Quo vadis ‘episodic memory’? – Past, present, and perspective

Journal Pre-proof Quo vadis ‘episodic memory’? – Past, present, and perspective Angelica Staniloiu, Andreas Kordon, Hans J. Markowitsch PII:

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https://doi.org/10.1016/j.neuropsychologia.2020.107362

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Neuropsychologia

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Please cite this article as: Staniloiu, A., Kordon, A., Markowitsch, H.J., Quo vadis ‘episodic memory’? – Past, present, and perspective, Neuropsychologia (2020), doi: https://doi.org/10.1016/ j.neuropsychologia.2020.107362. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2020 Published by Elsevier Ltd.

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Quo vadis ‘episodic memory’? – Past, present, and perspective Angelica Staniloiu,1,2,3 Andreas Kordon3, 4 and Hans J. Markowitsch1 University of Bielefeld, Germany, 2University of Bucharest, Romania, 3Oberberg Clinic Hornberg, Germany, 4University of Freiburg, Germany 1

Address for all correspondence: Hans Markowitsch University of Bielefeld Physiological Psychology POB 100131 33501 Bielefeld Germany [email protected]

2 Abstract The term ‘episodic memory’ was coined by Endel Tulving, who also created a classification in several memory systems. This classification is presented, and it is described which predecessors existed for the partition of memory into systems. The ‘episodic memory system’ is discussed as being in general equivalent with ‘episodic-autobiographical memory system’. It is seen as an emotionally colorized system. A special paragraph is devoted to the ‘perceptual memory system’, as this was not included in Tulving’s previous schemes of memory systems. More recent sub-categorizations of the ‘episodic memory system’ are presented and a perspective on the future of the episodic memory system is developed.

Keywords: Semantic memory Autonoetic consciousness Overgeneral memory effect Perceptual memory Emotional embedding

3 Introduction – Episodic Memory Endel Tulving likes to refer to history and historical concepts. For example, in 2010 he used the following sentence from William James as motto for his chapter: " We have to live today by what truth we can get today, and be ready tomorrow to call it falsehood.” Tulving likes to cite old sources such as Die Mneme from Richard Semon (1904) (e.g., in his publication from 2007; see also Schacter, 2011) and is also very careful in his formulations, in selecting terms, in observing the usage of words of others, and in terminology in general. For instance, in his 1972 seminal paper on “Episodic and semantic memory”, he referred to a scientist using the term “non-episodic”, while he was not aware of any source having used the term “episodic memory” up to that time. Tulving’s progress in defining ‘episodic memory’ from 1972 (Tulving, 1972) over his voluminous book on Elements of Episodic Memory from 1983 to his more recent (Tulving, 2002, 2005) works – in which he emphasized autonoetic consciousness as a prerequisite of episodic memory – is well known. However, old works on dividing and defining memory, which are of relevant for Tulving’s ideas on memory systems and memory processes (cf. Table 54.1 in Tulving, 1995), are likely less known. We therefore aim to discuss some of this early work and point to possible changes in the definition of episodic memory, which might be important for future work. _________________________ Insert Figure 1 about here _________________________ The most revolutionary of Tulving’s ideas was the division of memory into short-term memory and four or five long-term memory systems; within these memory systems the retrieval takes place consciously (or explicitly) or non-consciously (or implicitly) (Fig. 1 and Fig. 54.1 of Tulving, 1995). In 1972 Tulving initially wrote more cursorily (did not provide in depth elaborations) about “memory systems”: “I will refer to both kinds of memory as two stores, or as two systems, but I do this primarily for the convenience of communication, …” (p. 384). In his book from 1983, Tulving acknowledged that the distinction in 1972 “was not very well thought out” (p. 9). He therefore, for example, listed in Table 3.1 (p. 35) of his book 28 diagnostic features, differentiating between episodic and semantic memory. Later in 1995 he wrote of systems as of “major categories of human memory” (p. 840). For “kinds of memory” Tulving (2007) much later provided the definition: “A kind of memory is the noun ‘memory’ preceded by an appropriate adjectival modifier” (p. 44). (which in fact can be a noun as well; examples: event memory, spatial working memory). “Kinds of memory” are therefore loosely defined (see the Appendix of Tulving, 2007), while “systems” are strictly defined entities which contain specific attributes not common, or at least going beyond to those of other memory systems (Fig. 1). Further important ideas are that episodic memory refers to the self and is autonoetically conscious (Markowitsch and Staniloiu, 2011), and that processing of memory can be ‘anoetic’, ‘noetic’ or ‘autonoetic’. Anoetic (“without knowledge”) refers to procedural and priming memory systems in Figure 1, noetic (“knowing”) refers to the perceptual and semantic memory systems, and autonoetic is assigned to the episodic (or episodic-autobiographical) memory system. In 1972, Tulving stated that episodic memory “receives and stores information about temporally dated episodes or events, and temporal-spatial relations among these events.” (p. 385). He emphasized that an event is always stored with “reference to the already existing contents of the episodic memory store.” (p. 385f). At that time, Tulving had not yet introduced the ‘remember – know’ distinction, where ‘remembering’ refers to the episodic memory while the present-oriented

