MMemory systems of the brain
Alvaro PastorUniversitat Oberta de Catalunya, Computer Science, Multimedia andTelecommunications Department, Barcelona, [email protected] 1, 2020
Abstract
Humans have long been fascinated by how memories are formed, how they can bedamaged or lost, or still seem vibrant after many years. Thus the search for the locusand organization of memory has had a long history, in which the notion that is iscomposed of distinct systems developed during the second half of the 20th century. Afundamental dichotomy between conscious and unconscious memory processes was firstdrawn based on evidences from the study of amnesiac subjects and the systematicexperimental work with animals. The use of behavioral and neural measures togetherwith imaging techniques have progressively led researchers to agree in the existence of avariety of neural architectures that support multiple memory systems. This articlepresents 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 canencode, store, and retrieve a variety of information [1, 2]. It affords the foundation forthe adaptive nature of the organism, allowing to use previous experience and makepredictions in order to solve the multitude of environmental situations produced bydaily interaction. Not only memory allows to recognize familiarity and return to places,but also richly imagine potential future circumstances and assess the consequences ofbehavior. Therefore, present experience is inexorably interwoven with memories, andthe meaning of people, things, and events in the present depends largely on previousexperience.Questions concerning the nature and organization of memory systems arefundamental to our understanding of the processes underlying learning and memory inhumans and other animals. Due to its importance and complexity, the subject ofmemory is connected with some of the most profound questions of philosophy andbiology, and as such, has been approached from different perspectives andmethodologies. Along the way, idealists and materialists, empiricists and nativists,behaviorists and cognitivists, have confronted ideas about memory. First fromphilosophy through introspection and intuition, complemented later with anatomicaland physiological observations. Then neuropsychology, through observation of patientswith various defects in memory which developed the notion of a dichotomousorganization of memory. More recently, relevant contributions from neurobiology andcognitive neuroscience, using various behavioral and neural measures together with1/36 a r X i v : . [ q - b i o . N C ] S e p maging techniques, have progressively led researchers to postulate distinctions amongvarious memory systems supported by different neural architectures, for example, by thehippocampus and related structures, the amygdala, the striatum, and the cerebellum.The tradition of memory research considered in this article is that of experimentalpsychology and cognitive neuroscience amassed over the past decades. While a majorpart of early research assumed a unitary view on memory, some authors assumeddichotomous classifications based generally on the distinction of conscious andunconscious memory processes. Accordingly, relevant distinctions between memorysystems have been proposed including but not limited to: episodic and semanticmemory [3, 4], taxon and locale memory [5], habit memory and cognitive memory [6, 7],working memory and long term memory [8–10], 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 ofmemory. Supported on cognitive and neurobiological and neuropsychological evidence,memory is conceived as a set of separate, highly specialized, neural mechanisms thatinteract to reach a common goal. However, the complete extent of their features andinteractions is yet to be fully understood.The first part of this article presents a brief historical review with which toreevaluate and contextualize the current theories and frameworks on human memorysystems. The second part presents an account for the components of the multiplememory systems model, with some clues regarding the functional basis of memoryprocesses. The memory systems comprised in this article are part of the most acceptedand disseminated at present time. Debate about which of the different taxonomies ofmemory most appropriately organizes all available experimental data is beyond thescope of the present study. 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 philosophicalinquiry, cognitive psychology, biology and neuroscience. In looking at the history of thelocalisation and organization of memory it is necessary to turn to ancient theoriesregarding the nature of soul and its relation to the body [17].In early allusions to memory, ancient Egyptians considered it was solely supported bythe 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 techniquedevised 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. InTheatetus, 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 ourperceptions and thoughts stamp images of themselves. An early distinction was madebetween the passive retention of perceptions and active memory. Plato described activememory in its episodic features, as ”the power which the soul has of recovering, when byitself, some feeling which she experienced when in company with the body” [20]. Later inthe fourth century BCE, Aristotle returned to the notion that the soul is not a separatesubstance from the body, as Plato had taught, but inherently bound into it, affordingits form. Aristotle came from a medical family and his biological bent is shown in itsinfluence on most of his philosophy. Informed by his biological researches, in
Metaphysica , Aristotle presented a thoroughly materialistic theory, in which the soul orsouls were distributed throughout the entire living body [21]. Also in de Anima , the2/36oul was conceptualized as distributed in the body. While, according to Plato, memoryis one of the higher faculties and partakes of the eternal nature of the soul, for Aristotlememory is dependent upon a physical process, and perishes with the body. In spite ofthis, Aristotle acknowledged the existence of a center on which sensory input convergedand from which behavior was initiated. This, for Aristotle, is the location of commonsense or sensus communis , where besides the external senses such as sight and smellwere processed, internal senses such as memory and imagination were sustained.Aristotle established that the cognitive center was located at the heart, and that thevegetative soul was fluid and distributed everywhere in the body [22, 23]. The operationof memory as then conceived, may be inferred from the kinds of memory that theclassical philosophers observed. Aristotle worked on a tract devoted to the subject ofmemory called
De memoria et reminiscentia . Its second chapter was devoted mainly tothe recollection and association of ideas. In dichotomous fashion, Aristotle distinguishesthe mere persistence and direct reproduction of a presentation, from voluntaryrecollection, which is possible only by the association of ideas, by similarity, contrast,and contiguity. In the Aristotelian view, persistence memory is an attribute of animalsand humans, while the voluntary recollection is unique to humans [22, 24, 25].Increasingly, philosophical inquiry on memory was influenced by anatomical andphysiological studies. In the first century BCE the Byzantine surgeon Poseidoniusproduced the first written assignments of mental functions to specific cerebral regions.Based from observations of head injuries, Poseidonius argued that lesions at the front ofthe brain interfere with apprehension of all types of sensation, whereas trauma of theposterior part results in memory deficit, and damage to the middle ventricle produces adisturbance of reason [26]. At the end of the fourth century CE, Nemesius of Emesacarried forward the ideas of ventricular function and proposed a schema which remainedfairly standard for several centuries. In
De Natura Hominis , claimed that the anteriorventricles accounted for the mixing of sensations and for imagination, the middleventricle for cogitation and reason, and the posterior ventricle for memory [27, 28].Augustine of Hippo, Roman theologian and philosopher at the end of fourth centuryCE, presented an account of human memory orchestrated by the brain and divided indifferent and complementary instances: sensible memory, intellectual memory, memoryof memories, memory of feelings and passion, and memory of forgetting [29]. Sensememory, for example, preserved and reproduced idealized images of visible objects,sounds, odors and other items available to the senses. Intellectual memory on the otherhand, contained our knowledge of the sciences, of literature and dialectic, and of thequestions relating to these subjects. This memory, unlike the memory of sense,contained not the images of things, but the things themselves [30]. The philosopher’scontribution foresees in striking detail some of the most relevant theories of modernpsychology and neuroscience about memory, including the differences between sensememory and intellectual memory, similar to current episodic and semantic memorydefinitions.During the following decades, philosophical conceptions and directions in memoryresearch in the Western tradition remained divided between either the views of Aristotleor those of Plato and Augustine of Hippo.An important milestone is found in the mid 16th century. The work of AndreasVesalius in
De humani corporis fabrica libri septum , helped developed an opposition tothe medieval theory that the soul resides in the ventricles, believing these to be merechannels for the passage of the fluid anima and explicitly identified the brain as themain organ of intelligence, movement, and sensation [31]. Likewise, English physicianThomas Willis helped establish as well that activities are not carried out in theventricles but in the brain substance itself. Also, Willis proposed a direct correlationbetween complexity of gyri convolutions and availability of cognitive abilities including3/36emory. [32].Willis’ ideas were contemporary to those of the French mathematician andphilosopher Descartes, and the notion of the correlation between physical and psychicprocesses was clearly understood by the dualists of the seventeenth century. In
Dehomine
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 himlocated in the ventricles.
