Memory systems of the brain

Alvaro Pastor

Universitat Oberta de Catalunya, Computer Science, Multimedia and
Telecommunications Department, Barcelona, Spain

<EMAIL_ADDRESS>

January 1, 2020

## Abstract

Humans have long been fascinated by how memories are formed, how they can be
damaged or lost, or still seem vibrant after many years. Thus the search for
the locus and organization of memory has had a long history, in which the
notion that is is composed of distinct systems developed during the second
half of the 20th century. A fundamental dichotomy between conscious and
unconscious memory processes was first drawn based on evidences from the study
of amnesiac subjects and the systematic experimental work with animals. The
use of behavioral and neural measures together with imaging techniques have
progressively led researchers to agree in the existence of a variety of neural
architectures that support multiple memory systems. This article presents a
historical lens with which to contextualize these idea on memory systems, and
provides a current account for the multiple memory systems model.

## Introduction

Memory is a quintessential human ability by means of which the nervous system
can encode, store, and retrieve a variety of information [1, 2]. It affords
the foundation for the adaptive nature of the organism, allowing to use
previous experience and make predictions in order to solve the multitude of
environmental situations produced by daily interaction. Not only memory allows
to recognize familiarity and return to places, but also richly imagine
potential future circumstances and assess the consequences of behavior.
Therefore, present experience is inexorably interwoven with memories, and the
meaning of people, things, and events in the present depends largely on
previous experience.

Questions concerning the nature and organization of memory systems are
fundamental to our understanding of the processes underlying learning and
memory in humans and other animals. Due to its importance and complexity, the
subject of memory is connected with some of the most profound questions of
philosophy and biology, and as such, has been approached from different
perspectives and methodologies. Along the way, idealists and materialists,
empiricists and nativists, behaviorists and cognitivists, have confronted
ideas about memory. First from philosophy through introspection and intuition,
complemented later with anatomical and physiological observations. Then
neuropsychology, through observation of patients with various defects in
memory which developed the notion of a dichotomous organization of memory.
More recently, relevant contributions from neurobiology and cognitive
neuroscience, using various behavioral and neural measures together with
imaging techniques, have progressively led researchers to postulate
distinctions among various memory systems supported by different neural
architectures, for example, by the hippocampus and related structures, the
amygdala, the striatum, and the cerebellum.

The tradition of memory research considered in this article is that of
experimental psychology and cognitive neuroscience amassed over the past
decades. While a major part of early research assumed a unitary view on
memory, some authors assumed dichotomous classifications based generally on
the distinction of conscious and unconscious memory processes. Accordingly,
relevant distinctions between memory systems have been proposed including but
not limited to: episodic and semantic memory [3, 4], taxon and locale memory
[5], habit memory and cognitive memory [6, 7], working memory and long term
memory [8, 9, 10], implicit and explicit memory [11, 12], declarative and non
declarative memory [13], declarative and procedural memory [14], fast and slow
memory systems [15, 16].

In the last years, there is growing consensus about the nature and
organization of memory. Supported on cognitive and neurobiological and
neuropsychological evidence, memory is conceived as a set of separate, highly
specialized, neural mechanisms that interact to reach a common goal. However,
the complete extent of their features and interactions is yet to be fully
understood.

The first part of this article presents a brief historical review with which
to reevaluate and contextualize the current theories and frameworks on human
memory systems. The second part presents an account for the components of the
multiple memory systems model, with some clues regarding the functional basis
of memory processes. The memory systems comprised in this article are part of
the most accepted and disseminated at present time. Debate about which of the
different taxonomies of memory most appropriately organizes all available
experimental data is beyond the scope of the present study.

##  1 Historical background

The nature of human memory and its organization have been object of study,
speculation and debate for several centuries, in a variety of areas including
philosophical inquiry, cognitive psychology, biology and neuroscience. In
looking at the history of the localisation and organization of memory it is
necessary to turn to ancient theories regarding the nature of soul and its
relation to the body [17].

In early allusions to memory, ancient Egyptians considered it was solely
supported by the heart, as the centralized seat of cognitive processes [18].
Contrary to other organs, the hearts of Egyptian mummies were kept carefully
intact to ensure eternal life. Brains, on the other hand, were ideally removed
via transnasal excerebration, a technique devised for this purpose by Egyptian
embalmers [19]. In classical greek philosophy, memory was considered as part
of the eternal and immaterial nature of the soul. In Theatetus, a major work
written circa 369 BCE which explores the nature of knowledge, Plato introduces
the problem of remembering in the analogy of the wax into which our
perceptions and thoughts stamp images of themselves. An early distinction was
made between the passive retention of perceptions and active memory. Plato
described active memory in its episodic features, as _”the power which the
soul has of recovering, when by itself, some feeling which she experienced
when in company with the body”_ [20]. Later in the fourth century BCE,
Aristotle returned to the notion that the soul is not a separate substance
from the body, as Plato had taught, but inherently bound into it, affording
its form. Aristotle came from a medical family and his biological bent is
shown in its influence on most of his philosophy. Informed by his biological
researches, in _Metaphysica_ , Aristotle presented a thoroughly materialistic
theory, in which the soul or souls were distributed throughout the entire
living body [21]. Also in _de Anima_ , the soul was conceptualized as
distributed in the body. While, according to Plato, memory is one of the
higher faculties and partakes of the eternal nature of the soul, for Aristotle
memory is dependent upon a physical process, and perishes with the body. In
spite of this, Aristotle acknowledged the existence of a center on which
sensory input converged and from which behavior was initiated. This, for
Aristotle, is the location of common sense or _sensus communis_ , where
besides the external senses such as sight and smell were processed, internal
senses such as memory and imagination were sustained. Aristotle established
that the cognitive center was located at the heart, and that the vegetative
soul was fluid and distributed everywhere in the body [22, 23]. The operation
of memory as then conceived, may be inferred from the kinds of memory that the
classical philosophers observed. Aristotle worked on a tract devoted to the
subject of memory called _De memoria et reminiscentia_. Its second chapter was
devoted mainly to the recollection and association of ideas. In dichotomous
fashion, Aristotle distinguishes the mere persistence and direct reproduction
of a presentation, from voluntary recollection, which is possible only by the
association of ideas, by similarity, contrast, and contiguity. In the
Aristotelian view, persistence memory is an attribute of animals and humans,
while the voluntary recollection is unique to humans [22, 24, 25].

Increasingly, philosophical inquiry on memory was influenced by anatomical and
physiological studies. In the first century BCE the Byzantine surgeon
Poseidonius produced the first written assignments of mental functions to
specific cerebral regions. Based from observations of head injuries,
Poseidonius argued that lesions at the front of the brain interfere with
apprehension of all types of sensation, whereas trauma of the posterior part
results in memory deficit, and damage to the middle ventricle produces a
disturbance of reason [26]. At the end of the fourth century CE, Nemesius of
Emesa carried forward the ideas of ventricular function and proposed a schema
which remained fairly standard for several centuries. In _De Natura Hominis_ ,
claimed that the anterior ventricles accounted for the mixing of sensations
and for imagination, the middle ventricle for cogitation and reason, and the
posterior ventricle for memory [27, 28].

Augustine of Hippo, Roman theologian and philosopher at the end of fourth
century CE, presented an account of human memory orchestrated by the brain and
divided in different and complementary instances: sensible memory,
intellectual memory, memory of memories, memory of feelings and passion, and
memory of forgetting [29]. Sense memory, for example, preserved and reproduced
idealized images of visible objects, sounds, odors and other items available
to the senses. Intellectual memory on the other hand, contained our knowledge
of the sciences, of literature and dialectic, and of the questions relating to
these subjects. This memory, unlike the memory of sense, contained not the
images of things, but the things themselves [30]. The philosopher’s
contribution foresees in striking detail some of the most relevant theories of
modern psychology and neuroscience about memory, including the differences
between sense memory and intellectual memory, similar to current episodic and
semantic memory definitions.

