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Consciousness and Cognition xxx (2010) xxx–xxx Contents lists available at ScienceDirect Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog Memory, autonoetic consciousness, and the self q Hans J. Markowitsch a,b,⇑, Angelica Staniloiu a a b Physiological Psychology, University of Bielefeld, Bielefeld, Germany Alfried Krupp Institute for Advanced Study, Greifswald, Germany a r t i c l e i n f o a b s t r a c t Memory is a general attribute of living species, whose
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  Memory, autonoetic consciousness, and the self  q Hans J. Markowitsch a,b, ⇑ , Angelica Staniloiu a a Physiological Psychology, University of Bielefeld, Bielefeld, Germany b  Alfried Krupp Institute for Advanced Study, Greifswald, Germany a r t i c l e i n f o  Article history: Available online xxxx Keywords: Dissociative amnesiaSelf-consciousnessEmotionEpisodic-autobiographical memory (EAM)Perspective takingTime a b s t r a c t Memory is a general attribute of living species, whose diversification reflects both evolu-tionary and developmental processes. Episodic-autobiographical memory (EAM) isregarded as the highest human ontogenetic achievement and as probably being uniquelyhuman. EAM, autonoetic consciousness and the self are intimately linked, grounding, sup-porting and enriching each other’s development and cohesiveness. Their development isinfluenced by the socio-cultural–linguistic environment in which an individual grows upor lives. On the other hand, through language, textualization and social exchange, all threeelements leak into the world and participate to the dynamic shaping and re-shaping of thecultural scaffolding of the self, mental time traveling and EAM formation. Deficits in self-related processing, autonetic consciousness, emotional processing and mental time travel-ing can all lead to or co-occur with EAM disturbances, as we illustrate by findings fromEAM impairments associated with neurological or psychiatric disorders.   2010 Elsevier Inc. All rights reserved. 1. Introduction Memory is a multi-facetted attribute of all animals and may even be found in rudimentary forms in the flora and inso-called intelligent machines. This speaks for a million year-long process of memory evolution. More recent theories inpsychology and the neurosciences have acknowledged this process by proposing different memory systems, especially inphylogenetically advanced species. The endowment witha developed body that has enabled the exploration of the environ-ment over wide distances (embodiment; Pfeifer & Bongard, 2007) has most likely led to the diversification of memories aswell as the need to store informationlong term(cf. Campbell &Garcia, 2009). This is evident in species such as certainbirds(Miyata, Gajdon, Huber, & Fujita, 2010; Weir, Chappell, & Kacelnik, 2002), whales and dolphins (Reiss & Marino, 2001), ele- phants (Plotnik, de Waal, & Reiss, 2006), the great apes (Bard, Todd, Bernier, Love, & Leavens, 2006; Call & Tomasello, 2008; Kitchen, Denton, & Brent, 1996), and New World capuchin monkeys (de Waal, Dindo, Freeman, & Hall, 2005). Furthermore, beingasocial animal andengagingincooperativebehavior (Brosnan&Bshary, 2010; de Waal &Suchak, 2010; Melis &Sem-mann, 2010) required and enabled a more flexible application of mental capacities (Blakemore, 2010), though it is still de- bated whether and to what degree animals developed at least rudimentary abilities of foresight, prospection, and theory of mind (e.g., Gilbert & Wilson, 2007; Hare & Tomasello, 2005; Miyata et al., in press; Osvath, 2010; Roberts & Feeney, 2009;Suddendorf, Addis, &Corballis, 2009a; Suddendorf, Corballis, &Collier-Baker, 2009b). Similar to memory, basicself–non-self distinctions, such as the ones linked to physiological processes of immunity or digestion, are features of all viable species.The main unanswered question is the extent to which different species are capable of higher levels of conscious self-repre-sentations and self-awareness. Tulving (2005) has a clear position when stating ‘‘I argue that only human beings possess 1053-8100/$ - see front matter   2010 Elsevier Inc. All rights reserved.doi:10.1016/j.concog.2010.09.005 q This article is part of a special issue of this journal on Brain and Self: Bridging the Gap. ⇑ Corresponding author. Address: Physiological Psychology, University of Bielefeld, P.O.B. 100131, D-33501 Bielefeld, Germany. Fax: +49 5211066049. E-mail address:  hjmarkowitsch@uni-bielefeld.de (H.J. Markowitsch).Consciousness and Cognition xxx (2010) xxx–xxx Contents lists available at ScienceDirect Consciousness and Cognition journal homepage: www.elsevier.com/locate/concog Please cite this article in press as: Markowitsch, H. J., & Staniloiu, A. Memory, autonoetic consciousness, and the self.  