When the mind wills to recall anything,
Descartes wrote, thisvolition causes the pineal gland to incline itself successively this way and that, and impelthe animal spirits to various parts of the brain until they come to that part in which aretraces left by the object we would remember . Descartes explained the physical processesinvolved in memory in accordance with his crude physiology, following the belief thatthe soul resides in the ventricles and that the fluid in them can be animated. This ideasprevailed into the end of the 18th century [33].The doctrine of the Cartesians, that memory was conditioned by traces left in thebrain, was developed by the physiologists of the 18th century into a materialistic andmechanical view of memory. In an extreme example, the physiologist Albrecht vonHaller interested in the time occupied in psychic processes, estimated that a third of asecond was sufficient time for the production of one idea. Von Haller and others thencalculated that in a hundred years a human must collect during her wake period a totalof 1 577 880 000 traces. By assuming the weight of the brain elements that were thenconceived with the power for preserving impressions, then obtained 205 542 traces mustbe found in one gram of brain substance [23].Early in 19th century, Franz Joseph Gall aimed again at settling the conceptualdispute, and contributed to establish that memory was located solely in the brain andwas not located in the heart nor the ventricles as it was previously posited. Based on ananatomical and physiological data, Gall also acknowledged that the brain containsindependent but interacting regions, and later interpreted that differences in behaviorare 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 forparticular kinds of information. Noting that some individuals have excellent memory forplaces but not music whereas others exhibit the opposite pattern, Gall contended suchdifferences could not exist if memory constituted a unitary faculty [35, 36]. A few yearslater, physician Marie-Jean-Pierre Flourens investigated Gall’s controversial views oncerebral localization by removing anatomically defined areas of the brain of an animaland watching its behaviour. The results did not favour the idea of cerebral localizationand led him to conclude that the brain functioned as a whole and thus arose the conceptof cerebral equipotentiality [37, 38]. Much debate ensued, due to the fact that hisexperiments were mainly on birds, and the techniques used were considered imperfect.In contrast, French philosopher Maine de Biran published in 1804 a remarkableattempt to organize human memory within a taxonomic construct, distinguishingseparate memory systems instead of a single unity: representative memory, that is theconscious recall of facts and events, mechanical memory, responsible for learning ofhabits 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, anumber of very important observations were made. The distinction between memoryand habit, which led him to write separate chapters on both. Besides the distinction ofhabit, James also postulated two other different kinds of memory, establishing thedifference between primary and secondary memory, which could be interpreted as ananticipation of the modern distinctions of short term memory (STM) and long termmemory (LTM) [41, 42].Bergson’s reflections on memory in
Matter and Memory from 1896 also contributed4/36o the modern non unitary view of memory. The French philosopher proposeddistinctions between habit memory and episodic memories. For Bergson habit involvedrepetition, is effortless and, once formed, non-representational. Despite being nonrepresentational its effect percolates into the present and in part defines behavior. Incontrast, what he understood as episodic memories were representational, involved aunique non-repeatable event, and its recollection, requires an act of will which involvesan active letting go of the attachment to the present [43, 44]. In his 1949 work
TheConcept of Mind the English philosopher Gilbert Ryle also distinguished between twotypes of memory: knowing-that, a type of memory that does not directly inform actionbut is expressed through regulative propositions; and knowing-how, a type of executivememory that cannot be built up from pieces of knowing-that and is actualized throughenactment [45]. These suggestive approaches to the nature and organization of memoryand the subjective experience of recollection may be considered as the most influentialin Western philosophy of the twentieth century.While these are seen as the earliest attempts in the study of memory, what wasdemanded in order to fully understand its nature and organization was not onlyphilosophical discourse or psychological intuition, but experimental inquiry.In a major contribution in the study of memory, the psychologist HermannEbbinghaus published in 1885 [46] a pioneering experimental and quantitative treatmentof memory, displaying new ideas and methods for rigorous and systematic controlledexperiments on memory, that have had an enduring influence throughout the twentiethcentury of memory research. A revolutionary concept in ¨Uber das Ged¨achtnis was theidea that memory research was not deemed to be the investigation of pre existingmemories but that memory contents to be tested needed to be created and modified inthe laboratory as an integral part of the experimental procedure [46, 47]. Ebbinghausinvented the paradigm of the nonsense syllable as learning materials of homogenousdifficulty beyond the familiarity of words and prose. This notion defined a task in whicha multitude of variables can be defined and their influences on remembering behaviorsobserved. He used strict controls on the timing and number of study trials, allowed timefor recall, and retention interval, and measured the difficulty of learning a list by thenumber of study trials required to attain one correct recall. Moreover, Ebbinghausintroduced the idea of measurable degrees of learning by noting the savings in relearninga list he had learned earlier. Using this measure Ebbinghaus was able to devise hisfamous forgetting curve relating percent savings to retention interval. [48, 49].Even in Ebbinghaus’ earliest experiments it was clear that learning depended greatlyon the nature of the content, whether numbers, nonsense syllables, words, meaningfulsentences or poetry, as these vary greatly in their familiarity and meaningfulness tosubjects. By studying isolated variables, Ebbinghaus was able to observe the influenceof the different types of learnt contents on memory performance, as well as the mode oftheir presentation, and the strategies subjects used in learning them. The memoriesestablished can then be tested by direct measurement of recall, recognition andreconstruction, or by a variety of indirect measures. Ebbinghaus’ experimentalframework set the foundations for the modern era of memory studies, and remains theprototype for its research almost 150 years after.At the dawn of the twentieth century, two relevant contributions to theunderstanding of memory were presented in relation to the study of reflexes. TheRussian neurologist and anatomist Vladimir Mikhailovich Bekhterev presented