During the following decades, philosophical conceptions and directions in
memory research in the Western tradition remained divided between either the
views of Aristotle or those of Plato and Augustine of Hippo.

An important milestone is found in the mid 16th century. The work of Andreas
Vesalius in _De humani corporis fabrica libri septum_ , helped developed an
opposition to the medieval theory that the soul resides in the ventricles,
believing these to be mere channels for the passage of the fluid _anima_ and
explicitly identified the brain as the main organ of intelligence, movement,
and sensation [31]. Likewise, English physician Thomas Willis helped establish
as well that activities are not carried out in the ventricles but in the brain
substance itself. Also, Willis proposed a direct correlation between
complexity of gyri convolutions and availability of cognitive abilities
including memory. [32].

Willis’ ideas were contemporary to those of the French mathematician and
philosopher Descartes, and the notion of the correlation between physical and
psychic processes was clearly understood by the dualists of the seventeenth
century. In _De homine_ Descartes elaborated the mechanistic concept of human
sensation and motion, and retained the ancient idea of the soul residing in
the pineal gland, according to him located in the ventricles. _When the mind
wills to recall anything,_ Descartes wrote, _this volition causes the pineal
gland to incline itself successively this way and that, and impel the animal
spirits to various parts of the brain until they come to that part in which
are traces left by the object we would remember_. Descartes explained the
physical processes involved in memory in accordance with his crude physiology,
following the belief that the soul resides in the ventricles and that the
fluid in them can be animated. This ideas prevailed into the end of the 18th
century [33].

The doctrine of the Cartesians, that memory was conditioned by traces left in
the brain, was developed by the physiologists of the 18th century into a
materialistic and mechanical view of memory. In an extreme example, the
physiologist Albrecht von Haller interested in the time occupied in psychic
processes, estimated that a third of a second was sufficient time for the
production of one idea. Von Haller and others then calculated that in a
hundred years a human must collect during her wake period a total of 1 577 880
000 traces. By assuming the weight of the brain elements that were then
conceived with the power for preserving impressions, then obtained 205 542
traces must be found in one gram of brain substance [23].

Early in 19th century, Franz Joseph Gall aimed again at settling the
conceptual dispute, and contributed to establish that memory was located
solely in the brain and was not located in the heart nor the ventricles as it
was previously posited. Based on an anatomical and physiological data, Gall
also acknowledged that the brain contains independent but interacting regions,
and later interpreted that differences in behavior are due to differential
development of these brain regions [34]. To support his argument, Gall drew on
observations of within and between individual differences in memory for
particular kinds of information. Noting that some individuals have excellent
memory for places but not music whereas others exhibit the opposite pattern,
Gall contended such differences could not exist if memory constituted a
unitary faculty [35, 36]. A few years later, physician Marie-Jean-Pierre
Flourens investigated Gall’s controversial views on cerebral localization by
removing anatomically defined areas of the brain of an animal and watching its
behaviour. The results did not favour the idea of cerebral localization and
led him to conclude that the brain functioned as a whole and thus arose the
concept of _cerebral equipotentiality_ [37, 38]. Much debate ensued, due to
the fact that his experiments were mainly on birds, and the techniques used
were considered imperfect.

In contrast, French philosopher Maine de Biran published in 1804 a remarkable
attempt to organize human memory within a taxonomic construct, distinguishing
separate memory systems instead of a single unity: representative memory, that
is the conscious recall of facts and events, mechanical memory, responsible
for learning of habits and skills, and sensitive memory, regarding emotional
information [39, 40]. Psychologist and philosopher William James followed
along these lines with his _Principles of Psychology_ in 1890. Despite no
experimental evidences presented, a number of very important observations were
made. The distinction between memory and habit, which led him to write
separate chapters on both. Besides the distinction of habit, James also
postulated two other different kinds of memory, establishing the difference
between primary and secondary memory, which could be interpreted as an
anticipation of the modern distinctions of short term memory (STM) and long
term memory (LTM) [41, 42].

Bergson’s reflections on memory in _Matter and Memory_ from 1896 also
contributed to the modern non unitary view of memory. The French philosopher
proposed distinctions between habit memory and episodic memories. For Bergson
habit involved repetition, is effortless and, once formed, non-
representational. Despite being non representational its effect percolates
into the present and in part defines behavior. In contrast, what he understood
as episodic memories were representational, involved a unique non-repeatable
event, and its recollection, requires an act of will which involves an active
letting go of the attachment to the present [43, 44]. In his 1949 work _The
Concept of Mind_ the English philosopher Gilbert Ryle also distinguished
between two types of memory: knowing-that, a type of memory that does not
directly inform action but is expressed through regulative propositions; and
knowing-how, a type of executive memory that cannot be built up from pieces of
knowing-that and is actualized through enactment [45]. These suggestive
approaches to the nature and organization of memory and the subjective
experience of recollection may be considered as the most influential in
Western philosophy of the twentieth century.

While these are seen as the earliest attempts in the study of memory, what was
demanded in order to fully understand its nature and organization was not only
philosophical discourse or psychological intuition, but experimental inquiry.

In a major contribution in the study of memory, the psychologist Hermann
Ebbinghaus published in 1885 [46] a pioneering experimental and quantitative
treatment of memory, displaying new ideas and methods for rigorous and
systematic controlled experiments on memory, that have had an enduring
influence throughout the twentieth century of memory research. A revolutionary
concept in _Über das Gedächtnis_ was the idea that memory research was not
deemed to be the investigation of pre existing memories but that memory
contents to be tested needed to be created and modified in the laboratory as
an integral part of the experimental procedure [47, 46]. Ebbinghaus invented
the paradigm of the nonsense syllable as learning materials of homogenous
difficulty beyond the familiarity of words and prose. This notion defined a
task in which a multitude of variables can be defined and their influences on
remembering behaviors observed. He used strict controls on the timing and
number of study trials, allowed time for recall, and retention interval, and
measured the difficulty of learning a list by the number of study trials
required to attain one correct recall. Moreover, Ebbinghaus introduced the
idea of measurable degrees of learning by noting the savings in relearning a
list he had learned earlier. Using this measure Ebbinghaus was able to devise
his famous forgetting curve relating percent savings to retention interval.
[48, 49].

Even in Ebbinghaus’ earliest experiments it was clear that learning depended
greatly on the nature of the content, whether numbers, nonsense syllables,
words, meaningful sentences or poetry, as these vary greatly in their
familiarity and meaningfulness to subjects. By studying isolated variables,
Ebbinghaus was able to observe the influence of the different types of learnt
contents on memory performance, as well as the mode of their presentation, and
the strategies subjects used in learning them. The memories established can
then be tested by direct measurement of recall, recognition and
reconstruction, or by a variety of indirect measures. Ebbinghaus’ experimental
framework set the foundations for the modern era of memory studies, and
remains the prototype for its research almost 150 years after.

At the dawn of the twentieth century, two relevant contributions to the
understanding of memory were presented in relation to the study of reflexes.
The Russian neurologist and anatomist Vladimir Mikhailovich Bekhterev
presented _Pathways of brain and bone marrow_ in 1900, exposing an association
of memory with the hippocampus based on the study of amnesia in patients with
hippocampal degeneration. In addition to his later _Foundations for Brain
Functions Theory_ Bekhterev presented his views on the functions of the parts
of the brain and the nervous system and developed a theory of conditioned
reflexes which describe automatic responses to the environment called
_association reflex_ [50, 51].

