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Neuropsychological Investigations of Human Amnesia: Insights Into the Role of the Medial Temporal Lobes in Cognition

Published online by Cambridge University Press:  04 December 2017

Mieke Verfaellie*
Affiliation:
Memory Disorders Research Center, VA Boston Healthcare System and Boston University School of Medicine, Boston, Massachusetts
Margaret M. Keane
Affiliation:
Memory Disorders Research Center, VA Boston Healthcare System and Boston University School of Medicine, Boston, Massachusetts Wellesley College, Wellesley, Massachusetts
*
Correspondence and reprint requests to: Mieke Verfaellie, Memory Disorders Research Center (151A), VA Boston Healthcare System, 150 S Huntington Avenue, Boston, MA 02130. E-mail: verf@bu.edu

Abstract

The past 30 years of research on human amnesia has yielded important changes in our understanding of the role of the medial temporal lobes (MTL) in memory. On the one hand, this body of evidence has highlighted that not all types of memory are impaired in patients with MTL lesions. On the other hand, this research has made apparent that the role of the MTL extends beyond the domain of long-term memory, to include working memory, perception, and future thinking. In this article, we review the discoveries and controversies that have characterized this literature and that set the stage for a new conceptualization of the role of the MTL in cognition. This shift toward a more nuanced understanding of MTL function has direct relevance for a range of clinical disorders in which the MTL is implicated, potentially shaping not only theoretical understanding but also clinical practice. (JINS, 2017, 23, 732–740)

Type
Section 1 – Brain Systems and Assessment
Copyright
Copyright © The International Neuropsychological Society 2017 

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References

REFERENCES

Aggleton, J.P., & Shaw, C. (1996). Amnesia and recognition memory: A re-analysis of psychometric data. Neuropsychologia, 34, 5162.Google Scholar
Baddeley, A., & Warrington, E.K. (1970). Amnesia and the distinction between long- and short-term memory. Journal of Verbal Learning and Verbal Behavior, 9, 176189.Google Scholar
Barense, M.D., Ngo, J.K.W., Hung, L.H.T., & Peterson, M.A. (2012). Interactions of memory and perception in amnesia: The figure-ground perspective. Cerebral Cortex, 22, 26802691.Google Scholar
Barnabe, A., Whitehead, V., Pilon, R., Arsenault-Lapierre, G., & Chertkow, H. (2012). Autobiographical memory in mild cognitive impairment and Alzheimer’s disease: A comparison between the Levine and Kopelman interview methodologies. Hippocampus, 22, 18091825.Google Scholar
Ben-Zvi, S., Soroker, N., & Levy, D.A. (2015). Parietal lesion effects on cued recall following pair associate learning. Neuropsychologia, 73, 176194.Google Scholar
Berryhill, M.E., Phuong, L., Picasso, L., Cabeza, R., & Olson, I.R. (2007). Parietal damage and episodic memory: Bilateral damage causes impaired free recall of autobiographical memory. Journal of Neuroscience, 27, 1441514423.Google Scholar
Bertossi, E., Aleo, F., Braghittoni, D., & Ciaramelli, E. (2016). Stuck in the here and now: Construction of fictitious and future experiences following ventromedial prefrontal damage. Neuropsychologia, 81, 107116.CrossRefGoogle ScholarPubMed
Blackwell, A.D., Sahakian, B.J., Vesey, R., Semple, J.M., Robbins, T.W., & Hodges, J.R. (2004). Detecting dementia: Novel neuropsychological markers of preclinical Alzheimer’s disease. Dementia and Geriatric Cognitive Disorders, 17, 4248.CrossRefGoogle ScholarPubMed
Bohbot, V.D., Kalina, M., Stepankova, K., Spackova, M., Petrides, M., & Nadel, L. (1998). Spatial memory deficits in patients with lesions to the right hippocampus and to the right parahippocampal cortex. Neuropsychologia, 36, 12171238.Google Scholar