Pathways of brain and bone marrow in 1900, exposing an association of memory withthe hippocampus based on the study of amnesia in patients with hippocampaldegeneration. 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 nervoussystem and developed a theory of conditioned reflexes which describe automatic 5/36esponses to the environment called association reflex [50, 51].Similarly, the scientific mainstream of behaviorism, with its main exponentsThorndike, Pavlov, Watson and Skinner, held that all learning is the attachment ofresponses to stimuli [52]. Therefore they studied the characteristics and components ofa particular type of learning: that which is derived from repeated association between astimulus and a response,named classical conditioning, and that which is derived fromassociation 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 associativememory, while Fitts and Posner’s studies [54] are considered the first aiming to explainprocedural memory. It may be argued that the knowledge on memory produced bythese experimental works of behaviorism was among the most important in the earlydays of twentieth century.Guided by the then prevalent and straightforward view that stimulus-responselearning is supported by connections between sensory areas in the posterior corticalareas and motor areas in the frontal cortex, Karl Lashley’s conducted pioneering effortsin the search for engrams [55]. Engrams were viewed as fundamental to theunderstanding of memory, as the physical structures in which memory traces werestored. Using maze learning in rats he aimed to map the cortical areas and pathwaysthat support memory formation. As the search proved unsuccessful, Lashley subscribedFlourens’ view on the indivisible brain, meaning that there were no localizations ofmemory in different parts of the brain [56]. He concluded that the memory trace waswidely distributed both within cortical areas and throughout the cortex and that any ofthe neurons within cortical areas could support the engram, naming this principle equipotentiality . Also contributed the notion that involved brain areas acted together tosupport the engram, naming this principle mass action [57].Later in 1934 Donald Hebb, student of Lashley, followed the interest in how thebrain gets organized to generate abilities such as memory. His 1949 work
TheOrganization of Behavior presented cell assemblies and the connection between cellsthat fire together, advancing studies of memory consolidation [58, 59]. The dual-trace hypothesis of memory subsequently proposed by Hebb in 1949 offered a specificphysiological theory of memory consolidation. According to Hebb’s hypothesis, neuralactivity initiated by an experience persists in the form of reverberating activity inneural circuits of STM, and that the formation of LTM means the stabilization of thesecircuits leading to permanent synaptic change [60].During the following decades, as psychology struggled to assert itself as a scientificdiscipline, a large wealth of knowledge about memory was supported on an increasingnumber of experimental studies. The work of Edward Tolman distinguishes from manyof his behaviorist contemporaries on its focus on memory and behavior. Though Tolmanwas greatly influenced by Watson’s behaviorism, Tolman’s cognitive, anti-reductionistemphasis on purpose and macroscopic or molar behavior stood in stark contrast to manyof the learning theories of his contemporaries [61, 62]. The battle was sustained betweenthese two schools of thought, stimulus-response learning versus cognitive learning,specially at the level of animal behavior. Tolman proposed that there is more than onekind of learning in animals and humans. Unlike motor patterns, well understood bybehaviorists, other types of learning were postulated outside the stimuli-response logic.Importantly, a distinction between memory systems is rooted in this debate betweenplace-learning, a position advocated by Tolman [63], and response-learning, a positionadvocated by Hull who asserted that learning was a general process [64].Such behavioral findings suggested the potential co-existence of at least two distinctlearning systems. However they did not have the effect of shifting the debate concerninghow many memory systems there were. Other authors argued that these two kinds oflearning existed, but that they did not represent fundamentally different things, instead6/36hey are accountable by the use of different cues [65].A very important contribution of Tolman to the study of memory as set of dedicatedsystems was the
Cognitive Map theory, which provided deep insights into how animalsrepresent information about the world and how these representations inform behavior.Tolman developed this idea of a cognitive map as an alternative to the then-commonmetaphor of a central switchboard for learning and memory, typical ofstimulus-response formulations. According to this view, animals maintained a set ofcomplex, integrated expectancies or hypotheses of their world [66]. Tolman would latercall these complex integrated expectancies cognitive maps [63]. For Tolman, learning isacquiring expectancies, that is probability characteristics of the environment. Theorganism thus typically learns a cognitive map not a mere movement pattern. His laterwritings 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 storagecould not easily be separated from one another neurobiologically, the theory of thecognitive map was embodied within a multiple memory systems perspective.Importantly, it claimed that the brain memory systems differed based on the nature ofthe contents of the memories they processed, and not only based the length of time thatmemory storage was supported. As such, this view critically differed from the moretraditional perspectives of cognitive psychology and cognitive neuropsychology prevalenta the time which saw systems as differing primarily in terms of how long informationremained 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 thatrender memory systems distinct were settled. First, the distinct memory systems mightbe computationally different at their circuitry level in order to be efficient, a notionlater developed by Sherry and Shacter’s theory of functional incompatibility [16]. Fodoralso addresses the notion of modularity [69], understood as separate domain specificmodules that handle certain sort of contents. The functionalities of these modules arehardwired and not acquired through learning processes. Second, systems might differ interms of the length of time during which information is to be stored within them, whichcan require different underlying mechanisms. Beyond the study of animals, these twonon mutually exclusive approaches to memory systems were further expanded tohumans in the study of focal cerebral damage.Since the 1950’s Scoville, Penfield, Hebb and Milner, documented the effects ofsurgical lesions of temporal lobe on human declarative memory, finding severeanterograde amnesia and retrograde amnesia with temporal gradient [70–75]. A wellknown case of study was that of the severe epileptic patient Henri Molaison (H.M.) whoin 1953 underwent surgical removal of brain structures in the MTL (MTL) including thehippocampus to cure him of his epileptic seizures. As a result of this surgery, H.M. wasprofoundly impaired in the acquisition of certain forms of information. He becameunable 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. Whileother cognitive functions remained intact, H.M.’s experience was greatly influenced by apermanent 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 unableif distracted or when the amount of material to be remembered exceeded what can beheld in immediate memory.Early evidence from H.M’s case supported the mainstream view that memory iscomposed 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 theconsolidation of the LTM system [76].Subsequently, Milner reported that H.M. could learn and perform new sensorimotor7/36asks. 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 – eyecoordination skill, namely mirror drawing, over a period of 3 days even withoutawareness of having been previously trained or tested [77]. This selectivity of H.M.’samnesia related to the type of learned activity or content, suggested the existence oftwo distinct forms of memory corresponding to each type of material: declarativememory and procedural memory. It was presumed that these systems were dependanton separate neural systems, and that by lesion or degenerative processes, amnesiacpatients were only disabled in their declarative memory functions [78–80].These findings contrasted with prevailing views at the time by linking a memorydisturbance to damage to a specific part of the brain. However these theories wereattempted in animal models, namely monkeys and rats, leading to no amnesia, thusdiscussions and uncertainties about a content based organization of memory systemsensued for several years [81–84].In the following sections an account is provided regarding these two kinds oftaxonomies and a brief review of the relations and differences between memory systems.
