Sistemas Memoria Longo Prazo

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Received: 29 May 2022 Revised: 1 July 2022 Accepted: 3 July 2022
DOI: 10.1002/wcs.1617
ADVANCED REVIEW
Behavioral, neurological, and psychiatric frailty

of autobiographical memory
Hans J. Markowitsch1 | Angelica Staniloiu1,2,3
1
Department of Physiological Psychology,
University of Bielefeld, Bielefeld, Abstract
Germany Autobiographical-episodic memory is considered to be the most complex of
2
Oberberg Clinic, Hornberg, Germany the five long-term memory systems. It is autonoetic, which means, self-reflec-
3
Department of Psychology, University of tive, relies on emotional colorization, and needs the features of place and time;
Bucharest, Bucharest, Romania
it allows mental time traveling. Compared to the other four long-term memory
Correspondence systems—procedural memory, priming, perceptual, and semantic memory—it
Hans J. Markowitsch, Department of develops the latest in phylogeny and ontogeny, and is the most vulnerable of
Physiological Psychology, University of
Bielefeld, P. O. Box 100131, 33501 the five systems, being easily impaired by brain damage and psychiatric disor-
Bielefeld, Germany. ders. Furthermore, it is characterized by its fragility and proneness to distor-
Email: hjmarkowitsch@uni-bielefeld.de
tion due to environmental influences and subsequent information. On the
Edited by: Mohamad El Haj, Editor brain level, a distinction has to be made between memory encoding and con-
solidating, memory storage, and memory retrieval. For encoding, structures of
the limbic system, with the hippocampus in its center, are crucial, for storage
of widespread cortical networks, and for retrieval again a distributed recollec-
tion network, in which the prefrontal cortex plays a crucial role, is engaged.
Brain damage and psychiatric diseases can lead to what is called “focal
retrograde amnesia.” In this context, the clinical picture of dissociative or func-
tional or psychogenic amnesia is central, as it may result in autobiographical-
emotional amnesia of the total past with the consequence of an impairment of
the self as well. The social environment therefore can have a major impact on
the brain and on autobiographical-episodic memory processing.
This article is categorized under:

