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autobiographical memory

The fallibility of human memory

I don't often talk about eyewitness testimony, but it's not because of the lack of research. It's a big field, with a lot of research done. When  I say I don't follow it because I regard the main finding as a done deal - eyewitness testimony is useless - that's not meant to denigrate the work being done. There is, clearly, a great deal of value in working out the exact parameters of human failures, and in working out how we can improve eyewitness testimony. I just arbitrarily decided to ignore this area of research until they'd sorted it all out! (I can't follow everything, I'm swamped as it is!)

Nevertheless, I do want to remark on a recent report in The Scientist, to the effect that a New Jersey court has decreed that all juries must be informed of the unreliability of eyewitness testimony. I want to raise a hearty cheer. I regard it as practically criminal that eyewitness testimony is given the weight it is. I think everyone should be taught, from a young age, that memory is completely unreliable. And, in particular, that the certainty you hold in any specific memory, and the vividness it has, are not nearly as good proofs of the accuracy of the memory as we tend to believe.

You may think a belief in the fallibility of memory would create an unpleasant state of uncertainty, but I believe it would bring about a useful decline in many individuals' dogmatic certainty, and encourage more empathy with other, fallible human beings.

You may ask how my emphasis on the fallibility of human memory squares with my frequent comments on the danger of believing that you have a bad memory or that your memory will inevitably get worse as you age. But believing in human fallibility is very different from believing you personally have a bad or deteriorating memory. You need to find a nice balance between these beliefs, and part of achieving that lies in understanding how memory works and what aspects are more reliable and which less. I hope my site helps you with that!

Event boundaries and working memory capacity

In a recent news report, I talked about how walking through doorways creates event boundaries, requiring us to update our awareness of current events and making information about the previous location less available. I commented that we should be aware of the consequences of event boundaries for our memory, and how these contextual factors are important elements of our filing system. I want to talk a bit more about that.

One of the hardest, and most important, things to understand about memory is how various types of memory relate to each other. Of course, the biggest problem here is that we don’t really know! But we do have a much greater understanding than we used to do, so let’s see if I can pull out some salient points and draw a useful picture.

Let’s start with episodic memory. Now episodic memory is sometimes called memory for events, and that is reasonable enough, but it perhaps gives an inaccurate impression because of the common usage of the term ‘event’. The fact is, everything you experience is an event, or to put it another way, a lifetime is one long event, broken into many many episodes.

Similarly, we break continuous events into segments. This was demonstrated in a study ten years ago, that found that when people watched movies of everyday events, such as making the bed or ironing a shirt, brain activity showed that the event was automatically parsed into smaller segments. Moreover, changes in brain activity were larger at large boundaries (that is, the boundaries of large, superordinate units) and smaller at small boundaries (the boundaries of small, subordinate units).

Indeed, following research showing the same phenomenon when people merely read about everyday activities, this is thought to reflect a more general disposition to impose a segmented structure on events and activities (“event structure perception”).

Event Segmentation Theory postulates that perceptual systems segment activity as a side effect of trying to predict what’s going to happen. Changes in the activity make prediction more difficult and cause errors. So these are the points when we update our memory representations to keep them effective.

Such changes cover a wide gamut, from changes in movement to changes in goals.

If you’ve been following my blog, the term ‘updating’ will hopefully bring to mind another type of memory — working memory. In my article How working memory works: What you need to know, I talked about the updating component of working memory at some length. I mentioned that updating may be the crucial component behind the strong correlation between working memory capacity and intelligence, and that updating deficits might underlie poor comprehension. I distinguished between three components of updating (retrieval; transformation; substitution), and how transformation was the most important for deciding how accurately and how quickly you can update your contents in working memory. And I discussed how the most important element in determining your working memory ‘capacity’ seems to be your ability to keep irrelevant information out of your memory codes.

So this event segmentation research suggests that working memory updating occurs at event boundaries. This means that information before the boundary becomes less accessible (hence the findings from the walking through doorways studies). But event boundaries relate not only to working memory (keeping yourself updated to what’s going on) but also to long-term storage (we’re back to episodic memory now). This is because those boundaries are encoded particularly strongly — they are anchors.