The 60’s saw a growing interest in developing mathematical models of learning andmemory. Despite that the mainstream view accepted only one global memory systemresponsible for handling many kinds of information, this assumption did allow animplicit division of memory in memory systems which differed in terms of their capacityto store contents within them.In the previous section, a review on the historical evolution showed that allusions tomemory taxonomies based on time persistence had been present for several centuries,despite the apparent triviality of its insight on how memory is organized. One possiblecatalyst for the emergent importance of this perspective during the early 60’s, was theinfluence of the computer revolution which may have served as inspiration for thinkingabout memory from an information processing approach.In its most influential consolidation, Atkinson and Shiffrin [85] settled in 1968 amodel of human memory divided into three classes, ultra short-term memory, STM, andLTM, which became known as the multi store or modal model of memory. In additionto identifying the three different memory types, Atkinson and Shiffrin also suggestedthat they stand in a rather fixed relationship to one another. They proposed that storedinformation is processed sequentially entering the brain through the sensory system intoultra-short-term, passes through STM and ends up in LTM. This processing chain canterminate 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 inspiredby an information processing approach, in which systems differed in terms of duration,processing and storing information for varying periods of time. .1 Ultra short term memory
According to this model, Ultra short term memory, or sensory memory, makesinstantaneous sensory information available for processing for less than 120milliseconds [86]. This kind of memory is specific to a particular sensory system anddoes not appear to be shared across sensory systems. In the visual system, ultra shortterm memory is the reason, why, for example, apparent continuous motion is perceivedwhen watching a movie instead of 24 individual frames per second.Authors have suggested that ultra short term memory is limited to only a fewhundred milliseconds in duration because the memory traces decay naturally [85]. Dueto this timescale this form of memory would operate outside of awareness, and since it isentirely 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 thesensory system rather than a memory system.
In the late 50’s the consolidation of the notion of a STM system began with theempirical support which observed that, provided the prevention of active rehearsal, evensmall amounts of information showed rapid forgetting [87, 88]. The pattern of memorydecay appeared to differ from that observed in standard LTM experiments, which led tothe view that performance depended on a separate short term store. It was thenthought that STM operated as a crucial antechamber of LTM storage.During the 60s, methods were developed for studying visual perception and motorresponses with single-cell recordings from awake, behaving monkeys performing a classicdelayed response task, which requires holding information in memory for a brief period.This work identified cells in prefrontal cortex that were maximally active during thedelay portion of the task of 15 to 60 seconds [85, 89–91].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 LTMas a function of its maintenance on short term system. A number of studiesdemonstrated that active verbal rehearsal was not linked to durable LTM [92]. Thisargument gave way to the theory called levels of memory [93]. This theory proposedthat an item in order to be remembered, for instance a word on a page, could beprocessed at a series of encoding levels which started with the visual appearance of theitem, its sound when pronounced, and later its meaning and relationships with otherrelated memory experiences. A second challenge was provided by the neuropsychologicalevidence of patients with an STM deficit while preserving LTM intact. The thenprevalent STM model failed to provide explanation for this phenomena, as it arguedthat poor performance of STM should have also led to impaired LTM capacity. Thesechallenges led researchers to reformulate the STM hypothesis and postulate amulticomponent system which was termed working memory.Working memory refers to the capacity to maintain temporarily a limited amount ofinformation in mind, which can then be used to support various abilities, includinglearning, reasoning, and preparation for action [8]. It is generally acknowledged thatworking memory can store information for up to 20 seconds, and according to someexperimental studies its maximum capacity is four chunks of information [94]. Despiteits acquisition being without a conscious effort, working or short-term memory can becontrolled consciously and is less dependent on sensory inputs than ultra-short-termmemory. Most importantly, through rehearsal, the spontaneous decay of workingmemory may be prevented.According to Baddeley and his tripartite model [9, 95] working memory is comprisedby the phonological loop, which support retrieval temporary storage and rehearse of9/36honological material, the visuospatial sketchpad to perform maintenance of visualrepresentation of stimuli and their position in space [8, 9], and a central executive subsystem which is a limited capacity supervisory attentional system [96] that orchestratesand mediates the manipulation of contents from visuospatial and phonological subsystems. However, there is evidence indicating that spatial and object working memorymay be separable [95]. Single cell recording studies in nonhuman primates have revealeddifferent activations in ventral and dorsal prefontal cortex during object workingmemory performance for the first and spatial working memory performance for thelatter.In 2000 Baddeley included in this model the episodic buffer involved in linkinginformation across domains to form integrated units of visual, spatial, and verbalinformation with episodic chronological ordering. This episodic buffer is also assumed tohave links to LTM and semantic meaning. The working memory model currentlyconsists of four elements that process information: the central executive for attentioncontrol; the visuospatial sketchpad, which creates and maintains a visuospatialrepresentation; the phonological buffer, which stores and consolidates new words; andthe episodic buffer which stores and integrates information from different sources [10].
Figure 2.
The year 2000 version of the multi-component working memory model accordingto Baddeley which includes the episodic buffer. The episodic buffer is interpreted to becontrolled by the central executive, and it is capable of multi-dimensional informationstorage, providing a temporary interface between the phonological loop, the visuospatialsketchpad and long term memory (LTM). The buffer serves as a modelling space that isseparate 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-termknowledge, and unshaded areas represent fluid capacities such as attention and temporarystorage.
Working memory is therefore central to the ability to select and implementgoal-directed behavior, to exercise what are termed executive functions. Indeed, recentdiscussions emphasize a broad role of prefrontal cortex in cognitive control, an idea thatimplies top-down influences from prefrontal cortex that direct attention and organizeaction [97, 98]. The prefrontal cortex allows memory to be accessed strategically, and itorchestrates the use of learned rules so that knowledge relevant to current goals can bebrought to mind and put to flexible use.
