roFreund & Pettman.U.K Revierrs in theNeuroscience:. 17. 99- 109 ( 20t)6)

From Movementto Transitivity:The Roleof Hippocampal ParallelMaps in ConfiguralLearning

LuciaF. Jacobs

Departmentof Psycholog,,,University of California at Berkeley,CA, USA

SYNOPSIS KEYWORDS

Whether spatial is a specialcase of cognitive map, evolution, relational, transitive configural or relational learning, or whether inference.transvcrse patterning abstract principles evolved from the concrete needto navigatein space,is a questionof long- INTRODUCTION standing debate. The parallel map theory of hippocampalfunction offers a resolutionof the Somehow the allows the ver- 'spatial debate by redefining learning' as two tebrate brain to orient itself in external space. parallel, geometricprocesses, Euclidean metric updating new exploratory forays and carrying and topological.Moreover, these processesare around a referencevalue for future detours and subserved by independent hippocampal sub- shortcuts.Somehow it doesthis withoutan obvious fields that underlie two ways of representing topographiccode in the spatialpattern offiring. and space,the bearing and the sketch map. It is somehowthis ability is relatedto episodicmemory possiblethat configural and relationallearning, l6l. Did this remarkableability to associatethings like spatial learning, should also be distinguish- (whether real or abstract),flexibly rearrangeand ed in this way. Transitive inference,requiring encodethe new relationshipsevolve from the need the constructionof a value gradient, could be for spatialorientation? Or was c'rrientingin spacea analyzed as a Euclidean metric problem. In new applicationfor a recently evolved, flerible contrast,transverse patterning could be seenas cognitivetool? a topologicalanalysis of the relationshipsamong The parallel map theory of hippocampalfunc- discreteobjects. If this interpretationis correct, tion, a new model derivedfrom ethologicalprin- lesionsto the primary bearing map structure ciples of spatial orientationand based on the (dentategyrus) should impair transitivify while evolutionaryhistory of the medialpallium, atternpts lesions to the primary sketch map structure to addressthese questions /21 ,221. What had been (CAl) should impair transversepatterning and lacking in the literatureon the behavioralneuro- similar topological tasks. Recent results from scienceof the hippocampuswas an understanding diversespecies and tasks lend support to these of spatial lean-ringin the context of vertebrate predictions, suggestingthat the hippocampus evolution.Folloiving in the footstepsof ethologists, not only creates parallel maps but uses these suchas Kramerand Wallraffl45l,the parallelmap maps to solve more abstract configural or theory defined two ways that learningcould be relationalproblems. 'spatial':orienting to vectors(stinruli with rnagrri- tude and direction)and orientingr.vithin arravs of objects.The theoryalso proposedthat the hippo- campusprocesses these data separatelyinto the Reprintaddress: 'bearing map' (mediatedby the dentate gvrus LuciaJacobs 'sketch (mediated Departmentof [DCi])and the map' by the CAl TolmanHall subfield of Amnron's horn). The parallel map Universityof California theorythus provided a frameu'orkfor two tvpesof Berkeley,CA 94720-1650,USA geometries- Euclideanmetric and topological- to email: [email protected] vot-IrME17. No. r-2.2006 100 I,.F,JACOBS be integratedby the hippocampalformation (HPF). Wielding both maps together,a bird or mammal Becausethe two systemsrely on differentclasses of can determine the shortest route between two inputs (vectoror scalar).the theory predictsthat objectsin areasthat had not beenpreviously joined hippocampalsubfields are differentially activated by common exploratorypathways. Connecting the by explorationusing these two classesof cues.For disconnected sketch maps, by virtue of their example.the bearing map is constructedfrom encoding to the bearing map scaffold, is the gradedstimuli n'ith magnitudeand direction;i.e.. functionof CA3 121,221and indeedis the 'pattern where the magnitude of the relevant parameter completion'function discussed by others/28/. (size,loudness, color, chemical concentration, tem- It has iong beenrecognized that the three best- perature,altitude) changespredictably with the studiedhippocampal subfields (DG, CA3, CA1) directionof self-movement.Such gradedstimuli havedifferent computational properties by virtue of provide the axesof the bearingmap Cartesiangrid their neural architecture118,421. The parallel map (Fig 1A), which then acts as a scaffolding, theory offers a functionaland phylogeneticframe- allowing the integrationof multiple sketchmaps work for the mechanicsof thesedifferences - why (Fig. 1B) to the underlyingbearing map, creating eachfunction is found in eachsubfield, based on its the integratedmap (Fig. 1C). In contrastto the evolutionaryhistory. Another implication of this permanentdirectional axes provided by the bearing theoryis that thesethree subfields each constructs a map. the sketch map is an ephemeralrepresen- different type of map: DG (bearingmap). calcula- tation. created for the permanent encoding of ting a grid from intersectingvectors (Fig. lA);CAl objectsupon the bearingmap scaffold.An indivi- (sketchmap), calculatingthe relativeposition of dual sketchmap is a snapshotof the objectsin a objects(Fig. 1B); and CA3, integratingthe vector local area: the panoramicview from a single and scalarinformation in the integratedmap (Fig. vantagepoint rvhere the objects in the array are 1C). If the threemaps (Fig. 1: bearing,sketch and individuallyencoded and henceno one object is integrated)make fundamentallydifferent calcula- necessaryfor the retrievalof the map.The natureof tions,then evolutionary specialization arising from sketch maps is thus more topological than thesesubfields should show computationalhomo- Euclideanmetric: it is not the absolutedistance that logy,at leastat the level of function.For example. distinguishesone obiect or one sketchmap from thesefunctions could be: bearingmap/DG: extra- the otherbut the uniquespatial relationship among polationof gradedstimuli; sketch map/CA1: topology ob.jects.Because topology determinesorder in of object-definingstimuli; integratedmap/CA3: r.l'hichobjects are encountered(not necessarilythe aligningtopological and Euclidean metric maps via distancebetu,een them), temporal order would be extrapolationand pattern completion. an emergentpropefiy of sketch map encoding. Of these,the ability to calculateone's current 'super' Finally.for speciessuch as homing pigeons. positionby the rateof changeof a gradedstimulus. sketchmaps. established by high aerialflight. may and usingthis rateto projectthe distancerequired vie with the bearingmap asa tool for long-distance to reach the source, might be consideredthe navigation.We have revieweddifferent levels of ancestralmapping function. All mobile animals experimentalevidence for the parallelhippocampus may orientin spaceusing simple movement rules to mapselsewhere l2l.22l . exploitthe gradednature of stimuli in the physical world. An animal can use a taxis, for example. REDUNDANCYAND INTECRATION whetherphoto-, chemo- or othermodality, to move up or down an intensitygradient. detecting the 1'he pow'er of hippocampal processing is the magnitudeand the directionof a constructedvector manner by which the bearing and sketch maps of intensity1131.ln contrast, representing the topo- combine to create the emergent integrated map. logy of objectsin an array requiresboth image- This nrap can combine the extrapolatorypower of forming sensorystructures and considerablework- bearing map vectors with the specificity and detail ing /13/. Finally, the integrationand extra- of relationshipsamong objects in the sketchmap. polationbetween non-contiguous arrays in orderto

