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.
The views expressed in this article are those of the authors and do not reflect the official policy or position of the United States Air Force, Department of Defense, or the U.S. Government.
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Badre, D., & Wagner, A. D. (2005). Frontal lobe mechanisms that resolve proactive interference. Cerebral Cortex, 15, 2003–2012.
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.
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.
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.
Blank, H. (2005). Another look at retroactive and proactive interference: A quantitative analysis of conversion processes. Memory, 13(2), 200–224.
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.
Burgess, N., & OʼKeefe, J. (1996). Neuronal computations underlying the firing of place cells and their rolei n navigation. Hippocampus, 6, 749–762.
Crowder, R. G. (1976). Principles of learning and memory. New York: Lawrence Erlbaum Associates.
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.
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.
Duncan, K., Sadanand, A., & Davachi, L. (2012). Memoryʼs penumbra: Episodic memory decisions induce lingering mnemonic biases. Science, 337(6093), 485–487.
Ekstrand, B. R. (1967). The effect of sleep on memory. Journal of Experimental Psychology, Applied, 75, 64–72.
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.
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.
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.
Guzowski, J. F., Knierim, J. J., & Moser, E. I. (2004). Ensemble dynamics of hippocampal regions CA3 and CA1. Neuron, 44, 581–584.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Jenkins, J. B., & Dallenbach, K. M. (1924). Oblivescence during sleep and waking. American Journal of Psychology, 35, 605–612.
Johnson, M. K., Hashtroudi, S., & Lindsay, D. S. (1993). Source monitoring. Psychological Bulletin, 114(1), 3–28.
Keppel, G. (1984). Consolidation and forgetting theory. In H. Weingartner & E. S. Parker (Eds.), Memory consolidation: Psychobiology of cognition (pp. 149–161). Hillsdale: Erlbaum.
Kesner, R. P. (1991). The role of the hippocampus within an attribute model of memory. Hippocampus, 1(3), 279–282.
Kesner, R. P. (2009). Tapestry of memory. Behavioral Neuroscience, 123(1), 1–13.
Kesner, R. P., & Hopkins, R. O. (2006). Mnemonic functions of the hippocampus: A comparison between animals and humans. Biological Psychology, 73(1), 3–18.
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.
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.
Kinsbourne, M., & Winocur, G. (1980). Response competition and interference effects in paired-associate learning by Korsakoff amnesics. Neuropsychologia, 18, 541–548.
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.
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.
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.
Kumaran, D., & Maguire, E. A. (2009). Novelty signals: A window into hippocampal information processing. Trends in Cognitive Sciences, 13(2), 47–54.
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.
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.
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.
Leutgeb, S. (2008). Neuroscience. Detailed differences. Science, 319(5870), 1623–1624.
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.
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.
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.
Lustig, C., & Hasher, L. (2001). Implicit memory is not immune to interference. Psychological Bulletin, 127(5), 618–628.
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.
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.
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.
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.
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.
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.
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.
McGaugh, J. L. (2002). Memory consolidation and the amygdala: A systems perspective. Trends in Neurosciences, 25(9), 456.
McGeoch, J. A. (1932). Forgetting and the law of disuse. Psychological Review, 39, 352–370.
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.
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.
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.
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.
OʼReilly, R. C., & Rudy, J. W. (2000). Computational principles of learning in the neocortex and hippocampus. Hippocampus, 10, 389–397.
OʼReilly, R. C., & Rudy, J. W. (2001). Conjunctive representations in learning and memory: Principles of cortical and hippocampal function. Psychological Review, 108, 311–345.
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.
Robinson, E. S. (1927). The “similarity” factor in retroaction. American Journal of Psychology, 39, 297–312.
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.
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.
Rolls, E. T., & Treves, A. (1998). Neural networks and brain function. Oxford: Oxford University Press.
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.
Scoville, W. B., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery and Psychiatry, 20, 11–21.
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.
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.
Skaggs, E. B. (1925). Further studies in retroactive inhibition. Psychological Monographs 34(8), 1–60.
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.
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.
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.
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.
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.
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.
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.
Tulving, E. (2002). Episodic memory: From mind to brain. Annual Review of Psychology, 53(1), 1–25.
Underwood, B. J. (1957). Interference and forgetting. Psychological Review, 64(1), 49–60.
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.
Warrington, E., & Weiskrantz, L. (1974). The effect of prior learning on subsequent retention in amensic patients. Neuropsychologia, 12, 419–428.
Warrington, E., & Weiskrantz, L. (1978). Further analysis of the prior learning effect in amnesic patients. Neuropsychologia, 16, 169–177.
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.
Winocur, G., & Weiskrantz, L. (1976). An investigation of paired-associate learning in amnesic patients. Neuropsychologia, 14, 97–110.
Wixted, J. (2004). The psychology and neuroscience of forgetting. Annual Review of Psychology, 55, 235–269.
Yassa, M. A., & Stark, C. E. (2011). Pattern separation in the hippocampus. Trends in Neurosciences, 34(10), 515–525.
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.
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.
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.
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.
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Kirwan, C., Nash, M. (2016). Resolving Interference: The Role of the Human Hippocampus in Pattern Separation. In: Jackson, P., Chiba, A., Berman, R., Ragozzino, M. (eds) The Neurobiological Basis of Memory. Springer, Cham. https://doi.org/10.1007/978-3-319-15759-7_7
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