Multiple-Memory Systems

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In 1950 Karl Lashley published his influential manuscript In Search of the Engram, in which he concluded that memory was widely distributed in the mammalian brain and that there is no apparent localization of mnemonic traces within specific brain structures. Five decades' worth of research since then suggests that his conclusion may have been partially incorrect. Whereas it is clear that distributed brain structures do indeed participate in mnemonic functions, it is also the case that there is some degree of neuroanatomical localization of learning and memory. There is extensive evidence that memory is organized in multiple systems that differ in terms of the type of memory they mediate. The multiple-memory-systems hypothesis is supported by findings of neuroscientific research in several mammalian species, including rats, monkeys, and humans (Hirsh, 1974; O'Keefe and Nadel, 1978; Olton, Becker and Handelmann, 1979; Packard, Hirsh, and White, 1989; Kesner, Bolland, and Dakis, 1993; Mishkin and Petri, 1984; Zola-Morgan, Squire, and Mishkin, 1982; Cohen and Squire, 1980; Warrington and Weiskrantz, 1982; Knowlton, Mangels, and Squire, 1996). In addition to providing neuroanatomical dissociations of the role of various brain structures in different memory tasks, an important goal of multiple-memory-systems research is elucidation of the psychological operating principles that distinguish different types of memory.

Early Evidence of Multiple-Memory Systems

W. B. Scoville and B. Milner (1957) provided early indirect evidence suggesting the existence of multiple-memory systems in the human brain. In an attempt to alleviate seizure activity in epilepsy and to develop possible alternatives to the practice of performing frontal lobotomies in treating psychosis, they excised large regions of the medial temporal lobe of the brain in a number of patients. The discovery that a severe anterograde human amnesic syndrome resulted from removal of temporal lobe neural tissue sparked immense interest in the role of this brain region in learning and memory. A process of elimination, in which mnemonic deficits were contrasted following varying degrees of damage to different temporal-lobe structures, led to the hypothesis that damage to the hippocampus was primarily responsible for the memory deficits observed in these patients. However, these so-called "temporal lobe amnesics" performed normally on some perceptual and motor-skill learning tasks (e.g. Milner, 1962; Corkin, 1968). These early discoveries of a pattern of spared and impaired learning abilities following temporal lobe damage was consistent with the hypothesis that memory is organized in multiple brain systems. However, the development of dual-memory theories, which might distinguish independent memory systems, did not begin in earnest for several more years.

Lower Animal Research and the Development of Dual-Memory Theories

The ability to produce localized brain damage in animals allowed experimental psychologists to pursue the development of an animal model of the human amnesic syndrome, and the mid-1960s saw several studies examining the effects of hippocampal system damage in various learning tasks. However, these early studies often failed to reveal memory deficits following lesions of the hippocampus, leading some investigators to conclude that this brain structure is not particularly important for mnemonic processes. One explanation for the failure of some animal studies to reveal memory deficits following hippocampal damage is that this structure mediates the acquisition of a specific type of memory. This latter view implies that evidence for a mnemonic role for the hippocampus would emerge only with the use of appropriate learning tasks, and this hypothesis became one of the primary tenets of several dual-memory theories abroad in the mid-1970s.

In an extensive early review of the effects of hippocampal system damage on performance of various learning and memory tasks in rats, R. Hirsh (1974) published perhaps the earliest example of a neurobiological-based dual-memory theory. Hirsh proposed that one way to describe the psychological operating principles that distinguished putative hippocampus-dependent and nonhippocampus-dependent memory systems involved consideration of the historic debate between cognitive (e.g. Tolman, 1932) and stimulus-response (e.g. Hull, 1943) learning theorists. In view of the extraordinary emphasis placed by early learning theorists on the question of what animals learn, it is not surprising that the debate between cognitive and S-R learning theorists was extremely influential. Hirsh suggested, "The behavior of hippocampally ablated animals is held to be everything for which early S-R theorists could have wished" (Hirsh, 1974, p. 439). That same year, J. O'Keefe and L. Nadel introduced a précis of their dual-memory theory, later elaborated on in their influential book The Hippocampus as a Cognitive Map (1978). Their remarkable discovery that hippocampal neurons fired in relationship to a rat's spatial location led O'Keefe and Nadel to suggest that the hippocampus is the neuroanatomical substrate of E. C. Tolman's (1932) cognitive spatial map. Expanding on these ideas, M. Mishkin and colleagues (1984) subsequently offered a distinction between a hippocampal-based cognitive memory system and a nonhippocampal based S-R habit memory system in the monkey brain.

