A few weeks ago a long discussion
followed a tweet about the start of my “Memory & The Brain” module. I
promised to provide a summary of the content of the module, as several people
seemed to be interested. So here it is.
First, the context. This is an “advanced
module” that final year undergraduates (and some Masters students) take after
completing core 1st and 2nd year modules in “perception
and cognition” and “brain and behaviour”. They therefore have a relatively
strong background in undergraduate psychology, and the module is designed to
push them beyond this core knowledge. It consists of eight 2-hour seminars. In
several seminars (2, 3, 5, 6, & 7), I provide a 1-hour lecture and then the
students present two key papers on the topic. The idea is for them to digest
and then present the material to the other students, and to promote a
discussion on the broader theoretical topic. This can often lead to stimulating
discussion among the students where they learn how to critically evaluate the
studies (and sometimes it can lead to awkward silences).
In each seminar I typically
choose 2-3 “key papers” on the broader topic. Some of these papers I have
chosen because they are clearly the key papers in the area. Some I have chosen
because they are important, but also are written well, and have a clear
experimental design, to ensure the students are not overly stretched. I often
include my papers, not necessarily because I think they are THE key papers, but
because (1) students seem to like reading and discussing lecturer’s work and
(2) it allows them to understand that scientists are able to critically
evaluate their own work to the same degree as others. All this means that there
will undoubtedly be key papers related to the topic that aren’t covered. These
are the choices we sometimes must make when teaching.
Finally, the module has now run
for 4 years with relatively little change to the content (some tweaks to which
papers the students present), so this is perhaps a good moment to reflect on
whether anything needs changing or updating. If you have any suggestions along
these lines, please feel free to email me. With all that out of the way, here
is the content. Note, the content is largely taken from the online material the students have access to, in italics is my narrative/summary of each seminar and how they link together.
Module overview
Our memories make us who we are.
They allow us to delve into our past and project ourselves into the future. How
does the brain support something so complex, subjective and personal?
This module will explore the
cognitive neuroscience of long-term memory, with a specific focus on episodic
and spatial memory. We will explore this topic from a wide variety of
methodologies - from traditional experimental psychology, to neuropsychology,
to brain imaging, to eletrophysiological recordings.
Learning outcomes
On completing this module, the student will be able to:
- Appreciate the complexities involved in the
study of long-term memory
- Discuss memory research at multiple scales, from
individual neurons, to cortical networks, to behaviour
- Critically appraise research related to episodic
and spatial memory
- Identify different regions of the medial
temporal lobe (MTL), including subfields of the hippocampus
- Describe the main theoretical accounts of the
medial temporal lobe and hippocampus
Seminar 1 – Memory systems and declarative memory
The purpose of this lecture is to
teach and/or revise what is commonly taught at the undergraduate level – primarily
Squire’s taxonomy of memory, and the possible “types” of memory that have been
identified by neuropsychology and neuroimaging studies. Many of the students will
have covered some aspects of this before (i.e., the distinction between
episodic and semantic memory). Here I want to present the material in such as
way as to prepare them for the remainder of the module. In particular, I want
them to think carefully about what a “type” of memory might be, and whether this
is a good way of conceptualising long-term memory.
Learning outcomes
After the lecture, the student will be able to:
- Discuss evidence for multiple memory systems
- Understand the different sources of evidence
provided by neuropsychology and functional brain imaging
- Explain the role of the medial temporal lobes in
long-term declarative memory
Key Reading
- Squire, L.R., & Zola-Morgan, S. (1991) The
Medial Temporal Lobe Memory System, Science, 253(5026), 1380-1386.
- Scoville, W.B., & Milner, B. (1957) Loss of
recent memory after bilateral hippocampal lesions, Journal of Neurology,
Neurosurgery & Psychiatry, 20(11), 11-21.
Further Reading
- Chapter 7: Long-term memory systems, in Eysenck
& Keane, Cognitive Psychology: A Student's handbook
Seminar 2 – Episodic and semantic memory
Here we discuss the distinction between episodic and semantic memory. We
start off with evidence that seemingly provides a double dissociation between
episodic and semantic memory – MTL amnesic patients vs semantic dementia
patients. We then discuss how this difference may stem from that fact that
episodic memory tests typically assess anterograde memory (learning of new
material) whereas semantic memory tests typically assess retrograde memory
(retrieval of material learnt prior to brain injury/degeneration). Because of
this, we focus on research that assesses whether amnesic patients with damage
to the hippocampus/MTL can learn new semantic information.