4 ‘knowing’ indicates the semantic memory (Tulving, 1985, 1986). Tulving gave as one of five examples for episodic memory the following: “I know the word that was paired with DAX in this list was FRIGID” (p. 387). At that time, Tulving considered episodic memory as closely related to laboratory studies on verbal learning (“Laboratory studies of human memory and verbal learning have almost exclusively been concerned with phenomena of episodic memory”; p. 402). In his 1983 book, Tulving corrected this assumption, writing that such kind of studies do not involve episodic memory. Furthermore, in 1972 Tulving thought that it is “possible for the episodic system to operate relatively independently of the semantic system” (p. 386), while later he wrote that episodic memory depends in its operations upon semantic memory (Tulving, 1984, 1985, 1995). The simplest definition of episodic memory from 1972 was taken up by animal researchers, who focused on” temporal-spatial relations” and aimed to demonstrate that animals have episodic memory as well (e.g. Bierley et al., 1983; Gaffan, 1991). Tulving (2002) later wrote that he then adapted his definition of episodic memory by (a) emphasizing ‘mental time traveling’ – in both backward and forward directions (past and future; retro- and prospective memory) (Tulving, 1985) – aspect of episodic memory, and (b) introducing in 1983 the term “recollective experience” or conscious awareness of the respective event. The remember – know distinction appeared (Tulving, 1993) and had the differentiation ‘autonoetic’ versus ‘noetic awareness/consciousness’ as a complementary terminology (Tulving, 1985; see also Gardiner, 2001). Tulving and Markowitsch (1998) listed several common and distinctive features of episodic and semantic memory. In 2002 and 2005 Tulving provided new and refined definitions of episodic memory. In 2002, he wrote that episodic memory “makes possible mental time travel through subjective time, from the present to the past, thus allowing one to re-experience, through autonoetic awareness, one’s own previous experiences” (p. 5). In 2005 Tulving wrote that the episodic memory system “is oriented to the past”, that it “makes possible mental time travel through subjective time – past, present, and future. This mental time travel allows one, as an ‘owner’ of episodic memory (‘self’), through the medium of autonoetic awareness, to remember one’s own previous ‘thought-about’ experiences, as well as to ‘think about’ one’s own possible future experiences.” (p. 9).

Historical remarks It is generally accepted that laboratory memory research started with the early works of Hermann Ebbinghaus (1850–1909) (Ebbinghaus, 1885a, published in the same year also in English language; Ebbinghaus, 1885b), and Müller and Pilzecker (1900). Ebbinghaus worked with “nonsense” syllables (of usually 3 characters – such as REK, MIS, TOF [CVC – consonant-vowel-consonant]) and detected early laws of learning, illustrated in ‘learning curves’, ‘forgetting curves’, or as ‘savings’. Müller and Pilzecker (1900) created the expression ‘consolidation’ – in their eyes the process of formation of associations leading to long-term storage of new information – and worked on retrograde interference (cf. also Lechner et al., 1999). The tradition of using verbal material to study memory in humans remained prominent up to the 1960ies (see the section A historical sketch in Tulving’s chapter from 1995). And in fact, Endel Tulving was one of the most prominent researchers in this field, editing the Journal of Verbal Learning and Verbal Behavior. Theodule Ribot, a contemporary of Georg Elias Müller and a psychologist as well, had partly a biological perspective of memory and its disorders (Ribot, 1882a, b). He saw the process of memory consolidation or memory stabilization as a metabolic process. For him, memory was not “in the soul”, but was fixed in a part of the nervous system, as he stated on page 9 of the German edition of his

