Skip to main content

Analysis of Hippocampal Memory Replay Using Neural Population Decoding

  • Protocol
  • First Online:
Neuronal Network Analysis

Part of the book series: Neuromethods ((NM,volume 67))

Abstract

Large-scale recording of neural activity in waking animals provides us with a window on computations performed in the brain during behavior. In order to better understand these computations, population decoding techniques are used to study what information about the external environment is represented by neural ensemble activity. Decoding approaches are especially appealing when neural activity does not reflect the actual sensory experience or motor output, but is generated by internal cognitive processes, such as planning, memory, and decision making. This chapter describes the background of Bayesian decoding and outlines the general procedures for decoding ensemble activity during cognitive processes. The power of this method is demonstrated by applying it to recordings of hippocampal place cell activity in order to identify and characterize hippocampal memory replay.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 89.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 119.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Fujisawa S, Amarasingham A, Harrison MT et al (2008) Behavior-dependent short-term assembly dynamics in the medial prefrontal cortex. Nat Neurosci 11:823–833

    Article  PubMed  CAS  Google Scholar 

  2. Nicolelis MAL, Dimitrov D, Carmena JM et al (2003) Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Natl Acad Sci USA 100:11041–11046

    Article  PubMed  CAS  Google Scholar 

  3. Gray CM, Maldonado PE, Wilson M et al (1995) Tetrodes markedly improve the reliability and yield of multiple single-unit isolation from multi-unit recordings in cat striate cortex. J Neurosci Methods 63:43–54

    Article  PubMed  CAS  Google Scholar 

  4. Lütcke H, Murayama M, Hahn T et al (2010) Optical recording of neuronal activity with a genetically-encoded calcium indicator in anesthetized and freely moving mice. Front Neural Circuits 4:9

    PubMed  Google Scholar 

  5. Murayama M, Pérez-Garci E, Lüscher HR et al (2007) Fiberoptic system for recording dendritic calcium signals in layer 5 neocortical pyramidal cells in freely moving rats. J Neurophysiol 98:1791–1805

    Article  PubMed  Google Scholar 

  6. Sawinski J, Wallace DJ, Greenberg DS et al (2009) Visually evoked activity in cortical cells imaged in freely moving animals. Proc Natl Acad Sci USA 106:19557–19562

    Article  PubMed  CAS  Google Scholar 

  7. Brown EN, Kass RE, Mitra PP (2004) Multiple neural spike train data analysis: state-of-the-art and future challenges. Nat Neurosci 7:456–461

    Article  PubMed  CAS  Google Scholar 

  8. Paninski L, Pillow J, Lewi J (2007) Statistical models for neural encoding, decoding, and optimal stimulus design. Prog Brain Res 165:493–507

    Article  PubMed  Google Scholar 

  9. Quiroga RQ, Panzeri S (2009) Extracting information from neuronal populations: information theory and decoding approaches. Nat Rev Neurosci 10:173–185

    Article  Google Scholar 

  10. Brown EN, Frank LM, Tang D et al (1998) A statistical paradigm for neural spike train decoding applied to position prediction from ensemble firing patterns of rat hippocampal place cells. J Neurosci 18:7411–7425

    PubMed  CAS  Google Scholar 

  11. Georgopoulos AP, Schwartz AB, Kettner RE (1986) Neuronal population coding of movement direction. Science 233:1416–1419

    Article  PubMed  CAS  Google Scholar 

  12. Sanger TD (1996) Probability density estimation for the interpretation of neural population codes. J Neurophysiol 76:2790–2793

    PubMed  CAS  Google Scholar 

  13. Stanley GB, Li FF, Dan Y (1999) Reconstruction of natural scenes from ensemble responses in the lateral geniculate nucleus. J Neurosci 19:8036–8042

    PubMed  CAS  Google Scholar 

  14. Zhang K, Ginzburg I, McNaughton BL et al (1998) Interpreting neuronal population activity by reconstruction: unified framework with application to hippocampal place cells. J Neurophysiol 79:1017–1044

    PubMed  CAS  Google Scholar 

  15. Boloori AR, Jenks RA, Desbordes G et al (2010) Encoding and decoding cortical representations of tactile features in the vibrissa system. J Neurosci 30:9990–10005

