem. Each test began wth 3 practce stems. Partcpants were nstructed to say the frst Englsh word that came to mnd begnnng wth each stem. Twentyfour stems corresponded to study lst words, and the remanng 24 stems corresponded to words that had been predesgnated but had not been studed. These latter stems provded a measure of baselne completon probablty. For perceptual dentfcaton, each test conssted of 48 words (24 studed words and 24 new words). Each word was presented brefly at an exposure duraton (as determned earler by a thresholdng procedure) at whch partcpants could successfully dentfy approxmately 35% of the new words, and each word was followed by a 250ms maskng stmulus (#####). At test, partcpants attempted to dentfy each word by respondng aloud. Guessng was encouraged. All 8 prmng tests were completed before the 2 recognton memory tests were gven. For twoalternatve, forcedchoce recognton, each test conssted of 24 word pars presented one at a tme. Each par conssted of a word from the study lst together wth a nonstuded word ether to the rght or to the left. Partcpants were asked to say aloud the word that had been shown prevously. For yesno recognton, each test conssted of 24 old (studed) and 24 new (nonstuded) words presented one at a tme n a mxed order. Partcpants were asked to say yes f the word had been shown prevously or no f l had not. The full set of 30 studytest sequences (6 word stem completon tests, 2 perceptual dentfcaton tests, 6 yesno recognton tests, Table Characterstcs of Amnesc Patents WMSR Patent Age n years Leson WAISRIQ Attenton Verbal Vsual General Delay A.B. P.M. L.J. M E.P. a HF 04 HF 5 HF <50 57 < Note: The WAISR and the WMSR ndexes yeld a mean score of 00 n the normal populaton wth a standard devaton of 5. The WMSR does not provde scores for partcpants who score below 50. Therefore, the two scores below 50 were scored as 50 for calculatng a group mean. WAISR = Wechsler Adult Intellgence Scale Revsed; WMSR = Wechsler Memory Scale Revsed; HF = hppocampal formaton. a See Fgure.

3 852 BRIEF COMMUNICATIONS and 6 forcedchoce recognton tests') was gven n sx dfferent sessons durng a 4month perod. E.P.'s performance on the prmng tests and on the recognton tests was compared wth the performance of the controls and the 3 amnesc patents. Results On the prmng tests, E.P. performed consstently at the same level as the controls and other amnesc patents for both studed and nonstuded tems (Fgure 2). All three groups exhbted sgnfcant prmng for both stem completon and perceptual dentfcaton: for E.P., t(5) = 2.63, p <.05, and t(\l) = 4.66, p <.00, respectvely; for the amnesc and control groups, all K > 4.3. The amnesc and control groups performed ndstngushably. In addton, E.P. scored hgher than 4 of 7 controls on stem completon and hgher than 6 of 7 controls on perceptual dentfcaton. By contrast, E.P. performed at chance levels on the recognton tests. The amnesc group performed above chance but was mpared relatve to the control group on both yesno recognton and twoalternatve, forcedchoce recognton (rs > 2.9, ps <.05). Thus, E.P. could not recognze as famlar the words he had read 5 mn earler, ether when asked to choose whch of two words was famlar or when asked to say yes or no to ndcate whch words had been presented earler. Nevertheless, when asked to complete threeletter word stems to form the frst word that came to mnd, he performed lke the other partcpants and completed word stems wth words he had read earler substantally more frequently than would be expected f the words had not been presented (29% for studed tems vs. 4% for baselne tems; for amnesc patents, 38% for studed tems vs. 2% for baselne tems; and for controls, 33% for studed tems vs. 6% for baselne tems). Smlarly, when asked to dentfy brefly flashed words, he ,25 * a Stem Completon \ <» t ,25 EM *«0 5 n b Pwcoptu&l lowttflcrtlon T < E.P. AMN CON E.P. AMN CON u * C Foreedchoce R<K:ognlton I X E.P. AMN CON d. \ I ^ re«/n< ResognlHon E.P. AMN CON Fgure 2. (a) Stem completon prmng. Sx prmng tests were gven to patent E.P., amnesc patents (AMN, n = 3), and normal controls (CON, n = 7). Prmng scores were calculated as percentage correct for studed tems mnus percentage correct for baselne tems, (b) Perceptual dentfcaton prmng. Twelve tests were gven to patent E.P, AMN patents, and CON partcpants. Prmng scores were calculated as percentage of correct dentfcatons of studed tems mnus percentage of correct dentfcatons of nonstuded tems, (c) Twoalternatve, forcedchoce recognton. Percentage correct across 6 tests for patent E.P., AMN patents, and CON partcpants, (d) Yes/no recognton. Dscrmnaton accuracy (d'; Green & Swets, 966) s shown across 6 tests for patent E.P., AMN patents, and CON partcpants. Percentage of correct scores (hts plus correct rejectons) was 52%, 65%, and 8% for E.P, AMN patents, and CON partcpants, respectvely. Brackets for E.P. ndcate the standard error of the mean; the data ponts for AMN and CON groups ndcate ndvdual partcpant means across all the tests. Dashed lnes ndcate chance performance.