5 book from 1882 (Ribot, 1882b). Furthermore, he considered memory to be ‘seeing in time’, a view that can be seen as a forerunner of Tulving’s idea that episodic memory allows mental time travelling. Ribot compared the nervous system with a muscle, which improves in strength when trained. With respect to memory partitioning, Ribot (1882a, b) referred to an article of Sharpey (1879), in which a woman was described who seemed to have forgotten everything, but relearned quickly to play piano and other skills. This case apparently resembles what much later was described as preservation of ‘procedural memory’ in patients with retrograde amnesia (e.g., Markowitsch et al., 1993). A more specific finding – compared to the early memory literature, which largely dealt with association learning (e.g., Aschaffenburg,1895, 1899; Bleuler, 1905; Diehl, 1902; Höffding, 1889, 1890; Jost, 1897; Jung, 1905; Lipmann, 1904; Münsterberg, 1900; Wahle, 1885; Wreschner, 1900; Wundt, 1888)1 – was Ribot’s (1882a, b) contribution to memory research, which remained known and valid as ‘Ribot’s law’ over the centuries: Ribot detected that recently acquired information is lost earliest from conscious access, while the recall of remote memories is quite stable. Russell and Nathan in 1946 confirmed Ribot’s law in their description of brain-damaged veterans from the World War II. They wrote: “It is clear that the events forgotten are often of importance to the individual, yet for a time, and sometimes permanently, they are completely erased, while distant memories of little importance are returning freely.” (p. 299). The terms anterograde and retrograde memory are found early in the literature as well (Charcot, 1892; Souquet, 1892; Janet, 1892, 1893). Already on December 6, 1896, Freud wrote to Wilhelm Fliess about “the material present in the form of memory traces being subjected from time to time to a rearrangement in accordance with fresh circumstances — to a retranscription. the material present” (Masson, 1985, p.207). Afterwards, in 1932 then, Bartlett alerted to the phenomenon that memory retrieval is a process of reconstruction, although individuals might not be aware of memory changes over time. Even prior to Ebbinghaus, the physiologist Ewald Hering (1834-1918) – known for the formulation of the opponent-color-theory – wrote a book on memory in 1870 (English translation: 1895). In this book he stated: “Memory connects innumerable single phenomena into a whole, and just as the body would be scattered like dust in countless atoms if the attraction of matter did not hold it together so consciousness – without the connecting power of memory – would fall apart in as many fragments as it contains moments” (p. 12). So, implicitly, Hering wrote about consciousness and time – central topics of Tulving, who classified his memory systems in those not requiring consciousness (procedural memory – anoetic), requiring consciousness (semantic memory – noetic) and requiring self-consciousness (episodic memory – autonoetic). (Fig. 1). Furthermore, Tulving emphasized that episodic memory allows (and requires) mental time traveling.

Endel Tulving’s memory systems and its predecessors – content and awareness When considering episodic-autobiographical memory, one can refer to the content of the memories (e.g., personal events) and to their level of awareness (e.g., autonoetically relived). Interestingly, in the old examples we found, content and awareness aspects were usually 1

In 1929 Vogt from studying Lenin‘s brain named him an “Assoziationsathleten” (athlete of association), because he found huge pyramidal neurons in his cerebral cortex.