Consciousness andCognition  (2010), doi:10.1016/j.concog.2010.09.005  ‘autonoetic’ episodic memory and the ability to mentally travel into the past and into the future, and that in that sense theyare unique.” (p. 4). Though debated, his position has been supported by a number of findings also from human memoryresearch (Botzung, Denkova, & Manning, 2008). Firstly, not all human beings possess the ability for mental time traveling:Patients with severe mental retardation or dementia may lack this capacity and patients with other disorders may showdeficits in integrating autobiographic memories with autonoetic consciousness and their selfhood. Examples are individualswithAspergersyndromeorautism.Tanweer,Rathbone,andSouchav(2010)foundthatadultAspergerindividualsrecalledincomparison to matched controls fewer events from their personal past and rated them much less specifically (respondingmore frequently to them as being just ‘known’, but not ‘remembered’ – a finding typical for patients with amnesia; see,e.g., Bengner & Malina, 2008; Hirano, Noguchi, Hosokowa, & Takayama, 2002; Noulhiane et al., 2008; Yonelinas, Kroll,Dobbins, Lazzara, & Knight, 1998). They also made in comparison to the controls fewer social identity statements andprovided more abstract, trait-linked identities. Individuals with autism were found to have an atypical neural responsepattern to judgments about their self, when their brains were studied with functional neuroimaging methods (Lombardoet al., 2010). The authors also detected ‘‘that the magnitude of neural self-other distinctions in the ventro medial prefrontalcortex was strongly related to the magnitude of early childhood social impairments” (p. 611).Secondly, developmental studies have emphasized socio-cultural–linguistic mechanisms that may be unique to thedevelopment of EAM. Small children – similar to animals – live initially in the here and now (Nelson, 2005a, 2005b). Theirepisodic-autobiographical memory(EAM)developstogetherwiththeirself, theoryof mindcapacities, emotional conceptualknowledgeandcapacityformentaltimetraveling(Ghetti,DeMaster,Yonelinas,&Bunge,2010;Rochat,2010).Socialcontextplays a critical role in the development of all the above neuro-cognitive functions. It was, for example, shown that simplylistening to the voice froma tape recorder is not sufficient for learning early aspects of language, but instead infants requirethe social presence of a person (Adolphs, 2010; Kuhl, Tsao, & Liu, 2003). Theory of mind functions furthermore ‘‘appear onlyafter children have become experienced verbal communicators” (Surian, Caldi, & Sperber, 2007, p. 580). The onset of EAMandtheToMcapacities inthe offspring(Nelson&Fivush, 2004) dependonthe degreeof elaborationof the reminiscingstyleof their mothers. The importance of the social component for the emergence of ToM capacities is also reflected by findingsthat in institutionalized children ToM capacity correlated with the adult–child ratio (Bedny, Pascual-Leone, & Saxe, 2009).Developmental changes of EAM (e.g. pertaining to autonetic consciousness) extend however beyond childhood into earlyadolescentyears(Picard,Reffuveille,Eustache,&Piolino,2009)andmayincludeinlatechildhood(ages8–12years)theabil-ity to suppress memories (Paz-Alonso, Ghetti, Matlen, Anderson, & Bunge, 2009).On the brain level these EAM developmental changes in humans (from infancy to early adulthood) are reflected in theextensive structural and functional reorganization of different components of the neural networks supporting EAM, auton-oetic consciousness and self-referential processing, ToM capacities and ability for emotional regulation (Shing et al., 2010).From a comparative cognitive-neuroscience perspective, frontopolar cortex (BA10) shows the biggest relative increase be-tweengreat apes andhumanbeings. BA10activationrecentlyhas beenfoundto becorrelatedwithworkingmemorycapac-ity and general intelligence (Colom, Jung, & Haier, 2007). The basolateral nuclear group of amygdala shows a ‘‘progressiveenlargement from insectivores to prosimians and finally simians” (Sarter & Markowitsch, 1985b, p. 348), while vice versathe centromedial nuclear group ‘‘shows a clear regression” along this phylogenetic scale. This is in line with ideas that inmore phylogenetically evolved species