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What Versus Where: Non-spatial Aspects of Memory Representation by the Hippocampus

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Part of the book series: Current Topics in Behavioral Neurosciences ((CTBN,volume 37))

Abstract

Since the discovery of place cells and other findings indicating strong involvement of the hippocampus in spatial information processing, there has been continued controversy about the extent to which the hippocampus also processes non-spatial aspects of experience. In recent years, many experiments studying the effects of hippocampal damage and characterizing hippocampal neural activity in animals and humans have revealed a clear and specific role of the hippocampus in the processing of non-spatial information. Here this evidence is reviewed in support of the notion that the hippocampus organizes the contents of memory in space, in time, and in networks of related memories.

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References

  • Ainge JA, van der Meer MA, Langstron RF, Wood ER (2007a) Exploring the role of context-dependent hippocampal activity in spatial alternation behavior. Hippocampus 17:988–1002

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Alvarez P, Wendelken L, Eichenbaum H (2002) Hippocampal formation lesions impair performance in an odor-odor association task independently of spatial context. Neurobiol Learn Mem 8:79–86

    Article  Google Scholar 

  • Bachevalier J, Nemanic S, Alvarado MC (2015) The influence of context on recognition memory in monkeys: effects of hippocampal, parahippocampal, and perirhinal lesions. Behav Brain Res 285:89–98

    Article  Google Scholar 

  • Berger TW, Rinaldi PC, Weisz DJ, Thompson RF (1983) Single-unit analysis of different hippocampal cell types during classical conditioning of rabbit nictitating membrane response. J Neurophsiol 50:1197–1219

    Article  CAS  Google Scholar 

  • Broadbent NJ, Squire LR, Clark RE (2004) Spatial memory, recognition memory, and the hippocampus. Proc Natl Acad Sci USA 101:14515–14520

    Article  CAS  Google Scholar 

  • Bunsey M, Eichenbaum H (1996) Conservation of hippocampal memory function in rats and humans. Nature 379:255–257

    Article  CAS  Google Scholar 

  • Butterly DA, Petroccione MA, Smith DM (2012) Hippocampal context processing is critical for interference free recall of odor memories in rats. Hippocampus 22:906–913

    Article  Google Scholar 

  • Cameron KA, Yashar S, Wilson CL, Fried I (2007) Human hippocampal neurons predict how well word pairs will be remembered. Neuron 30:289–298

    Article  Google Scholar 

  • Clark RE, Zola SM, Squire LR (2000) Impaired recognition memory in rats after damage to the hippocampus. J Neurosci 20:8853–8860

    CAS  PubMed  Google Scholar 

  • Clark R, West AN, Zola S, Squire LR (2001) Rats with lesions of the hippocampus are impaired on the delayed nonmatching-to-sample task. Hippocampus 11:176–186

    Article  CAS  Google Scholar 

  • Cohen SJ, Stackman RW Jr (2015) Assessing rodent hippocampal involvement in the novel object recognition task. A review. Behav Brain Res 285:105–117

    Article  Google Scholar 

  • Cohen SJ, Munchow AH, Rios LM, Zhang G, Asgeirsdottir HN, Stackman RW (2013) The rodent hippocampus is essential for nonspatial object memory. Curr Biol 23:1685–1690

    Article  CAS  Google Scholar 

  • Davachi L (2006) Item, context and relational episodic encoding in humans. Curr Opin Neurobiol 16:693–700

    Article  CAS  Google Scholar 

  • Davachi L, Mitchell J, Wagner AD (2003) Multiple routes to memory: distinct medial temporal lobe processes built item and source memories. Proc Natl Acad Sci 100:2157–2162

    Article  CAS  Google Scholar 

  • Deadwyler SA, Bunn T, Hampson RE (1995) Hippocampal ensemble activity during spatial delayed-nonmatch-to-sample performance in rats. J Neurosci 16:354–372

    Google Scholar 

  • Diana RA, Yonelinas AP, Ranganath C (2007) Imaging recollection and familiarity in the medial temporal lobe: a three-component model. Trends Cogn Sci 11:379–386

    Article  Google Scholar 

  • Dusek JA, Eichenbaum H (1997) The hippocampus and memory for orderly stimulus relations. Proc Natl Acad Sci 94:7109–7114