Several other dual-memory theories have emerged based on research in rats, monkeys, and humans. One prominent theoretical distinction between different types of memory in humans is based on a pattern of spared and impaired learning in temporal lobe amnesia; it draws a distinction between hippocampus-dependent declarative memory and nonhippocampus-dependent procedural memory (Cohen and Squire, 1980). Declarative memory involves acquisition and expression of specific facts and events, whereas procedural memory involves acquisition of instrumental S-R habits and various forms of classically conditioned behaviors. A theoretical distinction between explicit and implicit memory processes in humans (Graf and Schacter, 1985) has also received extensive investigation and support. Explicit memory is held to involve the conscious recollection of facts and events, while implicit memory involves unconscious acquisition and expression of learned behavior. E. B Tulving's distinction between episodic and semantic memory represents an additional example of a multiple-memory-systems approach to memory organization in humans (Tulving, 1987).

Neuroanatomical Bases of Multiple-Memory Systems

Each dual-memory theory was developed from a consideration of the pattern of spared and impaired learning that follows damage to one particular brain region: the hippocampus. Thus, the existence of multiple-memory systems has often been suggested based on the observations of single dissociations—that is, damage to the hippocampus impairs performance of task X but not task Y. But, postulating functional independence of memory systems based on a single dissociation is difficult because of the potential existence of hierarchal relationships among the mnemonic role(s) of particular brain structures and task (Weiskrantz, 1989). A more compelling argument for the existence of multiple-memory systems in the brain requires the demonstration of a double dissociation, (a term coined by Teuber, 1955), in which damage to brain structure X impairs performance on task A but not task B, and damage to brain structure Y impairs performance on task B but not task A.

An early study in rats used two eight-arm radial-maze tasks to demonstrate a double dissociation between the mnemonic functions of the hippocampal system and caudate nucleus (Packard, Hirsh, and White, 1989). The radial maze consisted of a center platform with eight alley-shaped arms radiating away from the center and containing food cups at the distal end-points. In a standard win-shift version of the radial-maze task, rats obtained food rewards by visiting each arm of the radial maze once in a daily training session, and reentries into previously visited maze arms within a session were scored as errors. In a win-stay version of the radial-maze task, rats obtained food rewards by visiting four randomly selected and illuminated maze arms twice within a daily training session, and the spatial location of these maze arms varied by day. Two important features of these radial-maze tasks make them ideal for employing dissociation methodology to examine the hypothesis that the hippocampal system and caudate nucleus are parts of independent memory systems: 1. Performance in the win-shift task requires rats to remember those arms that have been previously visited, while performance in the win-stay task simply requires rats to learn to approach lit maze arms. Therefore, the win-shift task is often considered a prototypical test of spatial working memory and appears to involve the use of a cognitive mapping strategy. In contrast, the win-stay task is essentially a simultaneous visual discrimination and may involve acquisition of an S (light)-R (approach) habit; 2. The two tasks share the same motivational (appetitive), sensory (primarily visual), and motoric (maze running) characteristics; therefore, any differential effects of damage to separate brain areas on performance in the two tasks can be more readily ascribed to mnemonic processes.

When rats were tested in the acquisition of these two tasks following lesions of the hippocampal system and caudate nucleus, a double dissociation resulted: Hippocampal-system lesions selectively impaired acquisition of the win-shift task, while caudate-nucleus lesions selectively impaired acquisition of the win-stay task (Packard, Hirsh, and White, 1989). A double dissociation between the mnemonic functions of the hippocampus and caudate nucleus in these two radial maze tasks has also been demonstrated using post-training intracerebral infusions of memory-enhancing drugs (Packard and White, 1991). Evidence that the caudate nucleus is part of a memory system that mediates at least one form of nonhippocampal-dependent memory also comes from research in nonhuman primates and humans (Knowlton, Mangels, and Squire, 1996; Fernandez-Ruiz et al., 2001).

Besides the several studies that have dissociated the mnemonic functions of the mammalian hippocampus and caudate nucleus, other studies suggest that the cerebellum and amygdala mediate additional forms of learning and memory. R. Thompson and colleagues have described a role for the cerebellum in classically conditioned eyeblink behavior, providing a detailed analysis of the neural circuitry mediating the flow of information underlying the processing of unconditioned and conditioned stimuli in this form of Pavlovian conditioning (McCormick et al., 1981; Kim and Thompson, 1997). Other behavioral neuroscience research indicates that the mammalian amygdala mediates "stimulus-affect" memory, as evidence by a selective role for this brain region in fear conditioning (LeDoux, 1992; Davis, 1992), and stimulus-reward learning (e.g. Cador, Everitt, and Robbins, 1989; McDonald and White, 1993). Activation of efferent amygdala pathways by emotionally arousing events also modulates the distinct cognitive and S-R habit memory process subserved by the hippocampus and caudate nucleus (Packard, Cahill, and McGaugh, 1994).

Behavioral neuroscience research conducted largely over the last two decades has dramatically increased our understanding of neuroanatomical systems that mediate different types of memory in mammalian species ranging from the rat to the human. These findings suggest that elucidation of the neurobiological bases of memory organization will remain a complex task involving a consideration of patterns of spared and impaired memory function following various brain manipulations in lower animals, in neuropsychological studies of brain damaged humans, and in neuroimaging studies of memory processes in the intact human brain.



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Mark G.Packard

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Multiple-Memory Systems

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