Advertisement

Resolving Interference: The Role of the Human Hippocampus in Pattern Separation

  • C. Brock KirwanEmail author
  • Michelle I. Nash
Chapter

Abstract

The process of establishing sparse, orthogonalized memory representations, or pattern separation, allows a memory system to overcome interference between similar stimuli. Here, we review the literature on interference theory and the predictions of computational models of medial temporal lobe functioning regarding interference. Tests with rodent models supports the models’ prediction that the medial temporal lobe, and specifically the hippocampus, supports pattern separation processes that allow the organism to overcome interference in event-based memories. Functional magnetic resonance imaging (fMRI) studies, studies with patients with hippocampal damage, and studies of aging populations all support a role of the hippocampus in overcoming interference through pattern separation in this domain in humans. Finally, we review some promising studies that indicate ways in which pattern separation mechanisms may be improved in humans.

Keywords

Pattern separation fMRI Amnesia Hippocampus 

References

  1. Badre, D., & Wagner, A. D. (2005). Frontal lobe mechanisms that resolve proactive interference. Cerebral Cortex, 15, 2003–2012.CrossRefPubMedGoogle Scholar
  2. Bakker, A., Kirwan, C. B., Miller, M., & Stark, C. E. (2008). Pattern separation in the human hippocampal CA3 and dentate gyrus. Science, 319(5870), 1640–1642.PubMedCentralCrossRefPubMedGoogle Scholar
  3. Bakker, A., Krauss, G. L., Albert, M. S., Speck, C. L., Jones, L. R., Stark, C. E., Yassa, M. A., Bassett, S. S., Shelton, A. L., & Gallagher, M. (2012). Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron, 74(3), 467–474.PubMedCentralCrossRefPubMedGoogle Scholar
  4. Bayley, P. J., Wixted, J. T., Hopkins, R. O., & Squire, L. R. (2008). Yes/no recognition, forced-choice recognition, and the human hippocampus. Journal of Cognitive Neuroscience, 20(3), 505–512.PubMedCentralCrossRefPubMedGoogle Scholar
  5. Blank, H. (2005). Another look at retroactive and proactive interference: A quantitative analysis of conversion processes. Memory, 13(2), 200–224.CrossRefPubMedGoogle Scholar
  6. Brown, M. W., & Aggleton, J. P. (2001). Recognition memory: What are the roles of the perirhinal cortex and hippocampus? Nature Reviews Neuroscience, 2, 51–61.CrossRefPubMedGoogle Scholar
  7. Burgess, N., & OʼKeefe, J. (1996). Neuronal computations underlying the firing of place cells and their rolei n navigation. Hippocampus, 6, 749–762.CrossRefPubMedGoogle Scholar
  8. Crowder, R. G. (1976). Principles of learning and memory. New York: Lawrence Erlbaum Associates.Google Scholar
  9. Déry, N., Pilgrim, M., Gibala, M., Gillen, J., Wojtowicz, J. M., Macqueen, G., & Becker, S. (2013). Adult hippocampal neurogenesis reduces memory interference in humans: Opposing effects of aerobic exercise and depression. Frontiers in Neurosciences, 7, 66.Google Scholar
  10. Duff, M. C., Warren, D. E., Gupta, R., Vidal, J. P., Tranel, D., & Cohen, N. J. (2012). Teasing apart tangrams: Testing hippocampal pattern separation with a collaborative referencing paradigm. Hippocampus, 22(5), 1087–1091.PubMedCentralCrossRefPubMedGoogle Scholar
  11. Duncan, K., Sadanand, A., & Davachi, L. (2012). Memoryʼs penumbra: Episodic memory decisions induce lingering mnemonic biases. Science, 337(6093), 485–487.PubMedCentralCrossRefPubMedGoogle Scholar
  12. Ekstrand, B. R. (1967). The effect of sleep on memory. Journal of Experimental Psychology, Applied, 75, 64–72.CrossRefGoogle Scholar
  13. Fried, I., MacDonald, K., & Wilson, C. (1997). Single neuron activity in human hippocampus and amygdala during recognition of faces and objects. Neuron, 18, 753–765.CrossRefPubMedGoogle Scholar
  14. Fried, I., Cameron, K., Yashar, S., Fong, R., & Morrow, J. (2002). Inhibitory and excitatory responses of single neurons in the human medial temporal lobe during recognition of faces and objects. Cerebral Cortex, 12, 575–584.CrossRefPubMedGoogle Scholar
