Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition

Previous work (Mayes et al., Hippocampus 12:325–340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we fo...

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Published inHippocampus Vol. 14; no. 6; pp. 763 - 784
Main Authors Mayes, A.R., Holdstock, J.S., Isaac, C.L., Montaldi, D., Grigor, J., Gummer, A., Cariga, P., Downes, J.J., Tsivilis, D., Gaffan, D., Gong, Qiyong, Norman, K.A.
Format Journal Article
LanguageEnglish
Published Hoboken Wiley Subscription Services, Inc., A Wiley Company 2004
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Online AccessGet full text
ISSN1050-9631
1098-1063
DOI10.1002/hipo.10211

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Abstract Previous work (Mayes et al., Hippocampus 12:325–340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced‐choice recognition of both intra‐item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter‐item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra‐item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined. © 2004 Wiley‐Liss, Inc.
AbstractList Previous work (Mayes et al., Hippocampus 12:325–340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced‐choice recognition of both intra‐item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, abstract visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter‐item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra‐item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined. © 2004 Wiley‐Liss, Inc.
Previous work (Mayes et al., Hippocampus 12:325–340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced‐choice recognition of both intra‐item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter‐item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra‐item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined. © 2004 Wiley‐Liss, Inc.
Previous work (Mayes et al., Hippocampus 12:325-340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced-choice recognition of both intra-item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, abstract visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter-item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra-item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined.
Previous work (Mayes et al., Hippocampus 12:325-340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced-choice recognition of both intra-item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, abstract visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter-item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra-item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined.Previous work (Mayes et al., Hippocampus 12:325-340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed relatively preserved verbal and visual item recognition memory in the face of clearly impaired verbal and visual recall. In this study, we found that YR's Yes/No as well as forced-choice recognition of both intra-item associations and associations between items of the same kind was as well preserved as her item recognition memory. In contrast, YR was clearly impaired, and more so than she was on the above kinds of recognition, at recognition of associations between different kinds of information. Thus, her recognition memory for associations between objects and their locations, words and their temporal positions, abstract visual items or words and their temporal order, animal pictures and names of professions, faces and voices, faces and spoken names, words and definitions, and pictures and sounds, was clearly impaired. Several of the different information associative recognition tests at which YR was impaired could be compared with related item or inter-item association recognition tests of similar difficulty that she performed relatively normally around the same time. It is suggested that YR's familiarity memory for items, intra-item associations, and associations between items of the same kind was mediated by her intact medial temporal lobe cortices and was preserved, whereas her hippocampally mediated recall/recollection of these kinds of information was impaired. It is also suggested that the components of associations between different kinds of information are represented in distinct neocortical regions and that initially they only converge for memory processing within the hippocampus. No familiarity memory may exist in normal subjects for such associations, and, if so, YR's often chance recognition occurred because of her severe recall/recollection deficit. Conflicting data and views are discussed, and the way in which recall as well as item and associative recognition need to be systematically explored in patients with apparently selective hippocampal lesions, in order to resolve existing conflicts, is outlined.
Author Tsivilis, D.
Gong, Qiyong
Norman, K.A.
Cariga, P.
Montaldi, D.
Gummer, A.
Grigor, J.
Gaffan, D.
Holdstock, J.S.
Downes, J.J.
Mayes, A.R.
Isaac, C.L.
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References Holdstock JS, Mayes AR, Cezyirli E, Isaac CL, Aggleton JP, Roberts JN. 2000. A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage. Neuropsychologia 38: 410-425.
Baddeley A, Vargha-Khadem F, Mishkin M. 2001. Preserved recognition in a case of developmental amnesia: implications for the acquisition of semantic memory? J Cogn Neurosci 13: 357-369.
Squire LR, Zola SM. 1998. Episodic memory, semantic memory, and amnesia. Hippocampus 8: 205-211.
Yonelinas AP, Kroll NEA, Quamme JR, Lazzara MM, Sauve M-J, Widaman KF, Knight RT. 2002. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat Neurosci 5: 1236-1241.