Psychology > Memory
KEYWORDS
consciousness, dissociative amnesia, episodic memory, hippocampus, limbic system, self
1 | INTRODUCTION
Memory has been in the focus of scientific speculations for thousands of years and was considered fragile and
unreliable and as being affected by disease, injuries, and even by fright (Bostock, 1855). On the other hand, memory
was considered to be the glue which holds us together as a person or personality. Hering, a famous physiologist of the
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2 of 27 MARKOWITSCH AND STANILOIU
19th century wrote in 1870 a booklet on memory, which was translated into English in 1895 (Hering, 1870;
Hering, 1895), and which contains on p. 12 the following statement: “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” (Hering, 1895).
Nevertheless, except from a few exceptions (Markowitsch & Staniloiu, 2016a), memory was considered a unity until
Tulving (1972) proposed the division into “semantic” and “episodic memory.” At that time, “semantic memory” was
defined as presence-oriented fact-memory, and “episodic memory” as a system for events that can be traced back with
respect to the questions, when and where they happened in the past. Over the years, Tulving refined the definitions of
episodic memory (e.g., Tulving, 1983, 1995, 1999, 2002, 2005) and distinguished it from the later upcoming term
“declarative memory” (Tulving & Markowitsch, 1998). While Tulving rarely referred to “autobiographical memory,” he
implicitly—and also in personal communications with one of the authors (HJM; Figure 1)—largely equated it with epi-
sodic memory (e.g., when writing about his favorite patient K.C.: “much more severe for personal, autobiographical
experiences than generic, factual knowledge”; Tulving, 2005, p. 15). In fact, he always emphasized the “remember—
know distinction (R/K)” (Tulving, 1993; Wheeler et al., 1997). Wheeler—a former student of Tulving—wrote in 2001
together with McMillan on page 23 (Wheeler & McMillan, 2001): “Episodic memory makes possible the recollection of
personally experienced events as they were originally experienced; it is through the episodic memory system that indi-
viduals can remember their past. Semantic memory handles factual information, and retrieval from semantic memory
allows individuals to know things about the world.”
2 | T H E ME M O R Y SY S T E M S
Several years ago, Endel Tulving developed with one of the authors (HJM) a sketch of the five long-term memory sys-
tems, depicted in Figure 1. These systems include the usually nonconsciously processed procedural memory and prim-
ing systems, which Tulving termed anoetic, the two consciously processed perceptual and semantic memory systems,
named noetic, and the episodic-autobiographical memory system, which is considered to be autonoetic. In
Tulving's (1993, p. 68) words: “I refer to the kind of conscious awareness that characterizes remembering one's past as
autonoetic awareness, contrasting it with noetic awareness, which characterizes retrieval of information from semantic
memory, and anoetic awareness, which accompanies the expression of procedural knowledge.”
2.1 | Short-term memory and working memory
In addition to the long-term memory systems, short-term memory is used as an expression to describe a system in the
range of a few seconds (5–30 s, depending on existing or nonexisting interference effects, or 4–7 bits of information;
Cascella & Al Khalili, 2022; Cowan, 2000, 2015), which is responsible for the short-term storage of conscious informa-
tion that then is transferred into long-term memory (Atkinson & Shiffrin, 1968). A more recent term is working mem-
ory, which was introduced by Baddeley and Hitch (1974) to characterize “cognitive operations and executive functions
associated with the organization and manipulation of stored information” (Cascella & Al Khalili, 2022; see also:
Baddeley, 2000; Baddeley, 2012; Baddeley et al., 2019). This term also refers to a very limited amount of information.
2.2 | Procedural and priming memory
The procedural and priming memory systems are distinct systems which act quite differently from the other three. Pro-
cedures are mostly motor-related and the acquisition patterns rely to a high degree on exercise (e.g., cycling, skiing,
playing a game). Priming has been divided into “perceptual priming” and “conceptual priming.” Under “perceptual
priming,” the re-identification of previously perceived items or information is understood, while “conceptual priming”
refers to category verification, that is, to the identification of items or information related to the originally perceived
one (= belonging to the same category). This division has frequently been used in order to demonstrate that perceptual
priming is still possible in individuals with reduced memory abilities, while conceptual priming is impaired, and that
MARKOWITSCH AND STANILOIU 3 of 27
F I G U R E 1 The five long-term memory systems and their brain bases. Procedural memory is largely motor-based, but includes also
sensory and cognitive skills (routines). Priming refers to a higher likeliness of re-identifying previously perceived stimuli. Perceptual memory
allows distinguishing an object, item, or person based on distinct features. Semantic memory is context-free and refers to general facts; it
encompasses general knowledge of the world. The episodic-autobiographical memory (EAM) system is context-specific with respect to time
and place. It allows mental time travel and is based on self-reflection (autonoesis). Examples are events such as the last vacation or the
dinner of the previous night. The terms “remember” and “know” describe the distinction between EAM and semantic memory, as
remembering requires conscious recollection embedded in time and space and with an emotional flavoring, while knowing represents a
simple, though conscious, yes/no distinction without further connotations. Tulving (2005) assumes that during ontogeny (as well as during
phylogeny) memory development starts with procedural memory and ends with episodic-autobiographical memory, a system that he
reserves for human beings, while all other systems can be found in animals as well. With respect to dimensions of consciousness, Tulving
considered the first two memory systems as being anoetic, the next two noetic, and the EAM to be autonoetic. As the lower part of the neural
representation of the memory systems indicates, it is mainly the EAM that is dependent on a well-functioning limbic system. The precuneus
is not mentioned in this figure, though it is frequently active during conscious retrieval as a content-imagining area. A version of this sketch
was created together with Endel Tulving.
patients with mild cognitive impairment profit to a higher degree than nonimpaired individuals from priming effects
(De Wit et al., 2022; Rowe et al., 2021; Ward, 2022).
An extreme example of priming was given by Levinson (1965). He described 10 patients who during deep surgical
anesthesia were verbally confronted with indications of an anesthetic crisis. One month after this event they were hyp-
notized and regressed to the operation situation. Four of the patients were able to reproduce the words spoken by the
doctor, and four others became anxious and awake from the hypnosis. This report indicates that information retrieval
can be primed when a similar or related condition is induced (see below under Episodic-autobiographical memory:
“state-dependent retrieval”).
2.3 | Perceptual and semantic memory
Of the two noetic systems, semantic memory refers to a memory system with clear boundaries and an intuitive descrip-
tion. Items learned during child development from preschool to school periods, constitute the bulk of semantic infor-
mation: To know chemical formulas, animals and plants, the brands of cars, and so on, are all in the domain of
semantic knowledge. There are a few exceptions that blur the distinction between the semantic and the episodic-
autobiographical memory system, described below, which, however, become relevant only in cases with a distinct
psychopathology, especially so-called dissociative amnesia (cf. Figure 2, and the description of such cases under
Episodic-autobiographical memory).
The constituents of perceptual memory, on the other hand, are less obvious. This noetic system refers—as is men-
tioned in Figure 1—to familiarity. That means, items we perceive—the voice of the grandmother, the trout in the pond,
the fur of a cat—are instantaneously associated and unequivocally recognized, even if the respective person, perceiving
them, became unable to pronounce the words grandmother, trout, and fur, as may be the case in patients with semantic
dementia (Adlam et al., 2010; Graham et al., 2000; Hodges et al., 1992; Zannino et al., 2021).
2.4 | Episodic-autobiographical memory
Episodic-autobiographical memory is a term which, on the one hand, emphasizes that episodes are usually autobio-
graphical, but that in rare instances the equation between the two does not hold (Figure 2). Reasons for the incomplete
overlap between episodic and autobiographical can be traced back to the development of this memory system (C. A.
Nelson, 1995; K. Nelson & Fivush, 2004; Figure 3). It should be emphasized that episodic-autobiographical memories
usually are linked to emotions (Staniloiu & Markowitsch, 2020). During mental travel, not only the event is
reconstructed (Conway & Howe, 2022), but also the emotion or affect attached to it (Meconi et al., 2021). That this is
the case becomes evident from the results of patients with Urbach–Wiethe disease (Lipoid proteinosis), a rare very
genetic disease (Rosenberger et al., 2019), which leads to a reduced odor perception (Siebert et al., 2003) and to reduced
processing of memories with biological and social significance (El Haj, 2022; Iizuka et al., 2021; Larsson &
Willander, 2009; Markowitsch & Staniloiu, 2011b, 2012a, 2012b; Masaoka et al., 2021; Phelps, 2004). We demonstrated
this in a patient with Urbach-Wiethe disease by using a paradigm implying a short, narrated story, supported by a pic-
ture show. The story had three phases. In it, a young boy walked with his mother to visit his father at work. In the mid-
dle phase of the story, the boy obtained severe injuries in a terrible traffic accident (Cahill et al., 1995). While the
control group (six individuals matched with respect to age and education to the patient) remembered especially this
phase, the opposite was true for the patient, who remembered less compared to the neutral phase, indicating that she
could not appropriately attach the emotional to the fact content of the story.
There are several, probably related phenomena involved in processing episodic-autobiographical memories: Their
emotional content and detailedness diminish with repetitions over time (though not so much in the short run: Bradley
et al., 2022), with increased age (Charles et al., 2003), and with the progression of cognitive deterioration (as, e.g., in
Alzheimer-related symptomatology; Seidl et al., 2006; Aronson, 2022)—memories become more “semanticized”
(McWilliams et al., 2022). In a huge meta-analysis of 74 studies, T. J. Barry, Clark, and Maguire (2021) found that
patients with psychiatric diagnoses typically recall fewer specific, and more general (semanticized) memories than indi-
viduals without a psychiatric diagnosis. Nearly half of the patients had a diagnosis of Major Depressive Disorder, about
19% of Schizophrenia, 17% of Posttraumatic Stress Disorder, and a few studies manifested other psychiatric disorders
(e.g., 5% of Anxiety Disorders). Therefore, they consider autobiographical memory impairments as a transdiagnostic
feature of mental illness (see also Williams et al., 2007).
The findings on semantization also emphasize that episodic memory cannot just be equated with tests on verbal
memory, as was, for example, done in the study of Liampas et al. (2022) which otherwise is important, especially due to
a large number of analyzed subjects. Even the more cursory definition of episodic memory, given in Spaniol et al.
(2009), counteracts the inclusion of verbal memory tests; it says that episodic memory is “conscious memory for person-
ally experienced events within a particular spatio-temporal context” (p. 1766). However, it should be emphasized as
F I G U R E 2 Relations between episodic-autobiographical and semantic memory. Episodic-autobiographical memory is seen as an entity
containing memories with self-relevance which are autonoetically processed (Markowitsch & Staniloiu, 2011a; Staniloiu et al., 2020a).
“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”
(e.g., birthday and place, addresses of places lived, names of schools attended), “semantic facts of personal and emotional importance,” and
the “summary of representations of repeated events” (Klein & Markowitsch, 2014). With the second subcategory, we refer to facts of
