NBIO-160A-1
Cellular and Network Mechanisms of Memory Professor John Lisman
Fall 2016
Office: Volen 342A
Office hours by Appointment: Call Nonna at X63148 or .
Course material available on LATTE
Prerequisites: N140
Course Grading: 4 short writing assignments (5 points each); term paper (20 points); midterm (25 points); final (35 points).
The midterm and final will consist of questions about figures that we have discussed in class and definitions.
Goals of the course: To understand the types of memory, the underlying cellular and molecular mechanisms, and the brain networks involved. Physiological and behavioral methods for studying memory will be discussed. Students will learn skills necessary for researching the literature and writing a paper in scientific style. Through in class discussion of primary papers, students will learn how to read and analyze such papers.
Classes on Tuesdays and Thursdays, 3:30 - 4:50 PM at Shapiro Science Center, GL-14
Course Syllabus:
1. Thursday, August 25-th
Networks with recurrent modifiable excitatory connections can store memories and perform pattern completion. The underlying process is synapse-specific Hebbian modification.
· Kelso SR, Ganong AH, Brown TH. Hebbian synapses in hippocampus. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5326-30.
http://www.pnas.org/content/83/14/5326.long
· HestrinS, Nicoll RA, Perkel DJ, Sah P. Analysis of excitatory synaptic action in pyramidal cells using whole-cell recording from rat hippocampal slices. J Physiol. 1990 Mar; 422:203-25. http://www.ncbi.nlm.nih.gov/pmc/articles/PMC1190128/
· Picture of hippocampal circuit from me and Cajal.
2. Tuesday, August 30-th
Demonstration that LTP in the amygdala is a mechanism of memory in classical conditioning.
· Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R. Engineering a memory with LTD and LTP. Nature. 2014 Jul 17; 511(7509):348-52. doi: 10.1038/nature13294. Epub 2014 Jun 1.
3. Thursday, September 1-st
Evidence that LTP is a mechanism of episodic memory
· Abraham WC, Logan B, Greenwood JM, Dragunow M. Abraham WC, Logan B, Greenwood JM, Dragunow M. Induction and experience-dependent consolidation of stable long-term potentiation lasting months in the hippocampus. J Neurosci. 2002 Nov 1; 22(21):9626-34.
· Whitlock JR, Heynen AJ, Shuler MG, Bear MF. Learning induces long-term potentiation in the hippocampus. Science. 2006 Aug 25; 313(5790):1093-7.
· Brun VH, Ytterbo K, Morris RG, Moser MB, Moser EI. Retrograde amnesia for spatial memory induced by NMDA receptor-mediated long-term potentiation. J Neurosci. 2001 Jan 1; 21(1):356- 62.
http://www.jneurosci.org/content/21/1/356.full.pdf+html
· Nakazawa K, Quirk MC, Chitwood RA, Watanabe M, Yeckel MF, Sun LD, Kato A, Carr CA, Johnston D, Wilson MA, Tonegawa S. Requirement for hippocampal CA3 NMDA receptors in associative memory recall. Science. 2002 Jul 12; 297(5579):211-8. Epub 2002 May 30.
· Hill TC, Zito K. LTP-induced long-term stabilization of individual nascent dendritic spines. J Neurosci. 2013 Jan 9; 33(2):678-86. doi: 10.1523/JNEUROSCI.1404-12.2013.
4. Tuesday, September 6-th
The entry of Ca through NMDARs: role in LTP and LTD
· Nevian T, Sakmann B. Spine Ca2+ signaling in spike-timing-dependent plasticity. J Neurosci. 2006 Oct 25; 26(43):11001-13.
· Lisman J, Yasuda R, Raghavachari S. Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci. 2012 Feb 15; 13(3):169-82. doi: 10.1038/nrn3192.
5. Tuesday, September 13-th
Role of CaMKII in LTP induction
· Fukunaga K, Muller D, Miyamoto E. Increased phosphorylation of Ca2+/calmodulin-dependent protein kinase II and its endogenous substrates in the induction of long-term potentiation. J Biol Chem. 1995 Mar 17; 270(11):6119-24.
· Lee SJ, Escobedo-Lozoya Y, Szatmari EM, Yasuda R. Activation of CaMKII in single dendritic spines during long-term potentiation. Nature. 2009 Mar 19; 458(7236):299-304. doi: 10.1038/nature07842.
· Giese KP, Fedorov NB, Filipkowski RK, Silva AJ. Autophosphorylation at Thr286 of the alpha calcium-calmodulin kinase II in LTP and learning. Science. 1998 Feb 6; 279(5352):870-3.
