Advertisement

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

  • Howard EichenbaumEmail author
Chapter
Part of the Springer Series in Computational Neuroscience book series (NEUROSCI)

Abstract

Creating useful models of the hippocampus will rely upon our ability to bridge between local circuitry and behavior. A critical intermediate between these levels is the functional activity of hippocampal principal neurons, the elements of neuronal information processing. This chapter provides an overview of the functional correlates of hippocampal neuronal activity, focusing on the nature of inputs these neurons receive; the broad range of sensory, behavioral, and spatial and temporal features of events captured by firing patterns of hippocampal neurons; and a framework for thinking about how the hippocampus organizes information from its inputs to support memory coding and retrieval.

References

  1. 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 27:9769–9779PubMedCrossRefGoogle Scholar
  2. Anderson MI, Jeffery KJ (2003) Heterogeneous modulation of place cell firing by changes in context. J Neurosci 23:8827–8835PubMedCrossRefGoogle Scholar
  3. Bar M, Aminoff E (2003) Cortical analysis of visual context. Neuron 38:347–358PubMedCrossRefGoogle Scholar
  4. Best PJ, White AW, Minai A (2001) Spatial processing in the brain: the activity of hippocampal place cells. Annu Rev Neurosci 24:459–486PubMedCrossRefGoogle Scholar
  5. Bower MR, Euston DR, McNaughton BL (2005) Sequential-context dependent hippocampal activity is not necessary to learn sequences with repeated elements. J Neurosci 15:1313–1323CrossRefGoogle Scholar
  6. Brown MW, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neuroscience 2:51–61PubMedCrossRefGoogle Scholar
  7. Brown MW, Xiang JZ (1998) Recognition memory: neuronal substrates of the judgment of prior occurrence. Prog Neurobiol 55:149–189PubMedCrossRefGoogle Scholar
  8. Burwell RD (2000) The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci 911:25–42PubMedCrossRefGoogle Scholar
  9. Eichenbaum H (2000) A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 1:41–50PubMedCrossRefGoogle Scholar
  10. Eichenbaum H (2004) Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44:109–120PubMedCrossRefPubMedCentralGoogle Scholar
  11. Eichenbaum H (2013) Memory on time. Trends Cogn Sci 17:81–88PubMedPubMedCentralCrossRefGoogle Scholar
  12. Eichenbaum H (2014) Time cells in the hippocampus: a new dimension for mapping memories. Nat Rev Neurosci 15:732–744PubMedPubMedCentralCrossRefGoogle Scholar
  13. Eichenbaum H, Otto T, Cohen NJ (1994) Two functional components of the hippocampal memory system. Brain Behav Sci 17:449–518CrossRefGoogle Scholar
  14. 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 23:209–226PubMedCrossRefGoogle Scholar
  15. Eichenbaum H, Yonelinas AR, Ranganath C (2007) The medial temporal lobe and recognition memory. Annu Rev Neurosci 20:123–152CrossRefGoogle Scholar
  16. Ekstrom AD, Kahana MJ, Caplan JB, Fields TA, Isham EA, Newman EL et al (2003) Cellular networks underlying human spatial navigation. Nature 425:184–187CrossRefPubMedGoogle Scholar
  17. Epstein R, Kanwisher N (1998) A cortical representation of the local visual environment. Nature 392:598–601PubMedCrossRefGoogle Scholar
  18. Fenton AA, Wsierska M, Kaminsky Y, Bures J (1998) Both here and there: simultaneous expression of autonomous spatial memories in rats. PNAS USA 95:11493–11,498PubMedCrossRefGoogle Scholar
  19. Ferbinteanu J, Shapiro ML (2003) Prospective and retrospective memory coding in the hippocampus. Neuron 40:1227–1239PubMedCrossRefGoogle Scholar
  20. Frank L, Brown EN, Wilson M (2000) Trajectory encoding in the hippocampus and entorhinal cortex. Neuron 27:169–178PubMedCrossRefPubMedCentralGoogle Scholar
  21. Fyhn M, Molden S, Hollup S, Moser M-B, Moser EI (2002) Hippocampal neurons responding to first-time dislocation of a target object. Neuron 35:555–566PubMedCrossRefPubMedCentralGoogle Scholar