Assumed as a group of systems responsible for the capacity to store information overlong periods of time [99]. LTM differs from STM in that the memory contents would nolonger be vulnerable to spontaneous decay, nonetheless, some memories may beforgotten due to interference from memories that are stored later. Another keydifference to short-term memory is that subjects recall these items not in isolation, butincluding the relationships between them, and the spatiotemporal context in which they10/36re embedded. This makes LTM singular due to its larger capacity for the storage ofarbitrary combinations of different kinds of information [100].Analysis indicates that the hippocampus and associated structures of the MTL serveto generate LTM traces. Clinical evidence indicates that damage to the hippocampusproduces anterograde amnesia. At the cellular-molecular level, the intricacies ofsynaptic plasticity, a candidate model for memory storage, are being studied in greatdetail [101], however, the link between single neuron computation and computation atthe network level is poorly understood. It remains unclear how neuronal cooperativityin intact networks relates to memories or how network activity in the behaving animalbrings about synaptic modification [102].In recent years, psychologists have gathered numerous pieces of evidence for the viewthat our memories are in fact constructions of what happened in the past. Memories arestored in the brain in a distributed pattern in the outer layer of the cortex, related tothe area of the brain that initially processed them [99]. In this view, a visual aspect ofan experience is normally stored in the visual cortex, an auditory aspect of anexperience is stored in the auditory cortex, and a motion element of an experience isstored in the sensory motor cortex. When a memory is retrieved, all its fragments areput back together rarely identical to the initial experience [103].In past decades, little thought was given to the possibility that there might be someconstraint on the kind of information these memory systems could handle or the rules bywhich they operate. Over the years, several aspects of Atkinson and Shiffrin’s taxonomyhave been questioned. The main criticisms can be divided into two classes. First, theirtaxonomy artificially splits memories of the same kind into different taxa. Severalauthors have proposed that STM and LTM are instances of the same unitary memorythat happen to have different properties. Second, Atkinson and Shiffrin associatetogether disparate kinds of memories into a single system. Furthermore, The dominantview of a single memory system prevented the selective nature of amnesia from beingsystematically explored for several decades. For the most part neuropsychologistsworking with human subjects accepted the single system premise and the view thatdamage to the brain to varying degrees accounted for the global amnesia observed insubjects with various etiologies [104, 105]. Despite these controversies, Atkinson andShiffrin’s taxonomy has been one of the most influential taxonomies of memory.Advances in neurobiology and behavioral neuroscience contributed to modify thisapproach. 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 differenttasks to measure different specialized functionalities. Perceptual memory orrepresentation systems are an example of this broadening [106]. Phenomena like objectpriming or fragment completion, added to the view that processing and memory storageoccur in the same circuits has emerged from the neurobiological literature. [107–109].Importantly, the discovery of the declarative memory systems with the view that thehippocampus has a selective role in learning, began in the late 60s and took more than20 years to unfold.
The first observations of H.M., and the results of formal testing, were reported in 1957by Scoville and Milner [73] in a seminal paper that shed light on three fundamentalprinciples: a) memory is a distinct brain function, separable from general cognitive andlanguage functions; b) the MTL is not necessary for immediate memory since this waslargely normal in H.M; and c) MTL structures are not the final storage location formemories, since although the removal of these structures showed severe amnesia inH.M., the patient still retained large portions of memories of his childhood [110]. This11/36ublication became one of the most cited papers in neuroscience and is still frequentlycited.Importantly, subsequent findings from H.M. established that memory was not amonolithic system that handles all types of information, but a highly interconnected setof systems. Due to the the fact that H.M. and other amnesic patients demonstratedintact learning and retention of certain motor, perceptual and cognitive skills, memorywas thought to be comprised of at least two separate systems and that only one kind ofmemory, declarative memory, is impaired in amnesia [77, 79, 111, 112].Nevertheless, patients with hippocampal damage typically have a normal vocabulary,and their general knowledge of facts remains intact. Interestingly, the opposite patternof 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 ofwords and knowledge about world facts is greatly impaired [113].
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 frommultiple processing sources. It supports the encoding of memories in terms ofrelationships among multiple items and events. Declarative memory allows rememberedmaterial to be compared and contrasted. The stored representations are flexible and canguide performance under a wide range of test conditions [114]. A key characteristic isthat declarative memory is explicit and accessible to conscious awareness. That is, itmay be brought to mind verbally as a proposition, or non verbally as animage [13, 99, 115, 116].It is widely accepted that declarative memory has two major components: semanticmemory, responsible for processing facts about the world; and episodic memory, theability 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 inmemory extend to both verbal and nonverbal material, and involve informationacquired through all sensory modalities. Other etiologies of amnesia have alsocontributed useful data to support theories on declarative memory, includingencephalitis, anoxia and ischemia, Korsakoff’s syndrome, and psychiatric patients whosememories were impaired as a result of electroconvulsive therapy [117, 118].Several theories regarding the role of the hippocampus in memory have beenproposed over the years. All regard the hippocampus as being critical for episodicmemory, but there are key differences in whether they view the hippocampus as havinga time limited role in episodic memory and in whether they deem it to be necessary forthe acquisition of non-contextual information. The pattern of spared and impairedcognitive processes in patients with hippocampal damage, combined with results fromanimal models of amnesia, has lead to the
Declarative Theory of hippocampalfunction [119]. Some researchers have focused on building a neural level understandingof hippocampal function in a specific cognitive domain such as the theory of the
Cognitive Map [5]. While others have sought more specific characterizations ofhippocampal function, drawing on experimental data from animals and humans withthe
Multiple Trace Theory [120], the
Dual Process Theory [121], and the
RelationalTheory [122].In addition to MTL structures the acquisition of episodic memory requires theinvolvement of other brain systems, especially the frontal lobes [123–127].A number of considerations suggest that the capacity for declarative knowledge isphylogenetically recent, reaching its greatest development in mammals with the fullelaboration of medial temporal structures, especially the hippocampal formation and12/36ssociated cortical areas. This capacity allows an animal to record and access theparticular encounters that led to behavioral change. The stored memory is flexible andaccessible to all modalities [128].The declarative memory system has a distinct developmental evolution throughindividual’s lifetime. In most species hippocampus is not fully developed at birth andprocessess of neurogenesis are constant throughout life in some cases [129]. In humansthe hippocampus and related structures incur in a dramatic size change in the first twoyears of life, enabling the memory function after 18 to 24 months, and only reaching fulladult function after reaching 10 to 12 years of age. As such, phenomena such asinfantile amnesia defined as the inability to form episodic memory early in life isstarting to be understood [130–132]. Similarly, in spatial navigation tasks, childrenyounger than two years old fail at distal cue use in navigation, as it requires a fullyfunctioning hippocampus [128, 133, 134].
Tulving proposed the distinction between Episodic and semantic memory as two typesof declarative memory subsystems. Both types of memory are declarative due to thefact that retrieval of episodic and semantic information may be carried out explicitlyand subjects are aware that stored information is being accessed [3, 4, 135]. Thisdistinction 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 thecognitive neuroscience of memory.Of particular interest has been the extent to which semantic and episodic memoryhave a shared dependence on the hippocampus. In contrast to the definitive evidencefor the link between hippocampus and episodic memory, the role of the hippocampus insemantic memory has been a topic of considerable debate. Amnesic patients do havegreat difficulty acquiring semantic knowledge, but they can typically succeed to someextent after much repetition [136, 137]. In Tulving’s work on the severely amnesicpatient K.C., he reports how eventually the patient learned to complete arbitrarythree-word sentences during a large number of training trials distributed over manymonths despite the absence of any memory at all for training episodes [138]. Episodicmemory can be virtually absent in some severely amnesic patients who can stillaccomplish some semantic learning.The key structures that support declarative memory are the hippocampus and theMTL adjacent structures, such as entorhinal, perirhinal, and parahippocampal cortices,which make up much of the parahippocampal gyrus [115]. These structures areorganized hierarchically, and their anatomy suggests how the structures mightcontribute differently to the formation of declarative memory, for example, in theencoding of objects in perirhinal cortex, or scenes in parahippocampal cortex, and inthe forming of associations between them in the hippocampus [139–141].One interpretation is that both episodic and semantic memory depend on the brainsystem damaged in amnesia, the hippocampus and MTL related structures, and thatepisodic memory additionally depends on the integrity of the frontal lobes. Patientswith frontal lobe damage, who are not amnesic, exhibit a phenomenon termed sourceamnesia which refers to loss of information about when and where a remembered itemwas acquired [142, 143]. In this sense, source amnesia appears to reflect a loss of episodicmemory related to frontal lobe dysfunction, which in turn reflects a disconnectionbetween facts and their contexts. The greater contribution that frontal lobe functionmakes to episodic memory, compared to semantic memory, would give a 1biologicalsupport to the distinction between episodic memory and semantic memory [114].13/36n their infuential book
The Hippocampus as a Cognitive Map , O’Keefe and Nadelsuggested that the then recently discovered place cells found within the hippocampusprovided the neurobiological substrate of the
Cognitive Map [5]. Subsequentinvestigations of hippocampal place cell activity further developed the notion of thehippocampus mediating place information and the functions of such data coordinationbeyond spatial domains [144].
