Perspectives on object-recognition memory following hippocampal damage: lessons from studies in rats

One of the routine memory abilities impaired in amnesic patients with temporal-lobe damage is object-recognition memory--the ability to discriminate the familiarity of previously encountered objects. Reproducing this impairment has played a central role in animal models of amnesia during the past two decades, and until recent years most of the emphasis was on describing how hippocampal damage could impair object recognition. Today most investigators are looking outside the hippocampus to explain the impairment. This paper reviews studies of object-recognition memory in rats with hippocampal damage produced by ablation, fornix transection, or forebrain ischemia. Some new perspectives on previous findings reinforce the conclusion that damage to the hippocampus has little if any impact on the ability to recognize objects, while damage in some areas outside the hippocampus is far more effective. The few circumstances in which hippocampal damage can impair performance on object-recognition tasks are situations where ancillary abilities are likely to play a significant role in supporting task performance. Some of the factors that contributed to the origins and persistence of the hippocampalcentric view of object-recognition are considered, including lesion confounds, failure to distinguish between impaired task performance and impairment of a memory ability, and disproportionate attention to a few lesion studies in monkeys, even though the hypothesis was tested far more times in rats, under a greater variety of conditions, and rejected on nearly every occasion.

[1]  H. E. Rosvold,et al.  Delayed alternation in monkeys after removal of the hippocampus. , 1970, Neuropsychologia.

[2]  R. J. McDonald,et al.  Dorsal/ventral hippocampus, fornix, and conditioned place preference , 2001, Hippocampus.

[3]  Theo H. Hijzen,et al.  The object delayed non-matching to sample task in rats does not depend on working memory. , 1995, Neuroreport.

[4]  J. Delacour,et al.  A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data , 1988, Behavioural Brain Research.

[5]  H. Hodges,et al.  Cognitive deficits induced by global cerebral ischaemia: Relationship to brain damage and reversal by transplants , 1994, Behavioural Brain Research.

[6]  C. Trepel,et al.  Extrinsic modulation of theta field activity in the entorhinal cortex of the anesthetized rat , 1994, Hippocampus.

[7]  M Ingvar,et al.  Status epilepticus in well–oxygenated rats causes neuronal necrosis , 1985, Annals of neurology.

[8]  B. Meldrum,et al.  Systemic factors and epileptic brain damage. Prolonged seizures in paralyzed, artificially ventilated baboons. , 1973, Archives of neurology.

[9]  Lawrence A. Rothblat,et al.  Short-term object recognition memory in the rat: nonmatching with trial-unique junk stimuli. , 1987 .

[10]  Neuroanatomical Substrates RECOGNITION MEMORY IN RATS—II. , 1998 .

[11]  M. Mishkin Memory in monkeys severely impaired by combined but not by separate removal of amygdala and hippocampus , 1978, Nature.

[12]  J. Aggleton,et al.  Spontaneous object recognition and object location memory in rats: the effects of lesions in the cingulate cortices, the medial prefrontal cortex, the cingulum bundle and the fornix , 1997, Experimental Brain Research.

[13]  M. Meunier,et al.  Cerebral ischemia: Are the memory deficits associated with hippocampal cell loss? , 1996, Hippocampus.

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

[15]  J. Aggleton,et al.  The effects of fornix and medial prefrontal lesions on delayed non-matching-to-sample by rats , 1993, Behavioural Brain Research.

[16]  J. Rawlins,et al.  A comparison between the effects of medial septal lesions and entorhinal cortex lesions on performance of nonspatial working memory tasks and reversal learning , 1998, Behavioural Brain Research.

[17]  Neal J. Cohen,et al.  Erratum: The hippocampal memory system and its functional components: Further explication and clarification (Behavioral and Brain Sciences (1994) 17:3 (500)) , 1996 .

[18]  D. Mumby,et al.  Memory deficits following lesions of hippocampus or amygdala in rat: Assessment by an object-memory test battery , 1995, Psychobiology.