  15. Gilbert, P. E., Kesner, R. P., & DeCoteau, W. E. (1998). The role of the hippocampus in mediating spatial pattern separation. Journal of Neuroscience, 18, 804–810.PubMedGoogle Scholar
  16. Guzowski, J. F., Knierim, J. J., & Moser, E. I. (2004). Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron, 44, 581–584.CrossRefPubMedGoogle Scholar
  17. Hasselmo, M. E., & Wyble, B. (1997). Free recall and recognition in a network model of the hippocampus: Simulating effects of scopolamine on human memory function. Behavioral Brain Research, 89, 1–34.CrossRefGoogle Scholar
  18. Henson, R. N. A., Shallice, T., Josephs, O., & Dolan, R. J. (2002). Functional magnetic resonance imaging of proactive interference during spoken cued recall. NeuroImage, 17, 543–558.CrossRefPubMedGoogle Scholar
  19. Herrmann, M., Rotte, M., Grubich, C., Ebert, A. D., Schiltz, K., Munte, T. F., & Heinze, H. J. (2001). Control of semantic interference in episodic memory retrieval is associated with an anterior cingulate-prefrontal activation pattern. Human Brain Mapping, 13, 94–103.CrossRefPubMedGoogle Scholar
  20. Holden, H. M., & Gilbert, P. E. (2012). Less efficient pattern separation may contribute to age-related spatial memory deficits. Frontiers in Aging Neuroscience, 4, 9.Google Scholar
  21. Holden, H. M., Hoebel, C., Loftis, K., & Gilbert, P. E. (2012). Spatial pattern separation in cognitively normal young and older adults. Hippocampus, 22(9), 1826–1832.PubMedCentralCrossRefPubMedGoogle Scholar
  22. Holden, H. M., Toner, C., Pirogovsky, E., Kirwan, C. B., & Gilbert, P. E. (2013). Visual object pattern separation varies in older adults. Learning & memory, 20(7), 358–362.CrossRefGoogle Scholar
  23. Holdstock, J. S., Gutnikov, S. A., Gaffan, D., & Mayes, A. R. (2000). Perceptual and mnemonic matching-to-sample in humans: Contributions of the hippocampus, perirhinal and other medial temporal lobe cortices. Cortex, 36, 301–322.CrossRefPubMedGoogle Scholar
  24. Holdstock, J. S., Mayes, A. R., Roberts, N., Cezayirli, E., Isaac, C., OʼReilly, R. C., & Norman, K. A. (2002a). Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? Hippocampus, 12, 341–351.CrossRefPubMedGoogle Scholar
  25. Holdstock, J. S., Mayes, A. R., Roberts, N., Cezayirli, E., Isaac, C. L., OʼReilly, R. C., & Norman, K. A. (2002b). Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? Hippocampus, 12, 341–351.CrossRefPubMedGoogle Scholar
  26. Hopkins, R. O., & Kesner, R. P. (1993). Memory for temporal and spatial distances for new and previously learned geographical information in hypoxic subjects. Paper presented at the Society for Neuroscience Abstracts.Google Scholar
  27. Jenkins, J. B., & Dallenbach, K. M. (1924). Oblivescence during sleep and waking. American Journal of Psychology, 35, 605–612.CrossRefGoogle Scholar
  28. Johnson, M. K., Hashtroudi, S., & Lindsay, D. S. (1993). Source monitoring. Psychological Bulletin, 114(1), 3–28.CrossRefPubMedGoogle Scholar
  29. Keppel, G. (1984). Consolidation and forgetting theory. In H. Weingartner & E. S. Parker (Eds.), Memory consolidation: Psychobiology of cognition (pp. 149–161). Hillsdale: Erlbaum.Google Scholar
  30. Kesner, R. P. (1991). The role of the hippocampus within an attribute model of memory. Hippocampus, 1(3), 279–282.CrossRefPubMedGoogle Scholar
  31. Kesner, R. P. (2009). Tapestry of memory. Behavioral Neuroscience, 123(1), 1–13.CrossRefPubMedGoogle Scholar
  32. Kesner, R. P., & Hopkins, R. O. (2006). Mnemonic functions of the hippocampus: A comparison between animals and humans. Biological Psychology, 73(1), 3–18.CrossRefPubMedGoogle Scholar
  33. Kesner, R. P., Ravindranathan, A., Jackson, P., Giles, R., & Chiba, A. A. (2001). A neural circuit analysis of visual recognition memory: Role of perirhinal, medial, and lateral entorhinal cortex. Learning & Memory, 8(2), 87–95.CrossRefGoogle Scholar