Episodic memory was conceived by Tulving [3], at a time when information processingmodels dominated. Episodic memory refers to autobiographical memory for events in itswhen, what and how components, linked together in a coherent spatial and temporalcontext. This includes the spatiotemporal relations between events. A key feature ofepisodic memory is its unique role to allow the individual to mentally travel back intoher 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 [147–151].Episodic memory is affected by aging processes [152], and there have been findings ofsex differences in its performance [153, 154], but results are still inconclusive [155].It has been suggested that episodic memory in the hippocampus is formed bycombining spatial information from the medial entorhinal cortex [156, 157] with nonspatial information from the lateral entorhinal cortex [158, 159]. A number of imagingstudies have revealed evidence linking MTL activation with episodic encoding. MTLactivation has been observed under conditions in which exposure to novel stimulusmaterials is compared with exposure to familiar materials. Imaging studies have alsoilluminated the contributions of distinct prefrontal regions to encoding andretrieval [160–162].Recent studies have helped to establish that these neural systems also support thecapacity to imagine and to simulate episodes expected to occurr in thefuture [4, 145, 163, 164]. The ability to pre experience future events has been referred bysome authors as prospection [165] and by others as episodic future thinking [166–168].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 largebilateral hippocampal lesions which caused a remarkable case of memoryimpairment [109, 138, 169]. K. C. was unable to provide a description of his personalfuture 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 thinkabout the past [109, 170]. A later investigation in another patient, D. B., who becameamnesic 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 documentedbilateral hippocampal amnesia to imagine new experiences, such as being at a desiredlocation in an ideal situation [151]. Based on the content, spatial coherence andsubjective qualities of the participants’ imagined scenarios, the ability to imagine of thesubjects with hippocampal lesions was greatly reduced in richness and content.Due to the fact that hippocampal amnesics have difficulty imagining newexperiences, Hassabis concluded that the hippocampus plays a key role in recombiningdetails of previous experiences into a coherent new imagined construction.This interpretation that hippocampus mediates both future episode thinking andimagination, assumes that the episodic memory is constructive rather than areproductive system. Since the future is not an exact repetition of the past, it requires asystem that can draw on the past to flexibly extract and recombine elements of previousexperiences. In this view, fundamental features of a memory are distributed widely14/36cross different parts of the brain [139]. Therefore, retrieval of a past experienceinvolves a process of pattern completion, in which the process of recall pieces togethersome subset of distributed features that comprise a particular past experience [172, 173].Consistent with this approach, neuroimaging studies focused on the brain activityduring the construction of past and future events, have revealed regions exhibitingcommon activity, which included the left portion of the hippocampus and the rightoccipital gyrus, especially during the elaboration phase, when participants are focusedon generating details about the remembered or imagined event [174, 175].
Tulving postulated that semantic memory consists of a mental thesaurus encompassinga wide range of organized information including facts, concepts and vocabularynecessary for language [4, 135]. Semantic memory can be distinguished from episodicmemory by virtue of its lack of association with spatiotemporal contexts [1], and doesnot require subjective reexperiencing of the episode in which the knowledge wasacquired. These systems differed as well in terms of the conditions and consequences ofretrieval. Unlike episodic memory, retrieval from semantic memory was thought to leaveits contents unaltered and to provide new input into episodic memory. Retrieval fromepisodic 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 interms of recording and maintaining information, episodic memory could be stronglyinfluenced by, and depend on, information in semantic memory at encoding [176].Originally, Tulving viewed episodic and semantic memory as two functionallyseparate systems, but he also emphasized the features shared between them and theirclose interaction. For example, retention of information in both systems was thought tobe automatic, because it did not require ongoing effort; for both systems, retrieval ofinformation could be prompted by highly relevant cues or questions, even if the retrievalprocess itself is outside of awareness. Personal semantic memory, that is semanticknowledge that relates to the self, represents another common area of semantic andepisodic 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 temporalneocortex and ventrolateral pre frontal cortex [179–181]. Imaging studies have suggestedthat the semantic attributes of a stimulus are stored near the cortical regions thatunderlie perception of those attributes, while have also highlighted that retrieval fromsemantic memory and encoding into episodic memory share underlying componentprocesses [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 mem-ory was not yet fully understood, compelling evidence pointed at distinct specializedcomponents of memory outside of the episodic and semantic domains. .3 Non declarative memory
There were early suggestions in the animal literature that more than just motor skillswere intact after lesions of hippocampus or related structures [5, 183, 184]. However,these proposals greatly differed from each other, and they came at a time when thefindings in experimental animals was not in agreement with findings from humanamnesia and memory [78, 112].Evidences of the extent of non declarative systems in humans came from the task ofreading mirror-reversed words [111], a perceptual skill which amnesic patients acquiredat a normal rate despite poor memory for the words that they read. Thus, perceptualskills, not just motor skills, were intact. Later, amnesiac patients with the ability toresolve stereoscopic images [185], learning of an artificial grammar [186], and learning ofnew categories of items [187]. The accumulating data led to further arguments about theextent and nature of what is not included in the notion of declarative memory [105, 112].The notion of procedural memory was originally devised to contrast with declarativememory [111, 188]. Whereas this notion appropriately describes a wide variety ofskill-based kinds of learning, certain memory phenomena were clearly not declarative,but also not well accommodated by the notion of procedural memory. Subsequently, theconcept of non declarative memory emerged as an umbrella which would cover humanmemory capacities that support skill and habit learning, perceptual priming, and otherforms of behavior, which are expressed through performance rather thanrecollection [189]. For example procedural skills, such as knowing how to ride a bicycle,are expressed through performance in riding a bicycle; priming memory, whichunderpins our ability to recognize words and other perceptual skills, is accessedimplicitly as it is performed. Non declarative memory is neither true nor false, does notrequire conscious reflection on the past, or event knowledge that memories are beingformed by past events. Non declarative memory is shaped by experience, but unlikedeclarative memory which is flexible and can guide behavior in multiple contexts, theacquired knowledge in non declarative memory is thought to be rigidly organized [99].Authors have suggested that non declarative memory is phylogenetically old. andthat it may have developed as a set of special purpose learning abilities. Memoryformation is then thought as the result of cumulative changes stored within theparticular neural systems engaged during learning [114]. Most non declarative memoryfunctions are present at the onset of human life, few age-related improvements havebeen found from 3 months on, and evidences have highlighted that these systems remainstable since the 9th month of life [190–192]. The idea that non declarative memoryremains stable as age progresses has come to be widely accepted. For instance, severalstudies of priming in normal aging have not reported significant decline, whilecross-sectional studies employing a range of different tasks have reportednon-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 olderindividuals, and some have argued that these inconclusive results need to be furthersubstantiated [195].