[19]  L. Squire,et al.  Remembering the hippocampus , 1999, Behavioral and Brain Sciences.

[20]  R. Clark,et al.  Rats with lesions of the hippocampus are impaired on the delayed nonmatching‐to‐sample task † , 2001, Hippocampus.

[21]  G. Raisman,et al.  Sexual dimorphism in the neuropil of the preoptic area of the rat and its dependence on neonatal androgen. , 1973, Brain research.

[22]  Rolf Sattler,et al.  Concepts and Classification , 1986 .

[23]  M. Mishkin,et al.  Severe tactual as well as visual memory deficits follow combined removal of the amygdala and hippocampus in monkeys , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[24]  D. Olton,et al.  Neurobiology of Comparative Cognition , 1990 .

[25]  Robert E. Clark,et al.  Impaired Recognition Memory in Rats after Damage to the Hippocampus , 2000, The Journal of Neuroscience.

[26]  D. Gaffan,et al.  Effects of Fornix Transection on Spontaneous and Trained Non-Matching by Monkeys , 1984, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[27]  L. Rothblat,et al.  Short-term object recognition memory in the rat: nonmatching with trial-unique junk stimuli. , 1987, Behavioral neuroscience.

[28]  H. Eichenbaum,et al.  Two functional components of the hippocampal memory system , 1994, Behavioral and Brain Sciences.

[29]  D. Drachman,et al.  Memory and the hippocampal complex. II. Is memory a multiple process , 1966 .

[30]  J. Bachevalier,et al.  Ontogenetic Development of Habit and Memory Formation in Primates , 1990, Annals of the New York Academy of Sciences.

[31]  R. M. Nicol,et al.  The performance of amnesic subjects on tests of experimental amnesia in animals: delayed matching-to-sample and concurrent learning , 1988, Neuropsychologia.

[32]  J. Aggleton,et al.  Neurotoxic lesions of the perirhinal cortex do not mimic the behavioural effects of fornix transection in the rat , 1996, Behavioural Brain Research.

[33]  K. Pribram,et al.  Effects of lesions of the medial forebrain on alternation behavior of rhesus monkeys. , 1962, Experimental neurology.

[34]  B. Weinstein Matching-from-sample by rhesus monkeys and by children. , 1941 .

[35]  S. Zola-Morgan,et al.  Hippocampal resections impair associative learning and recognition memory in the monkey , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[36]  D. Mumby,et al.  Rhinal cortex lesions and object recognition in rats. , 1994, Behavioral neuroscience.

[37]  J. A. Horel,et al.  Lesions of the anterior temporal stem and the performance of delayed match-to-sample and visual discriminations in monkeys , 1989, Behavioural Brain Research.

[38]  A K OMMAYA,et al.  MEMORY AND THE HIPPOCAMPAL COMPLEX. , 1964, Archives of neurology.

[39]  D. Mumby,et al.  Dissociation in retrograde memory for object discriminations and object recognition in rats with perirhinal cortex damage , 2002, Behavioural Brain Research.

[40]  J. N. Rawlins,et al.  The hippocampus, objects, and their contexts. , 1997, Behavioral neuroscience.

[41]  D. Amaral,et al.  Lesions of perirhinal and parahippocampal cortex that spare the amygdala and hippocampal formation produce severe memory impairment , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[42]  M. Mishkin,et al.  Object Recognition and Location Memory in Monkeys with Excitotoxic Lesions of the Amygdala and Hippocampus , 1998, The Journal of Neuroscience.

[43]  D. Kimble The effects of bilateral hippocampal lesions in rats. , 1963, Journal of comparative and physiological psychology.

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

[45]  D. Bilkey,et al.  Lesions of rat perirhinal cortex exacerbate the memory deficit observed following damage to the fimbria-fornix. , 1995, Behavioral neuroscience.

[46]  J. Ringo Seemingly discrepant data from hippocampectomized macaques are reconciled by detectability analysis. , 1988, Behavioral neuroscience.