personal relevance for the individual; they, therefore, are linked to the rectangle with “Autobiographical events and related memories” by an
arrow (as are the two other subcategories). 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., Latin phrases, learned under conditions of personal and emotional relevance; Staniloiu et al., 2020b; Staniloiu &
Markowitsch, 2020).
F I G U R E 3 Relations of memory development during the first years of life. Double-headed arrows indicate reciprocal influences.
The scale indicates approximate ages when influences come into play in normal development (modified after figure 1 of K. Nelson &
Fivush, 2004).
well that it is the autonoetic aspect of recollection—more than the event-character—that defines episodic-
autobiographical memory (Klein & Markowitsch, 2014).
The autonoetic character of recollection is severely impaired in patients with hypoxia-/anoxia-related hippocampal
damage early in life, who may have a largely unimpaired semantic memory, but no episodic-autobiographical memories
(Staniloiu et al., 2013; Vargha-Khadem et al., 1997, 2003). It has been emphasized that the inability to imagine is a core
feature of these patients with so-called neurodevelopmental amnesia (Hassabis, Kumaran, & Maguire, 2007; Hassabis,
Kumaran, Vann, et al., 2007; Hassabis & Maguire, 2009). However, these individuals with hippocampal damage early
in life may have—possibly due to functioning hippocampal residuals—a (partly) preserved ability to construct fictitious
scenarios (Cooper et al., 2011).
A related feature to the imagination in episodic-autobiographical memory is that it is not only a memory of the past,
but also of the future—so-called prospective memory (McDaniel & Einstein, 2007; Schacter et al., 2007), or episodic
future thinking (Elliott et al., 2022; Gibson et al., 2022). In prospective memory, one remembers what one will do in the
future (e.g., having an appointment with a friend; or going to Madeira for hiking in a few months). La Corte et al.
(2021) distinguish the two expressions by stating that prospective memory refers to the ability to remember to execute
planned actions, while episodic future thinking refers to the ability to imagine future personal events. Prospective mem-
ory, similar to episodic-autobiographical memory in general, deteriorates in aged (Hsu et al., 2022) and demented peo-
ple (Lecouvey et al., 2019).
As mentioned above, another feature of episodic-autobiographical memory is its self-reflectance (autonoesis; Cabeza
et al., 2004; Fossati, 2013; Markowitsch, 2003) The importance of the self for episodic-autobiographical memory is
inherent in its definition (cf. Figure 1) and becomes most evident in individuals who lack episodic-autobiographical
remembrances due to the complex of psychiatric diseases named dissociative disorders—in particular dissociative
amnesia (Markowitsch & Staniloiu, 2011a, 2012a, 2012b, 2016b; Staniloiu et al., 2010; Staniloiu & Markowitsch, 2014).
Patients with dissociative amnesia have an “inability to recall autobiographical information” that (a) is “usually of a
traumatic or stressful nature,” (b) is “inconsistent with ordinary forgetting,”, (c) was “successfully stored,” (d) involves
a period of time when there is an “inability to recall,” (e) is not caused by “a substance” or “neurological… condition,”
and (f) is “always potentially reversible because the memory has been successfully stored” (American Psychiatric Asso-
ciation (APA), 2013, p. 298). Because of the last criterion, we termed the disease “mnestic block syndrome” in order to
emphasize the potential reversibility of psychogenic amnesia (Markowitsch, 2002). How far the lack of self-confidence
reaches can be exemplified by the words of a patient, who was described in Staniloiu et al. (2020b): The patient doubted
that he had done a criminal act because he did not think that this was his type. However, he stated: “But I cannot guar-
antee. Because so much is unsure, so much is gone, one must give such things a residual probability. … That brings a
huge uncertainty. If someone would persuade me, I would have to accept, though it would be totally strange. My mem-
ory are the others.”
The impossibility to refer to one's own past, leads to changes in personality dimensions. One patient with dissocia-
tive amnesia had been an enthusiastic car driver prior to the amnesia, while thereafter he avoided to enter a car, saying
that cars are too fast for human beings. Furthermore, he wanted to change his profession and altered his dietary habits.
Frequently, these patients show so-called belle indifference, implying that they do not seem to care much about their
present state (loss of job, problems with family). This unconcern was noted first by Janet (1893), who coined the expres-
sion. We described this condition in more detail in Reinhold and Markowitsch (2009) stating that the patients have a
lack of concern, especially about their own psychic condition and about their future. They do not seem to care about
their family. On the other hand, they can be guided and directed much more easily than normal individuals, that is,
they are suggestible to influences from others. Probably, their personal lability is a cause of their disease condition.
Interestingly, the condition of dissociative amnesia also points to variant of memory loss, which is depicted in
Figure 2 under “Semantic facts of personal and emotional importance”. A patient with dissociative amnesia, who ini-
tially wanted to study medicine, but was not admitted to do so, instead studied Latin in order to later work as a high
school teacher. After becoming amnesic, he also was unable to know or to translate most common and simple Latin
phrases (e.g., plenus venter nonstudet libenter). This can be interpreted as an emotional aversion toward his Latin studies
which led to the respective memory repression (Langnickel & Markowitsch, 2006).
This finding of a memory block leads to another important term, the state-dependency of memory. Known since long
as a concept for both memory encoding and memory retrieval, Tulving (1983) revived its importance for episodic mem-
ory processing. Basically, it is related to another old concept (Markowitsch & Staniloiu, 2016a), namely that of ecphory.
Tulving (1983) noted that ecphory implies the process in which retrieval cues interact with stored information in a way
that the respective information becomes an interplay of both. Consequently, we memorize an event best, if the present
retrieval conditions (emotional state, environment) resemble those present during encoding most closely, that is, if the
psychic state during encoding matches that during retrieval, the likelihood of an exact mental reconstruction of the
event is highest. So, as an example, if an event is encoded in a euphoric mood and in a social context during a party, it
is later retrieved most likely and in similar detail, if the person again is euphoric and in the midst of a joyful party.
These relations were confirmed experimentally with different subject groups (young and old people, patients with tem-
poral lobe excisions due to epilepsy; Sawczak et al., 2022).
If the matching process is impaired, or if already at the time-point of encoding distracting and interfering informa-
tion occurs, the phenomenon of false encoding and consequently, false memories may arise. But also interfering
retrieval hints can result in false memories. Damage to memory-processing brain regions frequently disturbs autobio-
graphical memory retrieval and may lead to memory distortions such as confabulations or false memories (Borsutzky
et al., 2008, 2010; El Haj, 2021).
3 | M E M O R Y D I S T O R T I ON S— F R O M F A L S E ME M O R I E S TO FO R G E T T I N G
Sigmund Freud (Breuer & Freud, 1895; Freud, 1899, 1900, 1901a, 1901b, 1910) as well as his temporary follower Carl
Gustav Jung (Jung, 1905a, 1905b; Jung & Riklin, 1904) addressed in a number of writings the topic of forgetting in vari-
ous facets. Freud in particular emphasized in his early writing the relationship between forgetting and emotion and that
much of the processing occurs below the cerebral cortical level (Peper & Markowitsch, 2001). Based on Freud's studies
at the Salpêtrière in Paris, where Charcot (e.g., Charcot, 1892) and Janet (e.g., Janet, 1892) worked, he expanded the
model of hysteria, which first was considered to be mainly a disease of women, but then—during World War
I—changed to disease affecting men as well (e.g., Bauer, 1917). (Already in Bennett, 1878, Bennett had concluded on
p. 120 from the case of a young woman: “Under any circumstances it serves to indicate what caution should be
exercised in diagnosing, and more especially in treating, as hysteria, any nervous affection in women which may appear
indefinite or mysterious.” [our italics].)
Hippocrates' term “hysteria” was frequently connected with amnesia—both by Freud (Breuer & Freud, 1895) and
others (e.g., Donath, 1908; Mai, 1995; Read, 1923; von Krafft-Ebing, 1898), rising, however, the question whether indi-
viduals with this condition are conscious of their state or not, or whether they even malinger or lie (e.g., Barbarotto
et al., 1996). Suarez and Pittluck (1975), for example, introduced the distinction between conscious liars and malin-
gerers, whom they named “suppressors,” and unconscious hysterics, termed “repressors” (cf. also the related distinction
of Freud, discussed in Langnickel & Markowitsch, 2006). Freud saw in memory repression a mechanism of instinct
gratification or drive reduction, or of conflict solution—an Abwehrmechanismus [defense mechanism]. He
(Freud, 1900) stated that earlier experiences which had not reached consciousness would be re-interpreted into new
situations.
Hartmann (1930) later took up Freud's ideas in a paper entitled “Memory and the lust principle”, stating that the
power of repression (Verdrängung) increases with the strength of aversion for the material to be memorized. From his
experiments with patients with Korsakoff's syndrome, he inferred that the ability to reproduce material is strongly
related to its positive or negative emotional colorization, a finding that had been proposed repeatedly by Freud
(Peper & Markowitsch, 2001).
Known since the descriptions of Sigmund Freud—who, for example, wrote that we have no guarantee for the cor-
rectness of our memories, but nevertheless trust them more than is objectively justified (Markowitsch &
Staniloiu, 2016a)—false memories are a topic which is of special importance in a forensic context (Markowitsch, 2008a;
Markowitsch & Staniloiu, 2011c). They are defined as memories of events that never occurred or did not occur in the
way in which they are described (during retrieval). The reconstruction of events both during encoding (false recognition;
Janik et al., 2022; Jou & Hwang, 2022) and retrieval can lead to a representation which does not match the original
scene and circumstances (cf. also Mace et al., 2021). The occurrence of false memories has been the subject of a number
of experiments in which it was demonstrated that such false memories even can be implanted (Loftus, 2000, 2003). In
such an experiment, Wade et al. (2002) demonstrated the creation of a false memory by showing an individual his pho-
tograph as a child with his father when they were standing in the basket of a hot-air balloon. (The original photo in fact
just showed the two together and was taken from a family album.) This created false memories about the experience in
the balloon in which he had never been.
A frequently used method to create false memories is the Deese-Roediger-McDermott paradigm (e.g., Roediger III &
McDermott, 1995). In this, a number of related words are presented (e.g., calm, emotion, fight, fear, and temper) which
are related to a lure word (e.g., anger), representing the gist of the list, which, however, is not presented. In a subse-
quent test phase, subjects disproportionately often falsely recall or recognize the critical lure (Borsutzky et al., 2010).
More naturalistic variants of the Deese–Roediger–McDermott paradigm were used in the studies of Kühnel et al.
(2008), Risius et al. (2013) and Abichou et al. (2022). The design of Děchtěrenko and Lukavský (2022) is as well related
to the former, especially to that of Kühnel et al. (2008). While Kühnel et al. showed single shots of pictures that were
similar to movie parts, or showed single shots that complemented portions of film scenes, Děchtěrenko and Lukavský
showed partial views of large photographs. The unpresented parts of the photographs were used as a source of dis-
tractors with similar semantic and perceptual information.
4 | PITFALLS IN EYEWITNESS MEMORY
We will shortly address the important topic of eyewitness testimony as it is intimately related to memory processing.
The correctness of eyewitness testimony depends on a number of sensitive factors. Among them are:
• Factors inherent to the eyewitness producer (e.g., age, education)

