Fractionation of memory in medial temporal lobe amnesia

We report a comprehensive investigation of the anterograde memory functions of two patients with memory impairments (RH and JC). RH had neuroradiological evidence of apparently selective right-sided hippocampal damage and an intact cognitive profile apart from selective memory impairments. JC, had neuroradiological evidence of bilateral hippocampal damage following anoxia due to cardiac arrest. He had anomic and "executive" difficulties in addition to a global amnesia, suggesting atrophy extending beyond hippocampal regions. Their performance is compared with that of a previously reported hippocampal amnesic patient who showed preserved recollection and familiarity for faces in the context of severe verbal and topographical memory impairment [VC; Cipolotti, L., Bird, C., Good, T., Macmanus, D., Rudge, P., & Shallice, T. (2006). Recollection and familiarity in dense hippocampal amnesia: A case study. Neuropsychologia, 44, 489-506.] The patients were administered experimental tests using verbal (words) and two types of non-verbal materials (faces and buildings). Receiver operating characteristic analyses were used to estimate the contribution of recollection and familiarity to recognition performance on the experimental tests. RH had preserved verbal recognition memory. Interestingly, her face recognition memory was also spared, whilst topographical recognition memory was impaired. JC was impaired for all types of verbal and non-verbal materials. In both patients, deficits in recollection were invariably associated with deficits in familiarity. JC's data demonstrate the need for a comprehensive cognitive investigation in patients with apparently selective hippocampal damage following anoxia. The data from RH suggest that the right hippocampus is necessary for recollection and familiarity for topographical materials, whilst the left hippocampus is sufficient to underpin these processes for at least some types of verbal materials. Face recognition memory may be adequately subserved by areas outside of the hippocampus.

[1]  L. Squire,et al.  Recall, recognition, and the hippocampus: Reply to Yonelinas et al. (2004) , 2004 .

[2]  J. Hodges,et al.  Is semantic memory consistently impaired early in the course of Alzheimer's disease? Neuroanatomical and diagnostic implications , 1995, Neuropsychologia.

[3]  R. O’Reilly,et al.  Under what conditions is recognition spared relative to recall after selective hippocampal damage in humans? , 2002, Hippocampus.

[4]  Russell A. Epstein,et al.  Perceptual deficits in amnesia: challenging the medial temporal lobe ‘mnemonic’ view , 2005, Neuropsychologia.

[5]  E. Maguire,et al.  A combined neuropsychological and neuroimaging study of topographical and non-verbal memory in semantic dementia , 2003, Neuropsychologia.

[6]  M. Farah,et al.  PROSOPAMNESIA: A SELECTIVE IMPAIRMENT IN FACE LEARNING , 2000, Cognitive neuropsychology.

[7]  Nick C. Fox,et al.  Differentiating AD from aging using semiautomated measurement of hippocampal atrophy rates , 2004, NeuroImage.

[8]  Neal J. Cohen,et al.  The Long and the Short of It: Relational Memory Impairments in Amnesia, Even at Short Lags , 2006, The Journal of Neuroscience.

[9]  Andy C. H. Lee,et al.  Specialization in the medial temporal lobe for processing of objects and scenes , 2005, Hippocampus.

[10]  E. Maguire,et al.  The Human Hippocampus and Spatial and Episodic Memory , 2002, Neuron.

[11]  T. Shallice,et al.  Long-term retrograde amnesia… the crucial role of the hippocampus , 2001, Neuropsychologia.

[12]  M. W. Brown,et al.  Episodic memory, amnesia, and the hippocampal–anterior thalamic axis , 1999, Behavioral and Brain Sciences.

[13]  N. Hunkin,et al.  Relative sparing of item recognition memory in a patient with adult‐onset damage limited to the hippocampus , 2002, Hippocampus.

[14]  M. Verfaellie,et al.  Acquisition of novel semantic information in amnesia: effects of lesion location , 2000, Neuropsychologia.

[15]  N Burgess,et al.  Bilateral hippocampal pathology impairs topographical and episodic memory but not visual pattern matching , 2001, Hippocampus.

[16]  R T Knight,et al.  Recollection and familiarity deficits in amnesia: convergence of remember-know, process dissociation, and receiver operating characteristic data. , 1998, Neuropsychology.