Neuroimaging studies have led researchers to attempt establishing the main neuralstructures identified in relation to current non declarative systems. For example, thestriatum has been linked to memory of skills and habits, and active sections of theneocortex have been related to priming. Classical conditioning of skeletal musculaturehas an essential dependence on the cerebellum, while emotional conditioning has beencorrelated to activation of the amygdala [2, 114].It is debated to this day the role of the hippocampus and related structures in non16/36eclarative learning. One proposal is that, whereas conscious recollection depends onthe hippocampus, it is also important for unconscious memory under somecircumstances [196, 197]. Other work, based on functional magnetic resonance imaging(fMRI), has implicated MTL structures in the unaware learning of sequences and othertasks with complex contingencies [198, 199]. Considering that fMRI data cannotestablish a necessary role for a particular structure, this remains a debated topic.The role of non declarative memory system in supporting syntactic processing is alsostill unclear. In studies with patients with Korsakoff’s syndrome who display deficits inall subdomains of declarative memory, yet their non declarative memory remains intact,patients showed robust syntactic priming effects, the phenomenon in which participantsadopt the linguistic behaviour of their partner [200].
Study of nondeclarative memory began with motor skills and perceptual skills. The bestunderstood example of nondeclarative memory in vertebrates is classical conditioning ofthe eyeblink response, specifically delay eyeblink conditioning. In delay conditioning, aneutral conditioned stimulus (CS), such as a tone, is presented just before anunconditioned stimulus (US), such as an airpuff to the eye. The essential memory tracefor the conditioned eyeblink response and other discrete conditioned motor responseswas discovered is formed and stored in the cerebellar interpositus nucleus [201].Critically, delay eyeblink conditioning is intact in amnesia and is acquired independentlyof awareness [202, 203]. Largely on the basis of work with rabbits, delay eyeblinkconditioning proved to depend on the cerebellum and associated brain stem circuitry.Forebrain structures are not necessary for acquisition or retention of classicallyconditioned eyeblink responses. These discoveries are on of the most successfulexamples of localizing a memory trace within the vertebrate brain [204].
The next of these to come under study was the phenomenon of priming. Priming wasdefined as the improvement in the ability to to detect or classify a stimulus as the resultof a recent encounter with the same or a related stimulus [205, 206].Evidence for the distinct priming phenomenon came from both normal subjects andamnesic patients that perform normally when tests are structured using non memorykind of instructions [108, 205, 206]. For example, amnesic patients often performed wellwhen they were given three-letter word stems as cues for previously presented words,event without recognizing the stimuli as having been presented before. Withconventional memory instructions (use each cue to help in remembering a recentlypresented word), healthy subjects outperformed the patients [207]. Thus, it becameevident that priming is an unconscious memory phenomenon and is entirelyindependent 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 sensorymodality 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 stimulithat are encountered once are likely to be encountered again. Perceptual priming wouldresult advantageous as improves the speed and fluency by which organisms interact withfamiliar stimuli. For example, in the case of visual priming, the posterior visual cortexbecomes more efficient at processing precisely those stimuli that have been processedrecently. This plasticity occurs well before information reaches the limbic structuresimportant for declarative memory [163]. 17/36vidence of independence of the phenomena of priming and the type of memoryimpaired in amnesia was reproduced by the studies of perceptual priming [208, 209], andconceptual priming [210]. These works showed that severely amnesic patients canexhibit fully intact priming while performing at chance on conventional recognitionmemory tests for the same test items.
Emotional conditioning is understood as system of non declarative memory that isresponsible for the assessment whether an encountered stimulus has positive or negativevalue. In humans, associative fear learning proceeded normally after hippocampallesions, even though the CS – US pairings could not be reported [211]. It has beenshown that the amygdala has a critical role in fear learning, and its function andconnectivity appears to be conserved widely across species. In human neuroimagingstudies, the amygdala was activated not only by fear but by strongly positive emotionsas well [212].The biological study of fear learning and its reversal, for instance fear extinction hasconsiderable relevance for clinical disorders such as phobias, post-traumatic stressdisorder, and other anxiety disorders [213].In addition to its importance for emotional learning, the amygdala also exerts animportant modulatory influence on both declarative and non declarativememory [214, 215]. Thus, activity in the amygdala, and the effect of this activity onother structures, is responsible for the fact that emotionally arousing events are typicallyremembered better than emotionally neutral events. The importance of the amygdalafor modulating memory has also been demonstrated with neuroimaging. Volunteersrated the arousing effects of either neutral scenes or emotionally distressing scenes andthen took a memory test for the scenes two weeks later [216]. Increased activity in theamygdala at the time of learning was associated with higher arousal ratings for thescenes and improved accuracy on the later memory test. Interestingly, this effectoccurred in the left amygdala for women and in the right amygdala for men [217].
One important discovery in the 1980s was that the gradual trial-and-error learning thatleads to the formation of habits was supported by the striatum [6, 218, 219]. Habitmemory is characterized by automatized, repetitive behavior and, unlike declarativememory, is insensitive to changes in reward value [220]. Tasks that assess habit learningare often structured so that explicit memorization is not useful, and individuals mustdepend more on intuition. In this learning, what is presumably acquired is a set ofdispositions to perform a task in a particular way, and not factual knowledge about theworld. Unlike declarative memory, which is flexible and can guide behavior in differentcontexts, the acquired knowledge in this case is rigidly organized. Habit memorysubsequently became an important focus of study [221].The difference between declarative memory and habit memory was shown formemory-impaired patients with hippocampal lesions and patients with Parkinson’sdisease [219]. Amnesic patients can acquire a variety of skills at an entirely normal rate.These include motor skills [222], perceptual and motor skills [111, 223], and cognitiveskills [224].Currently is known, striatal neuronal plasticity enables basal ganglia circuits tointeract with other structures and thereby contribute to the processing of proceduralmemory [225]. The cerebellum is involved in the execution of movements and theperfection of motor agility needed procedural skills. Damage to this area can impedeone from relearning motor skills and recent studies have linked it to the process of18/36utomating unconscious skills during the learning phase [226]. The limbic system sharesanatomical structures with a component of the striatum, which assumes primaryresponsibility for the control of procedural memory. Reward-based learning of this kinddepends on dopamine neurons in the midbrain, which project to the striatum and signalthe information value of the reward. The dorsolateral striatum is crucial for thedevelopment of habits in coordination with other brain regions while together with theinfralimbic cortex appear to work together to support a fully formed habit [227].
