Skip to main content
SpringerLink
Log in

Organization and Structure of Brain Systems Supporting Memory

  • Protocol
  • First Online:
Book cover The Maze Book

Part of the book series: Neuromethods ((NM,volume 94))

Abstract

For more than a century, clinical case studies have drawn a link between damage to the medial temporal lobe (MTL) and memory dysfunction. Declarative memory is supported by the MTL and provides us with the capacity to rapidly encode facts and episodes and to express this information in unique and flexible ways. This memory system encodes information in a way that allows us to be consciously aware of the content of our memory. Serving as the psychological accoutrements of a lifetime of experience, memories allow us to reconstruct our past, appreciate our present, and, to an extent, predict and control our future. In doing so, memories have the power of providing us with a sense of self and a connection to others and to our environment. This chapter discusses the anatomy and function of the MTL, which consists of multiple anatomically connected structures that are required for declarative memory. A historical perspective is provided throughout the chapter, which includes content on the organization of multiple memory systems, the development of animal models of MTL amnesia, the examination of spatial memory and non-declarative memory in animal models, and the interaction of memory systems. The overarching tenet is that memory is not a single entity, but rather a collection of independent memory systems.

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

Access this chapter

Log in via an institution
Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 84.99
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 139.00
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 109.99
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. Aggleton JP, Hunt PR, Rawlins JNP (1986) The effects of hippocampal lesions upon spatial and non-spatial tests of working memory. Behav Brain Res 19:133–146

    CAS  PubMed  Google Scholar 

  2. Ainge JA, Heron-Maxwell C, Theofilas P, Wright P, de Hoz L, Wood ER (2006) The role of the hippocampus in object recognition in rats: examination of the influence of task parameters and lesion size. Behav Brain Res 167:183–195

    PubMed  Google Scholar 

  3. Alvarez P, Zola-Morgan S, Squire LR (1995) Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys. J Neurosci 15:3796–3807

    CAS  PubMed  Google Scholar 

  4. Bachevalier J (1990) Ontogenetic development of habit and memory formation in primates. Ann N Y Acad Sci 608:457–474

    CAS  PubMed  Google Scholar 

  5. Bachevalier J, Brickson M, Hagger C (1993) Limbic-dependent recognition memory in monkeys develops early in infancy. Learn Mem 4:77–80

    CAS  Google Scholar 

  6. Baker KB, Kim JJ (2002) Effects of stress and hippocampal NMDA receptor antagonism on recognition memory in rats. Learn Mem 9:58–65

    PubMed Central  PubMed  Google Scholar 

  7. Baxter MG, Murray EA (2001) Opposite relationship of hippocampal and rhinal cortex damage to delayed nonmatching-to-sample deficits in monkeys. Hippocampus 11(1):61–71

    CAS  PubMed  Google Scholar 

  8. Beason-Held LL, Rosene DL, Killiany RJ, Moss MB (1999) Hippocampal formation lesions produce memory impairment in the rhesus monkey. Hippocampus 9:562–574

    CAS  PubMed  Google Scholar 

  9. Boccara CN, Sargolini F, Thoresen VH, Solstad T, Witter MP, Moser EI, Moser MB (2010) Grid cells in pre- and parasubiculum. Nat Neurosci 13:987–994

    CAS  PubMed  Google Scholar 

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

    PubMed Central  CAS  PubMed  Google Scholar 

  11. Broadbent NJ, Squire LR, Clark RE (2010) Sustained dorsal hippocampal activity is not obligatory for either the maintenance or retrieval of long-term spatial memory. Hippocampus 20:1366–1375

    PubMed Central  PubMed  Google Scholar 

  12. Christian KM, Thompson RF (2003) Neural substrates of eyeblink conditioning: acquisition and retention. Learn Mem 11:427–455

    Google Scholar 

  13. Clark RE, Martin SJ (2005) Interrogating rodents regarding their object and spatial memory. Curr Opin Neurobiol 15(5):593–598

