Memory is the process or processes by which the brain enables us to represent experience and permits experience to shape us. Rather than a unitary capacity supported by a single set of processes, however, there are different forms of memory, supported by multiple, functionally, and anatomically distinct memory systems. The form of memory upon which we seem to depend most in the activities of everyday life and about which we can most readily reflect is declarative memory.
Declarative and Procedural Memory
There are various proposed taxonomies of memory, each offering a different account of the divisions among the memory systems of the brain. Most such accounts distinguish between declarative memory and procedural memory (Cohen and Squire, 1980; Cohen, 1984). Declarative memory supports the on-demand accumulation, storage, and retrieval of new data about facts and events—the information that we capture from our experiences through our representations of it. In contrast, procedural memory supports the shaping of behavioral repertoires acquired through experience. Declarative memory differs from procedural memory in being a relational memory system.
The Nature of Declarative Memory
Declarative memory supports representations of relationships among the constituent elements of an experience. It also supports representations of relationships among various events, providing the larger record of one's experience. It provides the critical means for rapidly representing events, those onetime arbitrary or accidental concurrences of people, places, and things, and the spatial, temporal, and interactional relations among them.
Moreover, declarative memory enables one to learn arbitrary, nonderivable associations through experience—for example, learning the names connected with people's faces, or their addresses and telephone numbers. Declarative memory thereby provides for representations of relations beyond the province of events, encompassing the relations among the facts that constitute our knowledge of the world. This point leads to a further critical distinction: between episodic memory, which contains autobiographical records of personally experienced events, and semantic memory, consisting of world knowledge stored outside of personal contexts (Tulving, 1972). As fundamentally relational, capturing the relations among many different elements of knowledge, both episodic and semantic memory are supported by the declarative memory system.
A second critical property of declarative memory is representational flexibility (Cohen, 1984; Cohen and Eichenbaum, 1993). Declarative memories can be activated by all manner of external sensory or even purely internal inputs, regardless of the current context. And they can be accessed by any number of different brain processors, not only the ones involved in initially acquiring the memories. Once accessed, they can be manipulated and used flexibly to guide performance under an enormous range of testing conditions, including those differing significantly from the circumstances of original learning. In this manner, declarative memory serves as the relational database on which so much of cognitive processing and behavioral performance depends. Among the brain systems that access and manipulate the declarative-memory database are the frontal-lobe systems that support cognitively mediated and consciously aware processes, including conscious introspection and verbal reports of the contents of one's memories.
Deficit of Declarative Memory in Amnesia
Amnesia is a devastating memory impairment following damage to the hippocampal system. Patients with hippocampal amnesia typically have a combination of anterograde amnesia, an impairment in acquiring new memory, and retrograde amnesia, loss of memories preceding the trauma. The deficits seem confined to the domain of declarative memory (Cohen and Squire, 1980; Cohen, 1984; Ryan, Althoff, Whitlow, and Cohen, 2000). Thus, amnesic patients show marked impairment in tasks or situations in which performance depends on learning the relations among items, especially items associated only arbitrarily or accidentally. For example, such patients have great difficulty in remembering the events of daily life. The amnesic patient H.M., who has been studied fifty years, since undergoing a surgical resection of medial temporal lobe structures (Scoville and Milner, 1957; Corkin, 1984), exhibits marked impairment on various tests of memory for public events that occurred after the onset of amnesia and can barely recall any personal events since the time of his surgery (Sagar, Cohen, Corkin, and Growdon, 1985).
Formal laboratory testing confirms the deficit in memory for relations. Paired-associate learning is especially useful in diagnosing amnesia; in this procedure, in which one must learn a set of arbitrarily paired words, amnesic patients show severe impairment, as they do on most list-based recall or recognition-memory tasks, in which they are asked to commit to memory a set of common words, faces, or visual objects presented in a study list and then to report (in recall tests) or to judge (in recognition tests) which items appeared on that particular study list. Because such common stimuli are familiar from a lifetime of previous experience, remembering of specific study items requires the linkage of their identity to this particular study list or learning experience, thereby calling on declarative memory.
Amnesic patients are usually impaired on explicit or direct tests of memory (Graf and Schacter, 1985; Schacter, 1987; Richardson-Klavehn and Bjork, 1988), in which performance depends on using the test item to permit conscious recollection of some specific prior learning experience and then inspecting the contents. A successful outcome requires recall of the relation between the items to be tested and the study list or study experience.
