What is a memory system? Horel's critique revisited

J.A. Horel's critique of what he termed "the hippocampal memory hypothesis" turns out, 23 years later, to have been remarkably discerning and prophetic. There is now an overwhelming weight of evidence to confirm his four key proposals: that selective destruction of the hippocampus or fornix does not produce dense global amnesia; that the effects of hippocampal or fornix lesions are not primarily a memory impairment, but an impairment in processing spatial information; that damage to the anterior temporal stem is part of the explanation of dense temporal lobe amnesia; and that the interaction of temporal cortex with prefrontal cortex is essential in memory. This review summarizes the modern evidence that reinforces each of these four proposals. A final section argues that, not only in the case of the hippocampus but also in the case of other temporal and frontal cortical areas that are involved in normal memory, the concept of a "memory system" is harmful.

[1]  E. Murray,et al.  Monkeys with rhinal cortex damage or neurotoxic hippocampal lesions are impaired on spatial scene learning and object reversals. , 1998, Behavioral neuroscience.

[2]  Amanda Parker,et al.  Mamillary Body Lesions in Monkeys Impair Object-in-Place Memory: Functional Unity of the Fornix-Mamillary System , 1997, Journal of Cognitive Neuroscience.

[3]  D. Gaffan,et al.  Comparison of perirhinal cortex ablation and crossed unilateral lesions of the medial forebrain bundle from the inferior temporal cortex in the rhesus monkey: effects on learning and retrieval. , 2000, Behavioral neuroscience.

[4]  M. Delong,et al.  Fiber pathways of basal forebrain cholinergic neurons in monkeys , 1987, Brain Research.

[5]  D. Gaffan,et al.  The Recognition Memory Deficit Caused by Mediodorsal Thalamic Lesion in Non‐human Primates: A Comparison with Rhinal Cortex Lesion , 1997, The European journal of neuroscience.

[6]  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.

[7]  Moshe Naveh-Benjamin,et al.  Effects of Divided Attention on Encoding and Retrieval Processes in Human Memory: Further Support for an Asymmetry , 1998 .

[8]  Amanda Parker,et al.  Crossed unilateral lesions of medial forebrain bundle and either inferior temporal or frontal cortex impair object recognition memory in Rhesus monkeys , 2001, Behavioural Brain Research.

[9]  David Gaffan,et al.  Idiothetic input into object-place configuration as the contribution to memory of the monkey and human hippocampus: a review , 1998, Experimental Brain Research.

[10]  S. Gutnikov,et al.  Temporo‐frontal Disconnection Impairs Visual‐visual Paired Association Learning but not Configural Learning in Macaca Monkeys , 1997, The European journal of neuroscience.

[11]  K. Davis,et al.  Neurochemical Correlates of Dementia Severity in Alzheimer's Disease: Relative Importance of the Cholinergic Deficits , 1995, Journal of neurochemistry.

[12]  M. Mishkin,et al.  Hippocampectomized monkeys can remember one place but not two , 1993, Neuropsychologia.

[13]  D. Gaffan,et al.  Mediodorsal thalamic function in scene memory in rhesus monkeys. , 2000, Brain : a journal of neurology.

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

[15]  D. Gaffan,et al.  Amnesia in man following transection of the fornix. A review. , 1991, Brain : a journal of neurology.

[16]  D. Gaffan,et al.  Monkey hippocampus and learning about spatially directed movements , 1987, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[17]  D. Gaffan,et al.  A comparison of the effects of fornix transection and sulcus principalis ablation upon spatial learning by monkeys , 1989, Behavioural Brain Research.

[18]  D. Gaffan,et al.  Unilateral lesions of the cholinergic basal forebrain and fornix in one hemisphere and inferior temporal cortex in the opposite hemisphere produce severe learning impairments in rhesus monkeys. , 2002, Cerebral cortex.

[19]  D. Gaffan,et al.  Amnesia for Complex Naturalistic Scenes and for Objects Following Fornix Transection in the Rhesus Monkey , 1992, The European journal of neuroscience.