Learning outcomes
After the lecture, the student will be able to:
- Give clear real-world examples of episodic and
semantic memory
- Discuss evidence for possible dissociations
between episodic and semantic memory
- Report the key brain regions involved in
episodic and semantic memory
Key Reading
- Vargha-Khadem et al., (1997) Differential
effects on early hippocampal pathology on episodic and semantic memory,
Science, 227, 376-380.
- Tulving et al., (1991) Long-lasting perceptual
priming and semantic learning in amnesia: a case experiment, Journal of
Experimental Psychology: Learning, Memory & Cognition, 17(4), 595-617.
- Hodges et al., (1992) Semantic dementia. Progressive
fluent aphasia with temporal lobe atrophy, Brain, 115(6), 1783-1806.
- Hamann & Squire, (1995) On the acquisition
of new declarative knowledge in amnesia, Behavioural Neuroscience, 109(6),
1027-1044.
Further Reading
- Squire & Zola (1998) Episodic memory,
semantic memory and amnesia, Hippocampus, 8(3), 205-211.
Seminar 3 – Recollection and familiarity
We next focus on episodic memory,
and the distinction between familiarity and recollection. We cover the
strengths and weaknesses of three different approaches to dissociating between
these two plausibly distinct processes – the remember/know procedure, the process
dissociation procedure, and signal detection theory/ROC curves. We then discuss
neuropsychological data for/against this distinction.
Learning outcomes
After the lecture, the student will be able to:
- Explain the distinction between recollection and
familiarity
- Appreciate how signal detection theory has
contributed to the recollection/familiarity distinction
- Report the key brain regions involved in
recollection and familiarity
Key Reading
- Yonelinas (1994) Reciever-operating
characteristics in recognition memory: evidence for a dual-process model,
Journal of Experimental Psychology: Learning, Memory & Cognition, 20(6),
1341-1354.
- Bowles et al. (2010) Double dissociation of
selective recollection and familiarity impairments following two different
surgical treatments for temporal-lobe epilepsy, Neuropsychologia, 48(9),
2640-2647.
- Wais et al. (2006) The hippocampus supports both
the recollection and the familiarity components of recognition memory, Neuron,
49(3), 459-466.
- Horner et al., (2012) A rapid,
hippocampus-dependent, item-memory signal that initiates context memory in
humans, Current Biology, 22(24), 2369-2374.
Further Reading:
- Aggleton & Brown, (1999) Episodic memory,
amnesia, and the hippocampal-anterior thalamic axis, Behavioural Brain
Sciences, 22(3), 425-444.
- Brandt et al., (2009) Impairment of recollection
but not familiarity in a case of developmental amnesia, Neurocase, 15(1),
60-65.
Seminar 4 – Medial temporal lobe architecture
Prior to seminar 4, we discuss
the hippocampus, perirhinal cortex, and the medial temporal lobes but students
have learnt little of the underlying architecture of these regions. We
therefore cover the major inputs into the perirhinal and parahippocampal cortices,
the entorhinal cortex, and the trisynaptic loop. This is covered at this point,
given the following seminar requires knowledge of the individual subfields of
the hippocampus (in particular CA3 and DG). The emphasis of this seminar is to
understand how knowledge of the underlying architecture provides clues as to what
the functions of each region might be (e.g., if perirhinal cortex receives major
input from ventral visual stream, it is likely to process object/item information
relative to parahippocampal cortex).
The format of this seminar is
slightly different from other seminars, in that I give a 1-hour lecture and
then students go through a workbook of brain diagrams/images in groups, identifying
key regions (this replaces student presentations).
Learning outcomes
After the lecture, the student will be able to:
- Discuss the principal inputs into the medial
temporal lobes
- Identitify the subfields of the hippocampus
- Explain the circuitry of the hippocampal
trisynaptic loop
Key Reading
- Preston & Wagner, (2007) The medial temporal
lobe and memory, in Kestner & Martinez (Eds) The Neurobiology of Learning
and Memory, 305-337.
- Amaral (1999) Introduction: what is where in the
medial temporal lobe? Hippocampus, 9(1), 1-6.
- Lavenex & Amaral (2000)
Hippocampal-neocortical interaction: a hierachy of associativity, Hippocampus,
10(4), 420-430.