Event boundaries are beginnings and endings, and we have always known that beginnings and endings are better remembered than middles. In psychology this is known formally as the primacy and recency effects. In a list of ten words (that favorite subject of psychology experiments), the first two or three items and the last two or three items are the best remembered. The idea of event boundaries gives us a new perspective on this well-established phenomenon.

Studies of reading have shown that readers slow down at event boundaries, when they are hypothesized to construct a new mental model. Such boundaries occur when the action moves to a new place, or a new time, or new characters enter the action, or a new causal sequence is begun. The most important of these is changes in characters and their goals, and changes in time.

As I’ve mentioned before, goals are thought to play a major role (probably the major role) in organizing our memories, particularly activities. Goals produce hierarchies — any task can be divided into progressively smaller elements. Research suggests that higher-order events (coarse-grained, to use the terminology of temporal grains) and lower-order events (fine-grained) are sensitive to different features. For example, in movie studies, coarse-grained events were found to focus on objects, using more precise nouns and less precise verbs. Finer-grained events, on the other hand, focused on actions on those objects, using more precise verbs but less precise nouns.

The idea that these are separate tasks is supported by the finding of selective impairments of coarse-grained segmentation in patients with frontal lobe lesions and patients with schizophrenia.

While we automatically organize events hierarchically (even infants seem to be sensitive to hierarchical organization of behavior), that doesn’t mean our organization is always effortlessly optimal. It’s been found that we can learn new procedures more easily if the hierarchical structure is laid out explicitly — contrariwise, we can make it harder to learn a new procedure by describing or constructing the wrong structure.

Using these hierarchical structures helps us because it helps us use knowledge we already have in memory. We can co-op chunks of other events/activities and plug them in. (You can see how this relates to transfer — the more chunks a new activity shares with a familiar one, the more quickly you can learn it.)

Support for the idea that event boundaries serve as anchors comes from several studies. For example, when people watched feature films with or without commercials, their recall of the film was better when there were no commercials or the commercials occurred at event boundaries. Similarly, when people watched movies of everyday events with or without bits removed, their recall was better if there were no deletions or the deletions occurred well within event segments, preserving the boundaries.

It’s also been found that we remember details better if we’ve segmented finely rather than coarsely, and some evidence supports the idea that people who segment effectively remember the activity better.

Segmentation, theory suggests, helps us anticipate what’s going to happen. This in turn helps us adaptively create memory codes that best reflect the structure of events, and by simplifying the event stream into a number of chunks of which many if not most are already encoded in your database, you save on processing resources while also improving your understanding of what’s going on (because those already-coded chunks have been processed).

All this emphasizes the importance of segmenting well, which means you need to be able to pinpoint the correct units of activity. One way we do that is by error monitoring. If we are monitoring our ongoing understanding of events, we will notice when that understanding begins to falter. We also need to pay attention to the ordering of events and the relationships between sequences of events.

The last type of memory I want to mention is semantic memory. Semantic memory refers to what we commonly think of as ‘knowledge’. This is our memory of facts, of language, of generic information that is untethered from specific events. But all this information first started out as episodic memory — before you ‘knew’ the word for cow, you had to experience it (repeatedly); before you ‘knew’ what happens when you go to the dentist, you had to (repeatedly) go to the dentist; before you ‘knew’ that the earth goes around the sun, there were a number of events in which you heard or read that fact. To get to episodic memory (your memory for specific events), you must pass through working memory (the place where you put incoming information together into some sort of meaningful chunk). To get to semantic memory, the information must pass through episodic memory.

How does information in episodic memory become information in semantic memory? Here we come to the process of reconstruction, of which I have often spoken (see my article on memory consolidation for some background on this). The crucial point here is that memories are rewritten every time they are retrieved.

Remember, too, that neurons are continually being reused — memories are held in patterns of activity, that is, networks of neurons, not individual neurons. Individual neurons may be involved in any number of networks. Here’s a new analogy for the brain: think of a manuscript, one of those old parchments, so precious that it must be re-used repeatedly. Modern technology can reveal those imperfectly erased hidden layers. So the neural networks that are memory codes may be thought of as imposed one on top of each other, none of them matching, as different patterns re-use the same individual neurons. The strongest patterns are the most accessible; patterns that are most similar (use more of the same neurons) will provide the most competition.