Similarly, the scientific mainstream of behaviorism, with its main exponents
Thorndike, Pavlov, Watson and Skinner, held that all learning is the
attachment of responses to stimuli [52]. Therefore they studied the
characteristics and components of a particular type of learning: that which is
derived from repeated association between a stimulus and a response,named
classical conditioning, and that which is derived from association between a
stimulus and a behavior, called operative conditioning [50, 53]. Pavlov’s
studies are related to a type of memory that later would be called associative
memory, while Fitts and Posner’s studies [54] are considered the first aiming
to explain procedural memory. It may be argued that the knowledge on memory
produced by these experimental works of behaviorism was among the most
important in the early days of twentieth century.

Guided by the then prevalent and straightforward view that stimulus-response
learning is supported by connections between sensory areas in the posterior
cortical areas and motor areas in the frontal cortex, Karl Lashley’s conducted
pioneering efforts in the search for engrams [55]. Engrams were viewed as
fundamental to the understanding of memory, as the physical structures in
which memory traces were stored. Using maze learning in rats he aimed to map
the cortical areas and pathways that support memory formation. As the search
proved unsuccessful, Lashley subscribed Flourens’ view on the indivisible
brain, meaning that there were no localizations of memory in different parts
of the brain [56]. He concluded that the memory trace was widely distributed
both within cortical areas and throughout the cortex and that any of the
neurons within cortical areas could support the engram, naming this principle
_equipotentiality_. Also contributed the notion that involved brain areas
acted together to support the engram, naming this principle _mass action_
[57].

Later in 1934 Donald Hebb, student of Lashley, followed the interest in how
the brain gets organized to generate abilities such as memory. His 1949 work
_The Organization of Behavior_ presented cell assemblies and the connection
between cells that fire together, advancing studies of memory consolidation
[58, 59]. The _dual-trace_ hypothesis of memory subsequently proposed by Hebb
in 1949 offered a specific physiological theory of memory consolidation.
According to Hebb’s hypothesis, neural activity initiated by an experience
persists in the form of reverberating activity in neural circuits of STM, and
that the formation of LTM means the stabilization of these circuits leading to
permanent synaptic change [60].

During the following decades, as psychology struggled to assert itself as a
scientific discipline, a large wealth of knowledge about memory was supported
on an increasing number of experimental studies. The work of Edward Tolman
distinguishes from many of his behaviorist contemporaries on its focus on
memory and behavior. Though Tolman was greatly influenced by Watson’s
behaviorism, Tolman’s cognitive, anti-reductionist emphasis on purpose and
macroscopic or molar behavior stood in stark contrast to many of the learning
theories of his contemporaries [61, 62]. The battle was sustained between
these two schools of thought, stimulus-response learning versus cognitive
learning, specially at the level of animal behavior. Tolman proposed that
there is more than one kind of learning in animals and humans. Unlike motor
patterns, well understood by behaviorists, other types of learning were
postulated outside the stimuli-response logic. Importantly, a distinction
between memory systems is rooted in this debate between place-learning, a
position advocated by Tolman [63], and response-learning, a position advocated
by Hull who asserted that learning was a general process [64].

Such behavioral findings suggested the potential co-existence of at least two
distinct learning systems. However they did not have the effect of shifting
the debate concerning how many memory systems there were. Other authors argued
that these two kinds of learning existed, but that they did not represent
fundamentally different things, instead they are accountable by the use of
different cues [65].

A very important contribution of Tolman to the study of memory as set of
dedicated systems was the _Cognitive Map_ theory, which provided deep insights
into how animals represent information about the world and how these
representations inform behavior. Tolman developed this idea of a cognitive map
as an alternative to the then-common metaphor of a central switchboard for
learning and memory, typical of stimulus-response formulations. According to
this view, animals maintained a set of complex, integrated expectancies or
hypotheses of their world [66]. Tolman would later call these complex
integrated expectancies cognitive maps [63]. For Tolman, learning is acquiring
expectancies, that is probability characteristics of the environment. The
organism thus typically learns a cognitive map not a mere movement pattern.
His later writings emphasized the use of multiple expectancies to inform
behavioral performance, particularly when an animal is faced with a choice
[67, 68].

Consistent with the emerging understanding that processing and memory storage
could not easily be separated from one another neurobiologically, the theory
of the cognitive map was embodied within a multiple memory systems
perspective. Importantly, it claimed that the brain memory systems differed
based on the nature of the contents of the memories they processed, and not
only based the length of time that memory storage was supported. As such, this
view critically differed from the more traditional perspectives of cognitive
psychology and cognitive neuropsychology prevalent a the time which saw
systems as differing primarily in terms of how long information remained
within them, not in terms of the type of information involved.

It is relevant for the study of memory systems that two kind of differences
that render memory systems distinct were settled. First, the distinct memory
systems might be computationally different at their circuitry level in order
to be efficient, a notion later developed by Sherry and Shacter’s theory of
functional incompatibility [16]. Fodor also addresses the notion of modularity
[69], understood as separate domain specific modules that handle certain sort
of contents. The functionalities of these modules are hardwired and not
acquired through learning processes. Second, systems might differ in terms of
the length of time during which information is to be stored within them, which
can require different underlying mechanisms. Beyond the study of animals,
these two non mutually exclusive approaches to memory systems were further
expanded to humans in the study of focal cerebral damage.

Since the 1950’s Scoville, Penfield, Hebb and Milner, documented the effects
of surgical lesions of temporal lobe on human declarative memory, finding
severe anterograde amnesia and retrograde amnesia with temporal gradient [70,
71, 72, 73, 74, 75]. A well known case of study was that of the severe
epileptic patient Henri Molaison (H.M.) who in 1953 underwent surgical removal
of brain structures in the MTL (MTL) including the hippocampus to cure him of
his epileptic seizures. As a result of this surgery, H.M. was profoundly
impaired in the acquisition of certain forms of information. He became unable
to consciously recollect new events in his life or new facts about the world.
However, H.M. retained the ability to remember other types of information.
While other cognitive functions remained intact, H.M.’s experience was greatly
influenced by a permanent present tense. If rehearsed and attention was held,
a patient such as H.M. could keep a short list of numbers in mind for several
minutes. But would prove unable if distracted or when the amount of material
to be remembered exceeded what can be held in immediate memory.

Early evidence from H.M’s case supported the mainstream view that memory is
composed of systems which differed in terms of how long can they keep the
memory for. By having removed large portions of hippocampus H.M. had only
distorted the consolidation of the LTM system [76].

Subsequently, Milner reported that H.M. could learn and perform new
sensorimotor tasks. Although H.M.’s memory impairment disabled learning for
all forms of materials, including scenes, words or faces, he proved capable of
learning a complex hand – eye coordination skill, namely mirror drawing, over
a period of 3 days even without awareness of having been previously trained or
tested [77]. This selectivity of H.M.’s amnesia related to the type of learned
activity or content, suggested the existence of two distinct forms of memory
corresponding to each type of material: declarative memory and procedural
memory. It was presumed that these systems were dependant on separate neural
systems, and that by lesion or degenerative processes, amnesiac patients were
only disabled in their declarative memory functions [78, 79, 80].

These findings contrasted with prevailing views at the time by linking a
memory disturbance to damage to a specific part of the brain. However these
theories were attempted in animal models, namely monkeys and rats, leading to
no amnesia, thus discussions and uncertainties about a content based
organization of memory systems ensued for several years [81, 82, 83, 84].

In the following sections an account is provided regarding these two kinds of
taxonomies and a brief review of the relations and differences between memory
systems.

##  2 Persistence-based taxonomy

The 60’s saw a growing interest in developing mathematical models of learning
and memory. Despite that the mainstream view accepted only one global memory
system responsible for handling many kinds of information, this assumption did
allow an implicit division of memory in memory systems which differed in terms
of their capacity to store contents within them.

