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The Psychology and Neuroscience of Forgetting

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The Psychology and Neuroscience of Forgetting 2 Dec 2003 18:44 AR AR207-PS55-09.tex AR207-PS55-09.sgm LaTeX2e(2002/01/18) P1: GCE 10.1146/annurev.psych.55.090902.141555 Annu. Rev. Psychol. 2004. 55:235–69 doi: 10.1146/annurev.psych.55.090902.141555 Copyright c 2004 by Annual Reviews. All rights reserved First published online as a Review in Advance on November 3, 2003 THE PSYCHOLOGY AND NEUROSCIENCE OF FORGETTING John T. Wixted Department of Psychology, University of California, San Diego, La Jolla, California 92093-0109; email: [email protected] Key Words interference, consolidation, psychopharmacology, LTP, sleep ■ Abstract Traditional theories of forgetting are wedded to the notion that cue- overload interference procedures (often involving the A-B, A-C list-learning paradigm) capture the most important elements of forgetting in everyday life. However, findings from a century of work in psychology, psychopharmacology, and neuroscience con- verge on the notion that such procedures may pertain mainly to forgetting in the lab- oratory and that everyday forgetting is attributable to an altogether different form of interference. According to this idea, recently formed memories that have not yet had a chance to consolidate are vulnerable to the interfering force of mental activity and mem- ory formation (even if the interfering activity is not similar to the previously learned material). This account helps to explain why sleep, alcohol, and benzodiazepines all improve memory for a recently learned list, and it is consistent with recent work on the variables that affect the induction and maintenance of long-term potentiation in the hippocampus. CONTENTS INTRODUCTION .....................................................236 by STEWARD OBSERVATORY on 11/04/08. For personal use only. THE (ONCE) STANDARD STORY OF FORGETTING ......................237 Is Forgetting Due to Interference or Decay? ...............................237 Problems with the Standard Story of Forgetting ............................239 Annu. Rev. Psychol. 2004.55:235-269. Downloaded from arjournals.annualreviews.org Starting Over .......................................................241 PSYCHOLOGY ......................................................242 The Mathematical Form of Forgetting ...................................242 Temporal Gradient of Retroactive Interference .............................244 PSYCHOPHARMACOLOGY ...........................................254 The Curious Phenomenon of Retrograde Facilitation ........................254 Temporal Properties of Retrograde Facilitation ............................257 NEUROSCIENCE .....................................................258 Amnestic Drugs, Sleep, and LTP ........................................259 Induction of New LTP Interferes with Previously Induced LTP ................261 CONCLUSION .......................................................264 0066-4308/04/0204-0001$14.00 235 2 Dec 2003 18:44 AR AR207-PS55-09.tex AR207-PS55-09.sgm LaTeX2e(2002/01/18) P1: GCE 236 WIXTED INTRODUCTION The question of why people forget what they once knew has been continuously investigated for more than a century, and standard accounts of what we have learned about this fundamental issue can be found in almost any general psychol- ogy textbook. Unfortunately, the story that those books tell has changed over the years from a theoretically coherent (but ultimately incorrect) interference-based account of forgetting to an atheoretical laundry list of factors that may or may not play a role. Once, the standard story was that the lion’s share of forgetting is caused by interference and that the main culprit is interference from prior learn- ing (i.e., proactive interference) rather than subsequent learning (i.e., retroactive interference). Theoretical mechanisms such as unlearning, spontaneous recovery, and response competition initially offered a compelling theoretical explanation for the interfering effects of prior learning, but this way of thinking unraveled in the face of disconfirming evidence more than 30 years ago (Tulving & Madigan 1970). Because no new theory emerged to take its place, authors now typically claim that retroactive and proactive interference may both be important and that forgetting probably also involves retrieval failure due to changed or otherwise in- adequate retrieval cues. The notion that decay might play a role, which was once almost universally rejected, has also been resurrected to the status of a possible contributing factor. The tentative and atheoretical nature of the modern account of forgetting is somewhat disappointing after so many years of diligent effort. In the pages to follow, I review findings from psychology, psychopharmacology, and