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  15. 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 

  16. Cohen NJ (1984) Preserved learning capacity in amnesia: evidence for multiple memory systems. In: Squire LR, Butters N (eds) Neuropsychology of memory. Guilford, New York, pp 83–103

    Google Scholar 

  17. Cohen NJ, Squire LR (1980) Preserved learning and retention of pattern analyzing skill in amnesia: dissociation of knowing how and knowing that. Science 210:207–209

    CAS  PubMed  Google Scholar 

  18. Corkin S (1984) Lasting consequences of bilateral medial temporal lobectomy: clinical course and experimental findings in H. M. Semin Neurol 4:249–259

    Google Scholar 

  19. Corkin S, Amaral DG, Gonzalez RG, Johnson KA, Hyman BT (1997) H.M.’s medial temporal lobe lesion: findings from magnetic resonance imaging. J Neurosci 17:3964–3980

    CAS  PubMed  Google Scholar 

  20. Correll RE, Scoville WB (1965) Effects of medial temporal lesions on visual discrimination performance. J Comp Physiol Psychol 60:175–181

    CAS  PubMed  Google Scholar 

  21. de Lima MN, Luft T, Roesler R, Schroder N (2006) Temporary inactivation reveals an essential role of the dorsal hippocampus in consolidation of object recognition memory. Neurosci Lett 405:142–146

    PubMed  Google Scholar 

  22. Derdikman D, Moser EI (2010) A manifold of spatial maps in the brain. Trends Cogn Sci 14:561–569

    PubMed  Google Scholar 

  23. Diamond A (1990) Rate of maturation of the hippocampus and the developmental progression of children’s performance on the delayed non-matching to sample and visual paired comparison tasks. Ann N Y Acad Sci 608:394–426

    CAS  PubMed  Google Scholar 

  24. Duva CA, Floresco SB, Wunderlich GR, Lao TL, Pinel JPJ, Phillips AG (1997) Disruption of spatial but not object-recognition memory by neurotoxic lesions of the dorsal hippocampus in rats. Behav Neurosci 111:1184–1196

    CAS  PubMed  Google Scholar 

  25. Eichenbaum H, Cohen NJ (2001) From conditioning to conscious recollection: memory systems of the brain. Oxford Univ. Press, New York

    Google Scholar 

  26. Eichenbaum H, Fagan A, Cohen NJ (1986) Normal olfactory discrimination learning set and facilitation of reversal learning after medial-temporal damage in rats: implications for an account of preserved learning abilities in amnesia. J Neurosci 6:1876–1884

    CAS  PubMed  Google Scholar 

  27. Ennaceur A, Delacour J (1988) A new one-trial test for neurobiological studies of memory in rats: 1. Behavioural data. Behav Brain Res 31:47–59

    CAS  PubMed  Google Scholar 

  28. Ennaceur A, Neave N, Aggleton JP (1996) Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat. Behav Brain Res 80:9–25

    CAS  PubMed  Google Scholar 

  29. Fagan JF (1970) Memory in the infant. J Exp Child Psychol 9:217–226

    PubMed  Google Scholar 

  30. Fagan JF (1990) The paired-comparison paradigm and infant intelligence. Ann N Y Acad Sci 608:337–357

    PubMed  Google Scholar 

  31. Fanselow MS, Gale GD (2003) The amygdala, fear, and memory. Ann N Y Acad Sci 985:125–134

    PubMed  Google Scholar 

  32. Forwood SE, Winters BD, Bussey TJ (2005) Hippocampal lesions that abolish spatial maze performance spare object recognition memory at delays of up to 48 h. Hippocampus 15:347–355

    CAS  PubMed  Google Scholar 

  33. Frankland PW, Bontempi B (2005) The organization of recent and remote memories. Nat Rev Neurosci 6(2):119–130

    CAS  PubMed  Google Scholar 

  34. Frantz RL (1956) A method for studying early visual development. Percept Mot Skills 6:13–15

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  36. Gaffan D (1974) Recognition impaired and association intact in the memory of monkeys after transection of the fornix. J Comp Physiol Psychol 86:1100–1109