  22. Fyhn M, Molden S, Witter MP, Moser EI, Moser M-B (2004) Spatial representation in the entorhinal cortex. Science 305:1258–1264PubMedCrossRefPubMedCentralGoogle Scholar
  23. Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I (2008) Internally generated reactivation of single neurons in human hippocampus during free recall. Science 322:96–101PubMedPubMedCentralCrossRefGoogle Scholar
  24. Gill PR, Mizumori SJ, Smith DM (2011) Hippocampal episode fields develop with learning. Hippocampus 21:1240–1249PubMedCrossRefGoogle Scholar
  25. 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 16:823–835PubMedCrossRefGoogle Scholar
  26. 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 16:8027–8040PubMedCrossRefPubMedCentralGoogle Scholar
  27. 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 27:2416–2423PubMedCrossRefPubMedCentralGoogle Scholar
  28. Hampson RE, Pons TP, Stanford TR, Deadwyler SA (2004) Categorization in the monkey hippocampus: a possible mechanism for encoding information into memory. PNAS USA 101:3184–3189PubMedCrossRefPubMedCentralGoogle Scholar
  29. Hargreaves EL, Rao G, Lee I, Knierim JJ (2005) Major dissociation between medial and lateral entorhinal input to dorsal hippocampus. Science 5729:1792–1794CrossRefGoogle Scholar
  30. Hok V, Lenck-Santini P-P, Roux S, Save E, Muller RU, Poucet B (2007) Goal-related activity in hippocampal place cells. J Neurosci 27:472–482PubMedCrossRefGoogle Scholar
  31. 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 21:1635–1644PubMedCrossRefGoogle Scholar
  32. Howard MW, Eichenbaum H (2013) The hippocampus, time, and memory across scales. J Exp Psychol Gen 142:1211–1230PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hsieh LT, Gruber MJ, Jenkins LJ, Ranganath C (2014) Hippocampal activity patterns carry information about objects in temporal context. Neuron 81:1165–1178PubMedPubMedCentralCrossRefGoogle Scholar
  34. Itskov PM, Vinnik E, Diamond ME (2011) Hippocampal representation of touch-guided behavior in rats: persistent and independent traces of stimulus and reward location. PLoS One 6(1):e16462.  https://doi.org/10.1371/journal.pone.0016462 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Itskov PM, Vinnik E, Honey C, Schnupp J, Diamond ME (2012) Sound sensitivity of neurons in rat hippocampus during performance of a sound-guided task. J Neurophysiol 107:1822–1834PubMedPubMedCentralCrossRefGoogle Scholar
  36. Jackson J, Redish AD (2007) Network dynamics of hippocampal cell assemblies resemble multiple spatial maps within single trials. Hippocampus 17(12):1209–1229PubMedCrossRefGoogle Scholar
  37. Komorowski RW, Manns JR, Eichenbaum H (2009) Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens. J Neurosci 29:9918–9929PubMedPubMedCentralCrossRefGoogle Scholar
  38. Kraus BJ, Robinson RJ II, White JA, Eichenbaum H, Hasselmo ME (2013) Hippocampal ‘time cells’: time versus path integration. Neuron 78:1090–1101PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kraus BJ, Brandon MP, Robinson RJ 2nd, Connerney MA, Hasselmo ME, Eichenbaum H (2015) During running in place, grid cells integrate elapsed time and distance run. Neuron 88:578–589PubMedPubMedCentralCrossRefGoogle Scholar
  40. Kreiman G, Koch C, Fried I (2000) Category-specific visual responses of single neurons in the human medial temporal lobe. Nat Neurosci 3:946–953PubMedCrossRefGoogle Scholar
  41. Lee I, Yoganarasimha D, Rao G, Knierim JJ (2004) Comparison of population coherence of place cells in hippocampal subfields CA1 and CA3. Nature 430:456–459PubMedCrossRefGoogle Scholar
  42. 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 51:539–650Google Scholar
  43. Leutgeb S, Leutgeb JK, Treves A, Moser M-B, Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295–1298PubMedCrossRefGoogle Scholar
  44. 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 309:619–623PubMedCrossRefGoogle Scholar