Holdstock JS, Mayes AR, Roberts N, Cezayirli E, Isaac CL, O'Reilly RC, Norman KA. 2002a. Under what conditions is recognition spared relative to recall after selective hippocampal damage? Hippocampus 12: 341-351.
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Mishkin M, Vargha-Khadem F, Gadian DG. 1998. Amnesia and the organization of the hippocampal system. Hippocampus 8: 212-216.
Maguire EA, Vargha-Khadem F, Mishkin, M. 2001. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124: 1156-1170.
Burgess N, Maguire EA, O'Keefe J. 2002. The human hippocampus and spatial and episodic memory. Neuron 35: 625-641.
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Searcy JH, Bartlett JC. 1996. Inversion and processing of component and spatial-relation information in faces. J Exp Psychol Hum Percept Perform 22: 904-915.
Warrington EK. 1984. Recognition memory test. Windsor, UK: NFER-Nelson.
Montaldi, D, Spencer, T, Alvarez A, Roberts N, Mayes A. 2003. Strength of item familiarity memory is mediated by the perirhinal cortex not the hippocampus. Neuroimage 19: S25.
Stark CEL, Squire LR. 2003. Hippocampal damage equally impairs memory for single items and memory for conjunctions. Hippocampus 13: 239-250.
Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR. 2003. Recognition memory and the human hippocampus. Neuron 37: 171-180.
Eldridge LL, Knowlton BJ, Furmanski CS, Bookheimer SY, Engel SA. 2000. Remembering episodes: a selective role for the hippocampus during retrieval. Nat Neurosci 3: 149-1152.
Yonelinas AP, Kroll NEA, Dobbins, IG, Soltani, M. 1999. Recognition memory for faces: when familiarity supports associative memory judgments. Psychon Bull Rev 6: 654-661.
Aggleton JP, Brown M. 1999. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22: 425-489.
Holdstock JS, Mayes AR, Isaac CL, Roberts JN. 2002b. Differential involvement of the hippocampus and temporal cortices in rapid and slow learning of new semantic information. Neuropsychologia 40: 748-768.
Brown MW, Bashir ZI. 2002. Evidence concerning how neurons of the perirhinal cortex may effect familiarity discrimination. Philos Trans R Soc B 357: 1083-1096.
Reinitz MT, Verfaellie M, Milberg WP. 1996. Memory conjunction errors in normal and amnesic subjects. J Mem Lang 35: 286-299.
Manns JR, Squire LR. 1999. Impaired recognition memory on the Doors and People test after damage limited to the hippocampal region. Hippocampus 9: 495-499.
Murray EA, Mishkin M. 1985. Amydalectomy impairs crossmodal association in monkeys. Science 228: 604-606.
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Mayes AR, Holdstock JS, Isaac CL, Hunkin NM, Roberts N. 2002. Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus. Hippocampus 12: 325-340.
Cave CB, Squire LR. 1991. Equivalent impairment of spatial and non spatial memory following damage to the human hippocampus. Hippocampus 1: 329-340.
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Aggleton JP, McMackin D, Carpenter, K, Hornak J, Kapur N, Halpin S, Wiles CM, Kamel H, Brennan P, Carton S, Gaffan D. 2000. Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. Brain 123: 800-815.
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Yonelinas AP. 1997. Recognition memory ROCs for item and associative information: the contribution of recollection and familiarity. Mem Cogn 25: 747-763.
Murre JMJ. 1997. Implicit and explicit memory in amnesia: some explanations and predictions by the tracelink model. Memory 5: 213-232.
Caldwell JI, Masson MEJ. 2001. Conscious and unconscious influences for object location. Mem Cogn 29: 285-295.
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12099484 - Hippocampus. 2002;12(3):325-40
References_xml – reference: Simons JS, Verfaellie M, Galton CJ, Miller BL, Hodges JR, Graham KS. 2002. Recollection-based memory in frontotemporal dementia: implications for theories of long-term memory. Brain 125: 2523-2536.
– reference: Maguire EA, Vargha-Khadem F, Mishkin, M. 2001. The effects of bilateral hippocampal damage on fMRI regional activations and interactions during memory retrieval. Brain 124: 1156-1170.