  34. King, J. A., Hartley, T., Spiers, H. J., Maguire, E. A., & Burgess, N. (2005). Anterior prefrontal involvement in episodic retrieval reflects contextual interference. NeuroImage, 28(1), 256–267.CrossRefPubMedGoogle Scholar
  35. Kinsbourne, M., & Winocur, G. (1980). Response competition and interference effects in paired-associate learning by Korsakoff amnesics. Neuropsychologia, 18, 541–548.CrossRefPubMedGoogle Scholar
  36. Kirwan, C. B., & Stark, C. E. L. (2007). Overcoming interference: An fMRI investigation of pattern separation in the medial temporal lobe. Learning and Memory, 14(9), 625–6333.PubMedCentralCrossRefPubMedGoogle Scholar
  37. Kirwan, C. B., Hartshorn, J. A., Stark, S. M., Goodrich-Hunsaker, N. J., Hopkins, R. O., & Stark, C. E. L. (2012). Pattern separation deficits following damage to the hippocampus. Neuropsychologia, 50, 2408–2414.PubMedCentralCrossRefGoogle Scholar
  38. Koh, M. T., Haberman, R. P., Foti, S., McCown, T. J., & Gallagher, M. (2010). Treatment strategies targeting excess hippocampal activity benefit aged rats with cognitive impairment. Neuropsychopharmacology, 35(4), 1016–1025.PubMedCentralCrossRefPubMedGoogle Scholar
  39. Kumaran, D., & Maguire, E. A. (2009). Novelty signals: A window into hippocampal information processing. Trends in Cognitive Sciences, 13(2), 47–54.CrossRefPubMedGoogle Scholar
  40. Lacy, J. W., Yassa, M. A., Stark, S. M., Muftuler, L. T., & Stark, C. E. (2011). Distinct pattern separation related transfer functions in human CA3/dentate and CA1 revealed using high-resolution fMRI and variable mnemonic similarity. Learning & Memory, 18(1), 15–18.Google Scholar
  41. Law, J. R., Flanery, M. A., Wirth, S., Yanike, M., Smith, A. C., Frank, L. M., Suzuki, W. A., Brown, E. N., & Stark, C. E. L. (2005). Functional magnetic resonance imaging activity during the gradual acquisition and expression of paired-associate memory. Journal of Neuroscience, 25(24), 5720–5729.CrossRefPubMedGoogle Scholar
  42. LePage, M., Blondin, F., Achim, A. M., Menear, M., & Brodeur, M. (2005). The interfering effect of related events on recognition memory discriminability: A functional magnetic resonance imaging study. Cognitive Brain Research, 22, 429–437.CrossRefPubMedGoogle Scholar
  43. Leutgeb, S. (2008). Neuroscience. Detailed differences. Science, 319(5870), 1623–1624.CrossRefPubMedGoogle Scholar
  44. Leutgeb, S., Leutgeb, J. K., Treves, A., Moser, M., & Moser, E. I. (2004). Distinct ensemble codes in hippocampal areas CA3 and CA1. Science, 305, 1295–1298.CrossRefPubMedGoogle Scholar
  45. Leutgeb, J. K., Leutgeb, S., Moser, M., & Moser, E. I. (2007). Pattern separation in dentate gyrus and CA3 of the hippocampus. Science, 315(5814), 961–966.CrossRefPubMedGoogle Scholar
  46. Logothetis, N. K., Pauls, J., Augath, M., Trinath, T., & Oeltermann, A. (2001). Neurophysiological investigation of the basis of the fMRI signal. Nature, 412, 150–157.CrossRefPubMedGoogle Scholar
  47. Lustig, C., & Hasher, L. (2001). Implicit memory is not immune to interference. Psychological Bulletin, 127(5), 618–628.CrossRefPubMedGoogle Scholar
  48. Ly, M., Murray, E., & Yassa, M. A. (2013). Perceptual versus conceptual interference and pattern separation of verbal stimuli in young and older adults. Hippocampus, 23(6), 425–430.PubMedCentralCrossRefPubMedGoogle Scholar
  49. Mayes, A. R., & Downes, J. J. (1997). What do theories of the functional deficit(s) underlying amnesia have to explain? Memory, 5(1–2), 3–36.CrossRefPubMedGoogle Scholar
  50. Mayes, A. R., Pickering, A., & Fairbairn, A. (1987). Amnesic sensitivity to proactive interference: Its relationship to priming and the causes of amnesia. Neuropsychologia, 25(1B), 211–220.CrossRefPubMedGoogle Scholar
  51. Mayes, A. R., Isaac, C. L., Downes, J. J., Holdstock, J. S., Hunkin, N. M., Montaldi, D., MacDonald, C., Cezayirli, E., & Roberts, J. N. (2001). Memory for single items, word pairs, and temporal order in a patient with selective hippocampal lesions. Cognitive Neuropsychology, 18, 97–123.CrossRefPubMedGoogle Scholar