6 intermingled. Most of the old scientists – such as Ebbinghaus, Müller, Pilzecker, Ribot and Hering – did not touch on the issue of multiple memory systems. This was, however, done some years later by several scientists and partly as a consequence of studying or observing patients (e.g., Gregor, 1902, 1907, 1909; Ranschburg, 1911; overviews in: Markowitsch, 1992; Markowitsch and Staniloiu, 2019). For example, Oskar Kohnstamm (1917), reported the case of a former soldier who had been buried alive, but had no somatic complaints. The patient's short-term memory was normal; however, he did not recall dates from history or geography, which he had learned in school. His musical repertoire, however, was still existent; although he was not aware of the titles of the musical pieces, he was able to play them accurately. He recognized his closest relatives but was not able to recognize his more distant friends, although he still was aware of the fact that he had known them. Kohnstamm (p. 375) concluded that the “quality of familiarity” had survived in the patient. The patient, however, had a severe anterograde amnesia as well (but no trace of confabulation). Kohnstamm emphasized that the patient's remembering was greatly influenced (i.e., facilitated) by emotional stimuli and by the degree to which he was interested and engaged in a topic (p. 378). Kohnstamm remarked that this observation might be used pedagogically and for memory training. Here again, as in other studies from this time, similarities are apparent to Tulving’s classification of memory into systems. When Kohnstamm stated that “knowledge of language, calculation, and requirements for daily living” (p. 380) were preserved, one is reminded of preserved semantic memory and of grossly impaired episodic memory. Perceptual memory (‘sense of familiarity’) and procedural memory (musical repertoire) were preserved. Consequently, with Kohnstamm’s description we have an early example for the gradation of awareness in memory, of which William James was aware already in 1892 when he wrote “consciousness, then, does not appear to itself chopped up in bits …. It is nothing joined: it flows. A ‘river’ or a ‘stream’ are the metaphors by which it is most naturally described” (p. 145). Aside from Kohnstamm’s observations, which he himself did not discuss in the context of memory divisions, there were other researchers at that time, who indeed attempted to make such memory partitioning. One of them was Kurt Schneider, another one Theodor Ziehen; both of them were famous German psychiatrists. (Later Ziehen also worked as professor of philosophy and psychology). Schneider (1928) made a division into conscious and subconscious memory, writing about the part of mnestic functions, which are capable of consciousness or to enter consciousness2 , and the other part, which consists of dispositions for recognition without awareness. Subsequently, one might relate this division to episodic and semantic (or declarative; Tulving and Markowitsch, 1998) memory, on one hand and priming and procedural memory, on the other hand. Ziehen (1906, 1908) pointed out that brain physiology already had shown at the beginning of the (20th) century that there is no general memory, but that there are several forms of memories.3 An important finding is therefore that scientists of the early 20th century not only described different levels of content of memories, but also referred to different levels of consciousness – they distinguished between memories which entail processing on a conscious level, and memories with processing that is subconscious or devoid of the need for consciousness , for example those related to the ‘priming memory system’ (Fig. 1). In 1888 Emil Kraepelin, another famous Germany psychiatrist, who worked in Dorpat/Tartu, Heidelberg and Munich, gave a talk (published in 1889) at the Dorpat Medical Faculty in Estonia – the city, now named Tartu, where Endel Tulving went to high school. In this talk he addressed effects of training on the duration of associations and noted that even after 1¾ years many previously acquired associations were reproduced in spite of the subjects' 2 3

“bewußtseinsfähigen bzw. ins Bewußtsein tretender Teil der mnemischen Funktionen” (Schneider, 1928, p. 508). “daß ein allgemeines Gedächtnis nicht existiert, sondern nur Teilgedächtnisse“ (Ziehen, 1908, p. 16).

7 failure to realize that they had learned them. Implicitly, so to say, Kraepelin more than 130 years ago had described what nowadays is known as priming memory (implicitly processed memory). Claparede’s (1911) classical description of his patient – a woman with Korsakoff’s syndrome – deserves to be mentioned in relation to priming memory. Claparede had hidden a pin in his hand when shaking hands with the patient (which he did every morning), with the consequence that the next morning the patient refused to shake hands with him. But, as he wrote, the patient was apparently unaware of the reason for her behavior, or even of the fact that she had met him before. This is a classic example of the distinction between conscious remembering or recall – of which she was unable – and subconscious priming – which was preserved. Due to the many cases with alcoholabuse related Korsakoff’s syndrome, this disease was well known at the turn of the century; Bonhoeffer (1901), for example, devoted a whole book to these patients, which was entitled “Acute Mental Illnesses of Chronic Drinkers“ (our translation). In this book, Bonhoeffer mentioned four cardinal symptoms of Korsakoff’s syndrome: ‘anterograde amnesia’, ‘retrograde memory defects’, ‘disorientation’ and ‘confabulation’. Another classic example for subconscious processing came from Schneider (1912) and refers to what is named nowadays procedural memory. When reviewing “clinical-psychological methods of investigation and their results”, Schneider firstly broadly reviewed the available techniques and stated that at that time puzzles and related games were already in use (on p. 559 he wrote: "The presently again modern American 'puzzle game' also belongs in this list"). His test battery consisted of pictorial material (which had to be interpreted or in which details had to be identified), puzzles, and verbal learning tests. He applied it to 25 healthy participants (mainly hospital staff) and to many psychiatric and neurological patients. He was not quite satisfied with his test battery and subsequently he wrote that “our methods do not allow an exact determination of psychic disturbances in a satisfactory manner” (p. 615; our translation).