the basolateral nuclear group expands to encompass higher cognitive–emotionalfunctions such as EAM in the case of human beings (Cahill, Babinsky, Markowitsch, & McGaugh, 1995).OnequestionwhichremainsisconcernedwiththeroleofEAMinhumans.DoesindeedtheEAMthroughitsintrinsicfeatureofmentaltimetravelingplayamainfunctioninthesurvival,asithaslatelybeenemphasizedrepeatedly?AndiftheappearanceofEAMisindeedadaptive,whydiditnotoccurinotherspecies?Isitinfactpossiblethatcertainclaimsofcognitivedifferencesbetweenhumansandotherspeciesaretheproductofanunderdevelopedexperimentalmethodologyratherthanspeciesdif-ferencesperse?OrmayitbethecasethatthemainfunctionofEAMisinfactsocial–asuggestionthatwasputforthbyseveralauthors, thoughit has not beenanexplicit focus of extensiveexperimental investigations yet (Markowitsch&Welzer, 2009;Welzer&Markowitsch,2005).AhintinfavorofthishypothesiscomesfromtheworkwithpatientswithAlzheimer’sdementia:Fargeauetal. (inpress)foundthatthesocialselfwasimpairedearliestinthispatientgroup.In the current paper, after a presentation of memory systems and their neural correlates, we will provide a review of therelationship between EAM, autonoetic consciousness and self, by preponderantly drawing on the socio-cultural–linguisticdevelopmentalmodeladvancedbyNelsonandFivush(2004).WewillthenarguethatEAMdisturbancescanresultfromdef-icits in the accurate re-collectionof the encoding context, mental time traveling, emotional disturbances or self-related pro-cessing. By describing several EAM disturbances associated with both neurological and psychiatric diseases, we willdemonstrate that many (especially severe) EAM impairments arise or exist in combination with dysfunctions in the realmsof emotion, self, mental time traveling and social functioning. 2. Memory systems Memoryisnotunitary,butcanbedeconstructedalongatimeandcontentaxis,respectively.Alongthetimeaxis,memorywas traditionally divided into short-term and long-term memory. The short-term memory has a limited capacity of a fewbits(4–7)(Cowan, 2000;Miller, 1956) andencompassesatimerangeof secondstominutes.Anyinformationthat isnot lostand exceeds the limited capacity of short-term memory is assigned to long-term memory stores. The above time-related 2  H.J. Markowitsch, A. Staniloiu/Consciousness and Cognition xxx (2010) xxx–xxx Please cite this article in press as: Markowitsch, H. J., & Staniloiu, A. Memory, autonoetic consciousness, and the self.  Consciousness andCognition  (2010), doi:10.1016/j.concog.2010.09.005  dichotomyofmemorywaslaterexpandedbytheadditionof‘workingmemory’byAlanBaddeley(Baddeley,2000;Baddeley&Hitch, 1974). As capturedbyitsname, workingmemoryrefersto workingwithmemory–thisinvolvesnot onlytime-lim-ited online holding of new information, but also retrieving portions of old, already stored information.Anothertime-relatedcategorizationofmemoryconsistsofthedistinctionbetweenoldandnewandanterogradeandret-rograde memories, respectively. The compromised ability to access information that happened before the memory-impair-ing incident corresponds to retrograde memory impairment, while anterograde memory impairment refers to thecompromised capacity to long-term acquire new information after the incident. A different facet of the relation betweenmemory and time is concerned with the phenomenological experience of time in memory disturbances (inner time percep-tion, mental time traveling).The classification of long-term memory systems along the content dimension has undergone several changes, especiallysince Tulving had proposed a distinction between episodic and semantic memory in 1972. Presently two overlapping clas-sifications dominate the memory research literature – one was initiated by Larry Squire and the other one was advanced byEndel Tulving. InSquire’sclassification, a maindistinctionis madebetweendeclarativeandnon-declarative memory. Underdeclarativememory,episodicandsemanticmemories–thatis (biographical)eventsandgeneral facts–aresubsumed.Non-declarative memory contains several other forms of memory, which are considered to be automatically processed.Tulving’scontent-basedclassificationcontainsfivelong-termmemorysystems,whichareconsideredtobuild-uponeachother phylo- and ontogenetically. According to the SPI-model (SPI=serial, parallel, independent) that was proposed by Tul-ving (1995), it is assumed that information is encoded serially into these systems, may be stored in parallel in different sys-tems and can be retrievedindependentlyof the systemin whichencoding occurred. These five memory systems distinguishthemselves by