In the previous section, a review on the historical evolution showed that
allusions to memory taxonomies based on time persistence had been present for
several centuries, despite the apparent triviality of its insight on how
memory is organized. One possible catalyst for the emergent importance of this
perspective during the early 60’s, was the influence of the computer
revolution which may have served as inspiration for thinking about memory from
an information processing approach.

In its most influential consolidation, Atkinson and Shiffrin [85] settled in
1968 a model of human memory divided into three classes, ultra short-term
memory, STM, and LTM, which became known as the multi store or modal model of
memory. In addition to identifying the three different memory types, Atkinson
and Shiffrin also suggested that they stand in a rather fixed relationship to
one another. They proposed that stored information is processed sequentially
entering the brain through the sensory system into ultra-short-term, passes
through STM and ends up in LTM. This processing chain can terminate when
information is forgotten from one of the memory stores.

Figure 1:  In the 1950’s and early 60’s the conception of memory was largely
inspired by an information processing approach, in which systems differed in
terms of duration, processing and storing information for varying periods of
time.

###  2.1 Ultra short term memory

According to this model, Ultra short term memory, or sensory memory, makes
instantaneous sensory information available for processing for less than 120
milliseconds [86]. This kind of memory is specific to a particular sensory
system and does not appear to be shared across sensory systems. In the visual
system, ultra short term memory is the reason, why, for example, apparent
continuous motion is perceived when watching a movie instead of 24 individual
frames per second.

Authors have suggested that ultra short term memory is limited to only a few
hundred milliseconds in duration because the memory traces decay naturally
[85]. Due to this timescale this form of memory would operate outside of
awareness, and since it is entirely driven by external stimuli, it lies
outside conscious control. For these reasons, some researchers suggest that
ultra short term memory may be a component of the sensory system rather than a
memory system.

###  2.2 Short term and Working memory

In the late 50’s the consolidation of the notion of a STM system began with
the empirical support which observed that, provided the prevention of active
rehearsal, even small amounts of information showed rapid forgetting [87, 88].
The pattern of memory decay appeared to differ from that observed in standard
LTM experiments, which led to the view that performance depended on a separate
short term store. It was then thought that STM operated as a crucial
antechamber of LTM storage.

During the 60s, methods were developed for studying visual perception and
motor responses with single-cell recordings from awake, behaving monkeys
performing a classic delayed response task, which requires holding information
in memory for a brief period. This work identified cells in prefrontal cortex
that were maximally active during the delay portion of the task of 15 to 60
seconds [89, 85, 90, 91].

However, various problems stemmed from the view of STM held by this model.
First, it was challenged the notion that the probability of an item being
stored in LTM as a function of its maintenance on short term system. A number
of studies demonstrated that active verbal rehearsal was not linked to durable
LTM [92]. This argument gave way to the theory called _levels of memory_ [93].
This theory proposed that an item in order to be remembered, for instance a
word on a page, could be processed at a series of encoding levels which
started with the visual appearance of the item, its sound when pronounced, and
later its meaning and relationships with other related memory experiences. A
second challenge was provided by the neuropsychological evidence of patients
with an STM deficit while preserving LTM intact. The then prevalent STM model
failed to provide explanation for this phenomena, as it argued that poor
performance of STM should have also led to impaired LTM capacity. These
challenges led researchers to reformulate the STM hypothesis and postulate a
multicomponent system which was termed working memory.

Working memory refers to the capacity to maintain temporarily a limited amount
of information in mind, which can then be used to support various abilities,
including learning, reasoning, and preparation for action [8]. It is generally
acknowledged that working memory can store information for up to 20 seconds,
and according to some experimental studies its maximum capacity is four chunks
of information [94]. Despite its acquisition being without a conscious effort,
working or short-term memory can be controlled consciously and is less
dependent on sensory inputs than ultra-short-term memory. Most importantly,
through rehearsal, the spontaneous decay of working memory may be prevented.

According to Baddeley and his tripartite model [9, 95] working memory is
comprised by the phonological loop, which support retrieval temporary storage
and rehearse of phonological material, the visuospatial sketchpad to perform
maintenance of visual representation of stimuli and their position in space[8,
9], and a central executive sub system which is a limited capacity supervisory
attentional system [96] that orchestrates and mediates the manipulation of
contents from visuospatial and phonological sub systems. However, there is
evidence indicating that spatial and object working memory may be separable
[95]. Single cell recording studies in nonhuman primates have revealed
different activations in ventral and dorsal prefontal cortex during object
working memory performance for the first and spatial working memory
performance for the latter.

In 2000 Baddeley included in this model the episodic buffer involved in
linking information across domains to form integrated units of visual,
spatial, and verbal information with episodic chronological ordering. This
episodic buffer is also assumed to have links to LTM and semantic meaning. The
working memory model currently consists of four elements that process
information: the central executive for attention control; the visuospatial
sketchpad, which creates and maintains a visuospatial representation; the
phonological buffer, which stores and consolidates new words; and the episodic
buffer which stores and integrates information from different sources [10].

Figure 2:  The year 2000 version of the multi-component working memory model
according to Baddeley which includes the episodic buffer. The episodic buffer
is interpreted to be controlled by the central executive, and it is capable of
multi-dimensional information storage, providing a temporary interface between
the phonological loop, the visuospatial sketchpad and long term memory (LTM).
The buffer serves as a modelling space that is separate from LTM, but which
forms an important stage in long- term episodic learning. In this schematic
view, faded areas represent systems capable of accumulating long-term
knowledge, and unshaded areas represent fluid capacities such as attention and
temporary storage.

Working memory is therefore central to the ability to select and implement
goal-directed behavior, to exercise what are termed executive functions.
Indeed, recent discussions emphasize a broad role of prefrontal cortex in
cognitive control, an idea that implies top-down influences from prefrontal
cortex that direct attention and organize action [97, 98]. The prefrontal
cortex allows memory to be accessed strategically, and it orchestrates the use
of learned rules so that knowledge relevant to current goals can be brought to
mind and put to flexible use.

###  2.3 Long term memory

Assumed as a group of systems responsible for the capacity to store
information over long periods of time [99]. LTM differs from STM in that the
memory contents would no longer be vulnerable to spontaneous decay,
nonetheless, some memories may be forgotten due to interference from memories
that are stored later. Another key difference to short-term memory is that
subjects recall these items not in isolation, but including the relationships
between them, and the spatiotemporal context in which they are embedded. This
makes LTM singular due to its larger capacity for the storage of arbitrary
combinations of different kinds of information [100].

Analysis indicates that the hippocampus and associated structures of the MTL
serve to generate LTM traces. Clinical evidence indicates that damage to the
hippocampus produces anterograde amnesia. At the cellular-molecular level, the
intricacies of synaptic plasticity, a candidate model for memory storage, are
being studied in great detail [101], however, the link between single neuron
computation and computation at the network level is poorly understood. It
remains unclear how neuronal cooperativity in intact networks relates to
memories or how network activity in the behaving animal brings about synaptic
modification[102].

In recent years, psychologists have gathered numerous pieces of evidence for
the view that our memories are in fact constructions of what happened in the
past. Memories are stored in the brain in a distributed pattern in the outer
layer of the cortex, related to the area of the brain that initially processed
them [99]. In this view, a visual aspect of an experience is normally stored
in the visual cortex, an auditory aspect of an experience is stored in the
auditory cortex, and a motion element of an experience is stored in the
sensory motor cortex. When a memory is retrieved, all its fragments are put
back together rarely identical to the initial experience [103].