Episodic memory as emotional memory Patients with Korsakoff’s syndrome seem also suited to illustrate that emotions are constituent parts of episodic memories. A striking aspect of anterograde amnesia in Korsakoff’s patients is its variability: On one hand, its severity differs between patients, on the other hand, it is usually disproportionally more severe with respect to free recall as compared to recognition (e.g., Markowitsch et al., 1984, 1986; Staniloiu et al., in press). This points to an important aspect of episodic memory, namely that episodic memories are usually emotionally colored (e.g., Wheeler and McMillan, 2001; Rosenbaum et al., 2005; Moscovitch et al., 2016; Sawczak et al., in press; Staniloiu and Markowitsch, 2019). Rosenbaum et al. (2005) wrote that “emotional and contextual details … define a personal from a non-personal episodic experience (p. 1008). (In fact, Tulving already in 1983 had pointed out that for episodic memory affect is more important than for semantic memory; p. 9, p. 42f.) The importance of emotion as a supporting variable for remembering had been emphasized by Sigmund Freud at the end of the 19th century; he anticipated the concepts of ‘ecphory’ (Tulving, 1983, p. 175ff) and ‘state-dependent memory retrieval’ in his descriptions (Freud, 1895/1950, 1895/1954; cf. also the figure of Freud’s network theory of emotional memory in Peper and Markowitsch, 2001).

8 Tulving (1983) used the term ‘ecphory’ to describe the process by which retrieval cues interact with stored information so that the reconstruction of the queried information represents a complex interaction of the two (or: … describes the process by which retrieval cues interact with stored information so that an image or representation of the information in question appears). The consequence is ‘state-dependent memory’, which characterizes memory as already acknowledged by Bartlett (1932) (see also the section on “Memory Transformation” by Moscovitch et al., 2016, p. 108f). Interestingly, Edward Bradford Titchener, a famous British-American psychologist, who worked with Wilhelm Wundt in Leipzig, formulated related ideas in his Philosophical Review paper from 1895. He wrote: “But we may also mean to express by the term ‘memory’ the fact that affection is revivable: that a past pleasure-pain may appear in consciousness in virtue of its revivability, just as a past perception may appear in idea, as representation. Here the active attention may not be involved; the affection may be supposed to arise ‘of itself,’ the consequence of the automatic working of the laws of mental association.” (p. 65). Titchener cited the work of Alfred Lehmann (1892) who described, what he considered to be a law: ‘Emotional feelings are reproduced by producing again the imaginations, with which they were connected. And the more complete the reproduction of the intellectual elements is, the exacter and stronger the emotional elements are produced again.’4 Thus, already before Semon (1904), who created the term ‚ecphory’, other scientists – from Freud to Lehmann and Titchener – had formulated similar ideas on state-dependent memory retrieval and on its emotional embedding. Titchener (1916), however, later became more skeptical about the possibility that past memories are revived via emotions, while Bartlett in 1932 emphasized that memories are reconstructed and are therefore “state-dependent”.

