Wednesday, 18 March 2020

Memory and The Brain Module


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


  1. Squire, L.R., & Zola-Morgan, S. (1991) The Medial Temporal Lobe Memory System, Science, 253(5026), 1380-1386.
  2. 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


  1. 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


  1. Vargha-Khadem et al., (1997) Differential effects on early hippocampal pathology on episodic and semantic memory, Science, 227, 376-380.
  2. 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.
  3. Hodges et al., (1992) Semantic dementia. Progressive fluent aphasia with temporal lobe atrophy, Brain, 115(6), 1783-1806.
  4. Hamann & Squire, (1995) On the acquisition of new declarative knowledge in amnesia, Behavioural Neuroscience, 109(6), 1027-1044.

Further Reading


  1. 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


  1. 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.
  2. 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.
  3. Wais et al. (2006) The hippocampus supports both the recollection and the familiarity components of recognition memory, Neuron, 49(3), 459-466.
  4. 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:


  1. Aggleton & Brown, (1999) Episodic memory, amnesia, and the hippocampal-anterior thalamic axis, Behavioural Brain Sciences, 22(3), 425-444.
  2. 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


  1. Preston & Wagner, (2007) The medial temporal lobe and memory, in Kestner & Martinez (Eds) The Neurobiology of Learning and Memory, 305-337.
  2. Amaral (1999) Introduction: what is where in the medial temporal lobe? Hippocampus, 9(1), 1-6.
  3. Lavenex & Amaral (2000) Hippocampal-neocortical interaction: a hierachy of associativity, Hippocampus, 10(4), 420-430.

Further Reading


  1. 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


  1. Horner et al., (2015) Evidence for holistic episodic recollection via hippocampal pattern completion, Nature Communications, 6(7462), 1-11.
  2. Berron et al. (2016) Strong evidence for pattern separation in the human dentate gyrus, Journal of Neuroscience, 36(29), 7569-7579.

Further Reading


  1. Wills et al. (2005) Attractor dynamics in the hippocampal represention of the local environment, Science, 308(5723), 873-876.
  2. Neunuebel & Knierim, (2014) CA3 retrieves coherent representations from degraded input: Direct evidence for CA3 pattern completion and Dentate Gyrus Pattern Separation
  3. Bakker et al., (2008) Pattern separation in the human hippocampal CA3 and dentate gyrus, Science, 319(5870), 1640-1642.
  4. Nakazawa et al., (2002) Requirement for hippocampal CA3 NMDA receptors in associative memory recall, Science, 297(5579), 211-218.
  5. 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


  1. 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.
  2. Hafting et al., (2004) Microstructure of a spatial map in the entorhinal cortex, Nature, 436(7052), 801-806.
  3. Quiroga et al., (2005) Invariant visual representation by single neurons in the human brain, Nature, 435(7045), 1102-1107.

Further Reading


  1. Solstad et al. (2008) Representation of geometric borders in the entorhinal cortex, Nature, 322(5909), 1865-1868.
  2. Lever et al. (2009) Boundary vector cells in the subiculum of the hippocampal formation, Journal of Neuroscience, 29(31), 9771-9777.
  3. 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


  1. Ranganath et al. (2001) Medial temporal lobe activity associated with active maintenance of novel information, Neuron, 31(5), 865-873.
  2. Hartley et al. (2007) The hippocampus is required for short-term topographical memory in humans, Hippocampus, 17, 34-48.
  3. Lee et al. (2005) Specialization in the medial temporal lobe for processing of objects and scenes, Hippocampus, 15(6), 782-797.
  4. Barense et al (2007) The medial temporal lobe processes online representations of complex objects, Neuropsychologia, 45(13), 2963-2974.

Further Reading

  1. Lee et al. (2008) Activating the medial temporal lobe during oddity judgement for faces and scenes, Cerebral Cortex, 18(3), 683-696.
  2. Wang et al. (2010) The medial temporal lobe supports conceptual implicit memory, Neuron, 68(5), 835-842.
  3. Schnyer et al. (2006) Rapid response learning in amnesia: delineating associative learning components in repetition priming, Neuropsychologia, 44(1), 140-149.
  4. 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


  1. 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.
  2. Hassabis et al. (2007) Patients with hippocampal amnesia cannot imagine new experiences, Proceedings of the National Academy of Science, 104(5), 1726-1731.
  3. Wimmer et al. (2012) Preference by association: How memory mechanisms in the hippocampus bias decisions, Science, 338(6104), 270-273.

Further Reading


  1. McCormick et al. (2016) Hippocampal damage increases deontological responses during moral decision making, Journal of Neuroscience, 36(48), 12157-12167.
  2. Zeithamova et al. (2012) Hippocampal and ventral medial prefrontal activation during retrieval-mediated learning supports novel inference, Neuron, 75(1), 168-179.
  3. 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.

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