In past decades, little thought was given to the possibility that there might
be some constraint on the kind of information these memory systems could
handle or the rules by which they operate. Over the years, several aspects of
Atkinson and Shiffrin’s taxonomy have been questioned. The main criticisms can
be divided into two classes. First, their taxonomy artificially splits
memories of the same kind into different taxa. Several authors have proposed
that STM and LTM are instances of the same unitary memory that happen to have
different properties. Second, Atkinson and Shiffrin associate together
disparate kinds of memories into a single system. Furthermore, The dominant
view of a single memory system prevented the selective nature of amnesia from
being systematically explored for several decades. For the most part
neuropsychologists working with human subjects accepted the single system
premise and the view that damage to the brain to varying degrees accounted for
the global amnesia observed in subjects with various etiologies [104, 105].
Despite these controversies, Atkinson and Shiffrin’s taxonomy has been one of
the most influential taxonomies of memory.

Advances in neurobiology and behavioral neuroscience contributed to modify
this approach. During the 70s a genuine change occurred in the way memory is
thought of, and various new phenomena began to be addressed as memory related,
using different tasks to measure different specialized functionalities.
Perceptual memory or representation systems are an example of this broadening
[106]. Phenomena like object priming or fragment completion, added to the view
that processing and memory storage occur in the same circuits has emerged from
the neurobiological literature. [107, 108, 109]. Importantly, the discovery of
the declarative memory systems with the view that the hippocampus has a
selective role in learning, began in the late 60s and took more than 20 years
to unfold.

##  3 The discovery of declarative memory systems

The first observations of H.M., and the results of formal testing, were
reported in 1957 by Scoville and Milner [73] in a seminal paper that shed
light on three fundamental principles: a) memory is a distinct brain function,
separable from general cognitive and language functions; b) the MTL is not
necessary for immediate memory since this was largely normal in H.M; and c)
MTL structures are not the final storage location for memories, since although
the removal of these structures showed severe amnesia in H.M., the patient
still retained large portions of memories of his childhood [110]. This
publication became one of the most cited papers in neuroscience and is still
frequently cited.

Importantly, subsequent findings from H.M. established that memory was not a
monolithic system that handles all types of information, but a highly
interconnected set of systems. Due to the the fact that H.M. and other amnesic
patients demonstrated intact learning and retention of certain motor,
perceptual and cognitive skills, memory was thought to be comprised of at
least two separate systems and that only one kind of memory, declarative
memory, is impaired in amnesia [111, 77, 79, 112].

Nevertheless, patients with hippocampal damage typically have a normal
vocabulary, and their general knowledge of facts remains intact.
Interestingly, the opposite pattern of memory loss is associated with a
specific form of neurodegenerative disease known as _semantic dementia_ in
which recent events are retrieved accurately while the meaning of words and
knowledge about world facts is greatly impaired [113].

###  3.1 Declarative memory

Declarative memory provides a fast and flexible way to represent the external
world, and the ability to make inferences from and generalizations across
facts derived from multiple processing sources. It supports the encoding of
memories in terms of relationships among multiple items and events.
Declarative memory allows remembered material to be compared and contrasted.
The stored representations are flexible and can guide performance under a wide
range of test conditions [114]. A key characteristic is that declarative
memory is explicit and accessible to conscious awareness. That is, it may be
brought to mind verbally as a proposition, or non verbally as an image [115,
99, 13, 116].

It is widely accepted that declarative memory has two major components:
semantic memory, responsible for processing facts about the world; and
episodic memory, the ability to re-experience a time and place specific event
in its original context [4, 40].

Declarative memory depends on the integrity of neural systems damaged in
amnesia, namely the hippocampus and MTL associated structures. Amnesic
patients’ defects in memory extend to both verbal and nonverbal material, and
involve information acquired through all sensory modalities. Other etiologies
of amnesia have also contributed useful data to support theories on
declarative memory, including encephalitis, anoxia and ischemia, Korsakoff’s
syndrome, and psychiatric patients whose memories were impaired as a result of
electroconvulsive therapy [117, 118].

Several theories regarding the role of the hippocampus in memory have been
proposed over the years. All regard the hippocampus as being critical for
episodic memory, but there are key differences in whether they view the
hippocampus as having a time limited role in episodic memory and in whether
they deem it to be necessary for the acquisition of non-contextual
information. The pattern of spared and impaired cognitive processes in
patients with hippocampal damage, combined with results from animal models of
amnesia, has lead to the _Declarative Theory_ of hippocampal function [119].
Some researchers have focused on building a neural level understanding of
hippocampal function in a specific cognitive domain such as the theory of the
_Cognitive Map_ [5]. While others have sought more specific characterizations
of hippocampal function, drawing on experimental data from animals and humans
with the _Multiple Trace Theory_ [120], the _Dual Process Theory_ [121], and
the _Relational Theory_ [122].

In addition to MTL structures the acquisition of episodic memory requires the
involvement of other brain systems, especially the frontal lobes [123, 124,
125, 126, 127].

A number of considerations suggest that the capacity for declarative knowledge
is phylogenetically recent, reaching its greatest development in mammals with
the full elaboration of medial temporal structures, especially the hippocampal
formation and associated cortical areas. This capacity allows an animal to
record and access the particular encounters that led to behavioral change. The
stored memory is flexible and accessible to all modalities [128].

The declarative memory system has a distinct developmental evolution through
individual’s lifetime. In most species hippocampus is not fully developed at
birth and processess of neurogenesis are constant throughout life in some
cases [129]. In humans the hippocampus and related structures incur in a
dramatic size change in the first two years of life, enabling the memory
function after 18 to 24 months, and only reaching full adult function after
reaching 10 to 12 years of age. As such, phenomena such as infantile amnesia
defined as the inability to form episodic memory early in life is starting to
be understood [130, 131, 132]. Similarly, in spatial navigation tasks,
children younger than two years old fail at distal cue use in navigation, as
it requires a fully functioning hippocampus [128, 133, 134].

###  3.2 Declarative systems

Tulving proposed the distinction between Episodic and semantic memory as two
types of declarative memory subsystems. Both types of memory are declarative
due to the fact that retrieval of episodic and semantic information may be
carried out explicitly and subjects are aware that stored information is being
accessed [3, 4, 135]. This distinction devised by Tulving has in many ways
fulfilled its purpose of understanding, and accounting for, the broader range
of memory phenomena and experimental findings, and has formed the foundation
for decades of theoretical and experimental work in the cognitive neuroscience
of memory.

Of particular interest has been the extent to which semantic and episodic
memory have a shared dependence on the hippocampus. In contrast to the
definitive evidence for the link between hippocampus and episodic memory, the
role of the hippocampus in semantic memory has been a topic of considerable
debate. Amnesic patients do have great difficulty acquiring semantic
knowledge, but they can typically succeed to some extent after much repetition
[136, 137]. In Tulving’s work on the severely amnesic patient K.C., he reports
how eventually the patient learned to complete arbitrary three-word sentences
during a large number of training trials distributed over many months despite
the absence of any memory at all for training episodes [138]. Episodic memory
can be virtually absent in some severely amnesic patients who can still
accomplish some semantic learning.

The key structures that support declarative memory are the hippocampus and the
MTL adjacent structures, such as entorhinal, perirhinal, and parahippocampal
cortices, which make up much of the parahippocampal gyrus [115]. These
structures are organized hierarchically, and their anatomy suggests how the
structures might contribute differently to the formation of declarative
memory, for example, in the encoding of objects in perirhinal cortex, or
scenes in parahippocampal cortex, and in the forming of associations between
them in the hippocampus [139, 140, 141].