[47]  M Mishkin,et al.  An analysis of short-term visual memory in the monkey. , 1975, Journal of experimental psychology. Animal behavior processes.

[48]  J. Fagan Memory in the infant. , 1970, Journal of experimental child psychology.

[49]  L. W. Schmaltz,et al.  The effects of preliminary training conditions upon DRL performance in the hippocampectomized rat , 1966 .

[50]  B. Volpe,et al.  Further characterization of patients with amnesia after cardiac arrest , 1986, Neurology.

[51]  Leslie G. Ungerleider Two cortical visual systems , 1982 .

[52]  J. A. Horel The neuroanatomy of amnesia. A critique of the hippocampal memory hypothesis. , 1978, Brain : a journal of neurology.

[53]  A. Phillips,et al.  Ischemia-induced object-recognition deficits in rats are attenuated by hippocampal ablation before or soon after ischemia. , 1996, Behavioral neuroscience.

[54]  J. Aggleton,et al.  Effects of amygdaloid and amygdaloid-hippocampal lesions on object recognition and spatial working memory in rats. , 1989, Behavioral neuroscience.

[55]  D. Mumby Assessing working memory for objects in rats: no one said it was easy. , 1995, Neuroreport.

[56]  R. Deacon,et al.  Critical determinants of nonspatial working memory deficits in rats with conventional lesions of the hippocampus or fornix. , 1993, Behavioral neuroscience.

[57]  A. Santucci,et al.  Concurrent object-discrimination learning in rats , 1990 .

[58]  M. Mishkin,et al.  Effects on visual recognition of combined and separate ablations of the entorhinal and perirhinal cortex in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[59]  M. Mishkin,et al.  Differential effects of early hippocampal pathology on episodic and semantic memory. , 1997, Science.

[60]  J. Orbach,et al.  Learning and retention in monkeys after amygdala-hippocampus resection. , 1960, Archives of neurology.

[61]  J. Aggleton,et al.  Amnesia and recognition memory: A re-analysis of psychometric data , 1996, Neuropsychologia.

[62]  L. Squire,et al.  Enduring memory impairment in monkeys after ischemic damage to the hippocampus , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[63]  J. Rawlins,et al.  The effects of hippocampectomy on performance by rats of a running recognition task using long lists of non-spatial items , 1993, Behavioural Brain Research.

[64]  E. Wood,et al.  Object-recognition memory is only mildly impaired in rats with lesions of the hippocampus and amygdala , 1992, Psychobiology.

[65]  L. Squire,et al.  Human amnesia and animal models of amnesia: performance of amnesic patients on tests designed for the monkey. , 1988, Behavioral neuroscience.

[66]  D. Gaffan,et al.  Recognition impaired and association intact in the memory of monkeys after transection of the fornix. , 1974, Journal of comparative and physiological psychology.

[67]  R. Douglas,et al.  The effect of radical hippocampal ablation on acquisition of avoidance response. , 1961 .

[68]  Seth J. Ramus,et al.  Severity of memory impairment in monkeys as a function of locus and extent of damage within the medial temporal lobe memory system , 1994, Hippocampus.

[69]  L. Squire,et al.  Ischemic brain damage and memory impairment: A commentary , 1996, Hippocampus.

[70]  L. Squire,et al.  Lesions of the amygdala that spare adjacent cortical regions do not impair memory or exacerbate the impairment following lesions of the hippocampal formation , 1989, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[71]  A. Cowey,et al.  Effects of dorsal and ventral hippocampal lesions on spontaneous alternation, learned alternation and probability learning in rats. , 1973, Brain research.

[72]  S. Floresco,et al.  Reversible lesions of the rhinal cortex produce delayed non‐matching‐to‐sample deficits in rats , 2000, Neuroreport.

[73]  M. Mishkin,et al.  Mnemonic and neuropathological effects of occluding the posterior cerebral artery in Macaca mulatta , 1989, Neuropsychologia.