RtiVIEWSIN I'HENEUROSCIENCIES PARALLEL MAPS AND CONFI(JI,]RAT-I,EARNING t0l

A)BEARINGMAP B C) INTEGRATEDMAP

t B) SKETCH

h

r +l ib ,u '.e d/ D.'

Fig. l: Parallelmap theory.A) Bearingmap. Directionalcues indicared by capitalletters; size of letterindicates intensity of stimulus.Arrow indicatesdirection of gradient.B) Sketch maps.Positionalcues indicatedby lower case letters. C) Integratedmap. Seetext for explanation.

make a novel shortcut appearsto be an ability' For this reason, following the publication of foundto dateonly in birdsand mammals 114,401. O'Keefe's and Nadel's "The Hippocampusas a Cognitive Map" 1291,the relative importanceof THE ESSENTIALHIPPOCAMPAL CALCULATION: spatial versus working memory as the primary SPATIAL, WORKING OR CONFIGURAL LEARNING function of the HPF was a sourceof greatdebate, eventually settled by Olton, who concluded the What the parallel maps have in sommon, hippocampusis involvedin bothactivities l3ll. The however, is the encoding of stimuli that are working/ debate, however, was perceivedeither simultaneouslyor within the almost immediatelyreplaced by a new challenge window of u,orkingmemory. Spatial data (whether from Rudy, Sutherlandand colleaguesii,36,38i pointsexperienced as one movesup a gradientor andlater Eichenbaurn and colleagues /8,15/. Rather objectsperceived in relationto eachother) can be than working memory,a different kind of general bridged via working memory. to hold multiple learning was proposed: configural or relational stimuliand their locationssimultaneously in mind. learning,respectively. This type of learninghas had