    CAS  PubMed  Google Scholar 

  37. Gaskin S, Tremblay A, Mumby DG (2003) Retrograde and anterograde object recognition in rats with hippocampal lesions. Hippocampus 13:962–969

    PubMed  Google Scholar 

  38. Gilbert PE, Kesner RP, DeCoteau WE (1998) Memory for spatial location: role of the hippocampus in mediating spatial pattern separation. J Neurosci 18:804–810

    CAS  PubMed  Google Scholar 

  39. Gould TJ, Rowe WB, Heman KL, Mesches MH, Young DA, Rose GM, Bickford PC (2002) Effects of hippocampal lesions on patterned motor learning in the rat. Brain Res Bull 58:581–586

    CAS  PubMed  Google Scholar 

  40. Gunderson VM, Sackett GP (1984) Development of pattern recognition in infant pigtailed macaques (macaca nemestrina). Dev Psychol 20:418–426

    Google Scholar 

  41. Guzowski JF, Knierim JJ, Moser EI (2004) Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron 44:581–584

    CAS  PubMed  Google Scholar 

  42. Hafting T, Fyhn M, Molden S, Moser M, Moser EI (2005) Microstructure of a spatial map in the entorhinal cortex. Nature 436:801–806

    CAS  PubMed  Google Scholar 

  43. Hammond RS, Tull LE, Stackman RW (2004) On the delay-dependent involvement of the hippocampus in object recognition memory. Neurobiol Learn Mem 82:26–34

    PubMed  Google Scholar 

  44. Hintzman D (1990) Human learning and memory: connections and dissociations. Annu Rev Psychol 41:109–139

    CAS  PubMed  Google Scholar 

  45. Hirsh R (1974) The hippocampus and contextual retrieval of information from memory: a theory. Behav Biol 12:421–444

    CAS  PubMed  Google Scholar 

  46. James W (1890) Principles of psychology. Holt, New York

    Google Scholar 

  47. Kesner RP, Bolland BL, Dakis M (1993) Memory for spatial location, motor responses, and objects: triple dissociation among the hippocampus, caudate nucleus, and extrastriate visual cortex. Exp Brain Res 93:462–470

    CAS  PubMed  Google Scholar 

  48. Krupic J, Burgess N, O’Keefe J (2012) Neural representations of location composed of spatially periodic bands. Science 337:853–857

    CAS  PubMed  Google Scholar 

  49. Leutgeb S, Leutgeb JK, Treves A, Moser MB, Moser EI (2004) Distinct ensemble codes in hippocampal areas CA3 and CA1. Science 305:1295–1298

    CAS  PubMed  Google Scholar 

  50. Lever C, Burton S, Jeewajee A, O’Keefe J, Burgess N (2009) Boundary vector cells in the subiculum of the hippocampal formation. J Neurosci 29:9771–9777

    PubMed Central  CAS  PubMed  Google Scholar 

  51. Malamut BL, Saunders RC, Mishkin M (1984) Monkeys with combined amygdalo-hippocampal lesions succeed in object discrimination learning despite 24-hour intertrial intervals. Behav Neurosci 98:759–769

    CAS  PubMed  Google Scholar 

  52. Malkova L, Mishkin M (1997) Memory for the location of objects after separate lesions of the hippocampus and parahippocampal cortex in Rhesus monkeys. Soc Neursoci Abstracts 23:14

    Google Scholar 

  53. Marr D (1971) Simple memory: a theory for archicortex. Philos Trans R Soc Lond Ser B 262:23–81

    CAS  Google Scholar 

  54. McCormick DA, Lavond DG, Clark GA, Kettner RE, Rising CE, Thompson RF (1981) The engram found? Role of the cerebellum in classical conditioning of nictitating membrane and eyelid responses. Bull Psychon Soc 18:103–105