• Factors inherent in the eyewitness receiver (experience of the juror)
• Factors related to the event [stressfulness of the event, environmental conditions, psychic conditions of the witness
(e.g., mood), physical and physiological conditions of the witness (e.g., sharpness of the senses, intoxications)]
• Time delay between witnessing the event and reproducing it
• Duration and complexity of the event
• General retrieval conditions (e.g., interrogation effects, misinformation effect)
Personality variables are, of course, a major factor, starting with age: Children are usually considered to be less reli-
able in their testifying (Contreras et al., 2021; Murnikov & Kask, 2021) and old or very old people may show eyewitness
memory deteriorations as well (Zangrossi et al., 2020). Children are less versatile in their verbal expression capabilities
and more focused on particular details, neglecting the overall picture. They also focus more on specific (e.g., negative)
emotions (Karni-Visel et al., 2022). Emotional involvement in general may bias observations (Głomb, 2022; Kersten
et al., 2021). Personality factors are also of importance with respect to the features of the observed individuals—whether
they make a serious impression, or whether the observer is biased or has prejudices toward them (e.g., white persons or
persons from other races; McKone et al., 2021; Erickson et al., 2022).
The experience of the juror(s) in interrogating is of importance as well (Bjørndal et al., 2020; Helm, 2021; Marr
et al., 2021). Report building is of importance as well (verbal and/or behavioral; Nahouli et al., 2021), or the order in
which questions are asked. Michael and Garry (2016) suggest to start with simple questions and coming to more com-
plex and difficult ones at the end. They had found that eyewitnesses reported higher accuracy and were more confident
about their memory when questions seemed initially easy, than when they seemed initially difficult. Alcohol and other
drugs have a major effect on false memories and other memory distortions as well as on suggestibility (Kloft
et al., 2021). Szpitalak and Polczyk (2021) alerted in their study to the misinformation effect, which occurs when eyewit-
nesses include information in their account that is incongruent with the event they witnessed, and originates from
being exposed to incorrect external sources. They suggest “reinforced self-affirmation” to overcome this effect (together
with contingent self-esteem and feedback acceptance as moderator variables). Furthermore, time is a major variable
affecting accuracy. Chevroulet et al. (2021) asked participants to view a crime video and thereafter to complete a Self-
Administered Interview plus a recall questionnaire after different delay intervals. They found on optimal recall, if par-
ticipants completed questionnaires within 1 day (but not, when they did so after 1, 2, or 4 weeks).
Though all the above variables and influences are important for memory retrieval—especially in courtroom
situations—one should keep in mind the caveat of Alan Baddeley (2022) that memory biases and “memory sins”, found
in laboratory situations, are not “characteristic of the whole field of human memory, a system whose virtues far out-
weigh its sins” (p. 58).
5 | T H E SP I - M O D E L
Tulving proposed some 30 years ago (e.g., Tulving, 1995) his Serial Parallel Independent (SPI) model which is process-
specific, that is, dependent on the processes. Encoding of information into the episodic system depends critically on the
semantic system whereas encoding of information into the semantic system could operate without the episodic system.
During retrieval of stored information, on the other hand, the basic operations of the two systems are independent of
each other: retrieval can be supported by either of the two systems or by both of them. In Figure 4, a schematic outline
F I G U R E 4 Sketch of the relations between semantic and episodic memory as envisaged by the SPI model. Information can be encoded
into semantic memory independently of episodic memory, but must be encoded into episodic memory “through” semantic memory.
Encoded and stored information is potentially available for retrieval from one of the two systems, or from both of them.
of the basic propositions of the SPI model as applied to episodic and semantic memory are outlined. An important point
that the model makes is that only single dissociations are possible in encoding, whereas both single and double associa-
tions are possible in retrieval.
6 | ALTERNATIVE MODELS OF MEMORY SYSTEMS
As we have outlined in a chapter on the history of memory (Markowitsch & Staniloiu, 2016a), the first attempt to divide
memory occurred at the beginning of the 20th century. Ziehen wrote in 1908 that “only brain pathology has shown us
that a general memory does not exist at all, but only subdivisions of memory or partial memories” (p. 17, our transla-
tion; Ziehen, 1908). At that time, it was distinguished between verbal and procedural memory (Schneider, 1912, 1928).
Shortly after Tulving's (1983) book on Episodic memory, Mishkin and Petri (1984)—based on research with animals—
distinguished between a “memory” and a “habit” system. And, Squire et al. (1993) wrote “The major distinction is
between conscious memory for facts and events and various forms of nonconscious memory, including skill and habit
learning, simple classical conditioning, the phenomenon of priming, and other instances where memory is expressed
through performance rather than by recollection” (p. 457) (cf. the branching schema of memory systems in figure 1 of
Squire, 2004). In the review from 1993, the authors used the term “declarative memory” for conscious memory (know-
ing that), and nondeclarative memory (knowing how) for the other forms. They also pointed out that the declarative
memory system is dependent on the medial temporal lobe and diencephalon, and the nondeclarative system “on brain
systems outside of the medial temporal and diencephalon” (p. 457). Usage of the term “declarative memory” became
common in the subsequent years, as it held for human as well as animal research on memory functions and as it
seemed easier as an umbrella for both semantic and episodic-autobiographical memory. However, also with reference
to the brain, in most patients with neurological brain damage or psychiatric diseases, it is only the episodic-
autobiographical memory system, which is impaired, while the semantic one remains intact (cf. also the discussion of
Tulving & Markowitsch, 1998, on the declarative memory system).
There were especially in earlier years several authors, arguing against a separation of memory into systems. Many,
but not all, were experimental psychologists. Roediger III et al. (1990) took four principal criteria for differentiating
between memory systems and argued that they are rarely fulfilled in practice and research. The criteria were “func-
tional dissociation between tests,” “independent neural systems,” “stochastic independence between tests,” and “func-
tional incompatibility of operation.” Jacoby (1988) argued similar to these authors.
Another older—functionalistic—approach stems from Toth and Hunt (1999). These authors stressed the process-
character of memory, writing, for example, that “memory emerges in the interaction between a person with a prior his-
tory of experiences, and the environmental situation (e.g., the memory tasks) in which those prior experiences can be
identified as influencing performance” (p. 235). Similarly, to Roediger III et al. (1990), they named three criteria for
independent memory systems, namely (1) that they can be functionally differentiated, (2) store different kinds of infor-
mation, and (3) have a distinct neural implementation, arguing that all three together are rarely fulfilled. Furthermore,
with respect to the neural implementation, they wrote: “To ‘locate’ memory in the brain is to miss the larger (func-
tional) set of factors, external to the brain, by which memory is meaningfully defined.” (p. 252). Furthermore, there is a
circularity in the definition of a memory system: “structures (memory systems) are inferred from functional (task-spe-
cific) uses of memory, but are then used to explain the very effects observed on those tasks” (p. 254). Toth and Hunt
argue, as written above, that memory is not stored, but is an activity; it is the “interaction between a person and a
retrieval environment” (p. 258) (cf. the state-dependency of memory retrieval, discussed above).
From an integration-attempting psychological and neuroscientific perspective came Rubin's (2006) thesis, saying
“that episodic memory, and by extension all of cognition, can be understood only if the properties of basic cognitive,
behavioral, and neural systems are understood individually and in combination” (p. 278). Rubin basically equates epi-
sodic with autobiographical memory (p. 291: “In terms of theory, …, autobiographical memory is the same concept as
episodic memory as developed by Tulving and his colleagues.”). What he emphasizes is that for autobiographical mem-
ory processing many brain structures take part and interact. A similar view was proposed by Markowitsch (1985, 1988a,
1988b). Related from a neuroscientific view is Gaffan's (2002) view. He argued against Squire's “medial temporal lobe
memory system” by referring to the disconnection between cortical and subcortical structures and the importance of
fiber systems [also emphasized in an earlier review by Markowitsch (1988c)]. Furthermore, he underscored the plastic-
ity of the nervous tissue. Based on these arguments, he questioned the existence of a medial temporal lobe memory
system.
Of these alternatives to Tulving's model, only that of Larry Squire has survived and is used frequently, probably
because it is less theoretically loaded and less specific than Tulving's model. For its limitations with respect to declara-
tive memory, we refer to the paper of Tulving and Markowitsch (1998).
7 | S U M M A R Y O F TH E B EH A V IO R A L B A S E S OF TH E M E M O R Y S Y S T E M S
Memory is nowadays regarded as a detailed conglomerate of different processes (“conscious,” “nonconscious”) and sys-
tems, which partly interact, but partly act also independently of each other. It is assumed that there is a hierarchy of
the memory systems from simple and early developing to complex and late developing. Similarly, it is assumed that the
most complex is reserved for human beings and even in this species, may become vulnerable due to brain damage or
age-related deteriorations.
8 | B R A I N BA S E S O F T H E M E M O R Y SY S T E M S
In the last two decades, a large number of papers addressed the issue of brain correlates of memory processes. And even
earlier, for example, Endel Tulving and co-workers published an influencing series of three papers (S. Kapur
et al., 1994; Tulving, Kapur, Craik, et al., 1994; Tulving, Kapur, Markowitsch, et al., 1994), in which they analyzed with
fluorodeoxyglucose positron emission tomography the neural correlates of memory encoding and retrieval and observed
an asymmetry, indicating left-hemispheric retrieval of semantic memory and right-hemispheric retrieval of episodic
memory, together with a left-hemispheric encoding of novel aspects of the retrieved information into episodic memory.
Two years later, Fink et al. (1996) observed that the retrieval of episodic-autobiographical events recruited a right-
hemispheric areal combination of anterior temporal and inferior-lateral prefrontal regions of the right hemisphere. This
network included the right amygdala, as was confirmed in later studies (e.g., Markowitsch, Thiel, et al., 2000; see also
