Spatial memory deficits in patients with unilateral damage to the right hippocampal formation

Patients with unilateral temporal lobe damage resulting from intractable temporal lobe epilepsy (TLE, n = 30) or from temporal lobe resection (temporal lobectomy, TLR, n = 47) were investigated on the Nine-box Maze. The task, analogous to the radial arm maze, was designed to compare spatial mapping and working memory theories of the functions of the hippocampus. The task provides measures of spatial, object, working and reference memory, incorporated into a within subjects design. The spatial component was designed to encourage the formation of allocentric rather than egocentric spatial representations. Spatial memory deficits were found (across working and reference memory components) in both TLE and TLR patients with right temporal lobe damage, with intact spatial memory in patients with corresponding left temporal lobe damage. Performance on the matched non-spatial (object) working memory component was equal to healthy controls for all groups. However all patient groups showed a deficit on object reference memory. These findings are discussed in relation to the underlying temporal lobe pathology and particularly atrophy of the hippocampal formation. Overall, the results support the cognitive mapping theory of hippocampal function, with the demonstration of a selective (and probably allocentric) spatial memory deficit in patients with right hippocampal damage.

[1]  R. Morris,et al.  Place navigation impaired in rats with hippocampal lesions , 1982, Nature.

[2]  L. Goldstein Neuropsychological Investigation of Temporal Lobe Epilepsy , 1991, Journal of the Royal Society of Medicine.

[3]  J. O’Keefe,et al.  A computational theory of the hippocampal cognitive map. , 1990, Progress in brain research.

[4]  A. Canavan,et al.  Principal components of the WAIS–R , 1986 .

[5]  J. Engel Recent advances in surgical treatment of temporal lobe epilepsy , 1992, Acta neurologica Scandinavica. Supplementum.

[6]  G. Powell,et al.  The relationship between intelligence and verbal and spatial memory. , 1979, Journal of Clinical Psychology.

[7]  M. Mishkin,et al.  A selective mnemonic role for the hippocampus in monkeys: memory for the location of objects , 1988, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[8]  L. Goldstein,et al.  Short-term cognitive changes after unilateral temporal lobectomy or unilateral amygdalo-hippocampectomy for the relief of temporal lobe epilepsy. , 1993, Journal of neurology, neurosurgery, and psychiatry.

[9]  J. O’Keefe Place units in the hippocampus of the freely moving rat , 1976, Experimental Neurology.

[10]  H. Abikoff,et al.  Logical memory subtest of the Wechsler Memory Scale: age and education norms and alternate-form reliability of two scoring systems. , 1987, Journal of clinical and experimental neuropsychology.

[11]  D. Olton,et al.  Animal Behavior Processes , 2022 .

[12]  John O'Keefe,et al.  On the trail of the hippocampal engram , 1980 .

[13]  G. Leonard Temporal Lobe Surgery for Epilepsy: Neuropsychological Variables Related to Surgical Outcome , 1991, Canadian Journal of Neurological Sciences / Journal Canadien des Sciences Neurologiques.

[14]  J O'Keefe,et al.  An allocentric spatial model for the hippocampal cognitive map , 1991, Hippocampus.

[15]  T. Ono,et al.  The hippocampus and space: Are there “place neurons” in the monkey hippocampus? , 1991, Hippocampus.

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

[17]  C. B. Cave,et al.  Equivalent impairment of spatial and nonspatial memory following damage to the human hippocampus , 1991, Hippocampus.

[18]  Philip M. Corsi Human memory and the medial temporal region of the brain. , 1972 .

[19]  Brenda Milner,et al.  Visually-guided maze learning in man: effects of bilateral hippocampal, bilateral frontal, and unilateral cerebral lesions , 1965 .

[20]  A. Mayes,et al.  Disproportionate intentional spatial-memory impairments in amnesia , 1991, Neuropsychologia.

[21]  D. Olton,et al.  Hippocampal and amygdaloid involvement in working memory for nonspatial stimuli. , 1988, Behavioral neuroscience.

[22]  R. Saunders,et al.  Running Recognition of Configural Stimuli by Fornix-Transected Monkeys , 1985, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[23]  C. Polkey,et al.  The new Maudsley series of temporal lobectomy. I: Short-term cognitive effects. , 1985, The British journal of clinical psychology.

[24]  G A Press,et al.  Magnetic resonance imaging of the hippocampal formation and mammillary nuclei distinguish medial temporal lobe and diencephalic amnesia , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[25]  B. Milner,et al.  Right hippocampal impairment in the recall of spatial location: Encoding deficit or rapid forgetting? , 1989, Neuropsychologia.

[26]  L. Nadel The hippocampus and space revisited , 1991, Hippocampus.

[27]  B. Milner,et al.  Psychological aspects of focal epilepsy and its neurosurgical management. , 1975, Advances in neurology.

[28]  L. Jarrard On the neural bases of the spatial mapping system: Hippocampus vs. hippocampal formation , 1991, Hippocampus.