So, say you are told by your teacher that the earth goes around the sun. That’s the first episode, and there’ll be lots of contextual detail that relates to that particular event. Then on another occasion, you read a book showing how the earth goes around the sun. Again, lots of episodic detail, of which some will be shared with the first incident, and some will be different. Another episode, more detail, some shared, some not. And so on, again and again, until the extraneous details, irrelevant to the fact and always different, are lost, while those details that common to all the episodes will be strong, and form a new, tight chunk of information in semantic memory.

Event boundaries start off with an advantage — they are beginnings or endings, to which we are predisposed to attend (for obvious reasons). So they start off stronger than other bits of information, and by their nature are more likely to be vital elements, that will always co-occur with the event. So — if you have chosen your boundaries well (i.e., they truly are vital elements) they will become stronger with each episode, and will end up as vital parts of the chunk in semantic memory.

Let’s connect that thought back to my comment that the most important difference between those with ‘low’ working memory capacity and those with ‘high’ capacity is the ability to select the ‘right’ information and disregard the irrelevant. Segmenting your events well would seem to be another way of saying that you are good at selecting the changes that are most relevant, that will be common to any such events on other occasions.

And that, although some people are clearly ‘naturally’ better at it, is surely something that people can learn.

References

Culham, J. 2001. The brain as film director. Trends in Cognitive Sciences, 5 (9), 376-377.

Kurby, C. a, & Zacks, J. M. (2008). Segmentation in the perception and memory of events. Trends in cognitive sciences, 12(2), 72-9. doi:10.1016/j.tics.2007.11.004

Speer, N. K., Zacks, J. M., & Reynolds, J. R. (2007). Human Brain Activity Time-Locked to Narrative Event Boundaries. Psychological Science, 18(5), 449–455. doi:10.1111/j.1467-9280.2007.01920.x

Autobiographical memory

  • Autobiographical memory contains information about yourself, and about personal experiences.
  • Emotions, the "facts" that describe you and make you unique, the facts of your life, and the experiences you have had, are all contained in separate domains, and processed differently.
  • Your memory for emotions can help you modify your moods.
  • Specific events you have experienced are only memorable to the extent that they include details special to that specific occasion.
  • Most events in our lives are routine, and are merged in memory into one generic memory containing the common elements of the experience.

Autobiographical memory contains the information you have about yourself. It includes several domains:

  • self-description (the source of a large part of your sense of identity), containing information such as:
    • whether or not you like ice-cream
    • what your favorite color is
    • what you think about a political party
  • emotional memory, which not only contains our memories of emotional experiences, but also helps us control our moods. By dwelling on appropriate memories, we can sustain a mood. By recalling memories that involve a contrasting emotion, we can change a mood.
  • event memory

diagram

Your memory for events

This is the largest component of autobiographical memory, containing three separate but related domains:

  • memory for specific events that have happened to you
  • memory for general events, which tells you the broad sequence of actions in events such as going to a restaurant or going to the dentist
  • a potted summary of your life, which enables you to answer such questions as, “Where did you go to school?”, “Where were you working last year?”.

These may be thought of as being connected hierarchically:

diagram

Recalling specific events

Event memory is usually entered via the general-event level, although the information we are searching for is usually at the specific-event level. Thus, if you're trying to retrieve the memory of going to see the movie Titanic, you will probably start by accessing the general event "going to the pictures"

Specific events over time become merged into a general event - all the occasions you've been to the dentist, for example, have blurred into a generic "script", which encapsulates the key experiences and actions that are typical of the going-to-the-dentist event. After the specific event has become consolidated into the script, only distinctive events are likely to be specifically remembered. That is, events when something unusual/interesting/humorous happened.

The power of these scripts is such that people often "remember" details of a specific event that never happened, merely because they are typical of the script for that event.

Our memory for events reflects what we expect to happen.

It is perhaps because of this that unexpected events and new events (first-time experiences) are better remembered. If you don't have an existing script for the event, or if the event is atypical enough not to easily fit an existing script, then you can't mold the experience to your expectations.