One interpretation is that both episodic and semantic memory depend on the
brain system damaged in amnesia, the hippocampus and MTL related structures,
and that episodic memory additionally depends on the integrity of the frontal
lobes. Patients with frontal lobe damage, who are not amnesic, exhibit a
phenomenon termed _source amnesia_ which refers to loss of information about
when and where a remembered item was acquired [142, 143]. In this sense,
source amnesia appears to reflect a loss of episodic memory related to frontal
lobe dysfunction, which in turn reflects a disconnection between facts and
their contexts. The greater contribution that frontal lobe function makes to
episodic memory, compared to semantic memory, would give a 1biological support
to the distinction between episodic memory and semantic memory [114].

In their infuential book _The Hippocampus as a Cognitive Map_ , O’Keefe and
Nadel suggested that the then recently discovered place cells found within the
hippocampus provided the neurobiological substrate of the _Cognitive Map_ [5].
Subsequent investigations of hippocampal place cell activity further developed
the notion of the hippocampus mediating place information and the functions of
such data coordination beyond spatial domains [144].

####  3.2.1 Episodic memory

Episodic memory was conceived by Tulving [3], at a time when information
processing models dominated. Episodic memory refers to autobiographical memory
for events in its when, what and how components, linked together in a coherent
spatial and temporal context. This includes the spatiotemporal relations
between events. A key feature of episodic memory is its unique role to allow
the individual to mentally travel back into her personal past [145, 146].

The precise details that characterize episodic memory have been, and continue
to be, debated, but time, space and sense of self are widely accepted as key
elements [147, 148, 149, 150, 151].

Episodic memory is affected by aging processes [152], and there have been
findings of sex differences in its performance [153, 154], but results are
still inconclusive [155].

It has been suggested that episodic memory in the hippocampus is formed by
combining spatial information from the medial entorhinal cortex [156, 157]
with non spatial information from the lateral entorhinal cortex [158, 159]. A
number of imaging studies have revealed evidence linking MTL activation with
episodic encoding. MTL activation has been observed under conditions in which
exposure to novel stimulus materials is compared with exposure to familiar
materials. Imaging studies have also illuminated the contributions of distinct
prefrontal regions to encoding and retrieval [160, 161, 162].

Recent studies have helped to establish that these neural systems also support
the capacity to imagine and to simulate episodes expected to occurr in the
future [4, 145, 163, 164]. The ability to pre experience future events has
been referred by some authors as prospection [165] and by others as episodic
future thinking [166, 167, 168].

Some early observations along these lines were reported related to the patient
K.C., who was investigated extensively over 20 years since a head injury left
him with large bilateral hippocampal lesions which caused a remarkable case of
memory impairment [109, 138, 169]. K. C. was unable to provide a description
of his personal future for any time period, immediate or distant, describing
his mental state as _blank_. Interestingly he used exactly the same definition
of mental state when asked to think about the past [170, 109]. A later
investigation in another patient, D. B., who became amnesic as a result of
cardiac arrest and consequent anoxia revealed that he, like K. C., exhibited
deficits in both retrieving past events and imagining future events [171].

A study led by Hassabis examined the ability of five patients with documented
bilateral hippocampal amnesia to imagine new experiences, such as being at a
desired location in an ideal situation [151]. Based on the content, spatial
coherence and subjective qualities of the participants’ imagined scenarios,
the ability to imagine of the subjects with hippocampal lesions was greatly
reduced in richness and content.

Due to the fact that hippocampal amnesics have difficulty imagining new
experiences, Hassabis concluded that the hippocampus plays a key role in
recombining details of previous experiences into a coherent new imagined
construction.

This interpretation that hippocampus mediates both future episode thinking and
imagination, assumes that the episodic memory is constructive rather than a
reproductive system. Since the future is not an exact repetition of the past,
it requires a system that can draw on the past to flexibly extract and
recombine elements of previous experiences. In this view, fundamental features
of a memory are distributed widely across different parts of the brain [139].
Therefore, retrieval of a past experience involves a process of pattern
completion, in which the process of recall pieces together some subset of
distributed features that comprise a particular past experience [172, 173].

Consistent with this approach, neuroimaging studies focused on the brain
activity during the construction of past and future events, have revealed
regions exhibiting common activity, which included the left portion of the
hippocampus and the right occipital gyrus, especially during the elaboration
phase, when participants are focused on generating details about the
remembered or imagined event [174, 175].

####  3.2.2 Semantic memory

Tulving postulated that semantic memory consists of a _mental thesaurus_
encompassing a wide range of organized information including facts, concepts
and vocabulary necessary for language [4, 135]. Semantic memory can be
distinguished from episodic memory by virtue of its lack of association with
spatiotemporal contexts [1], and does not require subjective reexperiencing of
the episode in which the knowledge was acquired. These systems differed as
well in terms of the conditions and consequences of retrieval. Unlike episodic
memory, retrieval from semantic memory was thought to leave its contents
unaltered and to provide new input into episodic memory. Retrieval from
episodic memory, in contrast, was thought to modify the contents of the
system. Also, episodic and semantic memory were thought to differ in their
dependence on each other: whereas semantic memory was thought to be
independent from episodic memory in terms of recording and maintaining
information, episodic memory could be strongly influenced by, and depend on,
information in semantic memory at encoding [176].

Originally, Tulving viewed episodic and semantic memory as two functionally
separate systems, but he also emphasized the features shared between them and
their close interaction. For example, retention of information in both systems
was thought to be automatic, because it did not require ongoing effort; for
both systems, retrieval of information could be prompted by highly relevant
cues or questions, even if the retrieval process itself is outside of
awareness. Personal semantic memory, that is semantic knowledge that relates
to the self, represents another common area of semantic and episodic memory,
increasingly supported by neuropsychological evidence [177, 178]

Semantic memory has been associated with an overlapping network of neural
regions, with recent research invested in elucidating the roles of anterior
and lateral temporal neocortex and ventrolateral pre frontal cortex [179, 180,
181]. Imaging studies have suggested that the semantic attributes of a
stimulus are stored near the cortical regions that underlie perception of
those attributes, while have also highlighted that retrieval from semantic
memory and encoding into episodic memory share underlying component processes
[182].

Figure 3:  A taxonomy that includes declarative and non declarative memory
systems, including the different kinds of awareness of the subject. Although
non declarative memory was not yet fully understood, compelling evidence
pointed at distinct specialized components of memory outside of the episodic
and semantic domains.

###  3.3 Non declarative memory

There were early suggestions in the animal literature that more than just
motor skills were intact after lesions of hippocampus or related structures
[183, 184, 5]. However, these proposals greatly differed from each other, and
they came at a time when the findings in experimental animals was not in
agreement with findings from human amnesia and memory [78, 112].

Evidences of the extent of non declarative systems in humans came from the
task of reading mirror-reversed words [111], a perceptual skill which amnesic
patients acquired at a normal rate despite poor memory for the words that they
read. Thus, perceptual skills, not just motor skills, were intact. Later,
amnesiac patients with the ability to resolve stereoscopic images [185],
learning of an artificial grammar [186], and learning of new categories of
items [187]. The accumulating data led to further arguments about the extent
and nature of what is not included in the notion of declarative memory [112,
105].

The notion of procedural memory was originally devised to contrast with
declarative memory [188, 111]. Whereas this notion appropriately describes a
wide variety of skill-based kinds of learning, certain memory phenomena were
clearly not declarative, but also not well accommodated by the notion of
procedural memory. Subsequently, the concept of non declarative memory emerged
as an umbrella which would cover human memory capacities that support skill
and habit learning, perceptual priming, and other forms of behavior, which are
expressed through performance rather than recollection [189]. For example
procedural skills, such as knowing how to ride a bicycle, are expressed
through performance in riding a bicycle; priming memory, which underpins our
ability to recognize words and other perceptual skills, is accessed implicitly
as it is performed. Non declarative memory is neither true nor false, does not
require conscious reflection on the past, or event knowledge that memories are
being formed by past events. Non declarative memory is shaped by experience,
but unlike declarative memory which is flexible and can guide behavior in
multiple contexts, the acquired knowledge in non declarative memory is thought
to be rigidly organized [99].