volUME t7.NO. r-2. 2006 t02 L.F.JACOBS many definitions,but for presentpurposes, I will gradient of samplesordered by intensity. Therefore rely on the following definition by McDonald: "an orderingdiscrete objects (Fig. 24, stimuli A-F) or associationcomprising more than one distinguish- successivesamples may require essentially the able cue. Both the configural cue and the individual samecalculation. In both cases,what is constructed cues that it includescan be used independentlyas is both order and distance,whether the stimulus to information about the situation in which they are be encodedis a sample from a gradient or is itself found. That is, the meaningor significanceof the a separate,discrete stimulus. The result is a individual cues is different when they occur alone Euclidean linear representationof value. Such a and when they occur as part of the configuralcue. representation differs fundamentally from the Accordingto Sutherland'sand Rudy's theory,con- analysisof relative position that characterizesthe figural cues representboth spatial and nonspatial topologyof discreteobjects (e.g., Fig. 1B). information.This is becausespatial informationis The input into this map of relative value must made up of a series of configural associations come, as does most information, through some relatingthe individuallocations within any environ- form of conditioning.There has been an ongoing ment. Thus spatial maps are a special, complex debate on the nature uf configural leaming: Is caseof configurallearning." l24l. transitiveinference spatial or can it be derivedfrom Anotherpossibility, of course,is that configural/ conditioningprinciples, without recourseto spatial relational learning evolved as a type of spatial learning assumptions?Recently, Rudy and col- leaming.For example,if the sketchmap evolvedas leagueshave brought the two sides of this debate a new way of encoding simultaneous(or near- much closer with a new body of theoreticaland simultaneouslyperceived) stimuli, the spatialquality empirical work /16,43l. What they propose is a of this map is in its topologyand not in the distance reformulation of the value transfer theory of tran- between objects. Becausemany researcherscon- sitivity, as originally proposed1441. In the value sider spatialas synonymouswith Euclideanmetric, transfer explanation of transitive inference (Fig. non-metricspatial geometries, such as topology,are 2A), the animal learnsa*b'. Basedon conditioning describedas 'non-spatial'/35/. A classicexample theories, however, the value of b, having been of such a topological problem is the transverse establishedin the contextofa, is neverindependent patteming problem: a-b-, b-c-, c*a-, where one of a, regardlessof the actualreinforcement history stimulus in a set of two predicts the pattern of of b. The associationof a's value can therefore reinforcement.The arrangementof the cuesin this affect the value assignedto b, as value 'bleeds' problemis shownin Figure2C. It is not a problem from a to b or vice versa1261. Thus if a*b-learning that can be solvedby a gradient;in fact, settingup a is followed by the new associations(b* and c), the transitivityproblem in which the last premisepair value of c has already been predeterminedby its is linked to the first premisepair severelyimpairs a relationshipto b, which hasan existingrelationship laboratoryrat's ability to make the transitiveinfer- with a. As has beenargued eloquently by Rescorla, ence 1341.This result, among others derived from conditioning is a complex, flexible and cognitive studiesof children 13,201and adult humansll0l, processand the value of stimuli is often coloredby suggestedthat premise pairs are ordered and the contextin which they previouslyappeared /33/. encodedmetrically on a linear gradientof value An example of a value gradient would be (Fig.24, B). Sucha gradientcould be usedto order transitivity,measured by the ability of an animalto objectsthat differ in value, e.g., best to worst. make a transitiveinference (TI): if A>B and B>C, Instead of calculating a gradient from discrete then A>C. The ability to show this type of reason- samples,ordered in one dimensionsuch as intensity, ing in non-humanswas first demonstratedin the onecould calculate a gradientas a seriesof objects squinel monkey l25lbut sincethen has been shown of known value. As an example, an olfactory in a number of mammalian and avian species gradientmust be sampledwith discretesniffs; these (Table l). If the reinforcementhistory of one item could be used to constructa continuousgradient in a premisepair influencesthe other item in that through extrapolationbetween samples or as a pair, then it will also influence performancein

REVIEWSIN THENEUROSCIENCES PARALLEL MAPS AND CONFICURAL LEARNING 103

A)TRANSITIVE INFERENCE 1-series probtem

i"bcde- b-d ^ + cesr i ii b*o q,- r

B)TRANSITIVE INFERENCE 2-series orobtem

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test b, c v.i

ix trz

C) TRANSVERSEPATTERNING E) CONDITIONALCONTEXT

,\ i /l,/\ "-b. I <__ x Y I) F) BtCONDtTtONALCONTEXT

D) NEGATIVEPATTERNING

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Fig,2: Configurallearning tasks. A) Transitiveinference, single-series problem. B) Transitiveinference, two-series problem: shadingdemarcates the two series(ABC, XYZ). C) Transversepatterning. D) Negativepatterning. E) Conditional context.F) Biconditionalcontext. voLUME 17.NO. l-2.2006 101 t_F' .l,AcoBS

TABLEI Patternofresults ofconfigural tasks in five specres

Species Task Version Lesion Result Referenceno.