Further Reading
- Amaral & Lavenex, (2007) Hippocampal
neuroanatomy, in Per Andersen et al (Eds) The Hippocampus Book, 37-109.
Seminar 5 – Pattern separation and pattern completion
We cover the two computational
processes of pattern separation and pattern completion, and how these are
likely supported by DG and CA3 respectively. We then cover the related concept
of attractor dynamics, and how this might relate to pattern separation/completion.
The key readings are human fMRI study, though we start to cover more rodent
electrophysiology work from this point. We focus on how pattern separation/completion
might be useful computations in relation to episodic memory.
Learning outcomes
After the lecture, the student will be able to:
- Explain how pattern separation and pattern
completion might support memory
- Report the hippocampal subfields that support
pattern separation and pattern completion
- Discuss research in rodents and humans that
provide evidence for these computations
Key Reading
- Horner et al., (2015) Evidence for holistic
episodic recollection via hippocampal pattern completion, Nature
Communications, 6(7462), 1-11.
- Berron et al. (2016) Strong evidence for pattern
separation in the human dentate gyrus, Journal of Neuroscience, 36(29),
7569-7579.
Further Reading
- Wills et al. (2005) Attractor dynamics in the
hippocampal represention of the local environment, Science, 308(5723), 873-876.
- Neunuebel & Knierim, (2014) CA3 retrieves
coherent representations from degraded input: Direct evidence for CA3 pattern
completion and Dentate Gyrus Pattern Separation
- Bakker et al., (2008) Pattern separation in the
human hippocampal CA3 and dentate gyrus, Science, 319(5870), 1640-1642.
- Nakazawa et al., (2002) Requirement for
hippocampal CA3 NMDA receptors in associative memory recall, Science,
297(5579), 211-218.
- Steemers et al., (2016) Hippocampal attractor
dynamics predict memory-based decision making, Current Biology, 1-8.
Seminar 6 – Functional neurons in the medial temporal lobe
Prior to seminar 6, we have primarily covered fMRI and neuroimaging in
humans, and as such know little about what individual neurons in the MTL do.
Here we cover the major “functional neurons” in the MTL, as revealed by
single-unit electrophysiology in rodents and humans – place cells, head-direction
cells, grid cells, boundary/border cells, and “concept” cells. Towards the end
of the seminar we discuss how these cells are responding to (e.g.,) the rodent’s
current position or heading-direction, so seem not to serve an obvious “memory”
function. At this point, it is simply to think about this possible disconnect –
patients with MTL damage clearly show memory deficits, however individual
neurons in the MTL respond to stimuli in the present (i.e., appear somewhat
more “perceptual” in nature).
Learning outcomes
After the lecture, the student will be able to:
- Report the main functional neurons in the
hippocampus
- Describe the firing characteristics of these
neurons
- Appreciate how these neurons contribute to
spatial and episodic memory
Key Reading
- O'Keefe & Dostrovsky (1971) The hippocampus
as a spatial map. Preliminary evidence from unity activity in the freely-moving
rat, Brain Research, 34(1), 171-175.
- Hafting et al., (2004) Microstructure of a
spatial map in the entorhinal cortex, Nature, 436(7052), 801-806.
- Quiroga et al., (2005) Invariant visual
representation by single neurons in the human brain, Nature, 435(7045),
1102-1107.
Further Reading
- Solstad et al. (2008) Representation of
geometric borders in the entorhinal cortex, Nature, 322(5909), 1865-1868.
- Lever et al. (2009) Boundary vector cells in the
subiculum of the hippocampal formation, Journal of Neuroscience, 29(31),
9771-9777.
- Taube et al. (1990) Head-direction cells
recorded from the postsubiculum in freely moving rats. I. Description and
quantitative analysis, Journal of Neuroscience, 10(2), 420-435.
Seminar 7 – Process vs representational accounts of the medial temporal
lobes
Building on the content from
seminar 6, we cover two dominant theories in the literature in relation to how
to best characterise the medial temporal lobes – namely process vs representational
accounts. We discuss the key research in humans that provided some of the first
clear evidence in favour of representational accounts. We finish by trying to
reconcile the representational account with the “memory” deficits that patients
with MTL damage present with. In particular, we discuss how certain processes
(e.g., episodic memory) may rely more heavily on specific representations
(e.g., complex configural representations supported by the hippocampus) than
other representations.