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

[21]  J. Aggleton,et al.  Differential cognitive effects of colloid cysts in the third ventricle that spare or compromise the fornix. , 2000, Brain : a journal of neurology.

[22]  D. Gaffan,et al.  Reversal Learning by Fornix-Transected Monkeys , 1984, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[23]  J R Hodges,et al.  Anterograde amnesia with fornix damage following removal of IIIrd ventricle colloid cyst. , 1991, Journal of neurology, neurosurgery, and psychiatry.

[24]  Amanda Parker,et al.  The effect of anterior thalamic and cingulate cortex lesions on object-in-place memory in monkeys , 1997, Neuropsychologia.

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

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

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

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

[29]  D. Gaffan,et al.  Interaction of frontal and perirhinal cortices in visual object recognition memory in monkeys , 1998, The European journal of neuroscience.

[30]  D. Gaffan Scene-Specific Memory for Objects: A Model of Episodic Memory Impairment in Monkeys with Fornix Transection , 1994, Journal of Cognitive Neuroscience.

[31]  M. Mesulam,et al.  Trajectories of cholinergic pathways within the cerebral hemispheres of the human brain. , 1998, Brain : a journal of neurology.

[32]  Harry F. Baker,et al.  Visual discrimination learning impairments produced by combined transections of the anterior temporal stem, amygdala and fornix in marmoset monkeys , 2001, Brain Research.

[33]  John Patrick Aggleton,et al.  The Amygdala : a functional analysis , 2000 .

[34]  D. Gaffan,et al.  Dense amnesia in the monkey after transection of fornix, amygdala and anterior temporal stem , 2001, Neuropsychologia.

[35]  M Mishkin,et al.  Neural substrates of visual stimulus-stimulus association in rhesus monkeys , 1993, The Journal of neuroscience : the official journal of the Society for Neuroscience.

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

[37]  D. Gaffan,et al.  Delayed Matching by Fornix-Transected Monkeys: The Sample, the Push and the Bait , 1984, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[38]  M. J. Eacott,et al.  Inferotemporal‐frontal Disconnection: The Uncinate Fascicle and Visual Associative Learning in Monkeys , 1992, The European journal of neuroscience.

[39]  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.

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

[41]  D. Gaffan,et al.  Amnesia following damage to the left fornix and to other sites. A comparative study. , 1991, Brain : a journal of neurology.

[42]  M M Mesulam,et al.  Cholinergic Pathways and the Ascending Reticular Activating System of the Human Brain a , 1995, Annals of the New York Academy of Sciences.

[43]  J. Fisher,et al.  Neuropsychological Assessment, 2nd Ed , 1985 .

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

[45]  J. T. Erichsen,et al.  Using Fos Imaging in the Rat to Reveal the Anatomical Extent of the Disruptive Effects of Fornix Lesions , 2000, The Journal of Neuroscience.

[46]  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.

[47]  B T Hyman,et al.  H. M.’s Medial Temporal Lobe Lesion: Findings from Magnetic Resonance Imaging , 1997, The Journal of Neuroscience.

[48]  R. Saunders,et al.  Effects of Fornix Transection upon Associative Memory in Monkeys: Role of the Hippocampus in Learned Action , 1984, The Quarterly journal of experimental psychology. B, Comparative and physiological psychology.

[49]  E. Miller,et al.  Task-specific neural activity in the primate prefrontal cortex. , 2000, Journal of neurophysiology.

[50]  D. Gaffan,et al.  Crossed unilateral lesions of the medial forebrain bundle and either inferior temporal or frontal cortex impair object–reward association learning in Rhesus monkeys , 2001, Neuropsychologia.

[51]  Amanda Parker,et al.  Memory after frontal/temporal disconnection in monkeys: conditional and non-conditional tasks, unilateral and bilateral frontal lesions , 1998, Neuropsychologia.

[52]  D. Amaral,et al.  The afferent input to the magnocellular division of the mediodorsal thalamic nucleus in the monkey, Macaca fascicularis , 1987, The Journal of comparative neurology.