Rat NP Go/no-go;visual HP Irnpaired l36l Rat NP Leverpress; visual HP Facilitated ^7I

Rat NP Leverpress; visual HP No effectof lesion t9t -fl Rat 2-series;scented sand HP Impaired t5t Rat NP Leverpress; visual FF or HP impairedNP, BC l24l CD HP FF - no effect BC

Rat TI 1-series(A-E); scentedsand FF or Impaired tllt retroEC

Rat TVP ABC; scentedsand FF or Impaired t12t periEC

Rat TVP ABC; touch-screenvisuals FF Facilitated t7/

Rat TI l-series(A-F): scented sand CorrectBE, not BD t43t

Mouse TVP ABCI scentedsand CAI- Impaired t3st NMDA

Mouse TI l-series:scented sanc Aging Impaired t30t

Rhesus TI 2-series;visual (cookies) r,L Impaired t4t monkey

Pigeon TI 1-series(A-E); visual CorrectBD inference t44t Pigeon TI 2-series;visual HP No effectof lesion t31t

Human TI 2-series:'u'isual HP activation /)zl

Human TI l -series(A-E); visual AnteriorHP activation t19t

BC - biconditionaldiscrimination; CD = conditionaldiscrimination; EC = entorhinalcortex; FF = fimbria-fornix;HP - hippocampus:NP = negativepatterning; TI - transitiveinference; TVP - transversepatlerning. Rat, pigeon and mouse arecommon laboratory' strarns.

unrervardedprobe tests. In mosttests of transitivity result is not predictedby any other model of in non-humans.a f-rve-itemlist is usedand the test transitiveinference. yet this is exactlythe result for transitir.'ityis anchoredupon choosing B overD obtainedwith the laboratoryrat (Table l) (1431). rvhenthat novel pair is presented(Table 1). When Frank el al. have presenteda computationalmodel the serieslength is increasedfrom five to six, fbr this resultthat computes how conditioningwith however.an interestingsituation develops. Now simple stimuli can lead to the constructionof a several internal pairs can be used to measure gradedrelationship among them; in their words,a 'gradient transitivitv.such as BD and BE. In this case,value of associativestrength' /1 6/. transferpredicts that rats shouldchoose B in the Such a gradientis functionally identicalto the presenceof E but not in the presenceof D. This ideaof a spatialrelationship. Just as the rat cannot