neuroscience in an effort to extract a more compelling theoretical message from the large body of research on forgetting that has accumulated over the years. When grappling with fundamental questions about the nature of memory and retrieval, psychological theories have often been informed by progress in related fields. For example, theories concerned with the distinction between implicit and explicit memory have relied heavily on developments not only in psychology but also in neuropsychology and neuroscience (e.g., Gabrieli 1998, Schacter 1992). By contrast, theories of forgetting have rarely ventured beyond the traditional bound- by STEWARD OBSERVATORY on 11/04/08. For personal use only. aries of experimental psychology. As a case in point, consider the notion that memory traces consolidate over time (an idea that will figure prominently in the Annu. Rev. Psychol. 2004.55:235-269. Downloaded from arjournals.annualreviews.org account of forgetting that is presented below). According to this idea, memories become less fragile and, therefore, more resistant to interference as time passes. Consolidation theory is a standard account in neuroscience, but it is scarcely even mentioned in the psychology literature. To see that this is true, consider the num- bers shown in Table 1. This table shows, for various journals, the number of articles that include “memory” as a keyword relative to the number of articles that include both “memory” and “consolidation” as keywords (according to PsychInfo). For six standard psychology journals, an average of 379 articles about memory appears for every one article that happens to mention both memory and consolidation. For six standard neuroscience journals, the corresponding number is 14. Evidently, Keppel (1984) accurately expressed the attitude that implicitly pervades the study 2 Dec 2003 18:44 AR AR207-PS55-09.tex AR207-PS55-09.sgm LaTeX2e(2002/01/18) P1: GCE FORGETTING 237 TABLE 1 Number of articles that list “memory” as a key word (A), number that list “memory” and “consolidation” as key words (B), and the ratio of those two values (A/B) for each of six cognitive and six neuroscience journals Cognitive journal A B A/B Neuroscience journal A B A/B Journal of Verbal Learning 546 1 546 Journal of Neuroscience 363 26 14 & Verbal Behavior Journal of Memory 262 1 262 Neuroscience 216 18 12 & Language Journal of Experimental 3816 9 424 Learning & Memory 158 27 6 Psychology Journal of Experimental 875 3 292 Behavioral Neuroscience 493 29 17 Psychology: Learning, Memory & Cognition Cognitive Psychology 189 1 189 Brain Research 817 60 14 Memory & Cognition 1142 3 381 Brain 1691 70 24 Mean cognitive 1137 3 379 Mean neuroscience 623 46 14 of forgetting when he said, “For a cognitively oriented psychologist, I find little connection between the behavioral evidence obtained from human learning ex- periments on the one hand and neurophysiological theory on the other” (p. 157). What I hope to show here is that the situation has changed rather dramatically in that respect, and I begin with a more detailed consideration of what was once the standard theoretical account of forgetting. THE (ONCE) STANDARD STORY OF FORGETTING Is Forgetting Due to Interference or Decay? by STEWARD OBSERVATORY on 11/04/08. For personal use only. The question of whether forgetting is due to interference or to natural decay com- manded a great deal of attention early in the twentieth century. To answer this ques- Annu. Rev. Psychol. 2004.55:235-269. Downloaded from arjournals.annualreviews.org tion, an ideal experiment to perform is one in which a learning phase is followed by a retention phase during which the subject’s brain remains biologically active (allowing for natural decay processes to unfold) while his or her mind remains in a quiescent state (so that no new learning interferes with the prior learning). A clas- sic study by Jenkins & Dallenbach (1924) approximated this ideal experiment by comparing memory for nonsense syllables when subjects slept through the reten- tion interval compared to when they remained awake. Interference theory would predict less forgetting during sleep due to the absence of new learning, whereas decay theory would predict no difference between the two conditions. Because Jenkins & Dallenbach (1924) found that subjects recalled more items when they slept than when they remained awake, interference theory won the day and decay 2 Dec 2003 18:44 AR AR207-PS55-09.tex AR207-PS55-09.sgm LaTeX2e(2002/01/18) P1: GCE 238 WIXTED theory was essentially abandoned. Contributing to the demise of decay theory was McGeoch’s (1932) oft-cited observation that the passage of time, per se, is not the cause of forgetting anymore than it is the cause of the physical deterioration associated with aging. Thus, a version of decay theory that attributes a causal role to the passage of
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