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

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Book cover Hippocampal Microcircuits

Part of the book series: Springer Series in Computational Neuroscience ((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.

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References

  • 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  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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, Aggleton JP (2001) Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neuroscience 2:51–61

    Article  CAS  PubMed  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 

  • Burwell RD (2000) The parahippocampal region: corticocortical connectivity. Ann N Y Acad Sci 911:25–42

    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 (2013) Memory on time. Trends Cogn Sci 17:81–88

    Article  PubMed  PubMed Central  Google Scholar 

  • Eichenbaum H (2014) Time cells in the hippocampus: a new dimension for mapping memories. Nat Rev Neurosci 15:732–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  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, 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 95:11493–11,498

    Article  CAS  PubMed  PubMed Central  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 S, 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 

  • 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 322:96–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gill PR, Mizumori SJ, Smith DM (2011) Hippocampal episode fields develop with learning. Hippocampus 21:1240–1249

    Article  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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  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  PubMed Central  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  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howard MW, Eichenbaum H (2013) The hippocampus, time, and memory across scales. J Exp Psychol Gen 142:1211–1230

    Article  PubMed  PubMed Central  Google Scholar 

  • Hsieh LT, Gruber MJ, Jenkins LJ, Ranganath C (2014) Hippocampal activity patterns carry information about objects in temporal context. Neuron 81:1165–1178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 107:1822–1834

    Article  PubMed  PubMed Central  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 

  • Komorowski RW, Manns JR, Eichenbaum H (2009) Robust conjunctive item-place coding by hippocampal neurons parallels learning what happens. J Neurosci 29:9918–9929

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kraus BJ, Robinson RJ II, White JA, Eichenbaum H, Hasselmo ME (2013) Hippocampal ‘time cells’: time versus path integration. Neuron 78:1090–1101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 88:578–589

    Article  CAS  PubMed  PubMed Central  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 

  • 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 243–305

    Chapter  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  PubMed Central  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 

  • MacDonald CJ, Lepage KQ, Eden UT, Eichenbaum H (2011) Hippocampal “time cells” bridge the gap in memory for discontiguous events. Neuron 71:737–749

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • MacDonald CJ, Carrow S, Place R, Eichenbaum H (2013) Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J Neurosci 33:14607–14,616

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Manns JR, Eichenbaum H (2006) Evolution of the hippocampus. In: Kaas JH (ed) Evolution of nervous systems, vol 3. Academic, Oxford, pp 465–490

    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  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 83:202–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  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 

  • Modi MN, Dhawale AK, Bhalla US (2014) CA1 cell activity sequences emerge after reorganization of network correlation structure during associative learning. elife 3:e01982

    Article  PubMed  PubMed Central  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 (1996) A quarter of a century of place cells. Neuron 17:813–822

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naya Y, Suzuki WA (2011) Integrating what and when across the primate medial temporal lobe. Science 333:773–776

    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 Neurol 58:387–409

    Article  CAS  PubMed  Google Scholar 

  • Pastalkova E, Itskov V, Amarasingham A, Buzsaki G (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321(5894):1322–1327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 107:6046–6051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer BE, Foster DJ (2013) Hippocampal place cell sequences depict future paths to remembered goals. Nature 497:74–79

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfeiffer BE, Foster DJ (2015) Autoassociative dynamics in the generation of sequences of hippocampal place cells. Science 349:180–183

    Article  CAS  PubMed  Google Scholar 

  • Rawlins JNP (1985) Associations across time: The hippocampus as a temporary memory store. Behav Brain Sci 8:479–496

    Article  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  PubMed Central  Google Scholar 

  • Robitsek JR, White J, Eichenbaum H (2013) Place cell activation predicts subsequent memory. Behav Brain Res 254:65–72

    Article  PubMed  PubMed Central  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 

  • 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 35:13904–13,911

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  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 Neurol 350:497–533

    Article  CAS  PubMed  Google Scholar 

  • Suzuki W, Eichenbaum H (2000) The neurophysiology of memory. Ann N Y 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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tulving E (1983) Elements of episodic memory. Oxford Univ Press, New York

    Google Scholar 

  • Vinnik E, Antopolskiy S, Itskov PM, Diamond ME (2012) Auditory stimuli elicit hippocampal neuronal responses during sleep. Front Syst Neurosci 6:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Wallenstein GV, Eichenbaum H, Hasselmo ME (1998) The hippocampus as an associator of discontiguous events. Trends Neurosci 21:315–365

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  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 

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Authors and Affiliations

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

    Howard Eichenbaum

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  1. Howard Eichenbaum
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Correspondence to Howard Eichenbaum .

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Editors and Affiliations

  1. School of Computer Science, University of Lincoln, Lincoln, UK

    Vassilis Cutsuridis

  2. School of Natural Sciences, Department of Computing Science and Mathematics, University of Stirling, Stirling, UK

    Bruce P. Graham

  3. Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, UK

    Stuart Cobb

  4. Institute for Integrative Neuroanatomy, Charité – Universitätsmedizin Berlin, Berlin, Germany

    Imre Vida

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Eichenbaum, H. (2018). Spatial, Temporal, 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. Springer, Cham. https://doi.org/10.1007/978-3-319-99103-0_10

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