The more distinctive an event - the more the event breaks with your script for that type of event - the better your memory for that particular event will be. (Failures to remember trivial events, such as where you’ve put something, or whether you’ve done something, are reflections of the fact that we pay little attention to routine actions that are, as it were, already scripted).

To remember an event therefore, you should look for distinctive details.

What makes a good cue for remembering events?

One of the most interesting areas of research in the study of event memory is a small set of diary studies. In one such study, a Dutch psychologist called Willem Wagenaar recorded his day's events every day for six years, noting down:

  • who was involved
  • what the event was
  • where it occurred
  • when it occurred

Wagenaar was hoping to discover which of these different bits of information were the best retrieval cues. At the conclusion of his study he reported that what was the best cue, followed by who and where. When was the least effective (have you ever tried to remember an event on the basis of its approximate date?).

There is nothing particularly special about these types of information however. Later, Wagenaar reanalyzed his data, and found that most of the difference in the memorability of these cues was due to their relative distinctiveness. Thus, the nature of the event is usually the most distinctive aspect of the event, and the people involved, and the location, are usually more distinctive bits of information than the date or time of occurrence.

To remember a specific event, we need a key - a unique feature that allows us to readily distinguish that event from similar events.

The Memory Key

References
  • Barsalou, L.W. 1988. The content and organization of autobiographical memories. In U. Neisser & E. Winograd (eds.) Remembering reconsidered: Ecological and traditional approaches to the study of memory. Cambridge: Cambridge University Press.
  • Robinson, J.A. 1992. Autobiographical memory. In M.M. Gruneberg, & P. Morris (eds). Aspects of memory. Vol.1: The practical aspects. 2nd ed. London: Routledge.
  • Diagrams taken from The Memory Key.

The mediotemporal lobe

  • The mediotemporal lobe is critically involved in both initial learning of facts and events and their later consolidation.
  • Dysfunction in the mediotemporal lobe is a major factor in age-related cognitive decline.
  • The most significant component of the MTL is the hippocampus.
  • The hippocampus contains specialized neurons that categorize incoming sensory information, and others that are involved in the forming of new associations.
  • The hippocampus is crucial for episodic memory - the remembering of specific events and experiences. It is also particularly involved in spatial memory.
  • The hippocampus appears to be involved in consolidation processes, but only in the initial stages and for the first few years. The part of the hippocampus called the dentate gyrus is crucial for encoding new information (and is thus implicated in working memory).
  • The dentate gyrus is one of the few brain regions in which new nerve cells can be created in adult brains.
  • The main processing part of the hippocampus, the cornu ammonis, is distinguished by a high number of neurons which loop back on themselves - enabling the output of the neuron to influence its input; this may be critical for associative power.
  • Other components of the mediotemporal lobe include the rhinal cortex and the amygdala.
  • The entorhinal cortex appears to be involved in long-term memory consolidation beyond the first few years. It is one of the first regions damaged in Alzheimer's.
  • The perirhinal cortex is crucial for object recognition.
  • The amygdala is primarily responsible for processing emotional responses. The connection between hippocampus and amygdala underlies the role of emotion in memory.

The mediotemporal lobe (MTL) is a concept rather than a defined brain structure. It includes the hippocampus, the amygdala, and the entorhinal and perirhinal cortices - all structures within the medial area of the temporal lobe.The temporal lobe is in general primarily concerned with sensory experience - specifically, with hearing, and with the integration of information from multiple senses. Part of the temporal lobe also plays a role in memory processing. It is situated below the frontal and parietal lobes, and above the hindbrain.

Originally conceived as an integrated memory system with a common function, this view of the MTL has recently been questioned. For one thing, the region didn’t evolve as one unit — the different regions arose at different times during primate evolution. Therefore, can it really be an integrated system with a common function? Work with rhesus monkeys suggests rather that these different parts may serve cooperative and even competitive functions.

This question, however, is really one for the specialist. As far as most of us are concerned, the concept of a "mediotemporal lobe" serves as a handy label for a group of connected brain structures that are all absolutely crucial for learning and memory (and reminds us of the location of these structures).