Episodic versus autobiographical memory In his theoretical contributions Tulving mostly focused on ‘episodic memory’, but not ‘autobiographical memory’ (e.g., Tulving, 1995, 2002, 2005; Tulving and Markowitsch, 1998). Nevertheless, he in general subsumed autobiographical memory under episodic memory. For instance, in Table 54.1 of his chapter from 1995, Tulving wrote that ‘autobiographical’ is another term for ‘episodic’. Only in the article that he published together with Wheeler and Stuss (Wheeler et al., 1997), a distinction is made, such as that episodic memory is linked to awareness during retrieval while autobiographical memory is linked to content (p. 333). Tulving’s “neglect” of the term autobiographical memory changed when it came to clinical studies, where he – together with his co-workers – reviewed the memory disorders of his famous Toronto-based patient K.C. (Rosenbaum et al., 2005). In this review a number of expressions were used: “memories of autobiographical episodes” (p. 1009), “memory for autobiographical … events” (p. 989), “autobiographical memory” (p. 989), “autobiographical information” (p. 997), “autobiographical episodic memory” (p. 1000) “episodic amnesia” (p. 989), “personal episodic past” (p. 993), “single or infrequent episodic happenings” (p. 1004), “episodic information” (p. 1006), “personal episodic memory” (p. 1006, p. 1008), “… details that define a personal from a non-personal 4

„Gefühlstöne können dadurch reproduziert werden, dass die Vorstellungen, mit welchen sie verbunden gewesen sind, wiedererzeugt werden. Und je vollständiger die Reproduktion der intellectuellen Elemente stattfindet, um so genauer und stärker werden auch die emotionalen Elemente wiedererzeugt werden.“ (Lehmann, 1892, p. 262).

9 episodic experience” (p. 1008). It can be concluded from this list (as well as from the equating of the terms ‘episodic’ and ‘autobiographical’ in Tulving, 1995) that Tulving apparently sees a high degree of overlap between episodic and autobiographical memory. In the paper of Rosenbaum et al. several autobiographical memory tests were used to demonstrate K.C.’s lack of remembering his past. The first scientist, who in a very similar way tested early reminiscences of his patients by using semistructured autobiographical memory tests, was Breukink (1907) from Utrecht University. After Breukink, this kind of testing was largely forgotten, until it was revived by the works of Crovitz and Schiffman (1974) and Kopelman et al. (1990) (see also Piolino et al., 2007). A distinction between episodic and autobiographical memories has been made with respect to the ontogenetic development of memory. Here the very influential paper of Nelson and Fivush (2004) has to be mentioned, in which the authors differentiated between episodic and autobiographical memory, stating that the first develops prior to the second one (cf. their Figure 1). Pathman et al. (2011) followed the distinction into these two terms and suggested that in fact autobiographical memories might appear earlier than episodic ones. However, all the children in their study were already of older age, compared to the developmental trajectory described in Figure 1 of Nelson and Fivush (2004), in which episodic memory development is depicted as starting at age three and autobiographical memory development, around age five. Pathman et al. also suggested that their findings might be related to the specific paradigm used. Morrison and Conway (2010) argued in a different way: They consider a version of episodic memory (“sensory-perceptiveaffective”), which appears very early in life, and another version (“conceptual episodic memory”), which appears later; however, autobiographical is still considered by them to appear even later. Be that as it may, Tulving’s more recent definitions of episodic memory seem to combine episodic and autobiographical memories under the heading of ‘episodic-autobiographical memory’ (cf. Figure 1 and Tulving, 2002, 2005; Lemesle et al., 2017). And for Nelson and Fivush (2004), the “most distinctive form [of autobiographical memory] is episodic in Tulving’s sense (i.e., self-involved and temporally specific)” (p. 487). Similarly, Moscovitch et al. (2016) more recently wrote that episodic memory is “what laypeople may call an autobiographical episode” (p. 106). When autonoetic awareness is used in the definition of episodic memory, it apparently does not make sense to differentiate it from autobiographical memory.5 Still, however, there are semantic components in autobiographical memory – namely ‘factual self-knowledge’ and ‘trait self-knowledge’ (Staniloiu and Markowitsch, 2014; cf. their Fig. 3); also the “summary of representations of repeated events” (Klein and Markowitsch, 2014, their Fig. 1) can be subsumed under noetically-processed autobiographical information belonging to the semantic memory system. Tulving (2005, p. 14) acknowledged the existence of autobiographical-semantic memories, when he wrote: “Amnesic patients can tell stories about themselves that have to do with the past, but in doing so they rely on semantic memory (“personal semantic memory” …).”

Perceptual memory system – familiarity ‘Perceptual memory’ was not included in Tulving’s main work on memory systems. However, he listed it in personal discussion with one of the authors (HJM) and included it in Figure 1 as a memory system for familiarity. Recognizing an apple, no matter, whether it is red or green, or intact, sliced or half eaten, is a matter of perceptual memory. The ability to distinguish it from other fruits – 5

This conclusion was formulated by one of the anonymous reviewers.