REVIEWSIN TI IE NELIROSCIIINCES PARALLELMAPS AND CONFIGURALLEARNING solve the transitive inferenceproblem when pre- pattemingand biconditionaldiscrimination). Table mises are trained in a circular spacel34l so can 1 summarizesthe major studiesby task, lesion and pigeonsnot solve the transitiveinference problem species,while the tasksused in Table I are shown in an explicit test of the value transfertheory when in schematicform for comparisonin Figure 2. The two serialproblems are linked end to end, essenti- effects of lesions on these classesof confisural ally forming a circular, and hence nonsensical, learninsare summarized below. gradient l44l. lf, however, two logical series are linked one to the other,forming a seriesof greater MAP AND EUCLIDEAN length,then monkeyscan extrapolatefrom one to THE BEARING METRIC TASKS the other, solving TI problemsnot only within but betweensuch logical series,despite learning them Becauseof the proposedanatomical basis of the in isolatedpairs 1411. parallel maps, lesions of the fimbria-fornix (FF) shouldhave a proportionatelygreater impact on the ROLEOF THE PARALLEL MAPS bearingmap than on the sketchmap 1221. Therefore IN CONFIGURAL LEARNING the FF lesion should selectivelyimpair Euclidean metric tasks, such as l- and 2-series transitive Basedon Rudy and colleagues'model of value inferencetasks (Fig. 2A,B) and have little effect on transfer 116,431,one could make the argumentthat topological tasks (Fig. 2C,D,F). For example, value transferunderlies the constructionof spatial Dusek et al. found that FF lesions impaired per- gradientsand henceis the link from conditioningto formanceon the l-series TI task in the rat. using spatialrepresentation. The bearingmap, for exam- olfactory stimuli /11/. The parallel map inter- ple, might use value transfer as a mechanismto pretationof this result is thereforethat the metric constructspatial vectors. This has two important task was impaired by a bearing map lesion. In a implications for the understanding of spatial secondstudy of the effect of lesionson configural learning.First, transitiveinference should be medi- tasks,McDonald et al. l24lcomparedlesions of the ated by the bearing map, in particular the dentate FF and the hippocampusproper (HP) on three gyrus - a conclusion reached independentlyby configuraltasks, using visual and auditory stimuli: Frank e/ al, 116l, based on their computational negativepatterning (Fig. 2D), conditional context model. Second,it meansthat non-metricconfigural (Fig. 2E) and biconditionalcontext (Fig. 2F). FF problems should not be mediated by the dentate lesions had no effect on the first two tasks and gyrus. Instead,interpreting configural learning in facilitatedperformance on the biconditionalcontext light of the parallelmap theory leadsto a dissoci- task. HP lesions,in contrast,impaired both nega- ation of two classesof configuralproblems, linear tive patterning and biconditional context. These problems,such as transitiveinference (Fig. 2A,B), results support the parallel map interpretationof and topologicalproblems, such as transversepat- configurallearning: impairment of the bearingmap terning (Fig. 2C-E). Lesions of specific hippo- did not affect topological problem solving, which campal subfields should therefore differentially was only impaired by a combined lesion of the affect these two classesof configural problems. bearingmap and sketchmap (HP lesion). Lesionsof bearingmap components(dentate gyrus It is difficult to assessthe resultsof the rernain- or fimbria-fomix 122/) should impair transitive ing TI studies,however, because of the placement inferencebut not transversepatterning. Lesions of of lesions;the parallel map interpretationdemands the major sketch map component, CAl, should that the lesionis confinedto a specifichippocampal impair transversepatteming but not transitive subfield or component. For example, on the 2- inference.These predictions could be tested by series TI task, transitive judgments have been examiningthe effectsof different lesionson tasks impaired by completeHP lesion in the rat l5l, by that should be dependenton the bearing map normal aging in the mouse 1301,and by complete (transitiveinference, l- and 2-seriesversions) or on entorhinalcortex lesionsin the monkeyl4l. the sketch map (transversepatteming, negative In contrast to these results from mammalian