Authors have suggested that non declarative memory is phylogenetically old.
and that it may have developed as a set of special purpose learning abilities.
Memory formation is then thought as the result of cumulative changes stored
within the particular neural systems engaged during learning [114]. Most non
declarative memory functions are present at the onset of human life, few age-
related improvements have been found from 3 months on, and evidences have
highlighted that these systems remain stable since the 9th month of life [190,
191, 192]. The idea that non declarative memory remains stable as age
progresses has come to be widely accepted. For instance, several studies of
priming in normal aging have not reported significant decline, while cross-
sectional studies employing a range of different tasks have reported non-
significantly different priming between groups of young and older adults [193,
194].

Yet not all authors agree on the idea of preserved non declarative functions
in older individuals, and some have argued that these inconclusive results
need to be further substantiated [195].

###  3.4 Non declarative systems

Neuroimaging studies have led researchers to attempt establishing the main
neural structures identified in relation to current non declarative systems.
For example, the striatum has been linked to memory of skills and habits, and
active sections of the neocortex have been related to priming. Classical
conditioning of skeletal musculature has an essential dependence on the
cerebellum, while emotional conditioning has been correlated to activation of
the amygdala [114, 2].

It is debated to this day the role of the hippocampus and related structures
in non declarative learning. One proposal is that, whereas conscious
recollection depends on the hippocampus, it is also important for unconscious
memory under some circumstances [196, 197]. Other work, based on functional
magnetic resonance imaging (fMRI), has implicated MTL structures in the
unaware learning of sequences and other tasks with complex contingencies [198,
199]. Considering that fMRI data cannot establish a necessary role for a
particular structure, this remains a debated topic.

The role of non declarative memory system in supporting syntactic processing
is also still unclear. In studies with patients with Korsakoff’s syndrome who
display deficits in all subdomains of declarative memory, yet their non
declarative memory remains intact, patients showed robust syntactic priming
effects, the phenomenon in which participants adopt the linguistic behaviour
of their partner [200].

####  3.4.1 Conditioning: Skeletal responses

Study of nondeclarative memory began with motor skills and perceptual skills.
The best understood example of nondeclarative memory in vertebrates is
classical conditioning of the eyeblink response, specifically delay eyeblink
conditioning. In delay conditioning, a neutral conditioned stimulus (CS), such
as a tone, is presented just before an unconditioned stimulus (US), such as an
airpuff to the eye. The essential memory trace for the conditioned eyeblink
response and other discrete conditioned motor responses was discovered is
formed and stored in the cerebellar interpositus nucleus [201]. Critically,
delay eyeblink conditioning is intact in amnesia and is acquired independently
of awareness [202, 203]. Largely on the basis of work with rabbits, delay
eyeblink conditioning proved to depend on the cerebellum and associated brain
stem circuitry. Forebrain structures are not necessary for acquisition or
retention of classically conditioned eyeblink responses. These discoveries are
on of the most successful examples of localizing a memory trace within the
vertebrate brain [204].

####  3.4.2 Priming and perceptual learning

The next of these to come under study was the phenomenon of priming. Priming
was defined as the improvement in the ability to to detect or classify a
stimulus as the result of a recent encounter with the same or a related
stimulus [205, 206].

Evidence for the distinct priming phenomenon came from both normal subjects
and amnesic patients that perform normally when tests are structured using non
memory kind of instructions [206, 205, 108]. For example, amnesic patients
often performed well when they were given three-letter word stems as cues for
previously presented words, event without recognizing the stimuli as having
been presented before. With conventional memory instructions (use each cue to
help in remembering a recently presented word), healthy subjects outperformed
the patients [207]. Thus, it became evident that priming is an unconscious
memory phenomenon and is entirely independent of the MTL.

Priming effects are distinct from declarative memory in two other important
aspects. The information acquired by priming is fully accessible only through
the same sensory modality in which material was presented initially. And
priming effects are short lived, since in both normal control and amnesic
patients it declined after 2 hours [206].

Priming is presumably adaptive because animals evolved in a world where
stimuli that are encountered once are likely to be encountered again.
Perceptual priming would result advantageous as improves the speed and fluency
by which organisms interact with familiar stimuli. For example, in the case of
visual priming, the posterior visual cortex becomes more efficient at
processing precisely those stimuli that have been processed recently. This
plasticity occurs well before information reaches the limbic structures
important for declarative memory [163].

Evidence of independence of the phenomena of priming and the type of memory
impaired in amnesia was reproduced by the studies of perceptual priming [208,
209], and conceptual priming [210]. These works showed that severely amnesic
patients can exhibit fully intact priming while performing at chance on
conventional recognition memory tests for the same test items.

####  3.4.3 Conditining: Emotional responses

Emotional conditioning is understood as system of non declarative memory that
is responsible for the assessment whether an encountered stimulus has positive
or negative value. In humans, associative fear learning proceeded normally
after hippocampal lesions, even though the CS – US pairings could not be
reported [211]. It has been shown that the amygdala has a critical role in
fear learning, and its function and connectivity appears to be conserved
widely across species. In human neuroimaging studies, the amygdala was
activated not only by fear but by strongly positive emotions as well [212].

The biological study of fear learning and its reversal, for instance fear
extinction has considerable relevance for clinical disorders such as phobias,
post-traumatic stress disorder, and other anxiety disorders [213].

In addition to its importance for emotional learning, the amygdala also exerts
an important modulatory influence on both declarative and non declarative
memory [214, 215]. Thus, activity in the amygdala, and the effect of this
activity on other structures, is responsible for the fact that emotionally
arousing events are typically remembered better than emotionally neutral
events. The importance of the amygdala for modulating memory has also been
demonstrated with neuroimaging. Volunteers rated the arousing effects of
either neutral scenes or emotionally distressing scenes and then took a memory
test for the scenes two weeks later [216]. Increased activity in the amygdala
at the time of learning was associated with higher arousal ratings for the
scenes and improved accuracy on the later memory test. Interestingly, this
effect occurred in the left amygdala for women and in the right amygdala for
men [217].

####  3.4.4 Procedural: Skills and habits

One important discovery in the 1980s was that the gradual trial-and-error
learning that leads to the formation of habits was supported by the striatum
[6, 218, 219]. Habit memory is characterized by automatized, repetitive
behavior and, unlike declarative memory, is insensitive to changes in reward
value [220]. Tasks that assess habit learning are often structured so that
explicit memorization is not useful, and individuals must depend more on
intuition. In this learning, what is presumably acquired is a set of
dispositions to perform a task in a particular way, and not factual knowledge
about the world. Unlike declarative memory, which is flexible and can guide
behavior in different contexts, the acquired knowledge in this case is rigidly
organized. Habit memory subsequently became an important focus of study [221].

The difference between declarative memory and habit memory was shown for
memory-impaired patients with hippocampal lesions and patients with
Parkinson’s disease [219]. Amnesic patients can acquire a variety of skills at
an entirely normal rate. These include motor skills [222], perceptual and
motor skills [223, 111], and cognitive skills [224].