– reference: Zola SM, Squire LR, Amaral DG. 1986. Human amnesia and the medial temporal lobe region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus. J Neurosci 6: 2950-2967.
– reference: Aggleton JP, Brown M. 1999. Episodic memory, amnesia, and the hippocampal-anterior thalamic axis. Behav Brain Sci 22: 425-489.
– reference: Rabinowitz JC. 1986. Priming in episodic memory. J Gerontol 41: 204-213.
– reference: Henke K, Kroll NEA, Behniea H, Amaral DG, Miller MB, Rafal R, Gazzaniga MS. 1999. Memory lost and regained following bilateral hippocampal damage. J Cogn Neurosci 11: 682-697.
– reference: Small SA, Wu EX, Bartsch D, Perera GM, Lacefield CO, DeLaPaz R, Mayeux R, Stern Y, Kandel ER. 2000. Imaging physiologic dysfunction of individual hippocampal subregions in humans and genetically modified mice. Neuron 28: 653-664.
– reference: Reed JM, Squire LR. 1997. Impaired recognition memory in patients with lesions limited to the hippocampal formation. Behav Neurosci 111: 667-675.
– reference: Manns JR, Hopkins RO, Reed JM, Kitchener EG, Squire LR. 2003. Recognition memory and the human hippocampus. Neuron 37: 171-180.
– reference: Montaldi, D, Spencer, T, Alvarez A, Roberts N, Mayes A. 2003. Strength of item familiarity memory is mediated by the perirhinal cortex not the hippocampus. Neuroimage 19: S25.
– reference: Holdstock JS, Mayes AR, Cezyirli E, Isaac CL, Aggleton JP, Roberts JN. 2000. A comparison of egocentric and allocentric spatial memory in a patient with selective hippocampal damage. Neuropsychologia 38: 410-425.
– reference: Mandler G. 1980. Recognizing: the judgement of previous occurrence. Psychol Rev 87: 252-271.
– reference: Baddeley A, Emslie, H, Nimmo-Smith I. 1994. Doors and People test. Bury St. Edmunds, UK: Thames Valley Test Co.
– reference: Bogacz R, Brown MW, Giraud-Carrier C. 2001. Model of familiarity discrimination in the perirhinal cortex. J Comput Neurosci 10: 5-23.
– reference: Brasted PJ, Bussey TJ, Murray EA, Wise SP. 2003. Role of the hippocampal system in associative learning beyond the spatial domain. Brain 126: 1202-1223.
– reference: Searcy JH, Bartlett JC. 1996. Inversion and processing of component and spatial-relation information in faces. J Exp Psychol Hum Percept Perform 22: 904-915.
– reference: Murray EA, Mishkin M. 1985. Amydalectomy impairs crossmodal association in monkeys. Science 228: 604-606.
– reference: Baddeley A, Vargha-Khadem F, Mishkin M. 2001. Preserved recognition in a case of developmental amnesia: implications for the acquisition of semantic memory? J Cogn Neurosci 13: 357-369.
– reference: Mishkin M, Vargha-Khadem F, Gadian DG. 1998. Amnesia and the organization of the hippocampal system. Hippocampus 8: 212-216.
– reference: Warrington EK. 1984. Recognition memory test. Windsor, UK: NFER-Nelson.
– reference: Caldwell JI, Masson MEJ. 2001. Conscious and unconscious influences for object location. Mem Cogn 29: 285-295.
– reference: Davachi L, Mitchell JP, Wagner AD. 2003. Multiple routes to memory: distinct medial temporal lobe processes build item and source memories. Proc Natl Acad Sci USA 100: 2157-2162.
– reference: Brown MW, Aggleton JP. 2001. Recognition memory: what are the roles of the perirhinal cortex and hippocampus? Nat Rev Neurosci 2: 51-61.
– reference: King JA, Burgess N, Hartley T, Vargha-Khadem F, O'Keefe J. 2002. The human hippocampus and viewpoint dependence in spatial memory. Hippocampus 12: 811-820.
– reference: Holdstock JS, Mayes AR, Roberts N, Cezayirli E, Isaac CL, O'Reilly RC, Norman KA. 2002a. Under what conditions is recognition spared relative to recall after selective hippocampal damage? Hippocampus 12: 341-351.