    Article  CAS  Google Scholar 

  • Dusek JA, Eichenbaum H (1998) The hippocampus and transverse patterning guided by olfactory cues. Behav Neurosci 112:762–771

    Article  CAS  Google Scholar 

  • Eacott MJ, Norman G (2004) Integrated memory for object, place, and context in rats, a possible model of episodic-like memory? J Neurosci 24:1948–1953

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Eichenbaum H (2010) Spatial and behavioral correlates of hippocampal neuronal activity: a primer for computational analysis. In: Cutsuridis V, Graham B, Cob S, Vida I (eds) Hippocampal microcircuits: a computational modeller’s resource book. Springer, NY

    Chapter  Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Eichenbaum H, Fagan A, Mathews P, Cohen N (1988) Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. Behav Neurosci 102:331–339

    Article  CAS  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  Google Scholar 

  • Eichenbaum H, Yonelinas AR, Ranganath C (2007) The medial temporal lobe and recognition memory. Ann Rev Neurosci 30:123–152

    Article  CAS  Google Scholar 

  • Ergorul C, Eichenbaum H (2004) The hippocampus and memory for “what,” “where,” and “when”. Learn Mem 11:397–405

    Article  Google Scholar 

  • Ezzyat Y, Davachi L (2014) Similarity breeds proximity: pattern similarity within and across contexts is related to later mnemonic judgments of temporal proximity. Neuron 81:1179–1189

    Article  CAS  Google Scholar 

  • Farovik A, Dupont LM, Arce M, Eichenbaum H (2008) Medial prefrontal cortex supports recollection, but not familiarity, in the rat. J Neurosci 28:13428–13434

    Article  CAS  Google Scholar 

  • Fortin NJ et al (2002) Critical role of the hippocampus in memory for sequences of events. Nat Neurosci 5:458–462

    Article  CAS  Google Scholar 

  • Fortin NJ, Wright SP, Eichenbaum H (2004) Recollection-like memory retrieval in rats is dependent on the hippocampus. Nature 431:188–191

    Article  CAS  Google Scholar 

  • Fried I, MacDonald KA, Wilson CL (1997) Single neurons activity in human hippocampus and amygdala during recognition of faces and objects. Neuron 18:753–765

    Article  CAS  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  Google Scholar 

  • Gill PR et al (2011) Hippocampal episode fields develop with learning. Hippocampus. 21:1240–1249

    Article  Google Scholar 

  • Hannula DE, Ranganath C (2009) The eyes have it: hippocampal activity predicts expression of relational memory in eye movements. Neuron 63:592–599

    Article  CAS  Google Scholar 

  • Hartley T, Lever C, Burgess N, O’Keefe J (2014) Space in the brain: how the hippocampal formation supports spatial cognition. Phil Trans R Soc B 369:20120510

    Article  Google Scholar 

  • Hattori S, Chen L, Weiss C, Disterhoft JF (2015) Robust hippocampal responsivity during retrieval of consolidated associative memory. Hippocampus 25:655–669

    Article  Google Scholar 

  • Henke K, Buck A, Weber B, Wieser HG (1997) Human hippocampus establishes associations in memory. Hippocampus 7:249–256

    Article  CAS  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  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. doi: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  Google Scholar 

  • Jutras MJ, Buffalo EA (2010) Recognition memory signals in the macaque hippocampus. Proc Natl Acad Sci USA 107:401–406

    Article  CAS  Google Scholar 

  • Kesner RP et al (2002a) The role of the hippocampus in memory for the temporal order of a sequence of odors. Behav Neurosci 116(2):286–290

    Article  Google Scholar 

  • Kesner RP et al (2002b) The role of the hippocampus in memory for the temporal order of a sequence of odors. Behav Neurosci 116(2):286–290

    Article  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  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  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Kreiman G, Koch C, Fried I (2000b) Imagery neurons in the human brain. Nature 408:357–361

    Article  CAS  Google Scholar 

  • Langston RF, Wood ER (2010) Associative recognition and the hippocampus: differential effects of hippocampal lesions on object-place, object-context and object-place-context memory. Hippocampus 20:1139–1153

    Article  Google Scholar 

  • Lenck-Santini PP, Fenton AA, Muller RU (2008) Discharge properties of hippocampal neurons during performance of a jump avoidance task. J Neurosci 28:6773–6786