Currently is known, striatal neuronal plasticity enables basal ganglia
circuits to interact with other structures and thereby contribute to the
processing of procedural memory [225]. The cerebellum is involved in the
execution of movements and the perfection of motor agility needed procedural
skills. Damage to this area can impede one from relearning motor skills and
recent studies have linked it to the process of automating unconscious skills
during the learning phase [226]. The limbic system shares anatomical
structures with a component of the striatum, which assumes primary
responsibility for the control of procedural memory. Reward-based learning of
this kind depends on dopamine neurons in the midbrain, which project to the
striatum and signal the information value of the reward. The dorsolateral
striatum is crucial for the development of habits in coordination with other
brain regions while together with the infralimbic cortex appear to work
together to support a fully formed habit [227].

####  3.4.5 Non associative memory

Non associative memory is understood as a robust form of behavioral memory,
based on newly learned behavior through repeated exposure to an isolated
stimulus. This form of memory is developed even in invertebrate animals who do
not have a capacity for declarative memory. It differs from associative
learning in that it does not require the temporal pairing between two
different sensory stimuli or between a sensory stimulus and corresponding
response feedback [228, 229]. There are two well known types of non-
associative learning: habituation and sensitization. Habituation is a decrease
in response to a benign stimulus when the stimulus is presented repeatedly,
while sensitization describes an augmentation of the response. Habituation is
thought to be related to a decrease in the efficiency of synaptic
transmission, which may be caused by a conductivity change in the membrane of
the stimulated neuron. In turn, the process of sensitization may be due to a
provision in transmission, whether it may be presynaptic or postsynaptic
[230].

A well understood and simple form of non associative memory is olfactory
habituation, in which responsiveness to stable but behaviorally non
significant stimuli is decreased in relation to exposition [231, 232].

##  4 Multiple memory systems

In biology, a system is defined in terms of both structure and function. In
its application to the domain of memory, multiple memory systems is understood
as the set of different neurocognitive structures whose physiological workings
produced the introspectively apprehensible and objectively identifiable
consequences of learning and memory. The various memory systems can be
distinguished in terms of its brain mechanisms, the different kinds of
information they process and the principles by which they operate [233].

As it has been noted, early interpretations of memory assumed a unitary model
that could be used in many different ways [234, 235]. However, in most of the
history of the study of memory, dichotomous classifications of memory had been
put to use, such as procedural versus declarative [236], semantic and episodic
[3, 4], habit and memory [184, 6, 7], dispositional and representational
[237], taxon versus locale [5]. Although a minority, distinctions among three
and even more memory systems have also been put forward [170].

One of the earliest references to memory systems appeared in a 1972 paper by
Tulving [3]. There were other less known efforts in favor of memory systems
such as the 1979 article by Warrington in which she discussed
neuropsychological evidence supporting a distinction between STM and LTM
systems, and between two kinds of LTM systems, namely event memory and
semantic memory [238, 239, 240].

In the early 1980s, the cerebellum was discovered to be essential for delay
eyeblink conditioning [241] a form of learning preserved both in animals with
hippocampal lesions [242] and in severely amnesic patients [202]. Then, the
striatum was identified as important for the sort of gradual, feedback-guided
learning that results in habit memory [6, 218]. A similar contrast between
declarative memory and habit memory was later demonstrated for amnesic
patients and patients with Parkinson’s disease [219]. Finally, it was shown
that still other types of learning, which involve the attachment of positive
or negative valence to a stimulus, as in fear conditioning or conditioned
place preference, have an essential dependence on the amygdala [243, 244,
245].

Based on evidence from human studies, these and other models attempted to
embrace the large amount that has been learned about neuroanatomy, the
molecular and cellular biology of synaptic change, and the organization of
brain systems. Work with experimental animals, namely rats and monkeys without
which a systematic study of memory would have proved impossible, also
supported the notion of multiple memory systems.

Given this wide variety of evidence related to memory phenomena and its
supporting neural sustrates, in the mid 1980s the perspective abandoned an
account of human memory based on a two-part dichotomy and shifted to a more
complex taxonomy [239]. Critically, the notion of non declarative memory was
introduced and conceptualized as an umbrella term referring to several memory
systems supporting the wide panorama of memory related phenomena found in
human and animal research [189, 233].

Figure 4:  Taxonomy of mammalian long term memory systems according to Squire
[114]. The taxonomy lists the brain structures thought to be especially
important for each form of declarative and non declarative memory.

Sherry and Schacter approached the concept of memory systems from an
evolutionary perspective, proposing that different systems evolve as special
adaptations of information storage and retrieval for specific and functionally
incompatible purposes [16]. In their evolutionary view, Sherry and Shacter
elaborate the idea of functional incompatibility, examining components of this
evolution such as natural selection, heritable variation in memory, memory and
reproductive success, and adaptive specialization [246]. The notion assumes
that in order to solve different environmental problems, the animal must make
feasible different requirements of the information processing strategies, and
that these different requirements can call for distinct neural circuitries
[247, 148].

The memory systems of the mammalian brain operate independently and in
parallel to support different behaviors. In some circumstances, memory systems
are described as working cooperatively to optimize behavior and in other
circumstances are described as working competitively. How they compete or
substitute one for the other is a topic of current interest [248, 249, 250].
Packard demonstrated the parallel works of multiple memory systems in rats
[251].

When the stratial caudate nucleus was inactive, the parallel memory system
supported by the hippocampus was unmasked. A similar stance has been described
in humans performing a virtual navigation task that could be solved by either
a spatial or nonspatial strategy [252]. As training progressed participants
tended to shift to a nonspatial strategy, then showing increased activity in
the stratial caudate nucleus, which emerged as training progressed. Although
many tasks can be acquired by more than one memory system, other tasks
strongly favor one system over another. Prefrontal cortex may be important in
determining which memory system gains control over behavior [253]. Several
other factors increase the tendency to adopt one memory system over another,
in this case, a striatal strategy. In this sense, relevant evidence has been
obtained from studies of stress [254], and aging [255]. Although many tasks
can be acquired by more than one memory system, other tasks strongly favor one
system over another.

Similarly, a common feature of skill learning in humans is that trying to
memorize, and use declarative memory, can disrupt performance, as revealed by
fMRI activity in the MTL early during learning [256]. When learning
progressed, activity decreased in the MTL, and activity increased in the
striatum. Moreover, when the task was modified so as to encourage the use of
declarative memory, less activity was observed in the striatum and more
activity was observed in the MTL.

Using these notions of multiple memory systems, researchers were increasingly
more able to place theoretical speculation within a neurobiological framework,
thus reaching a more accurate understanding and classification of memory.

## Conclusion

The nature of memory and its organization has been central to discussion on
memory for several centuries. The evolution of the idea that there are
multiple forms of memory, each supported by a distinct brain system, began in
the mid 20th century and is now widely accepted and fundamental to the
contemporary study of learning and memory [103, 139, 1].

The multiple memory systems framework is supported by an enormous amount of
data learned in the past decades about neuroanatomy and cognitive
neuroscience, and it has been able to accommodate a large variety of empirical
observations of memory performance. It seems justifiable to conceptualize that
the various memory components of memory have distinct neural architectures and
operational principles, and serve different domain-specific purposes. Despite
these memory systems operate independently and in parallel to support
different behaviors, in some circumstances, memory systems may work
cooperatively to optimize behavior and in other circumstances work
competitively. It is still debated, however, how to best characterize their
mutual relations and interactions. It remains beyond the scope of this article
to evaluate the strengths and weaknesses of all proposed distinctions between
memory systems.

A relevant implication of the multiple memory systems framework is that the
therapeutic targets for various kinds of memory disorders would demand
different interventions based on the known supporting neural architectures.
Future investigation that combine cognitive, neuropsychological and
neuroimaging approaches will further our understanding of the relations among
the systems that together constitute the foundation of memory. Therefore, it
is foreseeable that the notion of multiple memory systems remains dynamic, and
that new specifications of memory systems emerge in the future grounded on
empirical evidence.

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