– reference: Mayes AR, Holdstock JS, Isaac CL, Hunkin NM, Roberts N. 2002. Relative sparing of item recognition memory in a patient with adult-onset damage limited to the hippocampus. Hippocampus 12: 325-340.
– reference: Squire LR, Zola SM. 1998. Episodic memory, semantic memory, and amnesia. Hippocampus 8: 205-211.
– reference: Brown MW, Bashir ZI. 2002. Evidence concerning how neurons of the perirhinal cortex may effect familiarity discrimination. Philos Trans R Soc B 357: 1083-1096.
– reference: Reinitz MT, Verfaellie M, Milberg WP. 1996. Memory conjunction errors in normal and amnesic subjects. J Mem Lang 35: 286-299.
– reference: Cave CB, Squire LR. 1991. Equivalent impairment of spatial and non spatial memory following damage to the human hippocampus. Hippocampus 1: 329-340.
– reference: Yonelinas AP, Kroll NEA, Dobbins, IG, Soltani, M. 1999. Recognition memory for faces: when familiarity supports associative memory judgments. Psychon Bull Rev 6: 654-661.
– reference: Eichenbaum H, Otto T, Cohen NJ. 1994. Two functional components of the hippocampal memory system. Brain Behav 17: 449-518.
– reference: Eldridge LL, Knowlton BJ, Furmanski CS, Bookheimer SY, Engel SA. 2000. Remembering episodes: a selective role for the hippocampus during retrieval. Nat Neurosci 3: 149-1152.
– reference: O'Reilly RC, Norman KA. 2002. Hippocampal and neocortical contributions to memory: advances in the complementary learning systems framework. Trends Cogn Sci 6: 505-510.
– reference: Yonelinas AP, Kroll NEA, Quamme JR, Lazzara MM, Sauve M-J, Widaman KF, Knight RT. 2002. Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity. Nat Neurosci 5: 1236-1241.
– reference: Aggleton JP, McMackin D, Carpenter, K, Hornak J, Kapur N, Halpin S, Wiles CM, Kamel H, Brennan P, Carton S, Gaffan D. 2000. Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. Brain 123: 800-815.
– reference: Holdstock JS, Mayes AR, Isaac CL, Roberts JN. 2002b. Differential involvement of the hippocampus and temporal cortices in rapid and slow learning of new semantic information. Neuropsychologia 40: 748-768.
– reference: Yonelinas AP. 1997. Recognition memory ROCs for item and associative information: the contribution of recollection and familiarity. Mem Cogn 25: 747-763.
– reference: Norman KA, O'Reilly RC. 2003. Modeling hippocampal and neocortical contributions to recognition memory: a complementary learning systems approach. Psychol Rev 110: 611-646.
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SSID ssj0011500
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Snippet Previous work (Mayes et al., Hippocampus 12:325–340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed...
Previous work (Mayes et al., Hippocampus 12:325-340, 2002) found that patient YR, who suffered a selective bilateral lesion to the hippocampus in 1986, showed...
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SubjectTerms Aged
associative memory
Brain Ischemia - chemically induced
Brain Ischemia - pathology
Brain Ischemia - physiopathology
Cerebral Cortex - pathology
Cerebral Cortex - physiopathology
Cerebral Infarction - chemically induced
Cerebral Infarction - pathology
Cerebral Infarction - physiopathology
Cognition Disorders - pathology
Cognition Disorders - physiopathology
Cognition Disorders - psychology
familiarity
Female
hippocampus
Hippocampus - pathology
Hippocampus - physiopathology
Humans
Language Disorders - chemically induced
Language Disorders - pathology
Language Disorders - physiopathology
medial temporal lobes
Memory Disorders - pathology
Memory Disorders - physiopathology
Memory Disorders - psychology
Narcotics - adverse effects
Neural Pathways - pathology
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Title Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition
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https://onlinelibrary.wiley.com/doi/abs/10.1002%2Fhipo.10211
https://www.ncbi.nlm.nih.gov/pubmed/15318334
https://www.proquest.com/docview/66800393
Volume 14
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