Markowitsch, 1998/1999). When comparing the activations when retrieving sad versus happy episodes or vice versa,
the sad ones engaged more lateral prefrontal and the happy ones medial prefrontal areas (Markowitsch et al., 2003).
Interestingly, imitating to have autobiographical episodes (lying) did not engage the amygdala, but the precuneus
region and the visual association cortices of both hemispheres (Markowitsch, Thiel, et al., 2000). The precuneus in ear-
lier studies had been termed “the mind's eye”, as it is activated during mental imagery (Fletcher et al., 1995; Mazzoni
et al., 2019; Tibon et al., 2019). This brain region is activated both during conditions of “remembering” (consciously
reinstalling a past event) and of “knowing” (feeling familiar with a past event; Dörfel et al., 2009). The importance of
perceptual representations for reinstating past episodic-autobiographical memories was underlined in a study, combin-
ing behavioral and functional magnetic resonance imaging data of 329 individuals (Petrican et al., 2020).
In the following, we will list the most important brain regions involved in memory encoding and recall.
8.1 | Memory encoding and consolidating and the brain
The initial encoding of autobiographical memories occurs via short-term (and working memory), as based on the
Atkinson and Shiffrin (1968) model and the extensions by Baddeley and co-workers (Baddeley et al., 2019; Baddeley &
Hitch, 1974). Relevant regions for short-term and working memory are lying in the prefrontal and premotor regions
(Fuster, 2022; Markowitsch & Pritzel, 1978; Vallar, 2006; Zimmer, 2008), as well as (for human beings) in the left-
hemispheric lateral parietal cortex (Markowitsch, Kalbe, Kessler, et al., 1999). Sometimes, it is also referred to an inter-
action between prefrontal and hippocampal regions in processing short-term memory (Twick & Levy, 2021; Zhang
et al., 2022). Furthermore, Voss et al. (2017) emphasized a hippocampal contribution to memory formation by providing
effective exploration, resulting in coherently organized memories.
Long-term autobiographical memory encoding is definitely dependent on the limbic system (Catani et al., 2013;
Markowitsch, 1999a, 1999b, 1999c; Markowitsch, 2008b), with a division into medial temporal regions (hippocampal
formation as principal structure; for other structures see figure 2 of Squire & Wixted, 2011; Corkin, 2002; Daviddi
et al., 2022; Scoville & Milner, 1957) and—for a synchronization between emotion and fact-like memory—the amygdala
(Markowitsch & Staniloiu, 2011b; Siebert et al., 2003), medial diencephalic regions (anterior and mediodorsal thalamus,
mammillary bodies; Aggleton & O'Mara, 2022; Borsutzky et al., 2008; Markowitsch, von Cramon, & Schuri, 1993) and
the basal forebrain (Borsutzky et al., 2010; Weniger et al., 1995; see reviews by Markowitsch, 2008b; Markowitsch &
Staniloiu, 2012c).
Well-known is the case of patient H.M. who received bilateral resection of medial temporal lobe structures and had
been involved in dozens of neuropsychological studies, serving as a par excellence example for anterograde (and later
also retrograde) amnesia, while having an intact short-term memory (Squire, 2009). A case report, related to H.M., but
with encephalitis as a cause of the amnesia, was published by Stefanacci et al. (2000). Cases with so-called neu-
rodevelopmental amnesia (anterograde amnesia for episodic-autobiographical material) emphasize damage to the hip-
pocampus (Staniloiu et al., 2013), but more recently also of diencephalic structures (Dzieciol et al., 2017). Many of these
patients have had insufficient oxygen supply shortly after birth and as the CA1-region of the hippocampus (Sommer's
sector) is especially vulnerable to hypoxic or ischemic damage, hippocampal damage is likely to occur. Our patient
(Staniloiu et al., 2013) had only one single autobiographical episode in his mind, namely that his father jumped out of
the closed window while quarreling with his mother; otherwise, he only knew semantic facts, but these to a degree that
he finished high school successfully.
Related to the early hemispheric-asymmetry findings from Tulving et al. (S. Kapur et al., 1994; Tulving, Kapur,
Craik, et al., 1994; Tulving, Kapur, Markowitsch, et al., 1994) is the study of Orth et al. (2022). In this study, transcranial
direct current stimulation (tDCS) over the left dorsolateral prefrontal cortex improved the encoding of words that were
processed semantically and increased memory formation for positive content while reducing that for negative content.
The authors concluded that the left dorsolateral prefrontal cortex assesses semantic properties of new memory content
at encoding and thereby influences how successful new episodic memories are established.
In an important study, Schott et al. (2013) tested the brain regions involved in shallow—perceptual (syllable cou-
nting)—and deep—semantic (pleasantness rating)—encoding of words. They found bilateral hippocampal and left pre-
frontal activations during successful encoding, plus an increased functional connectivity between left hippocampus and
bilateral medial prefrontal, cingulate, and extrastriate cortices. Successful deep processing additionally was related to
an increased functional connectivity between left hippocampus and bilateral ventrolateral prefrontal cortex and the
right temporoparietal junction area. Shallow, perceptual, encoding resulted in pronounced functional connectivity
increases between the right hippocampus and the frontoparietal attention network.
A meta-analysis of 74 studies, of which most 69 involved short-term (≤30 min) retention of verbal or pictorial mate-
rial (i.e., usually not autobiographical material), stressed five neural regions which are principally involved in memory
encoding: the left inferior frontal cortex, and bilaterally the fusiform, premotor, posterior parietal and hippocampal cor-
tex (Kim, 2011). Verbal material engaged mainly the left inferior frontal cortex, pictorial material the fusiform cortex;
hippocampal activation was more prominent for pictorial material, reflecting novelty as opposed to familiarity (and in
line with early previous data of Tulving, Markowitsch, Kapur, et al., 1994). The activations of the other two regions—
the premotor and lateral parietal cortex—were considered to reflect attention processes. Rubinstein et al. (2021),
however, found evidence for direct memory-related functions during encoding. Another voxel-wise quantitative
meta-analysis of 26 encoding studies, conducted 2 years earlier (Spaniol et al., 2009) basically revealed activations of
similar brain regions during memory encoding, namely the left ventrolateral prefrontal cortex and medial–temporal
regions as the main sites.
As these brain regions constitute a major part of the so-called default mode network, it is pointed out that in fact,
this network is in principal control of memory processing in general (e.g., Chai et al., 2014; De Simoni et al., 2016;
Maillet & Rajah, 2014; Oedekoven et al., 2019; Simony et al., 2016). Furthermore, Kim (2021) pointed out that the
default mode network supports the subjective experience of remembering and age-related memory decline may par-
tially be accounted for by failure to modulate activity in the default mode network (S. M. Nelson et al., 2016).
The process of further consolidating memories is related to the default mode network as well (Sneve et al., 2017);
the same probably holds for re-consolidation, that is, the new consolidation of already stored memories after retrieval
(e.g., Craig et al., 2021). D. N. Barry, Hallford, and Takano (2021) investigated how memory details persist over time by
performing a longitudinal study in which participants had to recall the same autobiographical memories on two visits
spaced 8 months apart. They found that within hippocampal subfields it is especially the volume of the left pre-/
parasubiculum subfield that determines the remembrance of events, perceptual observations, thoughts, and emotions.
Other hippocampal subfields are of importance when it comes to relearning as was demonstrated in the study of
Molitor et al. (2021). They found that memory reactivation during learning promoted the formation of differentiated
representations for overlapping memories in the dentate gyrus and the Cornu ammonis subfields 1 and 2 (CA1+2), as
well as in the subiculum. Simultaneously, the formation of integrated representations of related events depended on
subfield CA1. Success when inferring indirect relationships among events and memory reactivation depended on the
subiculum.
One of the very few studies testing episodic-autobiographical memory encoding with functional brain imaging in
children was performed by Nolden et al. (2021). Kindergarten children were given two learning tasks (photographs of
indoor and outdoor scenes; pairing of objects and scenes) inside and outside a scanner (magnetic resonance imaging).
They were tested initially at around age five and again when a year later. The main finding was that children's brains
rely strongly on the medial temporal lobe system and to a much lesser extent on prefrontal structures (while in adults
encoding activates prefrontal structures substantially; cf. above). This is most likely caused by the continuing develop-
ment of the prefrontal cortex which reaches over more than decades (Bourgeois et al., 2000; Goldman-Rakic, 1987;
Jerison, 1997; Smaers et al., 2011).
Prefrontal structures seem also to be relevant when it comes to memory encoding associated with affective attitude
formation (pairing of a neutral word with a positively or negatively valenced word; Forester et al., 2020). The authors
conclude from their findings that a common mechanism contributes to both episodic memory encoding and affective
attitude formation.
8.2 | Memory storage and the brain
For memory storage, widespread cortical areas and some associated nuclei are considered to be essential. This was pro-
posed in detail already by Mesulam (1998) under the expression of “large-scale distributed brain networks” (see also
Dickerson & Eichenbaum, 2010). Posterior (temporal and parietal) neocortical structures are usually seen as primary
storage places for autobiographical information, most likely in interaction with a network of emotion-flavoring regions
(Grilli & Verfaellie, 2014; Markowitsch & Staniloiu, 2012a, 2012b, 2012c; Sarter & Markowitsch, 1985a, 1985b). Some
authors—as Morris Moscovitch and Lynn Nadel—strongly argue for a continuing hippocampal involvement for reten-
tion (and retrieval) of autobiographical information (e.g., Korkki et al., 2021; Moscovitch et al., 2005); other authors see
this more critical and unsupported by data (e.g., Kopelman, 2000).
In a review from 2016, Moscovitch et al. (2016) emphasized the existence of process-specific alliances between brain
structures. They proposed temporary process-specific alliances whose composition is determined by moment-to-
moment demands of a task. Posterior neocortical components and the posterior hippocampus would be engaged in
local, spatio-perceptual aspects of the experience, while anterior hippocampal components and the anterior temporal
lobe, including the amygdala plus ventromedial and ventrolateral prefrontal cortical areas would represent conceptual
and emotional aspects. Emphasizing their “multiple-trace theory” (which implies continuing processing and updating
of stored information), Winocur and Moscovitch (2011) assumed that detailed, vivid autobiographical memories engage
the hippocampus, no matter how long ago they were acquired. This view generally is supported by other functional