· Lisman J, Schulman H, Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci. 2002 Mar;3(3):175-90.
6. Thursday, September 15-th
Evidence that LTP is mediated by enhancement of AMPARs
· Matsuzaki M, Honkura N, Ellis-Davies GC, Kasai H. Structural basis of long-term potentiation in single dendritic spines. Nature. 2004 Jun 17; 429(6993):761-6. Epub 2004 Jun 9.
· Patterson MA, Szatmari EM, Yasuda R. AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc Natl Acad Sci U S A. 2010 Sep 7; 107(36):15951-6. doi: 10.1073/pnas.0913875107. Epub 2010 Aug 23
· Liao D, Jones A, Malinow R. 1992. Direct measurement of quantal changes underlying long-term potentiation in CA1 hippocampus. Neuron 9: 1089-97
7. Tuesday, September 20-th. Led by Nick Otmakhov
How CaMKII enhances AMPAR function---CaMKII dependent phoshphorylation of SynGap produces early LTP. Role of PSD-95 in anchoring AMPAR
· Bats C, Groc L, Choquet D. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron. 2007 Mar 1; 53(5):719-34.
· Araki Y, Zeng M, Zhang M, Huganir RL. Rapid Dispersion of SynGAP from Synaptic Spines Triggers AMPA Receptor Insertion and Spine Enlargement during LTP. Neuron. 2015 Jan 7; 85(1):173-189. doi: 10.1016/j.neuron.2014.12.023.
8. Thursday, September 22-nd
Structural growth during late LTP: tag and capture
· Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y. Structural and Molecular Remodeling of Dendritic Spine Substructures during Long-Term Potentiation. Neuron. 2014 Apr 16; 82(2):444-59. doi: 10.1016/j.neuron.2014.03.021.
· Tanaka J, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GC, Kasai H. Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science. 2008 Mar 21; 319(5870):1683-7.
9. Tuesday, September 27-th
Role of CaMKII in long-term memory storage
· Sanhueza M, Lisman J. The CaMKII/NMDAR complex as a molecular memory. Mol Brain. 2013 Feb 14; 6:10. doi: 10.1186/1756-6606-6-10. Review.
· Lisman JE. Refreshing memories. Elife. 2014; 3:e02041. doi: 10.7554/eLife.02041. Epub 2014 Jan 29.
· Urakubo H, Sato M, Ishii S, Kuroda S. In vitro reconstitution of a CaMKII memory switch by an NMDA receptor-derived peptide. Biophys J. 2014 Mar 18; 106(6):1414-20.
· Study questions for exam.
10. Thursday, September 29-th
· Midterm:
11. Thursday, October 6-th
Place cells of the hippocampus (O’Keefe) and grid cells of the entorhinal cortex
· Electrophysiological recordings from the hippocampus: reading the mind of a rat http://www.youtube.com/watch?v=lfNVv0A8QvI
· Moser EI, Moser MB. 2013. Grid cells and neural coding in high-end cortices. Neuron 80: 765-74
12. Tuesday, October 11-th
Oscillations and the neural code; definition of a neural ensemble; predicting upcoming events (phase precession)
· Lisman J, Buzsáki G. A neural coding scheme formed by the combined function of gamma and theta oscillations. Schizophr Bull. 2008 Sep;34(5):974-80. doi: 10.1093/schbul/sbn060. Epub 2008 Jun 16.
13. Thursday, October 13-th
Memory replay offline
· Wikenheiser AM, David Redish A. The balance of forward and backward hippocampal sequences shifts across behavioral states. Hippocampus. 2013 Jan; 23(1):22-9.
· Jadhav SP, Kemere C, German PW, Frank LM. Awake hippocampal sharp-wave ripples support spatial memory. Science. 2012 Jun 15; 336(6087):1454-8.
· Girardeau G, Cei A, Zugaro M. Learning-induced plasticity regulates hippocampal sharp wave- ripple drive. J Neurosci. 2014 Apr 9; 34(15):5176-83
14. Tuesday, October 18-th
How the different hippocampal fields work together to subserve memory function. :
· Sanders H, Renno-Costa C, Idiart M, Lisman J. 2015. Grid Cells and Place Cells: An Integrated View of their Navigational and Memory Function. Trends Neurosci 38: 763-75
· http://www.huffingtonpost.com/entry/amnesia-lonni-sue-johnson_us_576afac6e4b09926ce5da503
15. Thursday, October 20-th
Manipulating the engram; false memories.
· Ramirez S, Liu X, Lin PA, Suh J, Pignatelli M, Redondo RL, Ryan TJ, Tonegawa S. Creating a false memory in the hippocampus. Science. 2013 Jul 26; 341(6144):387-91
· False memories Elizabeth Loftus Ted talk.