    Article  PubMed  CAS  Google Scholar 

  16. Johnson A, Fenton AA, Kentros C et al (2009) Looking for cognition in the structure within the noise. Trends Cogn Sci 13:55–64

    Article  PubMed  Google Scholar 

  17. Reijmers LG, Perkins BL, Matsuo N et al (2007) Localization of a stable neural correlate of associative memory. Science 317:1230–1233

    Article  PubMed  CAS  Google Scholar 

  18. Gelbard-Sagiv H, Mukamel R, Harel M et al (2008) Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322:96–101

    Article  PubMed  CAS  Google Scholar 

  19. Georgopoulos AP, Lurito JT, Petrides M et al (1989) Mental rotation of the neuronal population vector. Science 243:234–236

    Article  PubMed  CAS  Google Scholar 

  20. Georgopoulos AP, Crutcher MD, Schwartz AB (1989) Cognitive spatial-motor processes. 3. Motor cortical prediction of movement direction during an instructed delay period. Exp Brain Res 75:183–194

    Article  PubMed  CAS  Google Scholar 

  21. Davidson TJ, Kloosterman F, Wilson MA (2009) Hippocampal replay of extended experience. Neuron 63:497–507

    Article  PubMed  CAS  Google Scholar 

  22. Karlsson MP, Frank LM (2009) Awake replay of remote experiences in the hippocampus. Nat Neurosci 12:913–918

    Article  PubMed  CAS  Google Scholar 

  23. Johnson A, Redish AD (2007) Neural ensembles in CA3 transiently encode paths forward of the animal at a decision point. J Neurosci 27:12176–12189

    Article  PubMed  CAS  Google Scholar 

  24. O’Keefe J, Dostrovsky J (1971) The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res 34:171–175

    Article  PubMed  Google Scholar 

  25. Wilson MA, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055–1058

    Article  PubMed  CAS  Google Scholar 

  26. O’Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, Oxford

    Google Scholar 

  27. Lee AK, Wilson MA (2002) Memory of sequential experience in the hippocampus during slow wave sleep. Neuron 36:1183–1194

    Article  PubMed  CAS  Google Scholar 

  28. Ji D, Wilson MA (2007) Coordinated memory replay in the visual cortex and hippocampus during sleep. Nat Neurosci 10:100–107

    Article  PubMed  CAS  Google Scholar 

  29. Foster DJ, Wilson MA (2006) Reverse replay of behavioural sequences in hippocampal place cells during the awake state. Nature 440:680–683

    Article  PubMed  CAS  Google Scholar 

  30. Diba K, Buzsáki G (2007) Forward and reverse hippocampal place-cell sequences during ripples. Nat Neurosci 10:1241–1242

    Article  PubMed  CAS  Google Scholar 

  31. Csicsvari J, O’Neill J, Allen K et al (2007) Place-selective firing contributes to the reverse-order reactivation of CA1 pyramidal cells during sharp waves in open-field exploration. Eur J Neurosci 26:704–716

    Article  PubMed  Google Scholar 

  32. Fenton AA, Kao HY, Neymotin SA et al (2008) Unmasking the CA1 ensemble place code by exposures to small and large environments: more place cells and multiple, irregularly arranged, and expanded place fields in the larger space. J Neurosci 28:11250–11262

    Article  PubMed  CAS  Google Scholar 

  33. Seung HS, Sompolinsky H (1993) Simple models for reading neuronal population codes. Proc Natl Acad Sci USA 90:10749–10753

    Article  PubMed  CAS  Google Scholar 

  34. Salinas E, Abbott LF (1994) Vector reconstruction from firing rates. J Comput Neurosci 1:89–107

    Article  PubMed  CAS  Google Scholar 

  35. Zemel RS, Dayan P, Pouget A (1998) Probabilistic interpretation of population codes. Neural Comput 10:403–430

    Article  PubMed  CAS  Google Scholar 

  36. Daley DJ, Vere-Jones D (2003) An introduction to the theory of point processes. Springer, New York

    Google Scholar 

  37. Truccolo W, Eden UT, Fellows MR et al (2005) A point process framework for relating neural spiking activity to spiking history, neural ensemble, and extrinsic covariate effects. J Neurophysiol 93:1074–1089