[74]  A Gol,et al.  Effects of human hippocampal ablation. , 1967, Journal of neurosurgery.

[75]  A. Chiba,et al.  Continuous recognition of spatial and nonspatial stimuli in hippocampal-lesioned rats. , 1993, Behavioral and neural biology.

[76]  E. Wood,et al.  The role of experimenter-odor cues in the performance of object-memory tasks by rats , 1995 .

[77]  E. Murray,et al.  Aspiration lesions of the amygdala disrupt the rhinal corticothalamic projection system in rhesus monkeys , 1998, Experimental Brain Research.

[78]  M. Mishkin,et al.  The neuroanatomy of amnesia: amygdala-hippocampus versus temporal stem. , 1982, Science.

[79]  L. Squire,et al.  Korsakoff's syndrome: a study of the relation between anterograde amnesia and remote memory impairment. , 1986, Behavioral neuroscience.

[80]  M. Victor,et al.  [Memory loss with lesions of hippocampal formation. Report of a case with some remarks on the anatomical basis of memory]. , 1961, Archives of neurology.

[81]  W. Bechterew Demonstration eines Gehirns mit Zerstorung der vorderen und inneren Teile der Hirnrinde beider Schlafenlappen , 1996 .

[82]  J. Aggleton,et al.  One-Trial Object Recognition by Rats , 1985 .

[83]  J. Aggleton,et al.  RECOGNITION MEMORY IN RATS—I.CONCEPTS AND CLASSIFICATION , 1998, Progress in Neurobiology.

[84]  D S Olton,et al.  Hippocampus, fimbria-fornix, amygdala, and memory: object discriminations in rats. , 1992, Behavioral neuroscience.

[85]  B. Kaada,et al.  Effects of hippocampal lesions on maze learning and retention in rats. , 1961, Experimental neurology.

[86]  J. A. Horel,et al.  The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold , 1987, Behavioural Brain Research.

[87]  P Alvarez,et al.  Damage limited to the hippocampal region produces long-lasting memory impairment in monkeys , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  R. Racine,et al.  Hippocampal lesions and delayed alternation in the rat , 1965 .

[89]  W P Dunlap,et al.  Loss of hippocampal CA1 pyramidal neurons correlates with memory impairment in rats with ischemic or neurotoxin lesions. , 1992, Behavioral neuroscience.

[90]  H. Cassaday,et al.  Fornix-fimbria section and working memory deficits in rats: stimulus complexity and stimulus size. , 1995, Behavioral neuroscience.

[91]  W. Scoville,et al.  LOSS OF RECENT MEMORY AFTER BILATERAL HIPPOCAMPAL LESIONS , 1957, Journal of neurology, neurosurgery, and psychiatry.

[92]  J. A. Horel,et al.  THE NEUROANATOMY OF AMNESIA , 1978 .

[93]  M. Victor Memory loss with lesions of hippocampal formation , 1996 .

[94]  J. Aggleton,et al.  The performance of amnesic subjects on tests of delayed matching-to-sample and delayed matching-to-position , 1995, Neuropsychologia.

[95]  Dale Corbett,et al.  The problem of assessing effective neuroprotection in experimental cerebral ischemia , 1998, Progress in Neurobiology.

[96]  E. Murray,et al.  Opposite relationship of hippocampal and rhinal cortex damage to delayed nonmatching‐to‐sample deficits in monkeys † , 2001, Hippocampus.

[97]  K. Pribram,et al.  Visual discrimination performance following partial ablations of the temporal lobe. I. Ventral vs. lateral. , 1954, Journal of comparative and physiological psychology.

[98]  L. Squire,et al.  Medial temporal lesions in monkeys impair memory on a variety of tasks sensitive to human amnesia. , 1985, Behavioral neuroscience.

[99]  M. Mishkin Visual discrimination performance following partial ablations of the temporal lobe. II. Ventral surface vs. hippocampus. , 1954, Journal of comparative and physiological psychology.