imaging studies (Sheldon & Levine, 2013); some of which, however, stress more neocortical involvement. Gilboa (2004)
in his review, for example, did not mention the hippocampal formation at all, but emphasized differential involvements
of prefrontal structures in list-learning-based episodic memory studies as opposed to those studying true autobiographi-
cal memories. Only the first group reported right mid-dorsolateral prefrontal activations, while the second one showed
ventromedial prefrontal activations, particularly in the left hemisphere. Gilboa attributed these activations during auto-
biographical memory processing to a quick intuitive “feeling of rightness” related to monitoring the veracity and cohe-
siveness of memories. Episodic memory for lists, on the other hand, seems to require more conscious elaborate
monitoring in order to avoid omissions, commissions, and repetitions.
Our own data on patients with severe and lasting dissociative amnesias in the autobiographical memory domain
support the view of an engagement of anterior temporal and ventrolateral prefrontal regions, as these regions are hypo-
metabolic in fluorodeoxyglucose-activity in the amnesic condition (Brand et al., 2009), while they seem to return to a
normal metabolism when memories become reinstated (Markowitsch, Kessler, et al., 2000; Staniloiu et al., 2011).
Furthermore, the large literature on memory impairments in dementia—especially in Alzheimer's disease—
supports the view that major cortical degeneration strongly correlates with the decay in memory storage (Barnabe
et al., 2012; Donix et al., 2010; Leyhe et al., 2009).
8.3 | Memory retrieval and the brain
Early studies on recalling showed a primary activation of prefrontal regions (irrespective of whether the retrieval
involved recognition or recall; Cabeza et al., 1997). The prefrontal activation was later confirmed and extended to a
left orbitofrontal, in addition to bilateral prefrontal activation in a face-name paired paradigm, using 40-channel
functional near-infrared spectroscopy (Yu et al., 2021). Again, as during encoding and consolidating, the hippo-
campal formation and surrounding structures (parahippocampal gyrus, posterior cingulate, and retrosplenial cor-
tex) were implied in episodic memory retrieval (Rugg & Vilberg, 2013; Vanneste et al., 2021). Rugg and Vilberg
(2013) suggested that there is a content-independent general recollection network, composed of additional struc-
tures as well, namely the parahippocampus, retrosplenial/posterior cingulate, and lateral parietal cortices, as well
as of the medial prefrontal cortex. A distinct, synchronized coupling between these regions seems to exist during
episodic-autobiographical recall, as was demonstrated by electroencephalographic recordings (Roehri et al., 2022).
Other authors attribute only a time-limited role to the hippocampus for retrieving episodic-autobiographical mem-
ories (Gilmore et al., 2021).
Fossati (2013) assigned specific cognitive processes to the individual structures of this network, namely executive
control and retrieval monitoring to the (dorsolateral) prefrontal cortex, self-processing to the medial prefrontal and the
posterior cingulate cortex plus the precuneus, emotion-related processes to the ventromedial prefrontal cortex and the
amygdala, and visuospatial processing to the retrosplenial and parietal areas, as well to the precuneus (“the mind's
eye”; see above). (Precuneus involvement during spatial memory allocations was also found by Frings et al., 2006.)
There are studies, arguing for a major posterior cortical involvement in memory processing, particularly in retro-
grade amnesia after bilateral damage (Greenberg et al., 2005; Hunkin et al., 1995; Ogden, 1993; Rubin &
Greenberg, 1998). We agree with N. Kapur (1997), who wrote—after analyzing the paper of Hunkin et al., as well as
others—“that damage that is solely or predominantly to posterior brain areas cannot lead to a dense autobiographical
amnesia” (p. 126). As an example, we use the case of Hunkin et al. (1995): These authors wrote that their case was a
Naval officer with “absolutely no memory of his life prior to his accident at age 19” (p. 510). The authors argue that
functional amnesia as a diagnosis seems unlikely for a number of reasons They then list as arguments “that it is
unlikely that a functional amnesia persists for a period that is 18 years” (p. 510). Second, they did not find predisposing
factors associated with functional loss. Hunkin et al. (1995) write “there were some signs of organic deficit such as mild
hemiplegia” (p. 510). None of these arguments is convincing: We found in several of our cases with functional/
dissociative amnesia that especially officers are prone to dissociative amnesia, probably (as we agued) because they
were ambitious and eager to follow their attempted careers which then collapsed after the abrupt injury after an acci-
dent (Staniloiu et al., 2018, 2020b). Second, we had more than one case in whom their functional amnesia persisted for
more than 18 years [e.g., case C.D. in Fujiwara et al. (2008), and the case of Markowitsch, Kessler, Kalbe, & Herholz
(1999)]. Predisposing factors, of course, are sometimes difficult to detect, especially when the patient is totally amnesic
in the retrograde autobiographical domain. Hunkin et al.'s third argument of signs of mild hemiplegia is indeed is even
typical for some cases of functional/dissociative amnesia (“conversion syndrome”; e.g., in our case G.H. in Fujiwara
et al., 2008). This kind of argumentation can be applied to the other cases with damage in the visual and visual
association cortices as well. We therefore agree with N. Kapur (1997) view that damage in these brain areas is not caus-
ing the amnesia detected.
Using single-unit recordings in patients with epilepsy, the involvement of the parahippocampal gyrus and parietal
areas in retrieving episodes was confirmed and extended by finding so-called “boundary” and “ramping” neurons (Yoo
et al., 2022). “Boundary” cells are active at the beginning and the end of an episode and therefore show a U-shaped
activity pattern. “Ramping” cells react during the time elapsed across an episode. While especially the ramping neurons
are found in the hippocampal area (Umbach et al., 2020), the boundary neurons apparently are more frequent in the
parahippocampal cortex and in lateral parietal and frontal areas (Favila et al., 2018; Xiao et al., 2017; Zheng
et al., 2022). Together with the so-called place cells, representing spatial context in the hippocampus (Alme et al., 2014;
Colgin et al., 2008), these neuron types provide insight into the question, what neural contexts are re-evoked during
mental time travel and memory search (Polyn & Kahana, 2008). Xiao et al. (2017) emphasized that even within the
same brain areas, the nature of representation differed qualitatively during retrieval, compared to encoding. Therefore,
their results confirm the idea of memory reconstruction during retrieval (see above).
Retrieving verbal material may also engage the anterior temporal cortex, as was shown by Jang et al. (2017), using
high-density microelectrode arrays in the middle temporal gyrus. Furthermore, cerebral volumetric measurements of
the brains of patients with Alzheimer's disease indicated a strong involvement of medial temporal lobe structures and
the anterior lateral temporal neocortex (particularly of the right hemisphere) in autobiographical memory retrieval,
regardless of age (Gilboa et al., 2005). Personal semantic facts (cf. Figure 2) were related to a pattern of bilateral anterior
and posterior lateral temporal cortex degeneration, more pronounced on the left, and to right hemispheric frontal
degeneration. These data should, however, be interpreted in light of the critique of Kopelman (2000) and the methodo-
logical critique of the instrument used—the Autobiographical Memory Interview—by Barnabe et al. (2012).
That emotional valence is important for autobiographical memory retrieval has been known for long (Breuer &
Freud, 1895). Kensinger and Ford (2020) stressed this relationship again in their review and emphasized the differences
between retrieving positive and negative autobiographical memories. Their model, first stated in Bowen et al. (2018)
and then reinvestigated with longer delays by Kark and Kensinger (2019), emphasizes the role of valence among arous-
ing memories and underlines how sensory regions are incorporated into the memory networks. It shows that the
enhanced sensory recruitment during the retrieval of negative memories is linked to the tendency for participants to
retrieve more negative than positive memories. Furthermore, showing after encoding a greater coupling between amyg-
dala and sensory regions (cf. Markowitsch & Staniloiu, 2011b; measured by resting-state functional connectivity) had a
better memory for negative information and a greater tendency toward a negative memory bias (Kark &
Kensinger, 2019). Kensinger and Ford (2020) interpret these findings as demonstrating that memories with negative
content have a stronger sensory signature at retrieval and are associated with a greater tendency to reconfigure itself at
retrieval to resemble the state at encoding [cf. the NEVER Forget model, depicted in figure 2 of Kensinger and Ford
(2020)]. We in addition would point to the facts that most of our emotions are negative in character and that from an
evolutionary point of view it is of much higher survival importance to react to negative as compared to positive
emotions.
8.4 | Specific impairments of autobiographical memory retrieval
The richness in retrieving specific autobiographical memories is related to the individual's well-being (Hakamata
et al., 2021; Khan et al., 2021; Sutin et al., 2021). Traumatic brain injury for long is related to severe memory distur-
bances (Russell, 1935, 1971; Symonds, 1962). Alzheimer's disease and other dementias similarly are known to lead to
amnesia (e.g., Berntsen et al., 2022; Eustache et al., 2004; Piolino et al., 2003). However, in more recent years, several
case reports appeared on patients with total retrograde amnesia in the autobiographical domain, who all had a similar
brain injury, namely in the right-hemispheric lateral frontotemporal region (ventrolateral prefrontal cortex, anterior
temporal lobe; Calabrese et al., 1996; N. Kapur et al., 1992; Kroll et al., 1997; Markowitsch, von Cramon, &
Schuri, 1993, Markowitsch, Calabrese, et al., 1993). N. Kapur (1993) coined the term “focal retrograde amnesia” for
these cases, who do not have anterograde memory problems (or in whom there is a disproportionate retrograde and
only very minor anterograde amnesia; N. Kapur, 2000). While exactly this regional combination is activated during the
retrieval of autobiographical episodes (Fink et al., 1996), Kopelman (2000) argued that such cases may suffer from a
psychogenic (dissociative) component of their amnesia. In fact, one could argue that dysfunction of these regions
induces dissociative amnesia or—vice versa—that dissociative or psychogenic amnesia leads to a dysfunction of these
_________________________________________________________________________________
Psychological or biological stress or trauma condition
(frequently in childhood or youth)
Biological priming
(change in receptor structure)
Supersensitivity for excitatory neurotransmitters
Latency phase
(Re-)Activation via
Psychological mechanisms or biological events
(e.g., conflict, accident, infection, assault, injury)
Absence of adequate emotional-cognitive processing (coping)
Possible latency phase
Dissociation between cognition and emotion