    Article  PubMed  Google Scholar 

  38. Kloosterman F, Davidson TJ, Gomperts SN et al (2009) Micro-drive array for chronic in vivo recording: drive fabrication. J Vis Exp 26(pii):1094

    PubMed  Google Scholar 

  39. Nguyen DP, Layton SP, Hale G et al (2009) Micro-drive array for chronic in vivo recording: tetrode assembly. J Vis Exp 26(pii):1098

    PubMed  Google Scholar 

  40. Yamamoto J, Wilson MA (2008) Large-scale chronically implantable precision motorized microdrive array for freely behaving animals. J Neurophysiol 100:2430–2440

    Article  PubMed  Google Scholar 

  41. Buzsáki G (2004) Large-scale recording of neuronal ensembles. Nat Neurosci 7:446–451

    Article  PubMed  Google Scholar 

  42. Buzsáki G, Horváth Z, Urioste R et al (1992) High-frequency network oscillation in the hippocampus. Science 256:1025–1027

    Article  PubMed  Google Scholar 

  43. Csicsvari J, Hirase H, Mamiya A et al (2000) Ensemble patterns of hippocampal CA3-CA1 neurons during sharp wave-associated population events. Neuron 28:585–594

    Article  PubMed  CAS  Google Scholar 

  44. Ylinen A, Bragin A, Nádasdy Z et al (1995) Sharp wave-associated high-frequency oscillation (200 Hz) in the intact hippocampus: network and intracellular mechanisms. J Neurosci 15:30–46

    PubMed  CAS  Google Scholar 

  45. Schmitzer-Torbert N, Jackson J, Henze D et al (2005) Quantitative measures of cluster quality for use in extracellular recordings. Neuroscience 131:1–11

    Article  PubMed  CAS  Google Scholar 

  46. Quirk MC, Wilson MA (1999) Interaction between spike waveform classification and temporal sequence detection. J Neurosci Methods 94:41–52

    Article  PubMed  CAS  Google Scholar 

  47. Jensen O, Lisman JE (2000) Position reconstruction from an ensemble of hippocampal place cells: contribution of theta phase coding. J Neurophysiol 83:2602–2609

    PubMed  CAS  Google Scholar 

  48. Ego-Stengel V, Wilson MA (2007) Spatial selectivity and theta phase precession in CA1 interneurons. Hippocampus 17: 161–174

    Article  PubMed  Google Scholar 

  49. Quiroga RQ, Reddy L, Koch C et al (2007) Decoding visual inputs from multiple neurons in the human temporal lobe. J Neurophysiol 98:1997–2007

    Article  PubMed  Google Scholar 

  50. Treves A, Panzeri S (1995) The upward bias in measures of information derived from limited data samples. Neural Comput 7:399–407

    Article  Google Scholar 

  51. Toft PA (1996) The radon transform – theory and application. PhD thesis, Technical University of Denmark. http://petertoft.dk/PhD. Accessed on 2007

  52. Eden UT, Frank LM, Barbieri R et al (2004) Dynamic analysis of neural encoding by point process adaptive filtering. Neural Comput 16:971–998

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

I would like to thank Audrey Chang, Zhe Chen and Matt Wilson for their comments on an earlier version of this manuscript. Many thanks to Tom Davidson for the discussions about the methods presented in this chapter and for generously providing me with hippocampal unit data to prepare some of the figures.

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2011 Springer Science+Business Media, LLC

About this protocol

Cite this protocol

Kloosterman, F. (2011). Analysis of Hippocampal Memory Replay Using Neural Population Decoding. In: Fellin, T., Halassa, M. (eds) Neuronal Network Analysis. Neuromethods, vol 67. Humana Press. https://doi.org/10.1007/7657_2011_8

Download citation

  • DOI: https://doi.org/10.1007/7657_2011_8

  • Published:

  • Publisher Name: Humana Press

  • Print ISBN: 978-1-61779-632-6

  • Online ISBN: 978-1-61779-633-3

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics