Skip to main content
SpringerLink
Log in
Book cover

Hippocampal Microcircuits pp 293–312Cite as

Spatial and Behavioral Correlates of Hippocampal Neuronal Activity: A Primer for Computational Analysis

  • Chapter

Part of the book series: Springer Series in Computational Neuroscience ((NEUROSCI,volume 5))

Abstract

Hippocampal neurons are extraordinarily interesting to observe in action. As animals perform a variety of natural or learned behaviors, hippocampal principal cells of areas CA1 and CA3, which otherwise are characterized by very low baseline firing rates, suddenly fire at rapid rates related to the current location of the animal, its ongoing behavior, specific salient stimuli, or some combination of these factors and the context of the behavioral situation. Unlike in many brain areas where specific sensory or behavioral correlates of neuronal activity are difficult to observe, in the hippocampus it sometimes seems there are as many behavioral correlates as experimental paradigms in which they might be observed. The challenge is not to find correlates of neural activity in the hippocampus – it is to make sense of the broad range of sensory- and behavior-related firing properties observed.

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

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   219.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Further Reading

  • Ainge JA, Tamosiunaite M, Woergoetter F, & Dudchencko PA (2007) Hippocampal CA1 place cells encode intended destination on a maze with multiple choice points. J Neurosci 27: 9769–9779.

    Article  CAS  PubMed  Google Scholar 

  • Anderson MI, & Jeffery KJ (2003) Heterogeneous modulation of place cell firing by changes in context. J Neurosci 23: 8827–8835.

    CAS  PubMed  Google Scholar 

  • Bar M, & Aminoff E (2003) Cortical analysis of visual context. Neuron 38: 347–358.

    Article  CAS  PubMed  Google Scholar 

  • Best PJ, White AW, & Minai A (2001) Spatial processing in the brain: The activity of hippocampal place cells. Annu Rev Neurosci 24: 459–486.

    Article  CAS  PubMed  Google Scholar 

  • Bower MR, Euston DR, & McNaughton BL (2005) Sequential-context dependent hippocampal activity is not necessary to learn sequences with repeated elements. J Neurosci 15: 1313–1323.

    Article  CAS  Google Scholar 

  • Brown MW, & Xiang JZ (1998) Recognition memory: Neuronal substrates of the judgment of prior occurrence. Prog Neurobiol 55: 149–189.

    Article  CAS  PubMed  Google Scholar 

  • Brown MW, & Aggleton JP (2001) Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2: 51–61.

    Article  CAS  PubMed  Google Scholar 

  • Burwell RD (2000) The parahippocampal region: Corticocortical connectivity. Ann NY Acad Sci 911: 25–42.

    CAS  PubMed  Google Scholar 

  • Eichenbaum H, Otto T, & Cohen NJ (1994) Two functional components of the hippocampal memory system. Brain Behav Sci 17: 449–518.

    Google Scholar 

  • Eichenbaum H, Dudchencko P, Wood E, Shapiro M, & Tanila H (1999) The Hippocampus memory, and place cells: Is it spatial memory or a memory space? Neuron 23: 209–226.

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum H (2000) A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1: 41–50.

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum H (2004) Hippocampus: Cognitive processes and neural representations that underlie declarative memory. Neuron 44: 109–120.

    Article  CAS  PubMed  Google Scholar 

  • Eichenbaum H, Yonelinas AR, & Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 20: 123–152.

    Article  CAS  Google Scholar 

  • Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL, et al. (2003) Cellular networks underlying human spatial navigation. Nature 425: 184–187.

    Article  CAS  PubMed  Google Scholar 

  • Epstein R, & Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392: 598–601.

    Article  CAS  PubMed  Google Scholar 

  • Fenton AA, Wsierska M, Kaminsky Y, & Bures J (1998) Both here and there: Simultaneous expression of autonomous spatial memories in rats. PNAS USA, 95: 11493–11498.

    Article  CAS  PubMed  Google Scholar 

  • Ferbinteanu J, & Shapiro ML (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40: 1227–1239.

    Article  CAS  PubMed  Google Scholar 

  • Frank L, Brown EN, & Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27: 169–178.

    Article  CAS  PubMed  Google Scholar 

  • Fyhn M, Molden S, Hollup, Moser M-B, & Moser EI (2002) Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35: 555–566.

    Article  CAS  PubMed  Google Scholar 

  • Fyhn M, Molden S, Witter MP, Moser EI, & Moser M-B (2004) Spatial representation in the entorhinal cortex. Science 305: 1258–1264.

    Article  CAS  PubMed  Google Scholar 

  • Gothard KM, Skaggs WE, Moore KM, & McNaughton BL (1996a) Binding of hippocampal CA1 neural activity to multiple reference frames in a landmark-based navigation task. J Neurosci 16: 823–835.

    CAS  PubMed  Google Scholar 

  • Gothard KM, Skaggs W, & McNaughton BL (1996b) Dynamics of mismatch correction in the hippocampal ensemble code for space: Interaction between path integration and environmental cues. J Neurosci 16: 8027–8040.

    CAS  PubMed  Google Scholar 

  • Griffin AL, Eichenbaum H, & Hasselmo ME (2007) Spatial representations of hippocampal CA1 neurons are modulated by behavioral context in a hippocampus-dependent memory task. J Neurosci 27: 2416–2423.

    Article  CAS  PubMed  Google Scholar 

  • Hampson RE, Pons TP, Stanford TR, & Deadwyler SA (2004) Categorization in the monkey hippocampus: A possible mechanism for encoding information into memory. PNAS USA 101: 3184–3189.

    Article  CAS  PubMed  Google Scholar 

  • Hargreaves EL, Rao G, Lee I, & Knierim JJ (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 5729: 1792–1794.

    Article  CAS  Google Scholar 

  • Hok V, Lenck-Santini P-P, Roux S, Save E, Muller RU, & Poucet B (2007) Goal-related activity in hippocampal place cells. J Neurosci 27: 472–482.

    Article  CAS  PubMed  Google Scholar 

  • Hollup SA, Molden S, Donnett JG, Moser M-B, & Moser EI (2001) Accumulation of hippocampal place fields at the goal location in an annular watermaze task. J Neurosci 21: 1635–1644.

    CAS  PubMed  Google Scholar 

  • Jackson J, & Redish AD (2007) Network dynamics of hippocampal cell assemblies resemble multiple spatial maps within single trials. Hippocampus 17(12): 1209–1229.

    Article  PubMed  Google Scholar 

  • Kreiman G, Koch C, & Fried I (2000) Category-specific visual responses of single neurons in the human medial temporal lobe. Nat Neurosci 3: 946–953.

    Article  CAS  PubMed  Google Scholar 

  • Lee I, Yoganarasimha D, Rao G, & Knierim JJ (2004) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430: 456–459.

    Article  CAS  PubMed  Google Scholar 

  • Lee I, Griffin AL, Zilli EA, Eichenbaum H, & Hasselmo M (2006) Gradual translocation of spatial correlates of neuronal firing in the hippocampus toward prospective reward locations. Neuron 51: 539–650.

    Google Scholar 

  • Leutgeb S, Leutgeb JK, Treves A, Moser M-B, & Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305: 1295–1298.

    Article  CAS  PubMed  Google Scholar 

  • Leutgeb S, Leutgeb JK, Barnes CA, Moser EI, McNaughton BL, & Moser M-B (2005a) Independent codes for spatial and episodic memory in hippocampal neuronal ensembles. Science 309: 619–623.

    Article  CAS  PubMed  Google Scholar 

  • Leutgeb S, Leutgeb JK, Moser M-B, & Moser EI (2005b) Place cells, spatial maps, and the population code for memory. Curr Opin Neurobiol 15: 1–9.

    Article  CAS  Google Scholar 

  • Lipton PA, White J, & Eichenbaum H (2007) Disambiguation of overlapping experiences by neurons the medial entorhinal cortex. J Neurosci 27: 5787–5795.

    Article  CAS  PubMed  Google Scholar 

  • Louie K, & Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29: 145–156.

    Article  CAS  PubMed  Google Scholar 

  • Manns JR, & Eichenbaum H (2006) Evolution of the hippocampus. In J.H. Kaas, (Ed.), Evolution of nervous systems. Vol 3. (pp. 465–490) Oxford, UK: Academic Press.

    Google Scholar 

  • Manns JR, Howard M,& Eichenbaum H (2007) Gradual changes in hippocampal activity support remembering the order of events. Neuron 56: 530–540.

    Article  CAS  PubMed  Google Scholar 

  • McNaughton BL, Chen L, & Markus EJ (1991) “Dead reckoning”, landmark learning, and the sense of direction: A neurophysiological and computational hypothesis. J Cog Neuro 3: 190–202.

    Article  Google Scholar 

  • McNaughton BL, Battaglia FP, Jensen O, Moser EI, & Moser M-B (2007) Path integration and the neural basis of the ‘cognitive map’. Nat Rev Neurosci 7: 663–678.

    Article  CAS  Google Scholar 

  • Markus EJ, Qin Y-L, Leonard B, Skaggs WE, McNaughton BL, & Barnes CA (1995) Interactions between location and task affect the spatial and directional firing of hippocampal neurons. J Neurosci 15: 7079–7094.

    CAS  PubMed  Google Scholar 

  • Moita MA, Rosis S, Zhou Y, LeDoux JE, & Blair HT (2003) Hippocampal place cells acquire location-specific responses to the conditioned stimulus during auditory fear conditioning. Neuron 37: 485–497.

    Article  CAS  PubMed  Google Scholar 

  • Muller RU, Kubie JL,& Ranck JB Jr. (1987) Spatial firing patterns of hippocampal complex spike cells in a fixed environment. J Neurosci 7: 1935–1950.

    CAS  PubMed  Google Scholar 

  • Muller RU (1996) A quarter of a century of place cells. Neuron 17: 813–822.

    Article  CAS  PubMed  Google Scholar 

  • O’Keefe JA (1979) A review of hippocampal place cells. Prog Neurobiol 13: 419–439.

    Article  PubMed  Google Scholar 

  • O’Keefe J, & Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381: 425–428.

    Article  PubMed  Google Scholar 

  • Olton DS, Branch M,& Best PJ (1978) Spatial correlates hippocampal unit activity. Exp Neuro 58: 387–409.

    Article  CAS  Google Scholar 

  • Rivard B, Li Y, Lenck-Santini P-P, Poucet B, & Muller RU (2004) Representation of objects in space by two classes of hippocampal pyramidal cells. J Gen Physiol 124: 9–25.

    Article  PubMed  Google Scholar 

  • Rotenberg A, & Muller RU (1997) Variable place-cell coupling to a continuously viewed stimulus: evidence that the hippocampus acts as a perceptual system. Philos Trans R Soc Lond B 352: 1505–1513.

    Article  CAS  Google Scholar 

  • Sargolini F, Fyhn M, Hafting T, McNaughton BL, Witter MP, Moser M-B, Moser EI (2006) Conjunctive representation of position, direction, and velocity in entorhinal cortex. Science 312: 758–762.

    Article  CAS  PubMed  Google Scholar 

  • Shapiro ML, Tanila H, & Eichenbaum H (1997) Cues that hippocampal place cells encode: Dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7: 624–642.

    Article  CAS  PubMed  Google Scholar 

  • Skaggs WE, & McNaughton BL (1998) Spatial firing properties of hippocampal CA1 populations in an environment containing two visually identical regions. J Neurosci 18: 8455–8466.

    CAS  PubMed  Google Scholar 

  • Squire LR, Stark CE,& Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27: 279–306.

    Article  CAS  PubMed  Google Scholar 

  • Suzuki WA, & Amaral DG (1994) Perirhinal and parahippocampal cortices of the macaque monkey: Cortical afferents. J Comp Neuro 350: 497–533.

    Article  CAS  Google Scholar 

  • Suzuki W, & Eichenbaum H (2000) The neurophysiology of memory. Ann NY Acad Sci 911: 175–191.

    Article  CAS  PubMed  Google Scholar 

  • Tanila H, Shapiro M, Gallagher M, & Eichenbaum H (1997a) Brain aging: Impaired coding of novel environmental cues. J Neurosci 17: 5167–5174.

    CAS  PubMed  Google Scholar 

  • Tanila H, Shapiro ML, & Eichenbaum H (1997b) Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7: 613–623.

    Article  CAS  PubMed  Google Scholar 

  • Tanila H, Sipila P, Shapiro M, & Eichenbaum H (1997c) Brain aging: Changes in the nature of information coding by the hippocampus. J Neurosci 17: 5155–5166.

    CAS  PubMed  Google Scholar 

  • Wan H, Aggleton JP, & Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19: 1142–1148.

    CAS  PubMed  Google Scholar 

  • Wiener SI, Paul CA,& Eichenbaum H (1989) Spatial and behavioral correlates of hippocampal neuronal activity. J Neurosci 9: 2737–2763.

    CAS  PubMed  Google Scholar 

  • Wills TJ, Lever C, Cacucci F, Burgess N, & O’Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308: 873–876.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Wirth S, Yanike M, Frank LM, Smith AC, Brown EN, & Suzuki WA (2003) Single neurons in the monkey hippocampus and learning of new associations. Science 300: 1578–1581.

    Article  CAS  PubMed  Google Scholar 

  • Wood E, Dudchenko PA,& Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397: 613–616.

    Article  CAS  PubMed  Google Scholar 

  • Wood E, Dudchenko P, Robitsek JR, & Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27: 623–633.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Center for Memory and Brain, Boston University, Boston, MA, 02215, USA

    Howard Eichenbaum

Authors
  1. Howard Eichenbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Howard Eichenbaum .

Editor information

Editors and Affiliations

  1. Department of Computing Science and Mathematics, University of Stirling, Stirling, FK9 4LA, UK

    Vassilis Cutsuridis  & Bruce Graham  & 

  2. Neuroscience & Molecular Pharmacology, Faculty of Biomedical and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, UK

    Stuart Cobb  & Imre Vida  & 

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer Science+Business Media, LLC

About this chapter

Cite this chapter

Eichenbaum, H. (2010). Spatial and Behavioral Correlates of Hippocampal Neuronal Activity: A Primer for Computational Analysis. In: Cutsuridis, V., Graham, B., Cobb, S., Vida, I. (eds) Hippocampal Microcircuits. Springer Series in Computational Neuroscience, vol 5. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-0996-1_10

Download citation

Publish with us

Policies and ethics

Search

Navigation