  45. Leutgeb S, Leutgeb JK, Moser M-B, Moser EI (2005b) Place cells, spatial maps, and the population code for memory. Curr Opin Neurobiol 15:1–9CrossRefGoogle Scholar
  46. Levy WB (1989) A Computational approach to hippocampal function. In: Hawkins RD, Bowers GH (eds) Computational models of learning in simple neural systems. Academic, San Diego, pp 243–305CrossRefGoogle Scholar
  47. Lipton PA, White J, Eichenbaum H (2007) Disambiguation of overlapping experiences by neurons the medial entorhinal cortex. J Neurosci 27:5787–5795PubMedCrossRefGoogle Scholar
  48. Louie K, Wilson MA (2001) Temporally structured replay of awake hippocampal ensemble activity during rapid eye movement sleep. Neuron 29:145–156PubMedCrossRefGoogle Scholar
  49. MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H (2011) Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron 71:737–749PubMedPubMedCentralCrossRefGoogle Scholar
  50. MacDonald CJ, Carrow S, Place R, Eichenbaum H (2013) Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J Neurosci 33:14607–14,616PubMedPubMedCentralCrossRefGoogle Scholar
  51. Manns JR, Eichenbaum H (2006) Evolution of the hippocampus. In: Kaas JH (ed) Evolution of nervous systems, vol 3. Academic, Oxford, pp 465–490Google Scholar
  52. Manns JR, Howard M, Eichenbaum H (2007) Gradual changes in hippocampal activity support remembering the order of events. Neuron 56:530–540PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 15:7079–7094PubMedCrossRefPubMedCentralGoogle Scholar
  54. McKenzie S, Frank AJ, Kinsky NR, Porter B, Rivière PD, Eichenbaum H (2014) Hippocampal representation of related and opposing memories develop within distinct, hierarchically-organized neural schemas. Neuron 83:202–215PubMedPubMedCentralCrossRefGoogle Scholar
  55. McNaughton BL, Chen L, Markus EJ (1991) “Dead reckoning”, landmark learning, and the sense of direction: a neurophysiological and computational hypothesis. J Cogn Neurosci 3:190–202PubMedCrossRefPubMedCentralGoogle Scholar
  56. 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 7:663–678CrossRefGoogle Scholar
  57. Modi MN, Dhawale AK, Bhalla US (2014) CA1 cell activity sequences emerge after reorganization of network correlation structure during associative learning. elife 3:e01982PubMedPubMedCentralCrossRefGoogle Scholar
  58. 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 37:485–497PubMedCrossRefGoogle Scholar
  59. Muller RU (1996) A quarter of a century of place cells. Neuron 17:813–822PubMedCrossRefGoogle Scholar
  60. Muller RU, Kubie JL, Ranck JB Jr (1987) Spatial firing patterns of hippocampal complex spike cells in a fixed environment. J Neurosci 7:1935–1950PubMedCrossRefGoogle Scholar
  61. Naya Y, Suzuki WA (2011) Integrating what and when across the primate medial temporal lobe. Science 333:773–776PubMedCrossRefGoogle Scholar
  62. O’Keefe JA (1979) A review of hippocampal place cells. Prog Neurobiol 13:419–439PubMedCrossRefPubMedCentralGoogle Scholar
  63. O’Keefe J, Burgess N (1996) Geometric determinants of the place fields of hippocampal neurons. Nature 381:425–428PubMedCrossRefPubMedCentralGoogle Scholar
  64. Olton DS, Branch M, Best PJ (1978) Spatial correlates hippocampal unit activity. Exp Neurol 58:387–409PubMedCrossRefPubMedCentralGoogle Scholar
  65. Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321(5894):1322–1327PubMedPubMedCentralCrossRefGoogle Scholar
  66. Paz R, Gelbard-Sagiv H, Mukamel R, Harel M, Malach R, Fried I (2010) A neural substrate in the human hippocampus for linking successive events. Proc Natl Acad Sci U S A 107:6046–6051PubMedPubMedCentralCrossRefGoogle Scholar
  67. Pfeiffer BE, Foster DJ (2013) Hippocampal place cell sequences depict future paths to remembered goals. Nature 497:74–79PubMedPubMedCentralCrossRefGoogle Scholar
