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Perceptual Learning, Awareness, and the Hippocampus

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Perceptual Learning, Awareness, and the Hippocampus HIPPOCAMPUS11:776–782(2001) PerceptualLearning,Awareness,andtheHippocampus JosephR.Manns1 andLarryR.Squire2* 1DepartmentofPsychology,UniversityofCalifornia, SanDiego,California 2VeteranAffairsHealthcareSystem,SanDiego,and DepartmentsofPsychiatry,Neurosciences,and Psychology,UniversityofCalifornia, SanDiego,California ABSTRACT: Declarativememorydependsonthehippocampusand independentofthemedialtemporallobeanddience- relatedmedialtemporallobeanddiencephalicstructures.Declarative phalicstructuresimportantfordeclarativememory. memoryhasusuallybeenfoundtobeavailabletoconsciousrecollection. Afundamentalissueaboutthesememorysystemsis Arecentstudy(ChunandPhelps,NatNeurosci1999;2:844–847)found thatdamagetothemedialtemporallobe(includingthehippocampus) whatcriteria,asidefromanatomy,mightusefullydistin- impairedperformanceonaperceptuallearningtask,yetthelearningwas guishthem.Onecriterionthathasbeenusefulisthat accomplishedintheabsenceofmemoryforthestimuli.Thisfindingraised declarativememorysupportstheflexibleuseofacquired thepossibilitythatsomehippocampus-dependenttasksmaybeinacces- knowledge,whereasnondeclarativememoryismore sibletoawarenessandmaybeperformedwithoutevokingconscious closelytiedtotheoriginallearningsituationandisless memoryprocesses.Usingthesametask,weshowthatwhendamageis confinedlargelytothehippocampalformation,perceptuallearningis accessibletootherresponsesystems(Cohen,1984; intact.Thus,theavailabledatasuggestthatdamagelimitedtothehip- Gliskyetal.,1986a,b;SaundersandWeiskrantz,1989; pocampalformationdoesnotimpairnonconscious(nondeclarative) Eichenbaumetal.,1989,1990;Reberetal.,1996). memory.Further,thedatadonotcontradicttheideathathippocampus- Asecondcriterionisthatdeclarativememorytypically dependentmemoryisaccessibletoconsciousrecollection.Finally,per- includesknowledge,orawareness,aboutwhathasbeen ceptuallearningwasimpairedinpatients,withextensivedamagetothe medialtemporallobeandwithadditionalvariabledamagetolateral learned.Incontrast,nondeclarativememorydoesnot temporalcortex. Hippocampus 2001;11:776–782. requireawarenessofanyconsciousmemorycontent,and Published2001Wiley-Liss,Inc.† whenawarenessispresentitappearstobeepiphenom- enaltotaskperformance(ReberandSquire,1994;Clark KEYWORDS: memory;declarative;nondeclarative;amnesia;medial temporallobe andSquire,1998).Theavailabilityofmaterialtocon- sciousrecollectionhasbeenconsideredakeyfeatureof declarativememoryandhasbeensupposedtobefunda- mentaltothedistinctionbetweendeclarative(hippocam- INTRODUCTION pus-dependent)andnondeclarative(hippocampus-inde- pendent)memorysystems(TulvingandSchacter,1990; Tulving,1991;Schacter,1992;Squire,1992;Eichen- Memoryisnotasinglefacultybutiscomposedofseveraldifferentabilities baum,1997;Gabrieli,1998). thatdependondifferentbrainsystems(SchacterandTulving,1994;Squire Thelinkbetweenawarenessandhippocampus-depen- andZola,1997;Gabrieli,1998).Declarativememorysupportstheabilityto dentlearningwasquestionedinarecentstudyofpercep- acquirenewfactsandeventsanddependsontheintegrityofthehippocam- tuallearning(ChunandPhelps,1999).Oneachtrial, pusandanatomicallyrelatedstructuresinthemedialtemporallobeand healthycontrolssearchedfora90°-rotated,coloredT diencephalon.Nondeclarativememorysupportsskillandhabitlearning, amongcoloredrightangles,andindicatedthedirection simpleformsofconditioning,andotherformsoflearningthatareexpressed inwhichitsbasewaspointing.Afterpractice,they throughperformanceratherthanrecollection.Nondeclarativememoryis searchedrepeateddisplaysfasterthannewdisplays.Am- nesicpatientswithdamageinthemedialtemporallobe (includingthehippocampus)didnotshowthisadvan- Grantsponsor:MedicalResearchServiceofVeteransAffairsHealthcare tageforrepeateddisplays.Interestingly,despitethefact System;Grantsponsor:NIMHgrant;Grantnumber:MH24600;Grant thatthetaskappearedsensitivetoamnesia,taskknowl- sponsor:MetropolitanLifeFoundation. edgewasnotaccessibletoawareness.Neithercontrols *Correspondenceto:LarryR.Squire,Ph.D.,DepartmentofVeteransAffairs noramnesicpatientscouldrecognizewhichdisplayswere (116A), 3350 La Jolla Village Drive, San Diego, CA 92161. E-mail:[email protected] repeated.Theseresultssuggestthatlearningcanbede- Acceptedforpublication12June2001 pendentonthehippocampusyetinaccessibletoaware- ness. Published2001WILEY-LISS,INC. †ThisarticleisaUSgovernmentworkand,assuch,is inthepublicdomainintheUnitedStatesofAmerica. DOI10.1002/hipo.1093 _________________________________ PERCEPTUAL LEARNING, AWARENESS, AND HIPPOCAMPUS 777 TABLE 1. Performance on Standard Memory Testsa Paired associates Diagram Word Word Patient Group recall Trial 1 Trial 2 Trial 3 recall (%) recognition (%) A.B. Hϩ 4 1 1 1 33 83 H.C. Hϩ 7 0 4 5 37 85 L.J. Hϩ 3 0 0 0 40 93 M.J. Hϩ 7 3 5 6 44 81 P.H. Hϩ 