4 BRIEF COMMUNICATIONS 853 performed lke the other partcpants and dentfed the words that he had read 5 mn earler much better than words he had not read earler (55% correct for studed tems vs. 34% correct for nonstuded tems; for amnesc patents, 5% correct for studed tems vs. 34% correct for nonstuded tems; and for controls, 48% correct for studed tems vs. 32% correct for nonstuded tems). Exposure duraton of test tems was 28.5 ms, 25 ms, and 28 ms for E.P., amnesc patents, and controls, respectvely. Because these data were obtaned across 8 separate prmng tests and 2 separate recognton tests, the results provde a stable and accurate estmate of E.P.'s prmng and recognton memory abltes. Dscusson These fndngs provde compellng evdence that prmng depends on a separate and ndependent memory system from the system that supports declaratve memory. Prmng was fully ntact n patent E.P. even though no declaratve memory could be detected. Thus, prmng s ndependent of conscous memory and ndependent of the medal temporal lobe and the dencephalc bran system that supports conscous memory (Squre & ZolaMorgan, 99). Three prevous studes nvolvng the severely amnesc patents H.M. and K.C. made smlar ponts on the bass of the fndng of spared perceptual prmng n the face of poor recognton memory performance (Gabrel, Mlberg, Keane, & Corkn, 990; Keane, Gabrel, Mapstone, Johnson, & Corkn, 995; Tulvng, Hayman, & Macdonald, 99). However, t was not the objectve of those studes to fnd ntact prmng performance, ntact baselne performance, and atchance recognton performance wth tests that were fully matched wth respect to test materals, length of the study and test lsts, and the knd of cues avalable at test. The present study ncluded a matched par of tests (perceptual dentfcaton and yes no recognton) that was dentcal n all these respects. Each type of test was admnstered a mnmum of sx tmes to assure the relablty of the results. The results provde, to our knowledge, the frst demonstraton of normal prmng scores and normal baselne scores n amnesa despte atchance recognton memory performance on a matched test. An addtonal source of evdence also supports the concluson that perceptual prmng and recognton depend on separate and ndependent memory systems. Two studes reported the reverse dssocaton from the one descrbed here, that s, two patents wth mpared perceptual prmng and ntact recognton (Gabrel, Fleschman, Keane, Remnger, & Morrell, 995; Keane et a!., 995). Three caveats regardng ths dssocaton are (a) the dssocaton was based on only two tests of each type; (b) baselne performance n the prmng test was abnormal n one of the patents (Keane et al., 995; for the mportance of ths ssue, see Hamann et al., 995); and (c) as dscussed by Gabrel et al. (995), recognton memory was not tested n such a way that t clearly depended on the same perceptual operatons that supported prmng. Thus, recognton memory mght sometmes depend on the same perceptual processes that support prmng but depend addtonally on other processes. Nevertheless, these recent fndngs, taken together wth the present results, rule out the dea that perceptual prmng and recognton memory depend on the same, sngle memory system and that prmng tests smply make less strngent demands on ths system than recognton memory tests. The present results also bear on the ssue of when and to what extent recognton memory can be supported by some knd of famlarty process made avalable through prmng (Cermak, Verfaelle, Sweeney, & Jacoby, 992; Dorfman, Khlstrom, Cork, & Msaszek, 995; Mandler, 980). Recognton memory was at chance for E.P. and dd not beneft from the processes underlyng hs fully ntact prmng. These fndngs agree wth prevous suggestons that performance on recognton memory tests s supported entrely by declaratve memory and does not beneft from prmng phenomena (Graf, Shmamura, & Squre, 985; Hast, Shmamura, & Squre, 992; Hayman & Tulvng, 989; Knowlton & Squre, 995; Wagner, Gabrel, & Verfaelle, 997). Gabrel et al. (995) suggested that, when makng recognton memory judgments, normal ndvduals and amnesc patents do not naturally consult the memory system that medates perceptual prmng. Addtonal studes are needed to try to dentfy condtons under whch normal ndvduals mght draw on nformaton avalable from prmng to support recognton judgments (cf. Jacoby & Whtehouse, 989), as well as condtons under whch amnesc patents mght mprove ther recognton performance by drawng on nformaton avalable from the system that supports prmng (cf. Dorfman et al., 995). 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Journal of Expermental Psychology: Learnng, Memory, and Cognton, 23, Weskrantz, L. (990). Problems of learnng and memory: One or multple memory systems? Phlosophcal Transactons of the Royal Socety of London. Seres B. Bologcal Scences, 329, Receved January 4, 997 Accepted January 28, 997