  52. Mayes, A. R., Holdstock, J. S., Isaac, C., Hunkin, N., & Roberts, N. (2002). Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus. Hippocampus, 12, 325–340.CrossRefPubMedGoogle Scholar
  53. McClelland, J. L., McNaughton, B. L., & OʼReilly, R. C. (1995). Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. Psychological Review, 102, 419–457.CrossRefPubMedGoogle Scholar
  54. McCloskey, M., & Cohen, N. J. (1989). Catastrophic interference in connectionist networks: The sequential learning problem. In G. H. Bower (Ed.), The psychology of learning and motivation (Vol. 24, pp. 109–164). San Diego: Academic.Google Scholar
  55. McGaugh, J. L. (2002). Memory consolidation and the amygdala: A systems perspective. Trends in Neurosciences, 25(9), 456.CrossRefPubMedGoogle Scholar
  56. McGeoch, J. A. (1932). Forgetting and the law of disuse. Psychological Review, 39, 352–370.CrossRefGoogle Scholar
  57. McNaughton, B. L., & Morris, R. G. M. (1987). Hippocampal synaptic enhancement and information storage within a distributed memory system. Trends in Neurosciences, 10(10), 408–415.CrossRefGoogle Scholar
  58. Motley, S. E., & Kirwan, C. B. (2012). A parametric investigation of pattern separation processes in the medial temporal lobe. The Journal of Neuroscience, 32(38), 13076–13085.CrossRefPubMedGoogle Scholar
  59. Müller, G. E., & Pilzicker, A. (1900). Experimentelle Beiträge zur Lehre vom Gedächtnis [Experimental contributions to the science of memory]. Zeitschrift für Psychologie, 1, 1–300.Google Scholar
  60. Norman, K. A., & OʼReilly, R. C. (2003). Modeling hippocampal and neocortical contributions to recognition memory: A complementary learning systems approach. Psychological Review, 110(4), 611–646.CrossRefPubMedGoogle Scholar
  61. OʼReilly, R. C., & Rudy, J. W. (2000). Computational principles of learning in the neocortex and hippocampus. Hippocampus, 10, 389–397.CrossRefPubMedGoogle Scholar
  62. OʼReilly, R. C., & Rudy, J. W. (2001). Conjunctive representations in learning and memory: Principles of cortical and hippocampal function. Psychological Review, 108, 311–345.CrossRefPubMedGoogle Scholar
  63. Quiroga, R. Q., Reddy, L., Kreiman, G., Koch, C., & Fried, I. (2005). Invariant visual representation by single neurons in the human brain. Nature, 435, 1102–1107.CrossRefPubMedGoogle Scholar
  64. Robinson, E. S. (1927). The “similarity” factor in retroaction. American Journal of Psychology, 39, 297–312.CrossRefGoogle Scholar
  65. Roediger, H. L., & McDermott, K. B. (1995). Creating false memories: Remembering words not presented in lis. Journal of Experimental Psychology. Learning, Memory, and Cognition, 12(4), 803–814.CrossRefGoogle Scholar
  66. Rolls, E. T. (1989). Functions of neuronal networks in the hippocampus and neocortex in memory. In J. H. Byrne & W. O. Berry (Eds.), Neural models of plasticity: Experimental and theoretical approaches. San Diego: Academic.Google Scholar
  67. Rolls, E. T., & Treves, A. (1998). Neural networks and brain function. Oxford: Oxford University Press.Google Scholar
  68. Sahay, A., Scobie, K. N., Hill, A. S., OʼCarroll, C. M., Kheirbek, M. A., Burghardt, N. S., Fenton, A. A., Dranovsky, A., & Hen, R. (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature, 472(7344), 466–470.PubMedCentralCrossRefPubMedGoogle Scholar
  69. Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 20, 11–21.PubMedCentralCrossRefPubMedGoogle Scholar
  70. Segal, S. K., Stark, S. M., Kattan, D., Stark, C. E., & Yassa, M. A. (2012). Norepinephrine-mediated emotional arousal facilitates subsequent pattern separation. Neurobiology of learning and memory, 97(4), 465–469.PubMedCentralCrossRefPubMedGoogle Scholar
  71. Shimamura, A. P., Jurica, P. J., Mangels, J. A., Gershberg, F. B., & Knight, R. T. (1995). Susceptibility to memory interference effects following frontal lobe damage: Findings from paired-associate learning. Journal of Cognitive Neuroscience, 7, 144–152.CrossRefPubMedGoogle Scholar
  72. Skaggs, E. B. (1925). Further studies in retroactive inhibition. Psychological Monographs 34(8), 1–60.Google Scholar