It should also be remembered that brain structures are notoriously "fuzzy" — different researchers will use different names, and group different structures. For example, one report has contrasted the functions of the MTL with that of the basal ganglia, although the amygdala is a member of both. Other studies talk of the hippocampus AND the dentate gyrus, although others put the dentate gyrus as a substructure of the hippocampus. I mention this only to warn you, if you find trawl through various reports and find such discrepancies. They can be confusing. I have tried to integrate such discrepancies into a consistent description that seems to make most sense. Just bear in mind that dividing the brain into separate structures is not an exact science.

Functions of the MTL

The MTL has been particularly implicated in the process of memory consolidation - the process by which new memories become progressively more stable (see my article on consolidation for more details). Lesions in the MTL typically produce amnesia characterized by the disproportionate loss of recently acquired memories. A recent imaging study confirms this view by showing temporally graded changes in MTL activity in healthy older adults.

Progressive atrophy in the mediotemporal lobe also appears to be the most significant predictor of cognitive decline in seniors. Elderly persons with a poor memory have less activity in the mediotemporal lobe when storing new information than elderly persons with a normally functioning memory.

The MTL also appears to be particularly important during initial learning. Research has found rapid modulation of activity in the MTL at the beginning of learning, with this activity rapidly declining with training.

All this indicates that the MTL is not only hugely important, but that it covers a quite extraordinary range of functions. The reason for this lies in the fact that the MTL is not a single brain structure.

Components of the MTL

It is probably fair to say that the original concept of the MTL was, at least in part, a reflection of the inability of early researchers to "see" the activity in the brain in very much detail. Now, of course, neurological techniques have progressed to the point of being able to pinpoint activity to a quite fantastic level. It is therefore now possible to some degree to disentangle the functions of the various components of the MTL.

The most significant of the individual components of the MTL is the hippocampus. The hippocampus, one of the oldest parts of the brain, is important for the forming, and perhaps long-term storage, of associative and episodic memories. It is thus absolutely critical for learning and memory, and a brain region much studied by researchers.

The hippocampus

In recent years, the hippocampus has been specifically implicated in (among other things) the encoding of face-name associations, the retrieval of face-name associations, the encoding of events, the recall of personal memories in response to smells. It may also be involved in the processes by which memories are consolidated during sleep.

A variety of specialized neurons have been found in the hippocampus. For example,

  • "categorizing cells", which streamline and simplify sensory information, markedly reducing the brain's workload, by categorizing stimuli into various classes (categories that have been acquired through experience).
  • "changing cells", which appear to be involved in the initial formation of new associative memories, and may also, in some cases, be involved in the eventual storage of the associations in long-term memory.
  • "place cells", which become active in response to specific spatial locations; some of these cells also seem to be sensitive to recent or impending events, thus enabling you to place location within a temporal context (e.g., is this somewhere I've just been, or somewhere I intended to go?).

The existence of place cells is supported by other evidence for the role of the hippocampus in spatial navigation and memory. For example, London taxi drivers (famous for their extensive knowledge of London - a spatial task) have been found to have, on average, significantly bigger hippocampuses than "ordinary motorists". In similar vein, the chickadee, a tiny songbird, gathers and stores seeds in the fall, and at this time its hippocampus expands in volume by some 30% by adding new nerve cells. It shrinks back in the spring.

The role of the hippocampus in episodic (event) memory is underscored by findings that deficiencies in the hippocampus play a key role in alcoholism-related Korsakoff's syndrome (a memory disorder), as well as Alzheimer's disease.

The hippocampus has also been implicated in memory consolidation processes, but evidence now suggests the hippocampus may participate only in consolidation processes lasting a few years. It is probably critical for the initial consolidation of memories that appears to take place during sleep. Rat studies have found that, during sleep (mostly the slow-wave phase), the thalamus at the base of their brains produced bursts of electrical activity, which were then detected in the somatosensory neocortex. Some 50 msec later, the hippocampus responded with a pulse of electricity. It’s suggested that this pulse is the hippocampus sending back compressed waves of the information learned during the day to the neocortex where they are filed away for future reference.