    Article  CAS  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  Google Scholar 

  • MacDonald CJ, Carrow S, Place R, Eichenbaum H (2013) Distinct hippocampal time cell sequences represent odor memories in immobilized rats. J Neurosci 33:14607–14616

    Article  CAS  Google Scholar 

  • Manns J, Eichenbaum H (2009) A cognitive map for object memory in the hippocampus. Learn Mem 16:616–624

    Article  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  Google Scholar 

  • McKenzie S, Robinson NTM, Herrera L, Churchill JC, Eichenbaum H (2013) Learning causes reorganization of neuronal firing patterns to represent related experiences within a hippocampal schema. J Neurosci 33:10243–10256

    Article  CAS  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  Google Scholar 

  • Mishkin M (1978) Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus. Nature 273:297–298

    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

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Morris RGM, Garrud P, Rawlins JP, O’Keefe J (1982) Place navigation impaired in rats with hippocampal lesions. Nature 297:681–683

    Article  CAS  Google Scholar 

  • Mumby DG (2001) Perspectives on object-recognition memory following hippocampal damage, lessons from studies in rats. Behav Brain Res 127:159–181

    Article  CAS  Google Scholar 

  • Murray EA, Mishkin M (1998) Object recognition and location memory in monkeys with excitotoxic lesions of the amygdala and hippocampus. J Neurosci 18:6568–6582

    CAS  PubMed  Google Scholar 

  • Muzzio IA, Levita L, Kulkarni J, Monaco J, Kentros C, Stead M, Abbott LF, Kandel ER (2009) Attention enhances the retrieval and stability of visuospatial and olfactory representations in the dorsal hippocampus. PLoS Biol 7(6):e1000140. doi:10.1371/journal.pbio.1000140

    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  Google Scholar 

  • Nemanic S, Alvarado MC, Bachevalier J (2004) The hippocampal/parahippocampal regions and recognition memory: insights from visual paired comparison versus object-delayed nonmatching in monkeys. J Neurosci 24:2013–2026

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Olds J, Disterhoft JF, Segal M, Kornblith CL, Hirsh R (1972) Learning centers of rat brain mapped by latencies of conditioned unit responses. J Neurophysiol 35:202–219

    Article  CAS  Google Scholar 

  • Otto T, Eichenbaum H (1992) Neuronal activity in the hippocampus during delayed non-match to sample performance in rats: evidence for hippocampal processing in recognition memory. Hippocampus 2:323–334

    Article  CAS  Google Scholar 

  • Pastalkova E. et al (2008) Internally generated cell assembly sequences in the rat hippocampus. Science 321:1322–1327

    Article  CAS  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 USA 107:6046–6051

    Article  CAS  Google Scholar 

  • Phillips RG, LeDoux JE (1992) Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav Neurosci 106:274–285

    Article  CAS  Google Scholar 

  • Piaget J (1928) Judgment and reasoning in the child. Kegan, Paul, Trench, and Trubner, London

    Book  Google Scholar 

  • Preston AR, Shrager Y, Dudukovic NM, Gabrieli JD (2004) Hippocampal contribution to the novel use of relational information in declarative memory. Hippocampus 14:148–152

    Article  Google Scholar 

  • Qin S, Rijpkema M, Tendolkar I, Piekema C, Hermans EJ, Binder M, Petersson KM, Luo J, Fernandez G (2009) Dissecting medial temporal lobe contributions to item and associative memory formation. NeuroImage 46:874–881

    Article  Google Scholar 

  • Quiroga RQ, Reddy L, Kreiman G, Koch C, Fried I (2005) Invariant visual representation by single neurons in the human brain. Nature 43:1102–1107

    Article  Google Scholar 

  • Rampon C, Tang Y-P, Goodhouse J, Shimizu E, Kyin M, Tsien J (2000) Enrichment induces structural changes and recovery from non-spatial memory deficits in CA1 NMDAR1-knockout mice. Nat Neurosci 3:238–244

    Article  CAS  Google Scholar 

  • Ranck JB Jr (1973) Studies on single neurons in dorsal hippocampal formation and septum in unrestrained rats. Part I. Behavioral correlates and firing repertoires. Exp Neurol 41:461–531

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Rutishauser U, Schuman EM, Mamelak AN (2008) Activity of human hippocampal and amygdala neurons during retrieval of declarative memories. Proc Natl Acad Sci USA. 105:329–334

