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Neuropsychological Evidence for a Topographical Learning Mechanism in Parahippocampal Cortex

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Neuropsychological Evidence for a Topographical Learning Mechanism in Parahippocampal Cortex supplied as Poewrpoitn files, coped into document [1, 2, 3, 4, 5,6,7, 9, 11,] Scanned & edited [8, 10, 12] COGNITIVE NEUROPSYCHOLOGY, 2001, 18 (6), 481–508 NEUROPSYCHOLOGICAL EVIDENCE FOR A TOPOGRAPHICAL LEARNING MECHANISM IN PARAHIPPOCAMPAL CORTEX Russell Epstein Medical Research Council Cognition and Brain Sciences Unit, Cambridge, UK and MIT Department of Brain and Cognitive Sciences, Cambridge, USA Edgar A. DeYoe Medical College of Wisconsin, Milwaukee, USA Daniel Z. Press Beth Israel Deaconess Medical Center, Boston, USA Allyson C. Rosen Stanford University, Stanford, USA Nancy Kanwisher MIT Department of Brain and Cognitive Sciences, Cambridge, USA The ParahippocampalPlace Area (PPA;Epstein &Kanwisher, 1998)is a region within posterior parahippocampal cortex that respondsselectively to visual stimuli that conveyinformation about the layoutof localspace. Here wedescribe twopatients whosuffered damage tothe PPAafter vascular inci - dents.Both subsequently exhibited memory problems fortopographical materials and were unable to navigate unassisted in unfamiliar environments. Performance onacontinuous n -back visualmemory test wassignificantly lowerfor novel scene -likestimuli than fornovel object -likestimuli. In contrast, performance wasnormal ona famouslandmark recognition taskand ontwo perceptual tasksthat required on-line analysisof scene geometry. Bothpatients were able toproduce accurate maps of premorbidly learned placesbut were unable toproduce accurate maps ofnew places.These results con - verge with previous neuroimaging workto demonstrate that the PPA(1)is selectively involved in pro - cessing information about the geometry ofsurrounding space,and (2)may playa more critical rolein the encoding ofthis information into memory than in the initial perceptual processing,recognition, or recall of this information. Requests forreprints shouldbe addressedto RussellEpstein, MRC Cognition &Brain Sciences Unit, 15Chaucer Road,Cam - bridge CB2 2EF,UK (Tel:+44 (0) 1223 -355-294,ext. 800; Fax: +44 (0)1223 -359-062;Email: russell.epstein@mrc -cbu.cam.ac.uk). Wethank Damian Stanleyand Alison Harrisfor assistance with these experiments, Stephan Heckersand Facundo Manes for anatomical advice,Kim Graham forcomments on the manuscript, TomHammeke foradvice about neuropsychologicaltests, Matthew Brett forassistance with MRInormalisation, and MarvinChun, Frances Wang,and Liz Spelkefor helpful discussions. In addition, we wouldalso like to expressour thanks to GRand COfortheir cheerfuland enthusiastic participation in this research.This research was supported by NIMHpostdoctoral fellowship MH11459 to RE,NEI and NIMHgrants EY10244and MH51358to EAD, and NIMH grant MH56037 to NK. Ó 2001 Psychology Press Ltd 481 http://www.tandf.co.uk/journals/pp/02643294.html DOI:10.1080/02643290042000215 EPSTEINET AL. INTRODUCTION McCarthy, Evans, &Hodges,1996; Whiteley & Warrington, 1978). Allmobile organisms must solvethe fundamental Based oncomprehensive review of the topo - problemof navigation. One way togain insight into graphical disorientationliterature, Aguirre and thecognitive and neural mechanisms underlying D’Esposito(1999) argued that thelingual - navigation is toinvestigate thefunctional organisa - parahippocampal regionis oneof several areas that tionof thebrain areas involved.Research onani - are critically involvedin navigation. Damage tothis mals and humans has suggestedthat anumber of regionoften results in an inability touse salient top - regionsplay arole,including theparietal lobes ographical features such as landscapes and build - (Stark,Coslett, & Saffran, 1996),retrosplenial cor - ings toorient oneself (“ landmark agnosia,”e.g., tex(Chen, Lin,Green, Barnes, &McNaughton, Landis etal.,1986; Pallis, 1955) or in amoregen - 1994),hippocampus (Maguire etal.,1998; O’ Keefe eralinability tolearn new topographical informa - &Nadel,1978), and parahippocampal cortex tion(“ anterograde disorientation,” e.g., Habib & (Aguirre,Detre, Alsop, & D’Esposito,1996; Sirigu,1987, patients 1and 2).In arecentstudy of Bohbotet al., 1998). Here we focus onpara - 127patients withfocal lesions,Barrash, Damasio, hippocampalcortex. We describetwo patients who Adolphs,and Tranel (2000)observed that patients suffered damage tothis regionof cortex after vascu - withdamage tothis regionalmost always displayed lar incidents.Both subsequently developedsevere severeimpairment ona real -worldroute learning deficits in thetopographical domain, which we task. Furthermore,Bohbot et al.