The deficit in amnesia is evident in all manner of relations, whether verbal or nonverbal, spatial or nonspatial, or episodic or semantic. As regards the last, hippocampal amnesia typically affects both personal and public events (Sagar, Cohen, Corkin, and Growdon, 1985; Zola-Morgan, Cohen, and Squire, 1984); it includes not only autobiographical but also world knowledge. One example is the profound deficit shown by the patient H.M. in learning new vocabulary (word-definition relations) that has entered the language since the onset of his amnesia (Gabrieli, Cohen, and Corkin, 1988).
Despite profound and pervasive impairment of memory, amnesic patients show impressive preserved learning and memory abilities. Such patients can learn motor, perceptual, and cognitive skills even though they are unable to remember the experiences during which they acquired the skills. For example, amnesic patients were able to learn to read mirror-reversed text in training extended over several days; and they retained the skill after three months despite marked impairment in recollecting the training experiences or recognizing the words on which they were actually trained (Cohen and Squire, 1980). Preserved memory is characteristic of performance that can be based on tuning of skills in particular domains, built up of incremental improvements in performance with each exposure, and expressed in a repetition of the original learning situation—successful performance in this case does not require the flexible, relational representations of declarative memory (Cohen, 1984; Schacter, 1987; Gabrieli, 1998; Eichenbaum and Cohen, 2001).
Declarative Memory and Consciousness
Declarative memory is critical for conscious introspection and conscious recollection. But this system does not mediate any particular aspect of conscious processing; rather, it provides the flexible access to information about relations among people, places, objects, and actions—the relational database—that undergirds conscious recollection and introspective reports. This view accounts for the amnesic deficits in memory for relations, even those do not enter into the conscious awareness of normal subjects (Ryan, Althoff, Whitlow, and Cohen, 2000; Chun and Phelps, 1999). It also underscores the affinities between human and animal models of amnesia. Hippocampal amnesia in rodents and nonhuman primates produces the same dissociation among memory capacities that are typical of human amnesia. Such animals show impairments in learning and remembering spatial relations among environmental cues, configurations of multiple perceptually independent cues, contextual or conditional relations, and comparisons among temporally discontinuous events—all of which require a relational form of memory. Yet the same animals can show normal learning and remembering of a large variety of conditioning, discrimination, and skill tasks, none of which require a relational form of memory but rather only gradual, incremental changes in bias or reactivity to individual items with repeated exposure.
Brain Mechanisms of Declarative Memory
The critical role of the hippocampal system in declarative memory is evident in the phenomenology of amnesia. Neurophysiological and neuroimaging studies of the hippocampal system also demonstrate its association with memory for relations. Hippocampal neurons encode various relationships among significant elements of an experience, firing preferentially for particular conjunctions of the elements in studies of freely behaving rodents (Wood, Dudchenko, and Eichenbaum, 1999; Eichenbaum et al., 2000). In functional neuroimaging studies of humans, hippocampal system activation arises whenever the task engages memory for the relations among items (Henke, Buck, Weber, and Wieser, 1997; Cohen et al., 1999).
Amnesia indicates that the hippocampal system must interact with other brain systems to effect declarative memory. Retrograde amnesia in cases of hippocampal amnesia can extend backward over variable lengths of time, but it is never total; the storage of long-term memory is never completely lost. Hence the hippocampal system cannot be the repository, or permanent storage site, of all long-term memory. Instead, the reciprocal connections of the hippocampal system with all the higher-order cortical processors allow it to mediate storage in interaction with neocortical sites. After the various cortical processors identify the constituent elements of the event or experience, the hippocampal system binds together the multiple elements into long-term declarative memory representations that capture the relations among the elements, with the individual elements or attributes represented in distributed fashion in the relevant cortical processors. Thus, the interaction of the hippocampal system with neocortical processors and storage sites mediates the relational memory binding that allows the formation of declarative memory. Such memories are then flexibly accessible to various cortical processors in supporting cognitive processing and behavioral performance.
See also:AMNESIA, FUNCTIONAL; AMNESIA, INFANTILE; AMNESIA, ORGANIC; AMNESIA, TRANSIENT GLOBAL; EPISODIC MEMORY; GUIDE TO THE ANATOMY OF THE BRAIN; SEMANTIC MEMORY: COGNITIVE ASPECTS; SEMANTIC MEMORY: NEUROBIOLOGICAL PERSPECTIVE
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