Borders, A.A., Aly, M., Parks, C.M., & Yonelinas, A.P. (2017). The hippocampus is particularly important for building associations across stimulus domains. Neuropsychologia, 99, 335342.Google Scholar
Bowles, B., Crupi, C., Mirsattari, S.M., Pigott, S.E., Parrent, A.G., Pruessner, J.C., & Kohler, S. (2007). Impaired familiarity with preserved recollection after anterior temporal-lobe resection that spares the hippocampus. Proceedings of the National Academy of Sciences of the United States of America, 104, 1638216387.Google Scholar
Bowles, B., Crupi, C., Pigott, S., Parrent, A., Wiebe, S., Janzen, L., && Kohler, S. (2010). Double dissociation of selective recollection and familiarity impairments following two different surgical treatments for temporal-lobe epilepsy. Neuropsychologia, 48, 26402647.Google Scholar
Cohen, N.J., & Eichenbaum, H. (1993). Memory, amnesia, and the hippocampal system. Cambridge, MA: MIT Press.Google Scholar
Dede, A.J.O., & Smith, C.N. (2016). The functional and structural neuroanatomy of systems consolidation for autobiographical and semantic memory. Current Topics in Behavioral Neuroscience. [Epub ahead of print]. doi: 10.1007/7854_2016_452 Google Scholar
Della Sala, S., Parra, M.A., Fabi, K., Luzzi, S., & Abrahams, S. (2012). Short-term memory binding is impaired in AD but not in non-AD dementias. Neuropsychologia, 50, 833840.Google Scholar
Dewar, M., Della Sala, S., Beschin, N., & Cowan, N. (2010). Profound retrograde interference in anterograde amnesia: What interferes? Neuropsychology, 24, 357367.CrossRefGoogle Scholar
Diana, R.A., Yonelinas, A.P., & Ranganath, C. (2007). Imaging recollection and familiarity in the medial temporal lobe: A three-component model. Trends in Cognitive Sciences, 11, 379386.CrossRefGoogle ScholarPubMed
Duff, M.C., Kurczek, J., Rubin, R., Cohen, N.J., & Tranel, D. (2013). Hippocampal amnesia disrupts creative thinking. Hippocampus, 23, 11431149.CrossRefGoogle ScholarPubMed
Eichenbaum, H., Yonelinas, A.R., & Ranganath, C. (2007). The medial temporal lobe and recognition memory. Annual Review of Neuroscience, 30, 123152.Google Scholar
Foerde, K., Race, E., Verfaellie, M., & Shohamy, D. (2013). A role for the medial temporal lobe in feedback-driven learning: Evidence from amnesia. Journal of Neuroscience, 33, 56985704.Google Scholar
Giovanello, K.S., Verfaellie, M., & Keane, M.M. (2003). Disproportionate deficit in associative recognition memory in global amnesia. Cognitive, Affective and Behavioral Neuroscience, 3, 186194.Google Scholar
Graham, K.S., Barense, M.D., & Lee, A.C.H. (2010). Going beyond LTM in the MTL: A synthesis of neuropsychological and neuroimaging findings on the role of the medial temporal lobe in memory and perception. Neuropsychologia, 48, 831853.Google Scholar
Hanula, D.E., Tranel, D., & Cohen, N.J. (2006). The long and the short of it: Relational memory impairments in amnesia, even at short lags. Journal of Neuroscience, 26, 83528359.Google Scholar
Hassabis, D., Kumaran, D., Vann, S., & Maguire, E. (2007). Patients with hippocampal amnesia cannot imagine new experiences. Proceedings of the National Academy of Sciences of the United States of America, 104, 17261731.Google Scholar
Hayes, S.M., Salat, D.H., & Verfaellie, M. (2012). Default network connectivity in medial temporal lobe amnesia. Journal of Neuroscience, 32, 1462214629.Google Scholar
Henson, R.N., Greve, A., Cooper, E., Gregori, M., Simons, J.S., Geerligs, L., & Browne, G. (2016). The effects of hippocampal lesions on MRI measures of structural and functional connectivity. Hippocampus, 26, 14471463.Google Scholar
Jeneson, A., & Squire, L.R. (2012). Working memory, long-term memory, and medial temporal lobe function. Learning and Memory, 19, 1525.Google Scholar