  68. Pfeiffer BE, Foster DJ (2015) Autoassociative dynamics in the generation of sequences of hippocampal place cells. Science 349:180–183PubMedCrossRefGoogle Scholar
  69. Rawlins JNP (1985) Associations across time: The hippocampus as a temporary memory store. Behav Brain Sci 8:479–496CrossRefGoogle Scholar
  70. 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 124:9–25PubMedPubMedCentralCrossRefGoogle Scholar
  71. Robitsek JR, White J, Eichenbaum H (2013) Place cell activation predicts subsequent memory. Behav Brain Res 254:65–72PubMedPubMedCentralCrossRefGoogle Scholar
  72. 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 352:1505–1513CrossRefGoogle Scholar
  73. 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 312:758–762PubMedCrossRefGoogle Scholar
  74. Schiller D, Eichenbaum H, Buffalo EA, Davachi L, Foster DJ, Leutgeb S, Ranganath C (2015) Memory and space: towards an understanding of the cognitive map. J Neurosci 35:13904–13,911PubMedPubMedCentralCrossRefGoogle Scholar
  75. Shapiro ML, Tanila H, Eichenbaum H (1997) Cues that hippocampal place cells encode: Dynamic and hierarchical representation of local and distal stimuli. Hippocampus 7:624–642PubMedCrossRefGoogle Scholar
  76. Skaggs WE, McNaughton BL (1998) Spatial firing properties of hippocampal CA1 populations in an environment containing two visually identical regions. J Neurosci 18:8455–8466PubMedCrossRefGoogle Scholar
  77. Squire LR, Stark CE, Clark RE (2004) The medial temporal lobe. Annu Rev Neurosci 27:279–306PubMedCrossRefGoogle Scholar
  78. Suzuki WA, Amaral DG (1994) Perirhinal and parahippocampal cortices of the macaque monkey: cortical afferents. J Comp Neurol 350:497–533PubMedCrossRefGoogle Scholar
  79. Suzuki W, Eichenbaum H (2000) The neurophysiology of memory. Ann N Y Acad Sci 911:175–191PubMedCrossRefGoogle Scholar
  80. Tanila H, Shapiro M, Gallagher M, Eichenbaum H (1997a) Brain Aging: impaired coding of novel environmental cues. J Neurosci 17:5167–5174PubMedCrossRefGoogle Scholar
  81. Tanila H, Shapiro ML, Eichenbaum H (1997b) Discordance of spatial representation in ensembles of hippocampal place cells. Hippocampus 7:613–623PubMedCrossRefGoogle Scholar
  82. Tanila H, Sipila P, Shapiro M, Eichenbaum H (1997c) Brain aging: changes in the nature of information coding by the hippocampus. J Neurosci 17:5155–5166PubMedCrossRefGoogle Scholar
  83. Tulving E (1983) Elements of episodic memory. Oxford Univ Press, New YorkGoogle Scholar
  84. Vinnik E, Antopolskiy S, Itskov PM, Diamond ME (2012) Auditory stimuli elicit hippocampal neuronal responses during sleep. Front Syst Neurosci 6:49PubMedPubMedCentralCrossRefGoogle Scholar
  85. Wallenstein GV, Eichenbaum H, Hasselmo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21:315–365CrossRefGoogle Scholar
  86. Wan H, Aggleton JP, Brown MW (1999) Different contributions of the hippocampus and perirhinal cortex to recognition memory. J Neurosci 19:1142–1148PubMedCrossRefGoogle Scholar
  87. Wiener SI, Paul CA, Eichenbaum H (1989) Spatial and behavioral correlates of hippocampal neuronal activity. J Neurosci 9:2737–2763PubMedCrossRefGoogle Scholar
  88. Wills TJ, Lever C, Cacucci F, Burgess N, O’Keefe J (2005) Attractor dynamics in the hippocampal representation of the local environment. Science 308:873–876PubMedPubMedCentralCrossRefGoogle Scholar
  89. Wilson M, McNaughton BL (1993) Dynamics of the hippocampal ensemble code for space. Science 261:1055–1058PubMedCrossRefGoogle Scholar
  90. 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 300:1578–1581PubMedCrossRefGoogle Scholar
  91. Wood E, Dudchenko PA, Eichenbaum H (1999) The global record of memory in hippocampal neuronal activity. Nature 397:613–616PubMedCrossRefPubMedCentralGoogle Scholar
  92. 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 27:623–633PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2018

Authors and Affiliations

  1. 1.Center for Memory and BrainBoston UniversityBostonUSA

Personalised recommendations