· Lisman J, Schulman H, Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nat Rev Neurosci. 2002 Mar;3(3):175-90.
16. Thursday, October 27-th
Dopamine as the teacher: Dopamine cells signal reward, saliency and novelty.
· Cohen JY, Haesler S, Vong L, Lowell BB, Uchida N. Neuron-type-specific signals for reward and punishment in the ventral tegmental area. Nature. 2012 Jan 18; 482(7383):85-8. doi:
· Lisman J, Grace AA, Duzel E. A neoHebbian framework for episodic memory; role of dopamine-dependent late LTP. Trends Neurosci. 2011 Oct; 34(10):536-47. doi: 10.1016/j.tins.2011.07.006. Epub 2011 Aug 17. Review
17. Tuesday, November 1-st
Role of sleep in memory
· Goshen I, Brodsky M, Prakash R, Wallace J, Gradinaru V, Ramakrishnan C, Deisseroth K. Dynamics of retrieval strategies for remote memories. Cell. 2011 Oct 8;147(3):678-89. doi: 10.1016/j.cell.2011.09.033. Epub 2011 Oct 20.
· Manns JR, Hopkins RO, Squire LR. Semantic memory and the human hippocampus. Neuron. 2003;38(1):127-33.
· Ferrarelli F, Tononi G. Reduced sleep spindle activity point to a TRN-MD thalamus-PFC circuit dysfunction in schizophrenia. Schizophr Res. 2016
18. Thursday, November 3-rd:
The Neurosciece of classroom learning
· Ballarini F, Martínez MC, Díaz Perez M, Moncada D, Viola H. Memory in Elementary School Children Is Improved by an Unrelated Novel Experience. PLoS One. 2013 Jun 19; 8(6):e66875. Print 2013.
· Karpicke JD, Roediger HL 3rd. The critical importance of retrieval for learning. Science. 2008 Feb 15; 319(5865):966-8. doi: 10.1126/science.1152408.
19. Tuesday, November 8
Alzheimer’s disease
· Selkoe DJ, Hardy J. The amyloid hypothesis of Alzheimer's disease at 25 years. EMBO Mol Med. 2016;8(6):595-608.
20. Thursday, November 10-th
Procedural memory: habits and the unconscious
· Procedural memory: http://www.huffingtonpost.com/entry/amnesia-lonni-sue-johnson_us_576afac6e4b09926ce5da503
· Lisman J, Sternberg EJ. Habit and nonhabit systems for unconscious and conscious behavior: implications for multitasking. J Cogn Neurosci. 2013;25(2):273-83
21. Tuesday, November 15-th
Basal ganglia function during reinforcement learning
· Fee MS, Goldberg JH. A hypothesis for basal ganglia-dependent reinforcement learning in the songbird. Neuroscience. 2011;198:152-70.
· Freeze BS, Kravitz AV, Hammack N, Berke JD, Kreitzer AC. Control of basal ganglia output by direct and indirect pathway projection neurons. J Neurosci. 2013;33(47):18531-9.
· Kim KM, Baratta MV, Yang A, Lee D, Boyden ES, Fiorillo CD. Optogenetic mimicry of the transient activation of dopamine neurons by natural reward is sufficient for operant reinforcement. PLoS One. 2012;7(4):e33612.
22. Thursday, November 17-th
Short term memory: role of persistent firing of neurons
· Lisman J, Jensen O, Kahana MJ. The Role of Theta-Gamma Oscillations and NMDAR-Dependent LTP. In: Holscher C, editor. Neuronal Mechanisms of Memory Formation. Cambridge, MA, USA: Cambridge University Press; 2001. p. 195-223.
· Funahashi S, Bruce CJ, Goldman-Rakic PS. Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. J Neurophysiol. 1989;61(2):331-49.
· Lisman JE, Fellous JM, Wang XJ. A role for NMDA-receptor channels in working memory. Nat
Neurosci. 1998 Aug; 1(4):273-5.
· Harrison, S. A. & Tong, F. Decoding reveals the contents of visual working memory in early visual areas. Nature 458, 632–5 (2009).
23. Tuesday, November 22-nd
Role of theta-gamma oscillations in multiitem short-term memory:
· Bahramisharif A, Jensen O, Jacobs J, Lisman J. Serial representations of items during maintenance of working memory at content-specific cortical sites. Submitted.
24. Tuesday, November 29-th
What are the major unsolved problems in memory research?
25. Thursday, December 1
Review:
26. Tuesday, December 6
Last Class – Review
27. Study days – December 8-9
28. Final exams – December 12-19