Jones, D.T., Mateen, F.J., Lucchinetti, C.F., Jack, C.R., & Welker, K.M. (2011). Default mode network disruption secondary to a lesion in the anterior thalamus. Archives of Neurology, 68, 242247.Google Scholar
Kan, I.P., Giovanello, K.S., Schnyer, D.M., Makris, N., & Verfaellie, M. (2007). Role of the medial temporal lobes in relational memory: Neuropsychological evidence from a cued recognition paradigm. Neuropsychologia, 45, 25892597.Google Scholar
Kirwan, C., Bayley, P.J., Galvan, V., & Squire, L.R. (2008). Detailed recollection of remote autobiographical memory after damage to the medial temporal lobe. Proceedings of the National Academy of Sciences of the United States of America, 105, 26762680.Google Scholar
Knowlton, B.J., Mangels, J.A., & Squire, L.R. (1996). A neostriatal habit-learning system in humans. Science, 273, 13991402.Google Scholar
Knowlton, B.J., Ramus, S.J., & Squire, L.R. (1992). Intact artificial grammar learning in amnesia: Dissociation of classification learning and explicit memory for specific instances. Psychological Science, 3, 172179.Google Scholar
Knutson, A.R., Hopkins, R.A., & Squire, L.R. (2012). Visual discrimination performance, memory, and medial temporal lobe function. Proceedings of the National Academy of Sciences of the United States of America, 109, 1310613111.CrossRefGoogle ScholarPubMed
Knutson, A.R., Hopkins, R.A., & Squire, L.R. (2013). A pencil rescues impaired performance on a visual discrimination task in patients with medial temporal lobe lesions. Learning and Memory, 20, 607610.Google Scholar
Koen, J.D., Borders, A.A., Petzold, M.T., & Yonelinas, A.P. (2016). Visual short-term memory for high resolution associations is impaired in patients with medial temporal lobe damage. Hippocampus, 27, 184193.Google Scholar
Lah, S., & Miller, L. (2008). Effects of temporal lobe lesions on retrograde amnesia: A critical review. Neuropsychological Review, 18, 2452.Google Scholar
Lee, A.C.H., Buckley, M.J., Pegman, S.J., Spiers, H.J., Scahill, V.L., Gaffan, D., & Graham, K.S. (2005). Specialization in the medial temporal lobe for processing of objects and scenes. Hippocampus, 15, 782797.CrossRefGoogle ScholarPubMed
Lee, A.C.H., Bussey, T.J., Murray, E.A., Saksida, L.M., Epstein, R.A., Kapur, N., & Graham, K.S. (2005). Perceptual deficits in amnesia: Challenging the medial temporal lobe “mnemonic” view. Neuropsychologia, 43, 111.Google Scholar
Lee, A.C.H., Rahman, S., Hodges, J.R., Sahakian, B.J., & Graham, K.S. (2003). Associative and recognition memory for novel objects in dementia: Implications for diagnosis. European Journal of Neuroscience, 18, 16601670.Google Scholar
Lee, A.C.H., & Rudebeck, S.R. (2010). Human medial temporal lobe damage can disrupt the perception of single objects. Journal of Neuroscience, 30, 65886594.Google Scholar
Lee, A.C.H., Yeung, L.K., & Barense, M.D. (2012). The hippocampus and visual perception. Frontiers in Human Neuroscience, 6, 117.Google Scholar
Levine, B., Svoboda, E., Hay, J.F., Winocur, G., & Moscovitch, M. (2002). Aging and autobiographical memory: Dissociating episodic from semantic retrieval. Psychology and Aging, 17, 677689.Google Scholar
Mayes, A.R., Montaldi, D., & Migo, E. (2007). Associative memory and the medial temporal lobes. Trends in Cognitive Sciences, 11, 126135.Google Scholar
Mayes, A.R., Holdstock, J.S., Isaac, C.L., Montaldi, D., Grigor, J., Gummer, A., & Norman, K.A. (2004). Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition. Hippocampus, 14, 763784.Google Scholar
Milner, B. (1962). Les troubles de la memoire accompagnant des lesions hippocampiques bilaterales [Memory impairment accompanying bilateral hippocampal lesions]. In P. Passouant (Ed.), Physiologie de I’Hippocampe (pp. 257272). Paris: C.N.R.S.Google Scholar
