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Path Integration Deficits During Linear Locomotion After Human Medial Temporal Lobectomy

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Path Integration Deficits During Linear Locomotion After Human Medial Temporal Lobectomy Path Integration Deficits during Linear Locomotion after Human Medial Temporal Lobectomy John W.Philbeck 1,Marlene Behrmann 2,Lucien Levy 3, Samuel J.Potolicchio 3,andAnthony J.Caputy 3 Abstract & Animalnavigation studies have implicated structures inand both adecrease inthe consistency ofpath integration and a around the hippocampal formation as crucialin performing systematic underregistration oflinear displacement (and/or path integration (amethod ofdetermining one’s position by velocity) during walking.Moreover, the deficits were observable monitoring internally generated self-motion signals). Less is even when there were virtually no angular acceleration known about the role ofthese structures forhuman path vestibular signals. Theresults suggest that structures inthe integration. We tested path integration inpatients whohad medial temporal lobe participate inhuman path integration undergone left orright medial temporal lobectomy as therapy when individuals walkalong linearpaths and that thisis so to forepilepsy. Thisprocedure removed approximately 50% ofthe agreater extent inright hemisphere structures than left. anterior portion ofthe hippocampus, as wellas the amygdala Thisinformation is relevant forfuture research investigating and lateral temporal lobe. Participants attempted to walk the neural substrates ofnavigation, not only inhumans without vision to apreviously viewed target 2–6 mdistant. (e.g.,functional neuroimaging and neuropsychological studies), Patients withright, but not left,hemisphere lesions exhibited but also inrodents and other animals. & INTRODUCTION self-motionsignals is knownas pathintegration or dead An importantfunction of visionis to facilitate navigation reckoning (Etienne et al.,1996). An updated estimate of from one location to another. As importantas this one’s current positionmay be maintained byintegrating function is,however, visual information is frequently these self-motionsignals over time.Path integration is degraded or made unavailable bythe common occur- formallydistinct from other typesof navigation inwhich rences of occlusionsand poorlighting conditions. This one usesvision, or someother sensorymodality, to being thecase, itis advantageous for sightedindividuals determine one’s positionrelative to environmental fea- toremain able tonavigate withoutvision. Many animals tures (‘‘landmarks’’ )at knownlocations. have thisability (Etienne, Maurer, &Se´guinot,1996; Effective pathintegration entailsderiving a represen- Wehner, Michel,& Antonsen, 1996), and humansare no tationof thecurrent displacement from one’s last exception. The average humancan sighta target upto knownposition. There isabundant evidence thatthe 20 maway or more,and thenwalk to it quite accurately medial temporal lobe (MTL) playsan importantrole in whileblindfolded (for areview, see Mittelstaedt& theprocessing of spatialinformation. The firing rate of Mittelstaedt, 2001). The accuracy of thisnonvisual nav- pyramidalcells inthe rodent hippocampusis highly igation isevidence thatthe brain is exquisitely tuned to correlated withthe location of theanimal in space (for sense theself-motion signals generated bywalking and areview of thisextensive literature, see Redish,1999). to use themfor the purposeof controlling behavior.The One interpretation of sucha resultis that these so- neural processes underlyingnonvisual navigation re- called ‘‘place cells’’ participate inrepresenting the mainpoorly understood, however. layoutof theenvironment (O’ Keefe &Dostrovsky, When navigating withoutvision, the sensory informa- 1971). Consistentwith this view, rodents withlesions tionfor determining one’s positionis restricted to thatdamage thehippocampus or itsconnections tend signalsarising from thevestibular apparatus and signals to perform poorlyon taskssuch as theradial arm maze related to muscularactivity (e.g., proprioceptionand and water maze, whichrequire theanimal to demon- efference copy).The processof determining one’s po- strate itsmemory for locationsit has visited previously sitionon thebasis of internallygenerated (idiothetic) (e. g.,Morris, Garrud, Rawlins,& O’Keefe, 1982). Spatial memorydeficits are manifested after MTL injury inmonkeys as well,particularly after damage to the 1 TheGeorge Washington University, 2 Carnegie Mellon Uni- parahippocampalgyrus surrounding the hippocampus versity, 3 TheGeorge Washington University Medical Center (Murray &Mishkin,1998). © 2004Massachusetts Institute ofTechnology Journal ofCognitive Neuroscience16:4, pp. 510–520 There isevidence thatthe MTL’ s role innavigation muchless research hasfocused directlyon MTL partic- extends beyondsimply representing spatialinformation