10 such as peach or pear – also is a function of this memory system, which Tulving created in response to data from John Hodges on patients with semantic dementia (Hodges et al., 1992). Patients with semantic dementia are, for example, unable to name a specific object like a pigeon, though they appear to be familiar with the concept of birds and may be able to describe attributes of a pigeon and to distinguish it from a crow. This memory ability was subsumed under the ‘perceptual memory system’ by Tulving. Aside from Kohnstamm (1917), mentioned above, Boldt (1905), in his ‘Studies on defects in remembering’ [“Studies über Merkdefekte”], gave vivid descriptions of special abilities or disabilities of patients with particular professional backgrounds. Among them was a patient with Korsakoff’s syndrome, who worked as a waiter, who had severe problems recalling names, faces, and numbers; however, he still seemed to have god remote long-term memory for his regular guests (who were known to both the patient and the examiner). Therefore, the perceptual memory system (“familiarity”) (Fig. 1) still seemed to work, while standard tests on semantic memories, which Boldt had applied, had showed severe deficits. Several other early researchers – such as Müller-Freienfels (1915), Pick (1903) and Titchener (1895) – discussed the special nature of familiarity within the context of memory as well.

Conclusions and the future of episodic memory “Time present and time past Are both perhaps present in time future” (Eliot, 1969, p.171) Tulving’s memory systems have a scattered background in the history of memory research, but are still the most refined, comprehensive and integrative, and up-to-date classification compared to other ones (see e.g., Ferbinteanu, 2019; Goodman et al., 2014; Gupta and Cohen, 2002; Mishkin and Petri, 1984; Squire, 1993, 2004), though especially the term ‘episodic memory’ is still debated (e.g., Conway, 2009; Mahr and Csibra, 2018; Szunpar and Chan, 2018). Conway (2009) discussed ‘episodic memory’ not as a system, but “as memories” (p. 2305) and attributed in his Table 1 nine properties to them. Especially the distinction between episodic and semantic memory (Tulving, 1972) has a particular value for research in the neurosciences. In clinical neuroscience, both neurological and psychiatric patients have the most severe – and sometimes exclusive – deficits in the episodic memory domain (e.g., Palombo et al., 2019; Markowitsch and Staniloiu, 2012; Staniloiu and Markowitsch, 2014; Staniloiu et al., 2013, 2018). There are apparently no patients with an equivalent damage to both systems – sometimes combined under the heading of declarative memory (e.g., Squire, 2004). _________________________ Insert Figure 1 about here _________________________ As discussed repeatedly, autobiographical memories may include fact-based memories, such as a semantic component (all personal information such as birthplace and birthdate) acquired since birth (Conway, 2009; Staniloiu and Markowitsch, 2014; Lemesle et al., 2017) (Fig. 2). However, we also found another link to episodic-autobiographical memories, namely semantic facts of personal