[17]  G. Fink,et al.  Impaired episodic memory retrieval in a case of probable psychogenic amnesia , 1997, Psychiatry Research: Neuroimaging.

[18]  C. Caltagirone,et al.  Selective sparing of face learning in a global amnesic patient , 2001, Journal of neurology, neurosurgery, and psychiatry.

[19]  Eleanor A Maguire,et al.  Selective sparing of topographical memory , 1998, Journal of neurology, neurosurgery, and psychiatry.

[20]  D Tsivilis,et al.  Associative recognition in a patient with selective hippocampal lesions and relatively normal item recognition , 2004, Hippocampus.

[21]  L R Squire,et al.  Impaired recognition memory in patients with lesions limited to the hippocampal formation. , 1997, Behavioral neuroscience.

[22]  P. Garthwaite,et al.  Investigation of the single case in neuropsychology: confidence limits on the abnormality of test scores and test score differences , 2002, Neuropsychologia.

[23]  Tim Shallice,et al.  The Involvement of the Frontal Lobes in Cognitive Estimation , 1978, Cortex.

[24]  E. Renzi,et al.  Spatial Memory and Hemispheric Locus of Lesion , 1977, Cortex.

[25]  G. Mandler.  Recognizing: The judgment of previous occurrence. , 1980 .

[26]  J. Stevens,et al.  Bilateral lesions of CA1 and CA2 fields of the hippocampus are sufficient to cause a severe amnesic syndrome in humans. , 1995, Journal of neurology, neurosurgery, and psychiatry.

[27]  M. Rugg,et al.  Human recognition memory: a cognitive neuroscience perspective , 2003, Trends in Cognitive Sciences.

[28]  C. Polkey,et al.  Differential spatial memory impairment after right temporal lobectomy demonstrated using temporal titration. , 1999, Brain : a journal of neurology.

[29]  N. Roberts,et al.  Item recognition is less impaired than recall and associative recognition in a patient with selective hippocampal damage , 2005, Hippocampus.

[30]  A Wingfield,et al.  Response Latencies in Naming Objects , 1965, The Quarterly journal of experimental psychology.

[31]  E K Warrington,et al.  Testing for nominal dysphasia. , 1980, Journal of neurology, neurosurgery, and psychiatry.

[32]  Eleanor A. Maguire,et al.  Distinct Neural Systems for the Encoding and Recognition of Topography and Faces , 2001, NeuroImage.

[33]  W. Sturm,et al.  Neuropsychological assessment , 2007, Journal of Neurology.

[34]  E A Maguire,et al.  Hippocampal Amnesia , 2001, Neurocase.

[35]  M. Chun,et al.  Memory deficits for implicit contextual information in amnesic subjects with hippocampal damage , 1999, Nature Neuroscience.

[36]  M. Linden,et al.  Dissociation Between Recall and Recognition Memory Performance in an Amnesic Patient with Hippocampal Damage Following Carbon Monoxide Poisoning , 2004, Neurocase.

[37]  H. Nelson.  A Modified Card Sorting Test Sensitive to Frontal Lobe Defects , 1976, Cortex.

[38]  N C Andreasen,et al.  Direct comparison of the neural substrates of recognition memory for words and faces. , 1999, Brain : a journal of neurology.

[39]  M. Lezak.  Neuropsychological assessment, 3rd ed. , 1995 .

[40]  E. Maguire,et al.  The Well-Worn Route and the Path Less Traveled Distinct Neural Bases of Route Following and Wayfinding in Humans , 2003, Neuron.

[41]  Peter E. Wais,et al.  The Hippocampus Supports both the Recollection and the Familiarity Components of Recognition Memory , 2006, Neuron.

[42]  Robert T. Knight,et al.  Effects of extensive temporal lobe damage or mild hypoxia on recollection and familiarity , 2002, Nature Neuroscience.

[43]  Lisa Cipolotti,et al.  Amnesia and the hippocampus , 2006, Current opinion in neurology.

[44]  U. Frith,et al.  Fractionation of visual memory: Evidence from a case with multiple neurodevelopmental impairments , 1999, Neuropsychologia.

[45]  Nick C Fox,et al.  Interactive algorithms for the segmentation and quantitation of 3-D MRI brain scans. , 1997, Computer methods and programs in biomedicine.