    Google Scholar 

  55. McDonald RJ, White NM (1993) A triple dissociation of memory systems: hippocampus, amygdala, and dorsal striatum. Behav Neurosci 127(6):835–853

    Google Scholar 

  56. McDonald RJ, White NM (1994) Parallel information processing in the water maze: evidence for independent memory systems involving dorsal striatum and hippocampus. Behav Neural Biol 61(3):260–270

    CAS  PubMed  Google Scholar 

  57. McDougall W (1923) Outline of psychology. Scribners, New York

    Google Scholar 

  58. McGaugh JL (2000) Memory—a century of consolidation. Science 287(5451):248–251

    CAS  PubMed  Google Scholar 

  59. McGaugh JL, Roozendaal B (2009) Drug enhancement of memory consolidation: historical perspective and neurobiological implications. Psychopharmacology (Berl) 202:3–14

    CAS  Google Scholar 

  60. McKee RD, Squire LR (1993) On the development of declarative memory. J Exp Psychol Learn Mem Cogn 19:397–404

    CAS  PubMed  Google Scholar 

  61. McNaughton BL, Morris RGM (1987) Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends Neurosci 10:408–415

    Google Scholar 

  62. Milner B (1962) Les troubles de Ia memoire accompagnant des lesions hippocampiques bilaterales. Physiologie de/'hippocampe [Memory impairment associated with bilateral hippocampal lesions]. Centre National de Ia Recherche Scientifique, Paris, pp 257–272

    Google Scholar 

  63. Milner B (1972) Disorders of learning and memory after temporal lobe lesions in man. Clin Neurosurg 19:421–466

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  65. Mishkin M (1982) A memory system in the monkey. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences 298:85–92

    Google Scholar 

  66. Mishkin M, Delacour J (1975) An analysis of short-term visual memory in the monkey. J Exp Psychol Anim Behav Process 1:326–334

    CAS  PubMed  Google Scholar 

  67. Mishkin M, Malamut B, Bachevalier J (1984) Memories and habits: two neural systems. In: Lynch G, McGaugh JL, Weinberger NM (eds) Neurobiology of learning and memory. Guilford, New York, pp 65–77

    Google Scholar 

  68. Moscovitch M (1982) Multiple dissociations of function in amnesia. In: Cermak L (ed) Human memory and amnesia. Erlbaum, Hillsdale, NJ, pp 337–370

    Google Scholar 

  69. Mumby DG, Pinel JP (1994) Rhinal cortex lesions and object recognition in rats. Behav Neurosci 108:11–18

    CAS  PubMed  Google Scholar 

  70. Mumby DG, Pinel JPJ, Kornecook TJ, Shen MJ, Redila VA (1995) Memory deficits following lesions of hippocampus or amygdala in rat: assessment by an object-memory test battery. Psychobiology 23:26–36

    Google Scholar 

  71. Mumby DG, Pinel JPJ, Wood ER (1990) Nonrecurring-items delayed nonmatching-to-sample in rats: a new paradigm for testing nonspatial working memory. Psychobiology 18:321–326

    Google Scholar 

  72. Mumby DG, Tremblay A, Lecluse V, Lehmann H (2005) Hippocampal damage and anterograde object-recognition in rats after long retention intervals. Hippocampus 15:1050–1056

    PubMed  Google Scholar 

  73. Mumby DG, Wood ER, Duva CA, Kornecook TJ, Pinel JPJ, Phillips AG (1996) Ischemia-induced object-recognition deficits in rats are attenuated by hippocampal ablation before or soon after ischemia. Behav Neurosci 110:266–281

    CAS  PubMed  Google Scholar 

  74. Mumby DG, Wood ER, Pinel JPJ (1992) Object-recognition memory is only mildly impaired in rats with lesions of the hippocampus and amygdala. Psychobiology 20:18–27

