Psychobiology 1987, Vol. 15 (1), 21-36 Memory, amnesia, and frontal lobe dysfunction DANIEL L. SCHACTER University of Toronto, Toronto, Ontario, Canada Lesions restricted to the frontal lobes do not ordinarily produce an amnesic syndrome in man. However, recent research has demonstrated that amnesic patients who are characterized by signs of frontal lobe pathology show patterns of memory performance that are different from those shown by amnesic patients without frontal signs. This article reviews evidence concerning the influence of frontal lobe pathology on amnesic disorders, discusses different interpretations of this evidence, and draws on research from human and animal neuropsychology as well as cognitive psychology in an attempt to clarify the role of frontal damage in the amnesic syndrome. Organic amnesia is typically associated with neural tain kinds of spatial and temporal information, deficits that damage in either the diencephalic or medial temporal are not observed in amnesic patients without frontal signs. regions of the brain (e.g., Butters & Cermak, 1980; Next, relevant data from studies concerning the effects Scoville & Milner, 1957; Squire, 1982b, 1986; of restricted frontal lesions on memory functions in hu- Weiskrantz, 1985; Whitty & Zangwill, 1977). The cardi- mans and other primates are considered. These studies nal feature of the amnesia produced by lesions of these have demonstrated selective deficits of memory for structures is a severe impairment in the acquisition of spatiotemporal information following restricted frontal le- many kinds of new information that contrasts with rela- sions, thereby indicating that frontal regions playa specific tively intact intellectual function and normal or near- role in certain memory functions. Additionally, data from normal immediate memory (Cermak, 1982; Hirst, 1982; normal subjects showing that memory for spatiotemporal Moscovitch, 1982; Piercy, 1977; Squire & Cohen, 1984). information may be a relatively automatic process are dis- Recent evidence, however, indicates that the memory cussed. These data support the idea that deficits in memory function of amnesic patients can be influenced markedly for spatiotemporal information associated with frontal lobe by frontal lobe dysfunction (e.g., Moscovitch, 1982; pathology do not necessarily reflect a generalized inability Squire, 1982a). This observation represents a significant to engage in effortful or resource-demanding cognitive theoretical puzzle, because it has long been acknowledged processing. It is concluded that (1) special memory that lesions restricted to the frontal lobe do not produce deficits observed in amnesic patients with frontal lobe a full-blown amnesic syndrome (e.g., Milner, 1964, 1982; pathology are central to our theoretical understanding of Stuss & Benson, 1986). It has become increasingly clear organic amnesia, and (2) such deficits can provide im- that understanding of this puzzle may be crucial to the portant insights into the nature of normal memory that development of theoretical ideas concerning the nature of cannot be readily obtained from the study of "pure" am- organic amnesia. nesic patients. The present article examines evidence that links fron- tal lobe pathology with amnesic disorders, considers The Influence of Frontal Lobe Pathology different interpretations of this evidence, and draws on on Amnesic Disorders relevant research from neuropsychology and cognitive This section describes links between amnesia and frontal psychology in an attempt to clarify the nature of frontal lobe damage that have emerged in research concerning lobe influences on organic amnesia. The article begins amnesic patients' performance on tasks that tap process- with a review of data that demonstrate that amnesic pa- ing and remembering of certain kinds of spatial and tem- tients with frontal pathology exhibit special deficits on poral information. Studies of the relationship between pa- tasks in which performance depends on memory for cer- tients' recall or recognition of recently presented items and their memory for the items' spatiotemporal contexts This article was supported by the Natural Sciences and Engineering will be discussed first, followed by consideration of Research Council of Canada (Grant U0361) and by a Special Research research on the phenomenon of proactive interference. Program Grant from the Connaught Fund, University of Toronto. I am Memory for spatiotemporal context in amnesia. In- grateful to David Olton, Mary Lou Smith, Larry Squire, Endel Tul- ving, and Gordon Winocur for comments concerning earlier drafts of vestigators of memory disorders have long been concerned the article, and I thank Carol A. Macdonald for help with preparation with the question of whether the fundamental deficit in of the manuscript and James Worling for running the experiment on amnesia involves the encoding and retrieval of contex- recency judgments. Requests for reprints should be addressed to tual information (for reviews, see Mayes, Meudell, & Daniel L. Schacter, at Department of Psychology, University of Toronto, Toronto, Ontario, Canada M5S IAI (before August I, 1987) or at Pickering, 1985; Stern, 1981; Winocur, 1982). This is- Department of Psychology, University of Arizona. Tucson, AZ 85721 sue is far from settled, not in the least because it is difficult (after August 1. 