Psychobiological stress reaction
Dissociative amnesia / mnestic block syndrome
_________________________________________________________________________________
FIGURE 5 Sequence of proposed changes in brain–behavior interrelations triggered by stress and trauma conditions
areas. As mentioned above, these areas are hypometabolic in patients with dissociative or functional amnesia (see
figure 1 of Brand et al., 2009, or figure 36.4 of Markowitsch & Staniloiu, 2016b).
The possibility of organic (neuronal) correlates of autobiographical memory impairments in patients with a psychi-
atric disease had been proposed by Flechsig (1896), Meynert (1884), and Maudsley (1870). Maudsley (1870) wrote “Men-
tal disorders are neither more nor less than nervous diseases in which mental symptoms predominate, and their entire
separation from other nervous diseases has been a sad hindrance to progress….” (p. 41). One of us took up this idea in a
review on psychogenic and organic causes of retrograde amnesia by entitling it “two sides of the same coin”
(Markowitsch, 1996). In fact, brain correlates for memory impairments in psychiatric diseases have been found numer-
ously in the last decades (e.g., T. J. Barry, Clark, & Maguire, 2021; Guimond et al., 2022; He et al., 2022; Liu et al., 2021;
Wie et al., 2022).
As retrograde (and in a very few instances vice versa anterograde; Staniloiu & Markowitsch, 2014) amnesia is the
principal feature of dissociative amnesia (or “mnestic block syndrome,” as termed by Markowitsch, 2002; Markowitsch,
Kessler, Russ, et al., 1999; Markowitsch, Kessler, et al., 2000), neural mechanisms, leading to this usually suddenly
occurring disease condition have been proposed. Based on the fact that the disease manifests itself usually in individ-
uals with a more labile personality state and with a background of various psychological or physiological stress- and
trauma-related conditions, it is likely that these have an impact on psychological well-being. Kopelman (2000, p. 1068),
for instance, summarized some of such conditions from our cases as “loss of status or career, physical or minor brain
injury, being the victim of an assault or road traffic accident, and being incarcerated in prison. Staniloiu et al. (2018)
showed that such critical incidents preceded the amnesia in 25 out of 28 cases, often initially denied and sometimes
having delayed effect (incubation)”. How that impact may alter brain functions has been addressed in several papers of
us, but with an alternative or supplementary view also by Kopelman (2000) (see his figure 4 and our figure 3 in
Staniloiu et al., 2020b).
It is known that stress has a major impact on the brain, secreting stress hormones (glucocorticoids), which then
results in changes in regions with a high receptor density—particularly the hippocampal and amygdalar regions
(Bremner, Krystal, et al., 1995; Bremner, Randall, et al., 1995; Bremner et al., 1997; Lupien et al., 2009; Lupien &
McEwen, 1997; McGaugh et al., 1996; O'Brien, 1997; Sapolsky, 1996). Within this context, a predisposition in childhood
has been frequently suggested to enhance the likeliness of an outbreak of stress-related cognitive deteriorations in
adulthood (Parks & Balon, 1995; Schacter et al., 1996). Teicher et al. (1993), for instance, found that early physical or
sexual misuse can hinder the development of the limbic system. The central role of the hypothalamo-hypophyseal-
adrenocortical axis (Herman & Cullinan, 1997; Holsboer, 1989) was emphasized repeatedly to modulate these mecha-
nisms, and inappropriate coping mechanisms (Heim, 1988) were considered to enhance the likelihood of an outbreak
of this illness.
We proposed—based on a model of Aldenhoff (1997)—the model given in Figure 5 for the triggering of dissociative
states. In our experience with now more than 80 patients with dissociative amnesia, it is possible to find one or more
likely triggering conditions in almost all of them. Furthermore, brain imaging data were obtained in many of them
(Brand et al., 2009; Markowitsch, Calabrese, et al., 1997; Markowitsch, Fink, 1997; Markowitsch, Thiel, et al., 1997;
Markowitsch et al., 1998; Markowitsch, Kessler, Kalbe, et al., 1999; Markowitsch, Kessler, Russ, et al., 1999; Markowitsch,
Kessler, et al., 2000; Staniloiu et al., 2011) strongly speak in favor of a desynchronization and destabilization between fact
(hippocampus, prefrontal cortex) and emotion-processing (amygdala) regions in this patient group, leading to the dissocia-
tive condition. This amnesia is then perpetuated, as whenever the patients try to recollect personal memories, the stress
hormone cascade (O'Brien, 1997) is reactivated and floods the critical brain regions—a circulus vitiosus.
In fact, the research of Michael Anderson and his group—working for many years on the topic of active memory
suppression (retrieval stopping)—supports the view that hippocampal and amygdalar activities are suppressed via pre-
frontal inhibitory mechanisms when individuals attempt to stop retrieving memories (Anderson & Floresco, 2022;
Anderson & Hulbert, 2021).
9 | C ON C L U S I ON S
Autobiographical-episodic memory is the most advanced memory system we possess (cf. Figures 1 and 3). It developed
phylogenetically at the very end of the animal scale and therefore is also the most vulnerable of all memory systems.
The ability of mental time travel (Redshaw & Suddendorf, 2020; Suddendorf & Corballis, 1997) allows human beings to
have the foresight and therefore to plan their future. At the time, they can go back into their past so that they may not
repeat errors in complex behavior that they had made before. Autobiographical-episodic memory is dynamic, it changes
with time and environment—supported by neuroplasticity from the brain level. The dynamic nature of this memory
system goes in parallel with a certain affinity towards memory distortions and memory fragility. This becomes espe-
cially obvious under conditions of brain damage, but also in psychiatric conditions (which most likely have brain corre-
lates as well). As autobiographical-episodic memories are embedded in emotional contexts, they need a synchronous
coordination of emotion- or affect-processing brain structures and of those dealing with (semantic) facts. Phenomena,
such as the tip-of-tongue phenomenon, where a term or a name cannot be generated at a given time, underlines the
emotional colorization of autobiographical-episodic memory, as this happens particularly in stressful situations. When
stressful events predominate, there can be a more widespread blockade of memories (state-dependency of retrieval),
which in extreme and pathological cases leads to the condition of dissociative amnesia or mnestic block syndrome.
Based on the assumption that this disease condition is environmentally induced and leads to lasting alterations in the
brain (as proven by our investigations with positron emission tomography and diffusion tensor imaging), it shows that
the social (and biological) environment can damage the brain.
Processing memory from initial encoding to repeated retrieval shows the existence of complex interactions and
interplays between memory systems (cf., e.g., the SPI-model). Conscious and unconscious processes (cf. the legend of
Figure 1), as well as mental and action-based processes (Gilboa & Marlatte, 2017; Rolls et al., 2022), are intermingled
and contribute to the overall picture of memory. While autobiographical-episodic memory is the most complex memory
system, unraveling its components and functions in life remains one of the most fascinating endeavors.
A U T H O R C ON T R I B U T I O NS
Hans J. Markowitsch: conceptualization; part of writing; Angelica Staniloiu: part of writing.
A C K N O WL E D G M E N T
Open Access funding enabled and organized by Projekt DEAL.
CONFLICT OF INTEREST
The authors have declared no conflicts of interest for this article.
DATA AVAILABILITY STATEMENT