(1998) found that defineas thedomain of information relevantto patients withright -hemisphereparahippocampal spatial navigation. cortexlesions were impaired at ahuman analogue Previous reportsin theneuropsychological liter - oftheMorris water maze task in whichthey were ature have describedpatients with“ topographical requiredto remember the location of ahiddenfloor disorientation,”who are unable tosuccessfully find platformwithin aroom(a deficitnot found in theirway throughlocomotor space but donot patients whosedamage was restrictedto the hippo - exhibitgeneral cognitive or memory impairments campus proper). (seeAguirre & D’Esposito,1999, for review). The Neuroimaging studies have also implicatedthe nature ofthespecific problemvaries frompatient to lingual-parahippocampal regionin navigation. patient.For example,some patients showan inabil - Severalstudies have examinedbrain activity innor - ity tounderstand spatial relationships betweendif - malsubjects during performanceof a number of ferentlocations (Levine, Warach, &Farah, 1985, navigational tasks, including navigation througha patient 2),whereas others are unable torecognise virtual realityenvironment (Aguirre etal., 1996), navigationally relevantstimuli such as landmarks watching videotapesdepicting navigation through but can accurately describeroutes between the arealenvironment (Maguire, Frackowiak, &Frith, places theycannot identify(Pallis, 1955).Patients 1997),and mentallyimagining navigation through also differin theirrelative ability tohandle novel vs. arealenvironment (Ghaem etal.,1997; Maguire et familiar topographicalinformation. Someare able al.,1998). All ofthesestudies found greateractiva - tonavigate throughfamiliar environmentsor recall tionin theparahippocampal region(and sometimes oldtopographical information but cannot learn othermedial temporal regions as well,Ghaem et novelenvironments (Habib &Sirigu,1987, al.,1997; Maguire etal.,1997, 1998) when the nav - patients 1and 2;Ross, 1980;Teng &Squire,1999), igation task was comparedto a lessnavigationally whereasothers are impairedat bothlearning ofnew demanding control task. materials and recognition/recallof old materials What roledoes parahippocampal cortexplay in (Habib &Sirigu,1987, patients 3and 4;Incisa thesenavigational tasks? In earlierwork, we dellaRocchetta, Cipolotti, & Warrington, 1996; addressedthis question by using fMRI toexamine Landis, Cummings, Benson,& Palmer,1986; neural activity in parahippocampal cortexand other 482 COGNITIVE NEUROPSYCHOLOGY,2001,18 (6) PARAHIPPOCAMPUS &TOPOGRAPHICALLEARNING brain regionswhile subjects vieweda widevariety of infants (Hermer& Spelke,1994, 1996; Hermer - visual stimuli (Epstein &Kanwisher,1998). We Vazquez, Spelke,& Katsnelson,1999) that suggest foundthat aregionabutting thecollateral sulcus that information about thegeometry of surround - near theparahippocampal -lingual boundary ing space—the “ lay oftheland” — plays aprivileged respondedsignificantly morestrongly when sub - role in orientation and navigation. jectsviewed navigationally relevantstimuli such as What specific cognitivetask doesthe PPA per - streetscenes, landscapes, orbuildings than when form?Given thefact that landmark agnosia often theyviewed other kinds ofvisual stimuli such as results fromparahippocampal -lingual damage faces, objects,or scrambled scenes 1.This response (Landis etal., 1986), one might hypothesisethat was found evenwhen subjects simply watchedthe theprimary roleof thePPA is placerecognition: stimuli passively and werenot required to perform identification offamiliar locationsbased ontheir any navigational task. Wenamed this regionthe appearance and/orgeometric structure. If so,one “parahippocampal placearea,” or PPA, because it might expectthe PPA to besensitive tothe novelty/ respondedstrongly to depictions of places. The familiarity ofthe place depicted in thestimulus. PPAappears tooverlap with the regions activated However,we found that thePPA responds just as in previous neuroimaging studies ofnavigation stronglyto photographs of unfamiliar places (i.e., (e.g., Aguirre et al., 1996). places thesubjects had nevervisited) as it doesto Acritical determinantof PPA activation photographsof familiar places (Epstein etal., 1999, appears tobethe presence in thestimulus ofinfor - Expt.1). In contrast, thePPA is sensitive tothe mation about theshape orlayoutof theimmediate novelty/familiarity ofthestimulus itself,respond - environment.The PPA responds no more strongly ing morestrongly to new photographs than topho - tophotographs of roomsfilled with furniture and tographs viewedmany timespreviously even when objectsthan it doesto photographs of the same allthe photographs depict unfamiliar places roomsempty of all objects (i.e., just bare walls).It (Epstein etal.,1999, Expt. 4). From theseresults, also respondsmuch morestrongly to “ scenes”made weinferred that thePPA is moreinvolved in outof Legoblocks (which have ageometricstruc - encodinga representationof the spatial structure of turesimilar toa roomor streetscene) than itdoes
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