[29]  C. Polkey,et al.  Episodic memory dysfunction during sodium amytal testing of epileptic patients in relation to posterior cerebral artery perfusion. , 1996, Journal of clinical and experimental neuropsychology.

[30]  C. E. Polkey,et al.  Cognitive mapping after unilateral temporal lobectomy , 1989, Neuropsychologia.

[31]  David S. Olton,et al.  Hippocampal Function and Memory for Temporal Context , 1986 .

[32]  Suzanne Corkin,et al.  Tactually-guided maze learning in man: Effects of unilateral cortical excisions and bilateral hippocampal lesions ☆ , 1965 .

[33]  T. Mihara,et al.  MRI Lesion and Epileptogenic Focus in Temporal Lobe Epilepsy , 1989, The Japanese journal of psychiatry and neurology.

[34]  Brenda Milner,et al.  Memory for different aspects of complex visual scenes after unilateral temporal- or frontal-lobe resection , 1993, Neuropsychologia.

[35]  C. Elger,et al.  Visual Learning Deficits in Nonresected Patients with Right Temporal Lobe Epilepsy , 1991, Cortex.

[36]  B. Milner,et al.  Deficits on subject-ordered tasks after frontal- and temporal-lobe lesions in man , 1982, Neuropsychologia.

[37]  C R Jack,et al.  Temporal lobe seizures: lateralization with MR volume measurements of the hippocampal formation. , 1990, Radiology.

[38]  M. Petrides Deficits on conditional associative-learning tasks after frontal- and temporal-lobe lesions in man , 1985, Neuropsychologia.

[39]  D. Amaral,et al.  Hippocampal abnormalities in amnesic patients revealed by high-resolution magnetic resonance imaging , 1989, Nature.

[40]  D. Spencer,et al.  Specificity in the correlation of verbal memory and hippocampal neuron loss: dissociation of memory, language, and verbal intellectual ability. , 1992, Journal of clinical and experimental neuropsychology.

[41]  C. Barnes Spatial learning and memory processes: the search for their neurobiological mechanisms in the rat , 1988, Trends in Neurosciences.

[42]  P. Loiseau,et al.  Learning Impairment in Epileptic Patients , 1983, Epilepsia.

[43]  A. Mayes,et al.  Disproportionate incidental spatial-memory and recall deficits in amnesia , 1991, Neuropsychologia.

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

[45]  C R Jack,et al.  Magnetic resonance imaging–based volume studies in temporal lobe epilepsy: Pathological correlations , 1991, Annals of neurology.

[46]  M. Jones-Gotman,et al.  Localization of lesions by neuropsychological testing. , 1991, Epilepsia.

[47]  Gregory McCarthy,et al.  Quantitative magnetic resonance imaging in temporal lobe epilepsy: Relationship to neuropathology and neuropsychological function , 1992, Annals of neurology.

[48]  L. Nadel,et al.  The Hippocampus as a Cognitive Map , 1978 .

[49]  A. Paivio Imagery and verbal processes , 1972 .

[50]  E. Tulving Elements of episodic memory , 1983 .

[51]  M. Mishkin,et al.  Verbal memory impairment after right temporal lobe surgery , 1995, Neurology.

[52]  J H Kim,et al.  Imaging findings in hippocampal sclerosis: correlation with pathology. , 1991, AJNR. American journal of neuroradiology.

[53]  J. N. P. Rawlins,et al.  The effects of hippocampal lesions upon spatial and non-spatial tests of working memory , 1986, Behavioural Brain Research.

[54]  A. D. Pickering The hippocampus and space: are we flogging a dead (sea-)horse? , 1993, Hippocampus.

[55]  T. Sutula Experimental Models of Temporal Lobe Epilepsy: New Insights from the Study of Kindling and Synaptic Reorganization , 1990, Epilepsia.

[56]  L. Jarrard,et al.  Selective hippocampal lesions and behavior: effects of kainic acid lesions on performance of place and cue tasks. , 1983, Behavioral neuroscience.

[57]  G. Handelmann,et al.  Hippocampus, space, and memory , 1979 .

[58]  H. Eichenbaum,et al.  The hippocampus--what does it do? , 1992, Behavioral and neural biology.

[59]  L. Jarrard Selective Hippocampal Lesions and Behavior: Implications for Current Research and Theorizing , 1986 .

[60]  M Ashtari,et al.  Three-dimensional fast low-angle shot imaging and computerized volume measurement of the hippocampus in patients with chronic epilepsy of the temporal lobe. , 1991, AJNR. American journal of neuroradiology.

[61]  H Glowinski,et al.  COGNITIVE DEFICITS IN TEMPORAL LOBE EPILEPSY: An Investigation of Memory Functioning , 1973, The Journal of nervous and mental disease.

[62]  H. Okaichi,et al.  Choice behavior of hippocampectomized rats in the radial arm maze , 1990, Psychobiology.

[63]  H. Eichenbaum,et al.  Hippocampal system dysfunction and odor discrimination learning in rats: impairment or facilitation depending on representational demands. , 1988, Behavioral neuroscience.