Learning outcomes
After the lecture, the student will be able to:
- Appreciate the distinction between process and
representational accounts
- Critically appraise evidence for and against
these differing accounts
Key Reading
- Ranganath et al. (2001) Medial temporal lobe
activity associated with active maintenance of novel information, Neuron,
31(5), 865-873.
- Hartley et al. (2007) The hippocampus is
required for short-term topographical memory in humans, Hippocampus, 17, 34-48.
- Lee et al. (2005) Specialization in the medial
temporal lobe for processing of objects and scenes, Hippocampus, 15(6),
782-797.
- Barense et al (2007) The medial temporal lobe
processes online representations of complex objects, Neuropsychologia, 45(13),
2963-2974.
Further Reading
- Lee et al. (2008) Activating the medial temporal
lobe during oddity judgement for faces and scenes, Cerebral Cortex, 18(3),
683-696.
- Wang et al. (2010) The medial temporal lobe
supports conceptual implicit memory, Neuron, 68(5), 835-842.
- Schnyer et al. (2006) Rapid response learning in
amnesia: delineating associative learning components in repetition priming,
Neuropsychologia, 44(1), 140-149.
- Nadel & Hardt. (2011) Update on memory
systems and processes, Neuropsychopharmacology Reviews, 36(1), 251-273.
Seminar 8 – The medial temporal lobe beyond episodic memory
In the last seminar, I present
some of the studies I think are most interesting in relation to the medial
temporal lobes – suggesting they play a role in episodic future thinking, scene
construction, imagined navigation, decision-making, and moral judgements. For the second half of
the seminar, the students split into groups and go over the 8 seminars discussing
content they found most challenging. We then have a group revision session
where I help to clarify any material they may not understand, or we discuss
topics that they find particularly interesting. After this, they leave with
smiles on their faces and lead productive, happy, successful lives (this has
nothing to do with that fact they completed my module though).
Learning outcomes
After the lecture, the student will be able to:
- Appreciate that the medial temporal lobes aren't
solely a 'memory' structure
- Evaluate research showing medial temporal lobe
involvement in non-memory tasks
- Discuss what role the medial temporal lobes play
in our mental lives
Key Reading
- Addis et al. (2007) Remembering the past and
imagining the future: Common and distinct neural substrates during event
construction and elaboration, Neuropsychologia, 45(7), 1363-1377.
- Hassabis et al. (2007) Patients with hippocampal
amnesia cannot imagine new experiences, Proceedings of the National Academy of
Science, 104(5), 1726-1731.
- Wimmer et al. (2012) Preference by association:
How memory mechanisms in the hippocampus bias decisions, Science, 338(6104),
270-273.
Further Reading
- McCormick et al. (2016) Hippocampal damage
increases deontological responses during moral decision making, Journal of
Neuroscience, 36(48), 12157-12167.
- Zeithamova et al. (2012) Hippocampal and ventral
medial prefrontal activation during retrieval-mediated learning supports novel
inference, Neuron, 75(1), 168-179.
- Horner et al. (2016) Grid-like processing of
imagined navigation, Current Biology, 26, 842-847.
Areas not currently covered (but could be)
The module is necessarily
selective, and there are some topics I would like to cover but don’t feel I
have the time. These include:
- Systems consolidation – we mention this
in passing, but don’t cover it systematically. However, there is another
advanced module that focusses on sleep and memory, so if I were to include it
there might be too much overlap between modules.
- Brain networks – the module is heavily
focussed on the medial temporal lobes. That partly reflects my research
interests, but it also reflects my desire for the students to focus more on the
broader theoretical questions (e.g., process vs representational accounts) as
opposed to the neuroscience.
- Memory and emotion – this is a big topic,
but one students would definitely find interesting. If students are taking this
module as part of a Masters level degree, they do have the option of reading
some of this literature.
- Hippocampal longitudinal axis – the
module focusses on hippocampal subfields at the expense of the anterior-posterior
axis of the hippocampus. As in (3), if students are taking this module as part
of a Masters level degree, they do have the option of reading some of this literature.
- Forgetting – this reflects my own
shifting research interests but forgetting is a fascinating topic with a rich
psychological and neuroscientific history.
I’m sure there are other topics
as well, but these are the ones I have thought about including previously. As
above, if you have any thoughts or suggestions, feel free to email me. I think
that just about covers it. I hope this is useful to some – possibly just as a
way of figuring out what NOT to teach. Happy teaching to you all.