Data sharing is not applicable to this article as no new data were created or analyzed in this study.
ORCID
Hans J. Markowitsch https://orcid.org/0000-0002-5682-5912
R EL ATE D WIR Es AR TI CL E
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How to cite this article: Markowitsch, H. J., & Staniloiu, A. (2022). Behavioral, neurological, and psychiatric
frailty of autobiographical memory. WIREs Cognitive Science, e1617. https://doi.org/10.1002/wcs.1617

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19395086, 0, Downloaded from https://wires.onlinelibrary.wiley.com/doi/10.1002/wcs.1617 by Uni De Tras-Os-Montes E Alto, Wiley Online Library on [09/11/2022].

Behavioral, neurological, and psychiatric frailty

Hans J. Markowitsch1 | Angelica Staniloiu1,2,3

This article is categorized under:

WIREs Cogn Sci. 2022;e1617. wires.wiley.com/cogsci 1 of 27

2.1 | Short-term memory and working memory

2.2 | Procedural and priming memory

2.3 | Perceptual and semantic memory

2.4 | Episodic-autobiographical memory

4 | PITFALLS IN EYEWITNESS MEMORY

• Factors inherent to the eyewitness producer (e.g., age, education)

6 | ALTERNATIVE MODELS OF MEMORY SYSTEMS

8.1 | Memory encoding and consolidating and the brain

8.2 | Memory storage and the brain

8.3 | Memory retrieval and the brain

8.4 | Specific impairments of autobiographical memory retrieval

Supersensitivity for excitatory neurotransmitters

Absence of adequate emotional-cognitive processing (coping)

Possible latency phase

Dissociation between cognition and emotion

Dissociative amnesia / mnestic block syndrome

DATA AVAILABILITY STATEMENT

Bennett, A. H. (1878). Case of cerebral tumour-symptoms simulating hysteria. Brain, 1, 114–120.

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