voLUME17. NO. l-2. 2006 t06 L.F, JACOBS species,there was no effect of lesion on transitive THESKETCH MAP AND TOPOLOGICAL TASKS judgment on the 2-seriestask in the pigeon 1371. This resultraises several interesting questions. First Due to the convolutedshape of the HP, most amongthem is the questionof whetherimpairment lesionstudies are more likely to removedorsal than by HP lesion only occurs when the task demands ventral hippocampaltissue, and this is known to that stimuli be simultaneouslyprocessed, as sug- affect function126,271. One might thereforepredict gestedby McDonaldet al. l24l.ln this study,HP- that genericHP lesionswould have a largereffect lesionedrats were impaired on biconditional but on sketchmap function, and henceon topological not on conditionaldiscrimination. The authorssug- tasks, than Euclidean metric tasks. Another dif- gestedthat rats solved the conditionaldiscrimina- ficulty arises from different lesions and different tion task with a non-hippocampalmechanism, i.e., tasks often being used by different researchers. by associatingreward simply with context,either X Perhaps for this reason, the results have been or Y (Fig. 2E). In contrast,in the biconditional inconsistent:negative patterning (Fig. 2D) hasbeen discriminationtask (Fig. 2F), no one stimulus impaired124,361, facilitated llTl andunaffected /9/ efl-ectivelypredicted the outcome and hencepairs by HP lesion. Trarrsvsrsepatterning (Fig. 2C) has of stirnulihad to be processedsimultaneously. been both impaired l12l and facilitatedl7l by FF If a hippocampal task must demand simul- lesion.This last result is particularlypuzzling. The taneousprocessing of stimuli, thenthis may explain facilitationwould be predictedby the parallelmap the lack of impairment in HP-lesionedpigeons interpretation:with only residualsketch map func- (Fig. 2B). As a caveat,this important study is the tion, the rat would not attemptto orderstimuli in a first to examine the effect of brain lesions on gradientand shouldtherefore more easilysolve the configurallearning in any non-mammalianspecies. transversepatterning task. A possiblefactor in the The trainingprocedure, however, may havediffered differencebetween these studies (Bussey et al. l7l subtly from that used in mammal studies,in the and Duseket al. 112/)may be the sensorymodality 'a' followingway: the stimulus was followedby a of the stimuli: FF lesionimpaired transverse patter- choice ('b' or 'x') but did not simultaneously ning using olfactory stimuli ll2l but facilitated appear with them, as in the previous pigeon TI transversepatterning using visual stimuli 17l. Given studyofvon Fersenet al. 1441,using the l-series the differential pattern of sensoryinput into ventral task (Fig. 24; Table l). Becausestimuli werepre- and dorsalhippocampus from olfactoryand visual sentedserially, this may have resultedin activation areasl2l, one interpretationis that the FF lesion has and solutionby a different brain structurethan the a more significanteffect on olfactorythan visually- hippocampusand therefore this ability was left mediatedtasks. The FF lesion thereforeimpairs intact by later hippocampallesions. An alternative performanceon an olfactory task, but in a task hypothesisis that the inference was completed using visual stimuli, the impairmentof the bearing accurately using residual ventral hippocampal map might facilitatethe useof the sketchmap, with tissue. This would contradict the conclusion, its direct input from visual and corticalregions 1221, however,by this group and other researchersthat and hencefacilitate transversepatterning. Clearly, the dorsalhippocampal area in birds is homologous more specific lesionsare neededto test the hypo- to the mammaliandentate gyrus 123,39/. But if the thesis that transversepatterning is a topological ventral area is homologous to the mammalian problem, subservedby the CAl-mediated sketch dentate gyrus and sufficient ventral tissue was map. One exampleof such a lesion is the impair- spared,then this might explain why the bearing ment of CAI-NMDA receptors (see l22l for map was intactand hencewhy the birds showedno discussionof long-term potentiationand plasticity impairmentin transitivityjudgment. Granted this is of sketchand bearingmaps). Such an impairment, not a terribly convincing argument,but it under- usinggenetic manipulations, has been shown to impair scoresthe need for more comparativework with transversepatteming, as predicted,in mice /35/. other vertebrategroups, particularly birds and reptiles, Anothertest of the parallelmap interpretationof on the effectof HP lesionson confisuralleamins. configural learningcould come throughfunctional

REVIEWSIN THENEUROSCIENCES PARALLEL MAPS AND CONFIGURALLEARNING 107 imaging of humanhippocampus during transitivity denceat this point is sketchy,with simply enough judgments.Because the hippocampusshows func- data to provide fuel for the framing of a new tional differentiation in both rodents and primates hypothesis.Such a hypothesis,however, based on 127/, it may be possible to localize bearing map the parallel map theory, would offer a novel frame- structureto anterior regions and sketch map func- work within which to understandthe controversial tion to posterior regions of the human hippo- pattem of results collected over the past two campus,based on the relativerepresentation of DG decades in the area of configural and relational and CAI subfieldsin theseareas. Eucliddan metric learning.If these diverse ways of leaming spring problems, such as transitive inference,might be from the same root, then a theory of hippocampal more likely to activate the anterior hippocampus function, derived from two methods for spatial while transversepatterning should activate dorsal orientation,may shedlight on two waysto reason. and posteriorareas. Recent imaging studieshave reported results consistentwith this prediction. Heckerset al. found selectiveactivation in anterior ACKNOWLEDGEMENTS hippocampusin the l-seriesTI task /19/. Similarly, I would like to thank Shigeru Watanabe for Prestonet al. found anterior hippocampalactivation organizingan outstandingsymposium on compara- duringtransitive judgments in the 2-series taskl32l . tive hippocampal function. The ideas presented The parallelmap accountof theseresults suggests here were developedin light of past conversations that designinga study using TI and a topological with Frangoise Schenk (University of Lausanne) task, such as transversepatterning, could producea and MelissaAdams-Hunt (University of Califomia double dissociationof activation in anterior and at Berkeley),as well as more recentdiscussion with posteriorhippocampal regions. Moreover, given the Veme Bingman,Neil Burgess,NyazFqzal, Stephen pattem of facilitationof topologicaltasks with FF Lea, Lynn Nadel and Robert Osserman. Verne lesions,imaging studies might also reveala pattern Bingman provided helpful comments on the of inhibition of activity in anterior or posterior manuscript.Other costs of manuscriptpreparation hippocampalregions, depending on the task being were met by funds from the Hillblom Foundation solved. and the Committee on Research, University of Californiaat Berkeley. CONCLUSIONS

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