3 0 0 1 31 81 E.P. MTLϩ 0 0 0 0 24 65 G.P. MTLϩ 2 0 0 0 35 54 G.T. MTLϩ 0 0 0 0 20 70 Control M (n ϭ 8) 20.6 6.0 7.6 8.9 71.0 97.4 aThe diagram recall score is based on the delayed (12-min) reproduction of the Rey-Osterrieth figure (Osterrieth, 1944; maximum score ϭ 36). The paired-associates score is the number of word pairs recalled on three successive trials (maximum score ϭ 10 per trial). The word recall score is the mean percentage of 15 words recalled across five successive study-test trials (Rey, 1964). The word recognition score is the mean percentage of words identified correctly across five successive study and test trials (yes-no recognition of 15 new words and 15 old words). The mean scores for controls are from Squire and Shimamura (1986). Hϩ, damage to the hippocampal region and, in H.C. and P.H., to the parahippocampal gyrus. MTLϩ, large medial temporal lobe lesions and variable damage to anterolateral temporal cortex. A consideration of the neuropathology in the four amnesic pa- parahippocampal gyrus. The other 3 patients (MTLϩ) sustained tients who were tested suggests a different way to understand the extensive damage to the medial temporal lobe as a result of enceph- findings. Two of the 4 amnesic patients sustained damage to the alitis and also have variable damage to the lateral temporal cortex. medial temporal lobe as a result of encephalitis and “showed some additional atrophy of the surrounding temporal lobe consistent with this etiology.” (Chun and Phelps, 1999). Thus, for these 2 patients, the inability to benefit from the repeated displays may METHODS have been due, not to hippocampal damage, but to damage to the entorhinal, perirhinal, and parahippocampal cortices, or to the Five amnesic patients (4 men and 1 woman) with damage either lateral temporal cortex. Further, radiological information (from a limited to the hippocampal region (CA fields, dentate gyrus, and relatively insensitive CAT scan) was available for only 1 of the other 2 patients. Thus, it is unclear what damage was responsible subicular complex) or with some additional damage to the para- for the impairment that these patients exhibited. hippocampal gyrus were tested on the same task used by Chun and In another study (Ryan et al., 2000), participants viewed a scene Phelps (1999). Twenty-three controls (8 men and 15 women) were and then viewed it again after a change had sometimes been made also tested, 15 on the standard version of the task and 8 on a more Ϯ in one region of the scene. Controls, but not amnesic patients, difficult version (see below). The amnesic patients averaged 60.0 Ϯ ϭ Ϯ Ϯ tended to look more at the region of the scene in which the change 6.4 years of age (mean SEM; controls 66.9 1.1) and 17.8 ϭ Ϯ had occurred. By one measure (number of transitions into and out 1.7 years of education (controls 15.3 .5), and obtained an of the critical region), the effect appeared to occur only for those average Wechsler Adult Intelligence Scale-III (WAIS-III) score of controls who were unable to specify how the scene had changed. By 102.8 (subscale scores of 19.3 for Information and 55.5 for Vo- ϭ another measure (proportion of fixations in the critical region), cabulary; controls 22.4 and 57.4, respectively). aware and unaware subjects performed similarly. It was suggested The amnesic patients have moderately severe memory impair- that awareness might not always be needed for the expression of ment. All require supervisory care and are unable to live indepen- declarative memory. No anatomical information was provided for dently. Table 1 shows their performance on standard memory the amnesic patients, so that it is unclear what particular damage tasks. Immediate and delayed (12-min) recall of a short prose pas- might have been important. sage (Gilbert et al., 1968) averaged 5.8 and 0.0 segments, respec- We tested 8 amnesic patients on the same test of perceptual tively (maximum number of segments ϭ 21). The 23 controls learning that was used by Chun and Phelps (1999). Five of the recalled 7.8 and 6.4 segments, respectively. The patients averaged amnesic patients (Hϩ) have damage that appears to be restricted 106.0, 71.4, 72.2, 64.6, and 51.6 on the five indices of the Wech- either to the hippocampal region (CA fields, dentate gyrus, and sler Memory Scale-Revised (attention/concentration, verbal mem- subicular complex) or to involve some additional damage to the ory, nonverbal memory, general memory, and delayed memory, 778 MANNS AND SQUIRE respectively; each index yields a mean score of 100 in the normal prose passage (Gilbert et al., 1968) averaged 1.7 and 0.0 segments, population, with a standard deviation of 15). The memory impair- respectively (maximum number of segments ϭ 21). ment occurs in the context of otherwise intact cognition. For ex- For these 3 patients, MRI studies revealed extensive
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