Milner, B., Corkin, S., & Teuber, H.-L. (1968). Further analysis of the hippocampal amnesia syndrome: 14-year follow-up study of H.M. Neuropsychologia, 6, 215234.Google Scholar
Moscovitch, M., Nadel, L., Winocur, G., Gilboa, A., & Rosenbaum, R.S. (2006). The cognitive neuroscience of remote episodic, semantic and spatial memory. Current Opinion in Neurobiology, 16, 179190.Google Scholar
Moscovitch, M., Vriezen, E., & Gottstein, J. (1993). Implicit tests of memory in patients with focal lesions or degenerative brain disorders. In H. Spinnler & F. Boller (Eds.), Handbook of neuropsychology (Vol. 8, pp. 133173). Amsterdam: Elsevier.Google Scholar
Nadel, L., & Moscovitch, M.M. (1997). Memory consolidation, retrograde amnesia and the hippocampal complex. Current Opinion in Neurobiology, 7, 217227.CrossRefGoogle ScholarPubMed
Olson, I.R., Page, K., Moore, K.S., Chatterjee, A., & Verfaellie, M. (2006). Working memory for conjunctions relies on the medial temporal lobe. Journal of Neuroscience, 26, 45964601.Google Scholar
Palombo, D.J., Keane, M.M., & Verfaellie, M. (2015). The medial temporal lobes are critical for reward-based decision making under conditions that promote episodic future thinking. Hippocampus, 23, 345353.Google Scholar
Palombo, D.J., Keane, M.M., & Verfaellie, M. (2016). Using future thinking to reduce temporal discounting: Under what circumstances are the medial temporal lobes critical? Neuropsychologia, 89, 437444.Google Scholar
Pertzov, Y., Miller, T.D., Gorgoraptis, N., Caine, D., Schott, J.M., Butler, C., & Husain, M. (2013). Binding deficits in memory following medial temporal lobe damage in patients with voltage-gated potassium channel complex antibody-associated limbic encephalitis. Brain, 136, 24742485.Google Scholar
Quamme, J.R., Yonelinas, A.P., & Norman, K.A. (2007). Effect of unitization on associative recognition in amnesia. Hippocampus, 17, 192200.Google Scholar
Race, E., Keane, M.M., & Verfaellie, M. (2011). Medial temporal lobe damage causes deficits in episodic memory and episodic future thinking not attributable to deficits in narrative construction. Journal of Neuroscience, 31, 1026210269.Google Scholar
Race, E., LaRocque, K.F., Keane, M.M., & Verfaellie, M. (2013). Medial temporal lobe contributions to short-term memory for faces. Journal of Experimental Psychology: General, 142, 13091322.Google Scholar
Reber, P.J. (2013). The neural basis of implicit learning and memory: A review of neuropsychological and neuroimaging research. Neuropsychologia, 51, 20262042.CrossRefGoogle ScholarPubMed
Reed, L.J., Lasserson, D., Marsden, P., Stanhope, N., Stevens, T., Bello, F., & Kopelman, M. (2003). FDG-PET findings in the Wernicke-Korsakoff syndrome. Cortex, 39, 10271045.Google Scholar
Reed, L.J., Marsden, P., Lasserson, D., Sheldon, N., Lewis, P., Stanhope, N., & Kopelman, M.D. (1999). FDG-PET analysis and findings in amnesia resulting from hypoxia. Memory, 7, 599612.Google Scholar
Rensen, Y.C.M., Kessels, R.P.C., Migo, E.M., Wester, A.J., Eling, P.A.T.M., & Kopelman, M. (2017). Personal semantic and episodic autobiographical memories in Korsakoff syndrome: A comparison of interview methods. Journal of Clinical and Experimental Neuropsychology, 39, 534546.CrossRefGoogle ScholarPubMed
Romero, K., & Moscovitch, M. (2012). Episodic memory and event construction in aging and amnesia. Journal of Memory and Language, 67, 270284.Google Scholar
Rosenbaum, R.S., Gilboa, A., & Moscovitch, M. (2014). Case studies continue to illuminate the cognitive neuroscience of memory. Annals of the New York Academy of Sciences, 1316, 105133.Google Scholar