1987). to define precisely what is meant by such terms as con- 21 Copyright 1987 Psychonomic Society, Inc. 22 SCHACTER textual information or spatiotemporal context. In the frontal lobe pathology, such as the Wisconsin Card Sort- present paper, these terms refer to global information ing Test (Milner, 1963) and the Benton Word Fluency about when and where a specific event took place, such Test (Benton, 1968), than did either N.A. or the ECT pa- as the room in which a learning episode occurred, the tem- tients. Moreover, within the Korsakoff group, he found poral relationship of one episode to another episode, and a strong positive correlation between performance on the so forth. The terms item memory and item information frontal-sensitive tasks and performance on the temporal are used to refer to what occurred during a particular discrimination task, whereas there was no correlation be- episode. tween performance on the frontal tasks and level of sen- Clinical observations have indicated that amnesic pa- tence recognition. tients have poor memory for the spatiotemporal contexts A relationship between disproportionately poor contex- of recent episodes, even when they can recall some of tual memory and frontal lobe pathology was also observed the items imparted to them during the episodes (Claparede, in an experiment by Schacter, Harbluk, and McLachlan 191111951; Luria, 1976; MacCurdy, 1928; Williams & (1984) concerning the phenomenon of source amnesia: Zangwill, 1950; Zubin, 1948; see Schacter, in press, for retrieval of experimentally presented information without review). Such observations, however, are not sufficient recollection of the spatiotemporal context in which it was to establish that problems with spatiotemporal memory acquired (cf. Evans & Thorn, 1966). In this study, am- represent the fundamental deficit in amnesic patients. It nesics and controls were told fictional characteristics about is possible that poor contextual memory is a well-known and unknown people (e.g., "Bob Hope re- consequence-rather than a cause-of a generally' 'weak" fuses to eat chicken") by one of two experimental sources, or "degraded" memory (Mayes & Meudell, 1981a, and were later tested for retention of item and sources. 1981b). To argue that amnesic patients have special Level of item recall in the two groups was equated by problems remembering spatiotemporal context, it is im- testing amnesics after brief delays of seconds and minutes portant to demonstrate that amnesics have poor contex- and testing controls after a I-week delay. It was found tual memory relative to controls even when item recall that the amnesic patients exhibited more source amnesia and recognition performance of the two groups have been than did controls when level of item recall was held con- equated by appropriate experimental manipulations. stant: On nearly 40% of the trials on which they retrieved Several recent studies have attempted to do so by testing the correct answer, amnesics failed to recollect that either controls at long delays after study and comparing their of the sources had imparted it to them, whereas normals performance to that of amnesic patients who were tested tested at the I-week delay rarely failed to remember that at short delays. Issues pertaining to the role of frontal lobe a recalled item derived from one of the experimental pathology have arisen in these studies. sources. The amnesics in this study were characterized In an experiment reported by Squire (1982a), subjects by diverse etiologies (early stages of Alzheimer's disease, studied sentences presented on two different lists sepa- anoxia, ruptured anterior communicating artery rated by a short temporal interval, and were later tested aneurysm, and closed-head injury), but most of them per- for sentence recognition and temporal discrimination (i.e., formed quite poorly on tasks sensitive to frontal lobe whether a given sentence appeared on the first or second pathology (the Wisconsin Card Sorting Test and the Ben- list). The recognition performance of control subjects at ton Word Fluency Test). When amnesics' performance the long delay was equivalent to that of Korsakoff patients