ipationin processing human idiothetic self-motion sig- to include the assimilationof idiotheticself-motion nals.Observing the behaviorof patientswith MTL signalsinto existing spatial representations. Place cells, damage innonvisual locomotor navigation tasksis a for example, continue toshow location-dependent firing powerful toolfor investigatingthese issues.Walking even when the animal’s visionis occluded (Markus, generates strong idiotheticself-motion signals and cre- Barnes, McNaughton, Gladden, &Skaggs, 1994; Quirk, ates asituationin which vestibular and muscular cues are Muller, &Kubie, 1990), suggesting thatthese cells mutuallyconsistent, as theyare during real-world navi- participate inthe processing of idiotheticself-motion gation. The occlusion of visionduring locomotionex- signals.In themonkey, some hippocampal cells have cludes landmark-based navigation,thereby providing a been found torespondto whole-bodymotion (O’ Mara, narrow experimental focus on idiotheticself-motion Rolls,Berthoz, &Kesner, 1994). Several conceptualiza- signals.If theMTL participates inprocessing suchsignals, tionsof hippocampalfunction suggest thatthe MTL’ s MTL injuryshould result in path integration deficits. role inpath integration (including processing and stor- The MTL does seem tobe involvedin these tasks,but ing spatial,temporal, and self-motion information) importantdetails of itsrole remain to be characterized. emerges as part of amore general role for subserving Patientswith MTL lesions,particularly in theright hemi- episodicmemory (e.g., Burgess,Maguire, &O’Keefe, sphere,show path integration deficits during whole- 2002; Vargha-Khadem et al.,1997), declarative memory bodyrotations as well as innonvisual walking tasks (e.g., Squire, 1992), relational processing(e.g., Eichen- involvinga combinationof turnsand straightsegments baum& Cohen,2001), or contextual processing(e.g., (Worsleyet al.,2001; Wiest,Mu ¨ller, Glu¨ck,Deecke, & Redish,2001). Baumgartner, 2000). The abilityof suchpatients to Rodents and humansbehave similarlyin water-maze- perform pathintegration along purelylinear pathsis less typenavigation tasks (Hamilton, Driscoll, & Sutherland, clear, however.Worsley et al.(2001) concluded thatthe 2002), butclearly humansuse more sophisticatedrep- pathintegration errors manifested bytheirpatients were resentations tocontrol navigationthan do rodents,at attributable todeficits inrotational updatingonly, but least under certain circumstances (e.g., Wang &Spelke, speculated thattheir methods may not have been suffi- 2002). The extent to whichhuman navigation within the cientlysensitive to detect deficits inupdatingalong linear local environmentparallels rodent (and monkey)navi- paths.One possiblesource of insensitivitystems from gation isstill poorly understood, however. The need to theiruse of unimodaldistance and route reproduction understand thehomology between rodent and human tasks,in which participants are exposed toa stimulus brainstructures thatparticipate innavigationis particu- pathby walking and thenmust reproduce thatpath, larlypressing, given theenormous body of research that again usingthe walking modality.If participantsperform iscurrently available based on thisanimal model. A host pathintegration similarlyon thestimulus and response of neuropsychological and functional neuroimaging portionsof thepath, systematic errors inthe two seg- studiessupport the viewthat MTL structures playa mentscould cancel, therebyyielding a potentiallymis- critical role inhuman navigation. Much workhas impli- leading pattern of accurate performance. The possible cated theright hippocampus and/ or parahippocampal impairmentof linear pathintegration after MTL damage gyrusas importantsubstrates for spatialmemory in isimportant to verifyusing more sensitivemethods humans,particularly when informationmust be retained because itstands to elucidate whichsensory inputs to for more thanseveral seconds and lessthan several pathintegration are processed inthe MTLs. In natural minutes(Pierrot-Deseilligny, Mu ¨ri,Rivaud-Pechoux, Gay- situations,rotating one’s bodyto face another direction mard,& Ploner,2002; Feigenbaum, Polkey,& Morris, generates strong rotational vestibularsignals and arela- 1996; Owen, Milner, Petrides,& Evans,1996; Smith& tivelysmall amount of leg movement.Walking along Milner, 1981). Furthermore, humanswith MTL damage linear paths,meanwhile, produces theopposite pattern. showdeficits intasksthat require navigationto remem- If pathintegration isimpaired during bothlinear and bered locationsin real and virtualenvironments (Astur, rotational locomotionafter MTL damage, thiswould Taylor,Mamelak, Philpott,& Sutherland, 2002; Spiers indicate thatthe MTL’ s role inpath integration encom- et al.,2001; Skelton, Bukash,Laurance, Thomas,& passessignals from multiplesensory systems rather than Jacobs,2000; Bohbotet al.,1998). Functional
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