Non associative memory is understood as a robust form of behavioral memory, based onnewly learned behavior through repeated exposure to an isolated stimulus. This form ofmemory is developed even in invertebrate animals who do not have a capacity fordeclarative memory. It differs from associative learning in that it does not require thetemporal pairing between two different sensory stimuli or between a sensory stimulusand corresponding response feedback [228, 229]. There are two well known types ofnon-associative learning: habituation and sensitization. Habituation is a decrease inresponse to a benign stimulus when the stimulus is presented repeatedly, whilesensitization describes an augmentation of the response. Habituation is thought to berelated to a decrease in the efficiency of synaptic transmission, which may be caused bya conductivity change in the membrane of the stimulated neuron. In turn, the processof sensitization may be due to a provision in transmission, whether it may bepresynaptic or postsynaptic [230].A well understood and simple form of non associative memory is olfactoryhabituation, in which responsiveness to stable but behaviorally non significant stimuli isdecreased in relation to exposition [231, 232].
In biology, a system is defined in terms of both structure and function. In itsapplication to the domain of memory, multiple memory systems is understood as the setof different neurocognitive structures whose physiological workings produced theintrospectively apprehensible and objectively identifiable consequences of learning andmemory. The various memory systems can be distinguished in terms of its brainmechanisms, the different kinds of information they process and the principles by whichthey operate [233].As it has been noted, early interpretations of memory assumed a unitary model thatcould be used in many different ways [234, 235]. However, in most of the history of thestudy of memory, dichotomous classifications of memory had been put to use, such asprocedural versus declarative [236], semantic and episodic [3, 4], habit andmemory [6, 7, 184], dispositional and representational [237], taxon versus locale [5].Although a minority, distinctions among three and even more memory systems havealso been put forward [170].One of the earliest references to memory systems appeared in a 1972 paper byTulving [3]. There were other less known efforts in favor of memory systems such as the1979 article by Warrington in which she discussed neuropsychological evidencesupporting a distinction between STM and LTM systems, and between two kinds ofLTM systems, namely event memory and semantic memory [238–240].In the early 1980s, the cerebellum was discovered to be essential for delay eyeblinkconditioning [241] a form of learning preserved both in animals with hippocampallesions [242] and in severely amnesic patients [202]. Then, the striatum was identified asimportant for the sort of gradual, feedback-guided learning that results in habit 19/36emory [6, 218]. A similar contrast between declarative memory and habit memory waslater 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 ofpositive or negative valence to a stimulus, as in fear conditioning or conditioned placepreference, have an essential dependence on the amygdala [243–245].Based on evidence from human studies, these and other models attempted toembrace the large amount that has been learned about neuroanatomy, the molecularand cellular biology of synaptic change, and the organization of brain systems. Workwith experimental animals, namely rats and monkeys without which a systematic studyof memory would have proved impossible, also supported the notion of multiple memorysystems.Given this wide variety of evidence related to memory phenomena and its supportingneural sustrates, in the mid 1980s the perspective abandoned an account of humanmemory 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 asan umbrella term referring to several memory systems supporting the wide panorama ofmemory 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 formof declarative and non declarative memory.
Sherry and Schacter approached the concept of memory systems from anevolutionary perspective, proposing that different systems evolve as special adaptationsof information storage and retrieval for specific and functionally incompatiblepurposes [16]. In their evolutionary view, Sherry and Shacter elaborate the idea offunctional incompatibility, examining components of this evolution such as naturalselection, heritable variation in memory, memory and reproductive success, andadaptive specialization [246]. The notion assumes that in order to solve differentenvironmental problems, the animal must make feasible different requirements of theinformation processing strategies, and that these different requirements can call fordistinct neural circuitries [148, 247].The memory systems of the mammalian brain operate independently and in parallelto support different behaviors. In some circumstances, memory systems are described asworking cooperatively to optimize behavior and in other circumstances are described asworking competitively. How they compete or substitute one for the other is a topic ofcurrent interest [248–250]. Packard demonstrated the parallel works of multiple memorysystems in rats [251].When the stratial caudate nucleus was inactive, the parallel memory systemsupported by the hippocampus was unmasked. A similar stance has been described in20/36umans performing a virtual navigation task that could be solved by either a spatial ornonspatial strategy [252]. As training progressed participants tended to shift to anonspatial strategy, then showing increased activity in the stratial caudate nucleus,which emerged as training progressed. Although many tasks can be acquired by morethan one memory system, other tasks strongly favor one system over another.Prefrontal cortex may be important in determining which memory system gains controlover behavior [253]. Several other factors increase the tendency to adopt one memorysystem over another, in this case, a striatal strategy. In this sense, relevant evidence hasbeen obtained from studies of stress [254], and aging [255]. Although many tasks can beacquired by more than one memory system, other tasks strongly favor one system overanother.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 inthe MTL early during learning [256]. When learning progressed, activity decreased inthe MTL, and activity increased in the striatum. Moreover, when the task was modifiedso as to encourage the use of declarative memory, less activity was observed in thestriatum and more activity was observed in the MTL.Using these notions of multiple memory systems, researchers were increasingly moreable to place theoretical speculation within a neurobiological framework, thus reaching amore accurate understanding and classification of memory.
Conclusion
The nature of memory and its organization has been central to discussion on memoryfor 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 nowwidely accepted and fundamental to the contemporary study of learning andmemory [1, 103, 139].The multiple memory systems framework is supported by an enormous amount ofdata learned in the past decades about neuroanatomy and cognitive neuroscience, and ithas been able to accommodate a large variety of empirical observations of memoryperformance. It seems justifiable to conceptualize that the various memory componentsof memory have distinct neural architectures and operational principles, and servedifferent domain-specific purposes. Despite these memory systems operateindependently and in parallel to support different behaviors, in some circumstances,memory systems may work cooperatively to optimize behavior and in othercircumstances work competitively. It is still debated, however, how to best characterizetheir mutual relations and interactions. It remains beyond the scope of this article toevaluate the strengths and weaknesses of all proposed distinctions between memorysystems.A relevant implication of the multiple memory systems framework is that thetherapeutic targets for various kinds of memory disorders would demand differentinterventions based on the known supporting neural architectures. Future investigationthat combine cognitive, neuropsychological and neuroimaging approaches will furtherour understanding of the relations among the systems that together constitute thefoundation of memory. Therefore, it is foreseeable that the notion of multiple memorysystems remains dynamic, and that new specifications of memory systems emerge in thefuture grounded on empirical evidence. 21/36 eferences
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