Rosenbaum, R.S., Moscovitch, M., Foster, J.K., Schnyer, D.M., Gao, F.Q., Kovacevic, N., & Levine, B. (2008). Patterns of autobiographical memory loss in medial temporal lobe amnesic patients. Journal of Cognitive Neuroscience, 20, 14901506.Google Scholar
Sadeh, T., Ozubko, J., & Moscovitch, M. (2014). How we forget may depend on how we remember. Trends in Cognitive Sciences, 18, 2636.Google Scholar
Schacter, D.L., Addis, D.R., & Buckner, R.L. (2007). Remembering the past to imagine the future: The prospective brain. Nature Reviews Neuroscience, 8, 657661.Google Scholar
Scoville, W., & Milner, B. (1957). Loss of recent memory after bilateral hippocampal lesions. Journal of Neurology, Neurosurgery, and Psychiatry, 20, 1121.Google Scholar
Sheldon, S., McAndrews, M.P., & Moscovitch, M. (2011). Episodic memory processes mediated by the medial temporal lobes contribute to open-ended problem solving. Neuropsychologia, 49, 24392447.Google Scholar
Shohamy, D., Myers, C.E., Kalanithi, J., & Gluck, M.A. (2008). Basal ganglia and dopamine contributions to probabilistic category learning. Neuroscience and Biobehavioral Reviews, 32, 219236.CrossRefGoogle ScholarPubMed
Shohamy, D., & Turk-Browne, N.B. (2013). Mechanisms for widespread hippocampal involvement in cognition. Journal of Experimental Psychology: General, 142, 11591170.Google Scholar
Squire, L.R., & Alvarez, P. (1995). Retrograde amnesia and memory consolidation: A neurobiological perspective. Current Opinion in Neurobiology, 5, 169177.Google Scholar
Squire, L.R., Stark, C.E.L., & Clark, R.E. (2004). The medial temporal lobe. Annual Review of Neuroscience, 27, 279306.Google Scholar
Squire, L.R., van der Horst, A.S., McDuff, S.G., Frascino, J.C., Hopkins, R.O., & Mauldin, K.N. (2010). Role of the hippocampus in remembering the past and imagining the future. Proceedings of the National Academy of Sciences of the United States of America, 107, 1904419048.Google Scholar
Squire, L.R., & Wixted, J.T. (2011). The cognitive neuroscience of human memory since H.M. Annual Review of Neuroscience, 34, 259288.Google Scholar
Vargha-Khadem, F., Gadian, D.G., Watkins, K.E., Connelly, A., Van Paesschen, W., & Mishkin, M. (1997). Differential effects of early hippocampal pathology on episodic and semantic memory. Science, 277, 376380.Google Scholar
Verfaellie, M., & Keane, M.M. (2001). Scope and limits of implicit memory in amnesia. In B. De Gelder, E. De Haan & C. Heywood (Eds.), Unconscious minds (pp. 151162). Oxford: Oxford University Press.Google Scholar
Verfaellie, M., & Keane, M.M. (2002). Impaired and preserved memory processes in amnesia. In L.R. Squire & D.L. Schacter (Eds.), Neuropsychology of memory (3rd ed., pp. 3546). New York: Guilford Press.Google Scholar
Verfaellie, M., LaRocque, K.F., & Keane, M.M. (2012). Intact implicit verbal relational memory in medial temporal lobe amnesia. Neuropsychologia, 50, 21002106.Google Scholar
Verfaellie, M., Race, E., & Keane, M.M. (2012). Medial temporal lobe contributions to future thinking: Evidence from neuroimaging and amnesia. Psychologica Belgica, 52, 7794.Google Scholar
Watson, P.D., Voss, J.L., Warren, D.E., Tranel, D., & Cohen, N.J. (2013). Spatial reconstruction by patients with hippocampal damage is dominated by relational memory errors. Hippocampus, 23, 570580.Google Scholar
Winocur, G., Moscovitch, M., & Bontempi, B. (2010). Memory formation and long-term retention in humans and animals: Convergence towards a transformation account of hippocampal–neocortical interactions. Neuropsychologia, 48, 23392356.Google Scholar
Wixted, J.T., & Squire, L.R. (2011). The medial temporal lobe and the attributes of memory. Trends in Cognitive Sciences, 15, 210217.Google Scholar
Yonelinas, A.P. (2013). The hippocampus supports high-resolution binding in the service of perception, working memory and long-term memory. Behavioural Brain Research, 254, 3444.Google Scholar