different levels of consciousness (such as autonoetic, noetic or anoetic) and distinct or partly distinct neuralcorrelates. Wheeler, Stuss, and Tulving (1997, p. 335) defined autonoetic consciousness as the capacity ‘‘that allows adulthumanstomentallyrepresentandtobecomeawareoftheirprotractedexistenceacrosssubjectivetime”.Theydifferentiatedautonoetic from noetic consciousness (knowing) – which refers to the awareness of symbolic representations of the world,and from anoetic consciousness – that describes the simple awareness of external stimuli. The latter form of consciousnessapproximatestheoneevokedbythefollowingcitationof Mesulam(2000):‘‘theexistenceofconsciousnessmightbeinferredwhenalivingorganismrespondstoenvironmentaleventsinanadaptivewaythatisnotentirelyautomatic(p.93)(cf.Mark-owitsch, 2003).ThehierarchyofthememorysystemsproposedbyTulvingisdepictedinFig.1.Whileexcludingverybasicformsofmem-ories such as habituation, sensitization, classical conditioning, this hierarchy starts with procedural and priming memorysystems–twosimplememorysystemsthatarestilldevoidoftheneedforconsciousreflectionupontheenvironment(‘‘ano-etic”). Procedural memory is mainly motor-based, but includes also sensory and cognitive skills (‘‘routines”). Examples areriding a bike, skiing, playing piano, or reading words presented in a mirror-image. While procedural memory is largely anaction-based memory system, the reverse is true for the priming system: Priming refers to a higher probability to identifystimuli, which were previously perceived in the same (perceptual priming) or a related way (conceptual priming). The ‘per-ceptual memory system’ acts ‘consciously’ (noetically), but on a presemantic level and relies on familiarity judgments. Anexample is the conscious identification of an apple without hesitance, no matter what color it has or whether it is alreadyhalfeatenornot.Patientswithsemanticdementia,wholosethecapabilitiesforlanguageandsemanticmemory,maystillbe Fig. 1.  The five long-term memory systems and their assumed brain bases (for further description see the text). H.J. Markowitsch, A. Staniloiu/Consciousness and Cognition xxx (2010) xxx–xxx  3 Please cite this article in press as: Markowitsch, H. J., & Staniloiu, A. Memory, autonoetic consciousness, and the self.  Consciousness andCognition  (2010), doi:10.1016/j.concog.2010.09.005  abletodistinguishforexampleanapplefromapeachorpear withouttheneedtoaccesssemanticinformation, byaccessingperceptual representations of information via the perceptual memory system. Semantic memory, which was also termed‘knowledge system’ or – by Tulving and Markowitsch (1998) – ‘declarative memory’, is context-free and refers to generalfacts.Itisaccompaniedbynoeticawareness.Thedefinitionofepisodicmemoryhasbeensubmittedtoseveralrevisionsovertheyears.Whileseveraldecadesagothetermepisodicmemorycouldbeappliedtolaboratorystimuliwithaspecificembed-ding intime andplace(Tulving, 1972), theelicitingof what andwhereandwheninformationis nolonger regardedas a suf-ficient condition for fulfilling the requirement for being an episode memory (‘‘episodicity”). Nowadays episodic memory isdefined as the conjunction of subjective time, autonoetic consciousness and the experiencing self (Tulving, 2005) and sub-sequently the episodic memory system is currently viewed as being equivalent to the episodic-autobiographical memorysystem (EAM). Though the term autobiographical is still at times used interchangeably with the term episodic, not all thecomponentsof autobiographical memory, however, have anepisodicquality. Thereforeadistinctionis emphasizedbetweenautobiographical-episodic memory and autobiographical-semantic memory. The latter refers to  knowledge  of name, date of birth or self-traits and may be preserved or updated in spite of blocked access to episodic memory for personal events. Incomparison to autobiographical-semantic memory that requires noetic awareness only, the EAMpresupposes a higher levelof consciousness (‘‘autonoetic”). Autonoetic consciousness entails a ‘‘sense of self in time and the ability to relive subjectiveexperiences from the encoding context by mentally travelling back in time”  ( Lemogne et al., 2006, p. 260). Given that mostEAMreminiscencesareaffectively-laden,therelivingofthesubjectiveexperiencesfromtheencodingcontextisusuallyinti-mately linked to an emotional evaluation of the significance of these past experiences for oneself and with respect to one’sown position in his social and biological environment. This emotional evaluation may in turn shape someone’s motivationfor