The evidence that some memories might be held in the hippocampus for several years, only to move on, as it were, to another region, is an interesting complication to our earlier simple view of memory dividing into "short-term memory" and "long-term memory". It seems that long-term memory, now better labeled as permanent memory, is far from being the straightforward storage system that we once envisaged. Not only do memories become reconstructed, but they become, it would seem, re-filed. The implications of this, still speculative, relocation, are as yet unknown. Perhaps memories in this "permastore" are more resistant to change.

Substructures of the hippocampus

There are several substructures within the hippocampus. It is only very recently that researchers have been able to go inside the hippocampus, as it were, and pinpoint hippocampal activity to particular substructures.

  • the dentate gyrus: is the main entry point for nerve fibers into the hippocampal formation. Rat studies suggest that the dentate gyrus is crucial for the acquiring of new information, and the functioning of working memory. Most recently, it has been implicated with the cornu ammonis as being highly active during encoding offace-name pairs. The dentate gyrus is one of the very few regions in the adult brain that appears to allow neurogenesis (creation of new nerve cells). Neurogenesis in the dentate gyrus has been found to be significantly reduced in marmoset monkeys when exposed to stress. Dysfunction in the dentate gyrus appears to be linked to cognitive deficits in those suffering from Alzheimer's. The granule cells in the dentate gyrus project to the pyramidal cells in the cornu ammonis.
  • the cornu ammonis: is thought to be the main site of memory processing in the hippocampal formation. Most recently, it has been implicated with the dentate gyrus as being highly active during encoding offace-name pairs. Part of the cornu ammonis (CA3) has been of special interest due to its high number of recursive neurons (nerve fibers which loop back on themselves - enabling the output of the neuron to influence its input). Most recently, the CA3 has been found to be crucial for recalling memories from partial representations of the original stimulus (for example, when memories are triggered by smells).
  • the subiculum: can be thought of as the "last stage" of processing in the hippocampal formation. It is the primary target of the pyramidal cells in CA1. The subiculum is connected to the perirhinal, entorhinal and prefrontal cortices, and thus is in a position to integrate information from several sources and pass this information on. The subiculum however has been much less studied than the other substructures of the hippocampal formation. Recently, it has been found to be active during the retrieval of newly learned face-name associations.

The rhinal cortex

The entorhinal cortex is a region upon which nerve fibers from many sensory systems converge. It is the main input to the hippocampus, and also the main output. This is why damage to this region is so serious. The entorhinal cortex is one of the first regions damaged in the early stages of Alzheimer's.

It has also been suggested that the entorhinal cortex handles “incremental learning” — learning that requires repeated experiences. “Episodic learning” — memories that are stored after only one occurrence — might be mainly stored in the hippocampus.

While the hippocampus appears to participate in memory consolidation processes only for the first few years, the entorhinal cortex seems to be associated with temporally graded changes extending up to 20 years - suggesting that it is the entorhinal cortex, rather than the hippocampus, that participates in memory consolidation over decades.

The perirhinal cortex has been a largely neglected region. It is adjacent to the visual processing area, as well as the entorhinal cortex, and recent research demonstrates that it is important for recognizing objects. In particular, it is crucial for recognizing the many features of an object, while still recognizing it as a single entity. The perirhinal cortex also appears to be involved in associating objects with other objects, and even with abstractions such as a goal. Unsurprisingly, in view of its involvement in recognition memory, it appears to play a critical role in establishing the familiarity of an item.

While the hippocampus is also involved in object recognition, the functions of the two regions appear quite different.

The amygdala

The amygdala is part of the basal ganglia, large "knots" of nerve cells deep in the cerebrum, thought to be involved in various aspects of motor behavior (Parkinson's disease, for example, is an affliction of the basal ganglia). The amygdala has many connections with other parts of the brain, and is critically involved in computing the emotional significance of events. Recent research indicates it is responsible for the influence of emotion on perception, through its connections with those brain regions that process sensory experiences. Rat studies also suggest that the amygdala, in tandem with the orbitofrontal cortex, is involved in the forming of new associations between cues and outcomes - in other words, it is the work of the amygdala to teach us what happens to us when we do something.