    Google Scholar 

  75. Murray EA, Mishkin M (1984) Severe tactual as well as visual memory deficits following combined removal of the amygdala and hippocampus in monkeys. J Neurosci 4:2565–2580

    CAS  PubMed  Google Scholar 

  76. 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 

  77. 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(8):2013–2026

    CAS  PubMed  Google Scholar 

  78. O’Brien N, Lehmann H, Lecluse V, Mumby DG (2006) Enhanced context-dependency of object recognition in rats with hippocampal lesions. Behav Brain Res 170:156–162

    PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  80. O'Keefe J, Nadel L (1978) The hippocampus as a cognitive map. Oxford University Press, London

    Google Scholar 

  81. Olton DS, Becker JT, Handelmann GE (1979) Hippocampus, space and memory. Behav Brain Sci 2:313–365

    Google Scholar 

  82. Orbach J, Milner B, Rasmussen T (1960) Learning and retention in monkeys after amygdala-hippocampus resection. Arch Neurol 3:230–251

    CAS  PubMed  Google Scholar 

  83. Overman WH, Ormsby G, Mishkin M (1990) Picture recognition vs. picture discrimination learning in monkeys with medial temporal removals. Exp Brain Res 79:18–24

    CAS  PubMed  Google Scholar 

  84. Packard MG, Hirsh R, White NM (1989) Differential effects of fornix and caudate nucleus lesions on two radial maze tasks: evidence for multiple memory systems. J Neurosci 9:1465–1472

    CAS  PubMed  Google Scholar 

  85. Paller KA (1990) Recall and stem-completion priming have different electrophysiological correlates and are modified differentially by directed forgetting. J Exp Psychol Learn Mem Cogn 16:1021–1032

    CAS  PubMed  Google Scholar 

  86. Parkinson JK, Murray E, Mishkin M (1988) A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects. J Neurosci 8:4159–4167

    CAS  PubMed  Google Scholar 

  87. Pascalis O, Hunkin NM, Holdstock JS, Isaac CL, Mayes AR (2004) Visual paired comparison performance is impaired in a patient with selective hippocampal lesions and relatively intact item recognition. Neuropsychologia 42(10):1293–1300

    CAS  PubMed  Google Scholar 

  88. Poldrack RA, Packard MG (2003) Competition among multiple memory systems: converging evidence from animal and human brain studies. Neuropsychologia 41:245–251

    PubMed  Google Scholar 

  89. Polster M, Nadel L, Schacter D (1991) Cognitive neuroscience analysis of memory: a historical perspective. J Cogn Neurosci 3:95–116

    CAS  PubMed  Google Scholar 

  90. Prusky GT, Douglas RM, Nelson L, Shabanpoor A, Sutherland RJ (2004) Visual memory task for rats reveals an essential role for hippocampus and perirhinal cortex. Proc Natl Acad Sci U S A 101:5064–5068

    PubMed Central  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  92. Ramus SJ, Zola-Morgan S, Squire LR (1994) Effects of lesions of perirhinal cortex or parahipocampal cortex on memory in monkeys. Soc Neurosci Abstracts 20:1074

    Google Scholar 

  93. Ranck JB (1985) Head-direction cells in the deep cell layer of dorsal presubiculum in freely moving rats. In: Buzsaki G, Vanderwolf CH (eds) Electrical activity of the archicortex. Hungarian Academy of Sciences, Budapest, pp 217–220

    Google Scholar 

  94. Rempel-Clower NL, Zola SM, Squire LR, Amaral DG (1996) Three cases of enduring memory impairment following bilateral damage limited to the hippocampal formation. J Neurosci 16:5233–5255

    CAS  PubMed  Google Scholar 

  95. Ribot T (1882) Diseases of memory. Appleton-CenturyCrofts, New York (Original work published 1881)

    Google Scholar 

  96. Richardson-Klavehn A, Bjork RA (1988) Measures of memory. Annu Rev Psychol 39:475–542

    Google Scholar 

  97. Rolls ET (1996) A theory of hippocampal function in memory. Hippocampus 6:601–620

    CAS  PubMed  Google Scholar 

  98. Rolls ET, Kesner RP (2006) A computational theory of hippocampal function, and empirical tests of the theory. Prog Neurobiol 79:1–48