[100]  D. Drachman,et al.  Memory and the hippocampal complex. II. Is memory a multiple process? , 1996, Archives of neurology.

[101]  L. Squire,et al.  Memory impairment in monkeys following lesions limited to the hippocampus. , 1986, Behavioral neuroscience.

[102]  P. Glees,et al.  Bilateral destruction of the hippocampus (cornu ammonis) in a case of dementia. , 1952, Monatsschrift fur Psychiatrie und Neurologie.

[103]  Patricia S. Goldman TOPOGRAPHY OF COGNITION: Parallel Distributed Networks in Primate Association Cortex , 1988 .

[104]  L. Squire,et al.  Human amnesia and the medial temporal region: enduring memory impairment following a bilateral lesion limited to field CA1 of the hippocampus , 1986, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[105]  Gordon Winocur,et al.  Transfer between related and unrelated problems following hippocampal lesions in rats. , 1970 .

[106]  O. Ottersen,et al.  The role of epileptic activity in hippocampal and ‘remote’ cerebral lesions induced by kainic acid , 1980, Brain Research.

[107]  D. Knopman,et al.  Prolonged focal epilepsy and hypoxemia as a cause of focal brain damage: A case study , 1977, Annals of neurology.

[108]  J. Aggleton,et al.  The effects of neurotoxic lesions of the perirhinal cortex combined to fornix transection on object recognition memory in the rat , 1997, Behavioural Brain Research.

[109]  R. J. McDonald,et al.  Dissociation of the medial prefrontal, posterior parietal, and posterior temporal cortex for spatial navigation and recognition memory in the rat. , 1994, Cerebral cortex.

[110]  W. Scoville,et al.  Performance on delayed match following lesions of medial temporal lobe structures. , 1965, Journal of comparative and physiological psychology.

[111]  D. Mumby,et al.  Mediodorsal thalamic lesions and object recognition in rats , 1993, Psychobiology.

[112]  J. Aggleton,et al.  The effects of mammillary body and combined amygdalar-fornix lesions on tests of delayed non-matching-to-sample in the rat , 1990, Behavioural Brain Research.

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

[114]  John P Aggleton,et al.  Differential deficits in the Morris water maze following cytotoxic lesions of the anterior thalamus and fornix transection , 1998, Behavioural Brain Research.

[115]  J. Rawlins,et al.  The effects of hippocampal formation ablation or fimbria-fornix section on performance of a nonspatial radial arm maze task by rats , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[116]  M. Mishkin,et al.  Further evidence that amygdala and hippocampus contribute equally to recognition memory , 1984, Neuropsychologia.

[117]  L. F. Kromer,et al.  Object recognition memory in the rat: the role of the hippocampus , 1991, Behavioural Brain Research.

[118]  J. Aggleton,et al.  Recognition memory in rats—II. Neuroanatomical substrates , 1998, Progress in Neurobiology.

[119]  R. Clark,et al.  Impaired Recognition Memory in Monkeys after Damage Limited to the Hippocampal Region , 2000, The Journal of Neuroscience.

[120]  J. Aggleton,et al.  The Performance of Postencephalitic Amnesic Subjects on Two Behavioural Tests of Memory: Concurrent Discrimination Learning and Delayed Matching-To-Sample , 1992, Cortex.

[121]  R. Killiany,et al.  Hippocampal formation lesions produce memory impairment in the rhesus monkey , 1999, Hippocampus.

[122]  T. Alexinsky,et al.  A new behavioral model for studying delayed response in rats , 1978 .

[123]  A. Phillips,et al.  Impaired object recognition memory in rats following ischemia-induced damage to the hippocampus. , 1993, Behavioral neuroscience.

[124]  P. Jackson-smith,et al.  Hippocampal lesions impair rats’ performance of a nonspatial matching-to-sample task , 1990, Psychobiology.

[125]  S. Floresco,et al.  Disruption of spatial but not object-recognition memory by neurotoxic lesions of the dorsal hippocampus in rats. , 1997, Behavioral neuroscience.