planning for the future and engaging in future acts. This emphasizes that EAM has not only a ‘‘retrospective function”,such as ‘‘the conservation of certain conditions, their reproduction, and their localization in the past” (Ribot, 1882 p. 10),but also a prospective one.The classifications of Squire and Tulving, which were presented above, partly stem from opposing theoretical assump-tionsonthebrain’sprocessingofepisodicandsemanticmemoryinformation.Squire’stheoryemphasizesthecommonalitiesbetween episodic and semantic memory processing, both from a behavioral and an anatomical perspective, while Tulving’stheory stresses the dissimilarities. Apart from these two categorizations, we currently witness a search for new models formemory systems, such as a model based on processing modes (Henke, 2010) rather than consciousness. This search maypartly be prompted by the ‘‘grand challenge of consciousness” (Seth, 2010), in particular the challenge posed by designinga testing instrument (methodology) that provides an objective estimate (measure) of the subjective phenomenon of auton-oetic consciousness or mental time traveling, which can be used in young children and non-human beings (Perner, Kloo, &Rohwer, 2010; Roberts & Feeney, 2009). 3. EAM and the brain Theformationofstablelong-termEAMsrequiresseveralinformationprocessingstages(encodingandconsolidation). De-bate about the process of consolidation still exists, with some authors arguing that the process may extend to years (Haist,Bowden Gore, & Mao, 2001). Once the information is consolidated, it is stored and then usually available for retrieval. Eachretrieval is followed by re-encoding of the EAMin the newly present context. According to adherents to the reconsolidationtheory,consolidatedmemoriesthatarerecalledbyareminderenterafterretrievalavulnerability(labilization)phase,duringwhich they might become susceptible to disruption or strengthening or incorporation of new information (Forcato et al.,2010); this is followed by a process of stabilization (reconsolidation).The reconsolidation theory constitutes the basis forpharmacologicalstudiesinhumansthataimtoweakenthevividanddisturbingtraumaticmemoriesassociatedwithcertainformsofpost-traumaticstressdisorderbyinterferingwiththeirassumedpost-retrievalreconsolidation(Brunetetal.,2008).The incorporation of new information may have as the result a ‘‘re-contextualization” of the retrieved material (Modell,2006) or the introduction of falsified details that may lead to false memories or confabulations (Loftus, 2000; Loftus & Hoff-man, 1989; Loftus & Pickrell, 1995; Borsutzky, Fujiwara, Brand, & Markowitsch, 2008, 2010). Freud wrote about a re-tran-scription of memories ‘‘in accordance to fresh circumstances” (Masson, 1985, p. 207). And Bartlett (1932) and later Tulving(1995,2002,2005)andSchacter(2001)notedthathumanbeingsconstructandreconstructtheirpersonalmemories, perhaps in an attempt to support current aspects of the self and match future goals that are coherent with one individual’sgoals,selfimageandsystemofbeliefs(Conway,2009).Edelman(1998)remarkedthateveryactofmemoryistosomedegree an act of imagination – a remark that later on was substantiated by findings that the hippocampal formation may also beinvolvedinmentalconstructionofcomplexscenes.Furthermore,Edelmanwrotethat‘‘memoryhasthepropertiesthatallowperception to alter recall and recall to alter perception” (1998, cf. Modell, 2006, p. 37). This sentence hints to an importantfeatureofEAM–namelyitsstate-dependency.Thisfeatureimpliesthatmemoriesareoptimallyretrievediftheenvironmen-tal and mood and physical state conditions match those during encoding. Inspired by Semon’s description (1904), Tulving (1983, 1985, 1995) coined this state-dependency of memory retrieval ‘‘ecphorizing”. Tulving (1983) employed the term ‘ecphory’ to describe the process by which retrieval cues interact with stored information so that an image or a representa-tion of the information in question appears. A mismatch between encoding and retrieval conditions may lead to a spectrumof memory retrieval disturbances, ranging from common tip-of-the-tongue phenomena to complete pathological retrievalblockades (such as in dissociative amnesic conditions; see below). 4  H.J. Markowitsch, A. Staniloiu/Consciousness and Cognition xxx (2010) xxx–xxx Please cite this article in press as: Markowitsch, H. J., & Staniloiu, A. Memory, autonoetic consciousness, and the self.  Consciousness andCognition  (2010), doi:10.1016/j.concog.2010.09.005
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