    CAS  PubMed  Google Scholar 

  99. Rossato JI, Bevilaqua LR, Myskiw JC, Medina JH, Izquierdo I, Cammarota M (2007) On the role of hippocampal protein synthesis in the consolidation and reconsolidation of object recognition memory. Learn Mem 14:36–46

    PubMed Central  PubMed  Google Scholar 

  100. Rothblat LA, Kromer LR (1991) Object recognition memory in the rat: the role of the hippocampus. Behav Brain Res 42:25–32

    CAS  PubMed  Google Scholar 

  101. Ryle G (1949) The concept of mind. Hutchinson, San Francisco

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  103. Savelli F, Yoganarasimha D, Knierim JJ (2008) Influence of boundary removal on the spatial representations of the medial entorhinal cortex. Hippocampus 18:1270–1282

    PubMed Central  PubMed  Google Scholar 

  104. Schacter DL (1987) Implicit memory: history and current status. J Exp Psychol Learn Mem Cogn 13:501–518

    Google Scholar 

  105. Scoville WB, Milner B (1957) Loss of recent memory after bilateral hippocampal lesions. J Neurol Neurosurg Psychiatry 20:11–21

    PubMed Central  CAS  PubMed  Google Scholar 

  106. Sherry DF, Schacter DL (1987) The evolution of multiple memory systems. Psychol Rev 94:439–454

    Google Scholar 

  107. Solstad T, Boccara CN, Kropff E, Moser MB, Moser EI (2008) Representation of geometric borders in the entorhinal cortex. Science 322:1865–1868

    CAS  PubMed  Google Scholar 

  108. Squire LR (1982) The neuropsychology of human memory. Annu Rev Neurosci 5:241–273

    CAS  PubMed  Google Scholar 

  109. Squire LR (1992) Memory and the hippocampus: a synthesis from findings with rats, monkeys, and humans. Psychol Rev 99:195–231

    CAS  PubMed  Google Scholar 

  110. Squire LR (2004) Memory systems of the brain: a brief history and current perspective. Neurobiol Learn Mem 82:171–177

    PubMed  Google Scholar 

  111. Squire LR, Knowlton B (1999) The medial temporal lobe, the hippocampus, and the memory systems of the brain. In: Gazzaniga M (ed) The cognitive neurosciences, 2nd edn. MIT Press, Cambridge, pp 765–799, 1276 pp

    Google Scholar 

  112. Squire LR, Zola-Morgan S (1983) The neurology of memory: the case for correspondence between the findings for human and non-human primate. In: Deutsch JA (ed) The physiological basis of memory. Academic, San Diego, pp 199–268

    Google Scholar 

  113. Squire LR, Zola-Morgan S (1991) The medial temporal lobe memory system. Science 253:1380–1386

    CAS  PubMed  Google Scholar 

  114. Stefanacci L, Buffalo EA, Schmolck H, Squire LR (2000) Profound amnesia after damage to the medial temporal lobe: a neuroanatomical and neuropsychological profile of patient E.P. J Neurosci 20:7024–7036

    CAS  PubMed  Google Scholar 

  115. Sutherland RW, McDonald RJ (1990) Hippocampus, amygdala, and memory deficits in rats. Behav Brain Res 37:57–79

    CAS  PubMed  Google Scholar 

  116. Suzuki WA, Zola-Morgan S, Squire LR, Amaral DG (1993) Lesions of the perirhinal and parahippocampal cortices in the monkey produce long-lasting memory impairment in the visual and tactual modalities. J Neurosci 13:2430–2451

    CAS  PubMed  Google Scholar 

  117. Tang Y-P, Shimizu E, Dube GR, Rampon C, Kerchner GA, Zhuo M, Liu G, Tsien JZ (1999) Genetic enhancement of learning and memory in mice. Nature 401:63–69