[46]  Eleanor A. Maguire,et al.  The effect of adult-acquired hippocampal damage on memory retrieval: An fMRI study , 2005, NeuroImage.

[47]  L Cipolotti,et al.  Fractionation of visual memory: agency detection and its impairment in autism , 2002, Neuropsychologia.

[48]  H. Eichenbaum,et al.  From Conditioning to Conscious Recollection , 2001 .

[49]  L. Rapport,et al.  Validation of the Warrington theory of visual processing and the Visual Object and Space Perception Battery. , 1998, Journal of clinical and experimental neuropsychology.

[50]  E K Warrington,et al.  Cognitive retardation in a patient with preservation of psychomotor speed. , 1992, Behavioural neurology.

[51]  Elizabeth K. Warrington Pat McKenna Lisa Orpwood.  Single Word Comprehension: A Concrete and Abstract Word Synonym Test , 1998 .

[52]  E. Weigl,et al.  On the psychology of so-called processes of abstraction. , 1941 .

[53]  André A Fenton,et al.  Object–location memory impairment in patients with thermal lesions to the right or left hippocampus , 2004, Neuropsychologia.

[54]  R. Clark,et al.  The medial temporal lobe. , 2004, Annual review of neuroscience.

[55]  Andrew P. Yonelinas,et al.  Sparing of the familiarity component of recognition memory in a patient with hippocampal pathology , 2005, Neuropsychologia.

[56]  N. Burgess,et al.  The hippocampus is required for short‐term topographical memory in humans , 2007, Hippocampus.

[57]  B. Milner,et al.  The role of the left hippocampal region in the acquisition and retention of story content , 1990, Neuropsychologia.

[58]  J. Hodges,et al.  Non-verbal semantic impairment in semantic dementia , 2000, Neuropsychologia.

[59]  Brenda Milner,et al.  The role of the right hippocampus in the recall of spatial location , 1981, Neuropsychologia.

[60]  Joseph R. Manns,et al.  Recognition Memory and the Human Hippocampus , 2003, Neuron.

[61]  D. Wade,et al.  The Adult Memory and Information Processing Battery (AMIPB) test of information-processing speed: a study of its reliability and feasibility in patients with multiple sclerosis , 2003, Clinical rehabilitation.

[62]  D G Gadian,et al.  Hierarchical organization of cognitive memory. , 1997, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.

[63]  Tim Shallice,et al.  The Hayling and Brixton Tests , 1997 .

[64]  Sven Joubert,et al.  Preserved visual recognition memory in an amnesic patient with hippocampal lesions , 2005, Hippocampus.

[65]  E K Warrington,et al.  Selective impairment of topographical memory: a single case study. , 1978, Journal of neurology, neurosurgery, and psychiatry.

[66]  L. Kartsounis,et al.  Retrograde amnesia: clinical and methodological caveats , 1998, Neuropsychologia.

[67]  Tim Shallice,et al.  Recollection and familiarity in dense hippocampal amnesia: A case study , 2006, Neuropsychologia.

[68]  E. Balint.  Memory and consciousness. , 1987, The International journal of psycho-analysis.

[69]  R. Sutherland,et al.  Configural association theory and the hippocampal formation: An appraisal and reconfiguration , 1995, Hippocampus.

[70]  P. Osterrieth.  Le test de copie d'une figure complexe , 1944 .

[71]  Klaus P. Ebmeier,et al.  Memory impairment in out-of-hospital cardiac arrest survivors is associated with global reduction in brain volume, not focal hippocampal injury. , 2000, Stroke.

[72]  D. Amaral,et al.  Three Cases of Enduring Memory Impairment after Bilateral Damage Limited to the Hippocampal Formation , 1996, The Journal of Neuroscience.

[73]  Brenda Milner,et al.  Right temporal-lobe contribution to image-mediated verbal learning , 1978, Neuropsychologia.

[74]  E. Warrington,et al.  Topographical Disorientation: Selective Impairment of Locomotor Space? , 1996, Cortex.

[75]  Andy C. H. Lee,et al.  Differentiating the Roles of the Hippocampus and Perirhinal Cortex in Processes beyond Long-Term Declarative Memory: A Double Dissociation in Dementia , 2006, The Journal of Neuroscience.

[76]  B. Milner,et al.  Interhemispheric differences in the localization of psychological processes in man. , 1971, British medical bulletin.