    Article  CAS  Google Scholar 

  • Ryan JD, Althoff RR, Whitlow S, Cohen NJ (2000) Amnesia is a deficit in relational memory. Psychol Sci 11:6454–6461

    Article  Google Scholar 

  • Sauvage MM, Fortin NJ, Owens CB, Yonelinas AP, Eichenbaum H (2008) Recognition memory: opposite effects of hippocampal damage on recollection and familiarity. Nat Neurosci 11:16–18

    Article  CAS  Google Scholar 

  • Sauvage MM, Beer Z, Eichenbaum H (2010) Recognition memory: adding a response deadline eliminates recollection but spares familiarity. Learn Mem 17:104–108

    Article  Google Scholar 

  • Solomon PR, Vander Schaaf ER, Thompson RF, Weisz DJ (1986) Hippocampus and trace conditioning of the rabbit’s classically conditioned nictitating membrane response. Behav Neurosci 100:729–744

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Squire LR, Wixted JT, Clark RE (2007) Recognition memory and the medial temporal lobe, a new perspective. Nat Rev Neurosci 8:872–883

    Article  CAS  Google Scholar 

  • Tse D, Langston RF, Kakeyama M, Bethus I, Spooner PA, Wood ER, Witter MP, Morris RGM (2007) Schemas and memory consolidation. Science 316:76–82

    Article  CAS  Google Scholar 

  • Tulving E (1984) Précis of elements of episodic memory. Behav Brain Sci 7:223–268

    Article  Google Scholar 

  • Vinnik E, Antopolskiy S, Itskov PM, Diamond ME (2012) Auditory stimuli elicit hippocampal neuronal responses during sleep. Front Syst Neurosci 6:49. doi:10.3389/fnsys.2012.00049

    Article  PubMed  PubMed Central  Google Scholar 

  • Watson PD, Voss JL, Warren DE, Tranel D, Cohen NJ (2013) Spatial reconstruction by patients with hippocampal damage is dominated by relational memory errors. Hippocampus 23:570–580

    Article  Google Scholar 

  • Wiebe SP, Stäubli UV (1999) Dynamic filtering f recognition codes in the hippocampus. J Neurosci 19:10562–10574

    CAS  PubMed  Google Scholar 

  • Wimmer GE, Shohamy D (2012) Preference by association. How memory mechanisms in the hippocampus bias decisions. Science 338:270–273

    Article  CAS  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  Google Scholar 

  • Wixted JT, Squire LR, Jang Y, Papesh MH, Goldinger SD, Kuhn JR, Smith KA, Treiman DM, Steinmetz PN (2014) Sparse and distributed coding of episodic memory ini neurons of the human hippocampus. Proc Natl Acad Sci USA 111:9621–9626

    Article  CAS  Google Scholar 

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

    Article  CAS  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  Google Scholar 

  • Yonelinas AP (2001) Components of episodic memory, the contribution of recollection and familiarity. Phil Trans Roy Soc Lond Biol Sci 356:1363–1374

    Article  CAS  Google Scholar 

  • Zeineh MM, Engel SA, Thompson PM, Brookheimer SY (2003) Dynamics of the hippocampus during encoding and retrieval of face-name pairs. Science 299:577–580

    Article  CAS  Google Scholar 

  • Zeithamova D, Dominick AL, Preston AR (2012) Hippocampal and ventral medial prefrontal activation during retrieval-mediated learning supports novel inference. Neuron 75:168–179

    Article  CAS  Google Scholar 

  • Zola SM, Squire LR, Teng E, Stefanacci L, Buffalo EA, Clark RE (2000) Impaired recognition memory in monkeys after damage limited to the hippocampal region. J Neurosci 20:451–643

    CAS  PubMed  Google Scholar 

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Acknowledgments

NIMH MH094263, MH51570; MH52090, MH095297; ONR MURI N00014-0-1-0936.

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Eichenbaum, H. (2016). What Versus Where: Non-spatial Aspects of Memory Representation by the Hippocampus. In: Clark, R.E., Martin, S. (eds) Behavioral Neuroscience of Learning and Memory. Current Topics in Behavioral Neurosciences, vol 37. Springer, Cham. https://doi.org/10.1007/7854_2016_450

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