    CAS  PubMed  Google Scholar 

  118. Taube JS, Muller RU, Ranck JB (1990) Head-direction cells recorded from the postsubiculum in freely moving rats. II. Effects of environmental manipulations. J Neurosci 10:436–447

    CAS  PubMed  Google Scholar 

  119. Teng E, Stefanacci L, Squire LR, Zola SM (2000) Contrasting effects on discrimination learning after hippocampal lesions and conjoint hippocampal-caudate lesions in monkeys. J Neurosci 20(10):3853–3863

    CAS  PubMed  Google Scholar 

  120. Treves A, Rolls ET (1992) Computational constraints suggest the need for two distinct input systems to the hippocampal CA3 network. Hippocampus 2:189–199

    CAS  PubMed  Google Scholar 

  121. Tulving E (1985) How many memory systems are there? Am Psychol 40:385–398

    Google Scholar 

  122. Tulving E, Schacter DL (1990) Priming and human memory systems. Science 247:301–306

    CAS  PubMed  Google Scholar 

  123. Vazdarjanova A, Guzowski JF (2004) Differences in hippocampal neuronal population responses to modifications of an environmental context: evidence for distinct, yet complementary, functions of CA3 and CA1 ensembles. J Neurosci 24:6489–6496

    CAS  PubMed  Google Scholar 

  124. von Bechterew W (1900) Demonstration eines gehirns mit zerstorung der vorderen und inneren theile der hirnrinde beider schlafenlappen. Neurol Zentralb 19:990–991

    Google Scholar 

  125. Weinstein B (1941) Matching-from-sample by rhesus monkeys and by children. J Comp Psychol 31:195–213

    Google Scholar 

  126. Weiskrantz L (1987) Neuroanatomy of memory and amnesia: a case for multiple memory systems. Hum Neurobiol 6:93–105

    CAS  PubMed  Google Scholar 

  127. White NM, Packard MG, McDonald RJ (2013) Dissociation of memory systems: the story unfolds. Behav Neurosci 127(6):813–834

    PubMed  Google Scholar 

  128. Wickelgren WA (1979) Chunking and consolidation: a theoretical synthesis of semantic networks, configuring, S-R versus cognitive learning, normal forgetting, the amnesic syndrome, and the hippocampal arousal system. Psychol Rev 86:44–60

    CAS  PubMed  Google Scholar 

  129. Wiig KA, Bilkey DK (1995) Lesions of rat perirhinal cortex exacerbate the memory deficit observed following damage to the fimbria-fornix. Behav Neurosci 109:620–630

    CAS  PubMed  Google Scholar 

  130. Winograd T (1975) Frame representations and the declarative-procedural controversy. In: Bobrow D et al (eds) Representation and understanding: studies in cognitive science. Academic, New York, pp 185–210

    Google Scholar 

  131. Winters BD, Forwood SE, Cowell RA, Saksida LM, Bussey TJ (2004) Double dissociation between the effects of peri-postrhinal cortex and hippocampal lesions on tests of object recognition and spatial memory: heterogeneity of function within the temporal lobe. J Neurosci 24:5901–5908

    CAS  PubMed  Google Scholar 

  132. Winters BD, Saksida LM, Bussey TJ (2008) Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neurosci Biobehav Rev 32(5):1055–1070

    PubMed  Google Scholar 

  133. Witter MP, Amaral DG (2004) Hippocampal formation. In: Paxinos G (ed) The rat nervous system, 3rd edn. Academic, San Diego, pp 637–703

    Google Scholar 

  134. Wood ER, Dudchenko PA, Robitsek RJ, Eichenbaum H (2000) Hippocampal neurons encode information about different types of memory episodes occurring in the same location. Neuron 27:623–633