11 and emotional importance (Fig. 2). This is material that apparently is emotionally laden, because it was acquired under special conditions (such as under stress during education/studies). Patients with psychogenic amnesic conditions (such as ‘dissociative amnesia’) may have a retrieval blockade (Markowitsch, 2002; Staniloiu and Markowitsch, 2014) of this material in addition to their retrieval blockade of autobiographical and personal semantic facts (e.g., Staniloiu and Markowitsch, in subm.) Another related finding was derived from assessing different patient groups, using a different methodology: This is the ‘overgeneral memory effect’ (as assessed with the Autobiographical Memory Test [AMT]) (Williams and Broadbent 1986), meaning that individuals requested to recall events from their life (usually in response to a cue), mainly give a factual account. (For example, instead of describing in detail an episode from their school life, they just give the name of the school and tell that something happened there.) This effect has been observed in abused, neglected, and maltreated children (Valentino et al., 2009), in patients with depression (Watkins et al., 2000), with Alzheimer’s (Seidl et al., 2006) and Parkinson’s disease (Smith et al., 2010), and in patients with Dissociative Identity Disorders (Huntjens et al., 2014).6 Although the AMT paradigm does not explicitly integrate the Tulving’s distinction between episodic and semantic memory systems, the description of overgeneral memories shares certain similarities with that of semantic memories, whereas that of specific memories resembles to a certain degree of semantic memories (Söderlund et al. 2014; Staniloiu and Zaretsky, 2015). The differences in content-based retrieval that are seen in the specific versus overgeneral memories may gain a new understanding through the work of Stanley Klein (2013). He proposed that the retrieval of episodic(-autobiographical) memory requires distinct, interacting enabling systems: “ownership, self, subjective temporality, and agency” (Abstract); or, as he wrote in another article (Klein, 2015), that episodic memory is related to “a feeling of direct acquaintance with one’s past.” This feeling of acquaintance had been already poignantly described by William James in 1890 (James,1950, p. 650): “Memory requires more than mere dating of a fact in the past. It must be dated in my past. In other words, I must think that I experienced its occurrence”. Klein (2016) furthermore emphasized the mechanism or process of autonoesis/autonoetic consciousness as being crucial, not episodic memory as such. Moscovitch et al. (2016) in their recent review on “Episodic memory and beyond: …” emphasized along the same line as Klein that episodic memory is embedded in and related to many other cognitive domains like attention, perception, emotions, locations, social environment. Such interactions were more recently the subject of several investigations (e.g., Hutchinson et al., 2009; Dunsmoor et al., 2013, 2019; Talmi et al., 2013; Staresina and Wimber, 2019). Based on these additional sub-categories – and the distinctions proposed by others (e.g., Conway, 2009) – it may be that, in the near future, we may have a further refined description of “episodic memory”, though it is very unlikely that we will end up with many more memory systems (cf. Tulving, 2007). On the process-level, distinctions seem to multiply as well: Kihlstrom (2020) differentiated recollective experience into ‘remembering’, ‘knowing’, ‘feeling’, and ‘believing’. These differentiations – similarly as argued by Moscovitch et al. (2016) – have implications for the neural basis of the episodic memory system. While marching into the future of episodic memory, it is worth mentioning two more important aspects. One aspect is related to the grand challenge of proving the existence of an episodic memory system in non-human animals, by fulfilling all the criteria that the most reason definition of episodic memory of Endel Tulving entails (Tulving, 2005). The other aspect pertains to 6

One of the reviewers mentioned that patient H.M. (Squire, 2009; Luke, 2016) as well responded in this way.

12 implementing episodic memory for an intelligent agent that will subsequently render it capable of passing the spoon test, which was proposed by Endel Tulving (2005) to assess whether non-human animals (and by extension artificial intelligence agents) are capable of mental time travel, an intrinsic feature and enabled characteristic of episodic memory (Kühnel et al., 2013).

13 References

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19 Figure legends Figure 1. The five long-term memory systems. (A version of this sketch was created together with Endel Tulving.)

Figure 2. Relations between autobiographical memory and semantic memory. Episodic-autobiographical memory is seen as an entity which contains memories with self-relevance which are autonoetically processed (Markowitsch and Staniloiu, 2011). ‘Autonoetic consciousness’ allows the individual “to become aware of their protracted existence across subjective time’ (Wheeler et al., 1997, p. 335). Semantic memory is divided into four parts: ‘general world knowledge’, ‘semantic-autobiographical facts’ (birthday and place, and similar facts), ‘semantic facts of personal and emotional importance’, and the ‘summary of representations of repeated events’ (Klein and Markowitsch, 2014). With the second sub-category we mean facts which have a personal relevance for the individual; they therefore are linked to autobiographical cube by an arrow (as are two other sub-categories). We had found in patients with dissociative amnesia, a disease that usually features retrograde amnesia, that some patients not only lack access to episodic-autobiographical memories, but also to semantic memories that have a personal relevance to them (e.g., words in Latin, learned under conditions of personal and emotional relevance) (Staniloiu and Markowitsch, in subm.).

FIGURE 2 SHOULD IN PRINT BE BLACK AND WHITE.

20 Figure 1

21 Figure 2 (in print in black and white/noncolored)

Highlights

The term episodic memory was coined by Endel Tulving. The episodic memory system is equivalent to episodic-autobiographical memory system. The episodic memory system is seen as linked to emotions. Current memory systems had forerunners according to content and type of processing. The episodic memory is embedded in other cognitive domains.