  73. Slamecka, N. J., & Ceraso, J. (1977). Retroactive and proactive inhibition of verbal learning. In W. L. Mikulas (Ed.), Psychology of learning: Readings. Chicago: Nelson-Hall.Google Scholar
  74. Small, S. A., Tsai, W. Y., DeLaPaz, R., Mayeux, R., & Stern, Y. (2002). Imaging hippocampal function across the human life span: Is memory decline normal or not? Annals of Neurology, 51(3), 290–295.CrossRefPubMedGoogle Scholar
  75. Squire, L. R., Haist, F., & Shimamura, A. P. (1989). The neurology of memory: Quantitative assessment of retrograde amnesia in two groups of amnesic patients. Journal of Neuroscience, 9(3), 828–839.PubMedGoogle Scholar
  76. Squire, L. R., Clark, R. E., & Bayley, P. J. (2004). Medial temporal lobe function and memory. In M. Gazzaniga (Ed.), The cognitive neurosciences(3rd ed.). Cambridge: MIT Press.Google Scholar
  77. Stark, S. M., Yassa, M. A., & Stark, C. E. (2010). Individual differences in spatial pattern separation performance associated with healthy aging in humans. Learning & Memory, 17(6), 284–288.Google Scholar
  78. Sutherland, R. W., & Rudy, J. W. (1989). Configural association theory: The role of the hippocampal formation in learning, memory and amnesia. Psychobiology, 17, 129–144.Google Scholar
  79. Toner, C. K., Pirogovsky, E., Kirwan, C. B., & Gilbert, P. E. (2009). Visual object pattern separation deficits in nondemented older adults. Learning & Memory, 16(5), 338–342.CrossRefGoogle Scholar
  80. Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53(1), 1–25.CrossRefPubMedGoogle Scholar
  81. Underwood, B. J. (1957). Interference and forgetting. Psychological Review, 64(1), 49–60.CrossRefPubMedGoogle Scholar
  82. van Praag, H., Kempermann, G., & Gage, F. H. (1999). Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nature Neuroscience, 2(3), 266–270.CrossRefPubMedGoogle Scholar
  83. Warrington, E., & Weiskrantz, L. (1974). The effect of prior learning on subsequent retention in amensic patients. Neuropsychologia, 12, 419–428.Google Scholar
  84. Warrington, E., & Weiskrantz, L. (1978). Further analysis of the prior learning effect in amnesic patients. Neuropsychologia, 16, 169–177.CrossRefPubMedGoogle Scholar
  85. Winocur, G., & Moscovitch, M. (1996). Heightened interference on implicit, but not explicit, tests of negative transfer: Evidence from patients with unilateral temporal lobe lesions and normal old people. Brain and Cognition, 30, 44–58.CrossRefPubMedGoogle Scholar
  86. Winocur, G., & Weiskrantz, L. (1976). An investigation of paired-associate learning in amnesic patients. Neuropsychologia, 14, 97–110.CrossRefPubMedGoogle Scholar
  87. Wixted, J. (2004). The psychology and neuroscience of forgetting. Annual Review of Psychology, 55, 235–269.CrossRefPubMedGoogle Scholar
  88. Yassa, M. A., & Stark, C. E. (2011). Pattern separation in the hippocampus. Trends in Neurosciences, 34(10), 515–525.PubMedCentralCrossRefPubMedGoogle Scholar
  89. Yassa, M. A., Lacy, J. W., Stark, S. M., Albert, M. S., Gallagher, M., & Stark, C. E. (2011a). Pattern separation deficits associated with increased hippocampal CA3 and dentate gyrus activity in nondemented older adults. Hippocampus, 21(9), 968–979.PubMedCentralPubMedGoogle Scholar
  90. Yassa, M. A., Mattfeld, A. T., Stark, S. M., & Stark, C. E. (2011b). Age-related memory deficits linked to circuit-specific disruptions in the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 108(21), 8873–8878.Google Scholar
  91. Yonelinas, A. P. (2002). The nature of recollection and familiarity: A review of 30 years of research. Journal of Memory and Language, 46, 441–517.CrossRefGoogle Scholar
  92. Young, W. S., 3rd, & Kuhar, M. J. (1980). Noradrenergic alpha 1 and alpha 2 receptors: Light microscopic autoradiographic localization. Proceedings of the National Academy of Sciences of the United States of America, 77(3), 1696–1700.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Psychology and Neuroscience CenterBrigham Young UniversityProvoUSA

Personalised recommendations