    CAS  PubMed  Google Scholar 

  135. Zhang SJ, Ye J, Miao C, Tsao A, Cerniauskas I, Ledergerber D, Moser MB, Moser EI (2013) Optogenetic dissection of entorhinal-hippocampal functional connectivity. Science 340:1232627. doi:10.1126/science/1232627

    PubMed  Google Scholar 

  136. Zola SM, Squire LR (2001) Relationship between magnitude of damage to the hippocampus and impaired recognition memory in monkeys. Hippocampus 11:92–98

    CAS  PubMed  Google Scholar 

  137. 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 20:451–463

    CAS  PubMed  Google Scholar 

  138. Zola-Morgan S, Squire LR (1984) Preserved learning in monkeys with medial temporal lesions: sparing of motor and cognitive skills. J Neurosci 4:1072–1085

    CAS  PubMed  Google Scholar 

  139. Zola-Morgan S, Squire LR (1985) Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. Behav Neurosci 99:22–34

    CAS  PubMed  Google Scholar 

  140. Zola-Morgan S, Squire LR (1986) Memory impairment in monkeys following lesions of the hippocampus. Behav Neurosci 100:155–160

    CAS  PubMed  Google Scholar 

  141. Zola-Morgan S, Squire LR, Amaral DG (1986) Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6:2950–2967

    CAS  PubMed  Google Scholar 

  142. Zola-Morgan S, Squire LR, Amaral DG (1989) Lesions of the hippocampal formation but not lesions of the fornix or the mammillary nuclei produce long-lasting memory impairment in monkeys. J Neurosci 9:898–913

    CAS  PubMed  Google Scholar 

  143. Zola-Morgan S, Squire LR, Mishkin M (1982) The neuroanatomy of amnesia: amygdala-hippocampus vs. temporal stem. Science 218:1337–1339

    CAS  PubMed  Google Scholar 

  144. Zola-Morgan S, Squire LR, Ramus SJ (1994) Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory systems. Hippocampus 4:483–495

    CAS  PubMed  Google Scholar 

  145. Zola-Morgan S, Squire LR, Rempel NL, Clower RP, Amaral DG (1992) Enduring memory impairment in monkeys after ischemic damage to the hippocampus. J Neurosci 12:2582–2596

    CAS  PubMed  Google Scholar 

  146. Gabrieli JD, Brewer JB, Poldrack RA (1998) Images of medial temporal lobe functions in human learning and memory. Neurobiol Learn Mem 70:275–283

    CAS  PubMed  Google Scholar 

  147. Ritchie BF, Aeschliman B, Peirce P (1950) Studies in spatial learning; place performance and the acquisition of place dispositions. J Comp Physiol Psychol 43:73–85

    Google Scholar 

  148. Thompson WG, Guilford MO, Hicks LH (1980) Effects of caudate and cortical lesions on place and response learning in rats. Physiol Psychol 8:473–479

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Psychiatry, School of Medicine, University of California, San Diego, MC 0603, 9500 Gilman Drive, La Jolla, CA, 92093, USA

    Jena B. Hales & Robert E. Clark Ph.D.

  2. Veterans Affairs San Diego Healthcare System, San Diego, CA, 92161, USA

    Robert E. Clark Ph.D.

Authors
  1. Jena B. Hales
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Robert E. Clark Ph.D.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robert E. Clark Ph.D. .

Editor information

Editors and Affiliations

  1. Arizona State University, Tempe, Arizona, USA

    Heather A. Bimonte-Nelson

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer Science+Business Media New York

About this protocol

Cite this protocol

Hales, J.B., Clark, R.E. (2015). Organization and Structure of Brain Systems Supporting Memory. In: Bimonte-Nelson, H. (eds) The Maze Book. Neuromethods, vol 94. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-2159-1_6

Download citation

  • DOI: https://doi.org/10.1007/978-1-4939-2159-1_6

  • Published:

  • Publisher Name: Humana Press, New York, NY

  • Print ISBN: 978-1-4939-2158-4

  • Online ISBN: 978-1-4939-2159-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics

Search

Navigation