The connection between the amygdala and the hippocampus helps explain why emotion can have such powerful effect on learning and memory (to put it crudely, the amygdala remembers the feelings, and the hippocampus remembers what event elicited those feelings). (see article on emotion and memory)

The brain is a network

It must always be remembered that no structure within the brain acts on its own. This is reinforced by a recent study that found that, as subjects studied word lists, clusters of neurons in the rhinal cortex and the hippocampus fired synchronized electrical bursts, with this coordinated activity plummeting for a fraction of a second just after participants remembered a word from the list. This has led to speculation that memory relies more on the timing (coordination) than on the strength of neural activity.

We still know very little about the ways in which these structures interact; only as we gain more knowledge about this will we know whether we are justified in talking about a "mediotemporal lobe". Nevertheless, this region of the brain is undoubtedly vital for what we might term "stereotypical" memory - the memory domains we are most likely to be thinking of when we think of memory.

References

Anderson, A.K. & Phelps, E.A. 2001. Lesions of the human amygdala impair enhanced perception of emotionally salient events. Nature, 411, 305-309.

Ekstrom, A.D., Kahana, M.J., Caplan, J.B., Fields, T.A., Isham, E.A., Newman, E.L. & Fried, I. 2003. Cellular networks underlying human spatial navigation.Nature, 425 (6954), 184-7.

Fell, J., Klaver, P., Lehnertz, K., Grunwald, T., Schaller, C., Elger, C.E. & Fernández, G. 2001. Human memory formation is accompanied by rhinal-hippocampal coupling and decoupling. Nature Neuroscience 4(12), 1259-1264.

Haist, F., Gore, J.B. & Mao, H. 2001. Consolidation of human memory over decades revealed by functional magnetic resonance imaging. Nature neuroscience, 4 (11), 1139-1145.

Hampson, R.E., Pons, T.P., Stanford, T.R. & Deadwyler, S.A. 2004. Categorization in the monkey hippocampus: A possible mechanism for encoding information into memory. PNAS, 101, 3184-3189.

McLeod, P., Plunkett, K. & Rolls, E.T. 1998. Introduction to Connectionist Modelling of Cognitive Processes. Oxford: Oxford University Press.

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Poldrack, R.A., Clark, J., Paré-blagoev, E.J., Shohamy, D., Moyano, J.C., Myers, C. & Gluck, M.A. 2001. Interactive memory systems in the human brain. Nature, 414, 546-550.

Ribeiro, S., Gervasoni, D., Soares, E.S., Zhou, Y., Lin, S-C., Pantoja, J., Lavine, M. & Nicolelis, M.A.L. 2004. Long-Lasting Novelty-Induced Neuronal Reverberation during Slow-Wave Sleep in Multiple Forebrain Areas. PLoS Biol 2(1): e24 DOI:10.1371/journal.pbio.0020024.

Rusinek, H., De Santi, S., Frid, D., Tsui, W-H., Tarshish, C.Y., Convit, A., & de Leon, M.J. 2003. Regional Brain Atrophy Rate Predicts Future Cognitive Decline: 6-year Longitudinal MR Imaging Study of Normal Aging. Radiology, 229, 691-696.

Schoenbaum, G., Setlow, B., Saddoris, M.P. & Gallagher, M. 2003. Encoding Predicted Outcome and Acquired Value in Orbitofrontal Cortex during Cue Sampling Depends upon Input from Basolateral Amygdala. Neuron, 39, 855-867.

Sirota, A., Csicsvari, J., Buhl, D. & Buzsáki, G. 2003. Communication between neocortex and hippocampus during sleep in rodents. Proc. Natl. Acad. Sci. USA, 100 (4), 2065-2069.

Wirth, S., Yanike, M., Frank, L.M., Smith, A.C., Brown, E.N. & Suzuki, W.A. 2003. Single Neurons in the Monkey Hippocampus and Learning of New Associations. Science, 300, 1578-1581.

Zeineh, M.M., Engel, S.A., Thompson, P.M. & Bookheimer, S.Y. 2003. Dynamics of the Hippocampus During Encoding and Retrieval of Face-Name Pairs, Science, 299, 577-580.