Psychobiology 1987, Vol. 15 (1), 21-36 , , and 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' 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, , 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 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 on these tasks was related to how frequently they forgot at the short delay. Nevertheless, Korsakoff patients' per- when and where a recalled item was acquired, a strong formance on the temporal discrimination task at the short positive correlation was observed. However, there was delay was significantly impaired with respect to controls' a nonsignificant relationship between performance on the performance at the long delay. Because recognition per- frontal-sensitive tasks and level of item recall. formance of the two groups was equivalent at the two de- Taken together, the data reported by Squire (1982a) and lays, it is plausible to argue that Korsakoff patients ex- by Schacter et al. (1984) suggest that impairments of hibited a selective temporal memory impairment that spatiotemporal memory that are disproportionately severe cannot be entirely accounted for by their "weak" or relative to impairments of item recall and recognition are "degraded" recognition performance. By contrast, the associated with signs of frontal lobe dysfunction. The fact temporal discrimination performance of patients rendered that level of item recall or recognition was unrelated to amnesic by bilateral electroconvulsive therapy (ECT) and performance on the frontal-sensitive tasks in both studies patient N.A., whose amnesia was caused by a lesion in suggests that this association is not simply a reflection of the dorsomedial nucleus of the thalamus, was no worse overall level of impairment: If patients with signs of fron- than controls' performance when recognition memory of tal lobe damage were generally more impaired than non- the two groups was equated. Squire suggested that the frontal patients, one would have expected them to per- Korsakoff patients' disproportionately poor memory for form more poorly on item recall and recognition tasks. temporal information might be related to the frontal lobe It is important to emphasize that the notion of dispropor- dysfunction that is known, to occur in conjunction with tionately poor spatiotemporal memory is a relative one long-term alcohol abuse. Squire found that his Korsakoff that has meaning only with respect to a particular level patients performed worse on tasks that were sensitive to of item recall or recognition. For example, a patient such AMNESIA AND FRONTAL LOBES 23

as the well-known amnesic H.M., who performs quite controls, when learning and testing were carried out in well on frontal-sensitive tasks, would no doubt perform a highly distinctive environmental context (consisting of quite poorly on tasks that tapped memory for spatiotem- colored lights and classical music) versus when they were poral context. However, the results of Squire (1982a) and done in an ordinary context. This fmding suggests that Schacter et al. (1984) suggest that ifH.M. 's level of item Korsakoff patients have special difficulties in responding recall or recognition could be brought to the level of con- to environmental cues, difficulties than can be overcome trois' (e. g., by long presentation time and testing at a brief when the patients are placed in a distinctive and unusual delay), his memory for spatiotemporal context would also environmental context. Mayes, Meudell, and Som (1981) approximate that of controls. These ideas imply that fur- compared paired-associate performance of normal sub- ther instances of disproportionately poor memory for jects in unusual and in ordinary contexts when testing was spatiotemporal context will be observed in amnesics in carried out after a long delay. Normal subjects performed whom there are grounds for suspecting frontal lobe no better in the unusual context than they did in the ordi- damage, such as Korsakoff patients, Alzheimer patients, nary context, suggesting that Winocur and Kinsbourne's or patients with ruptures of the anterior communicating data cannot be accounted for in terms of generally weak artery. Although there is as yet little relevant evidence, or degraded memory on the part of amnesic patients. several studies are consistent with this suggestion. Hup- The foregoing studies support the view that the difficul- pert and Piercy (1976) found that Korsakoff patients ties amnesic patients who are characterized by signs of recognized pictures that had been presented on one of 2 frontal lobe pathology have in processing and remember- days as efficiently as controls did. The Korsakoff patients, ing contextual information are not entirely accounted for however, were severely impaired at discriminating be- by their deficits in item recall and recognition. Is there tween the temporal contexts in which the pictures oc- any evidence that such disproportionately poor contex- curred: They performed poorly when required to state on tual memory occurs in patients without signs of frontal which of the 2 days they had seen a presented picture. lobe pathology? The only study to report such evidence In a related study, Huppert and Piercy (1978) presented is one by Hirst and Volpe (1982), which included a vari- pictures to normals and controls either once or three times ety of amnesic patients who, the authors stated, performed on 2 separate days, and asked them to make recency judg- relatively well on frontal-sensitive tasks. These patients ments concerning whether a picture had been presented demonstrated little, if any, impairment on recognition "today" or "yesterday." Korsakoff patients responded tests, but performed more poorly than controls when re- "today" equally often to pictures that had been presented quired to make temporal order judgments concerning re- three times the previous day (36 %) and once on the day cently presented words or past public events. Several of the test (36%), whereas control subjects responded "to- points about this study should be noted. On the word- day" much less often to pictures presented three times memory task, the overall pattern of results for recogni- the previous day (9 %) than to pictures presented once on tion and temporal order judgments were quite similar: the day of the test (68%). These data indicate that Kor- Normal subjects' performance was higher in both cases. sakoff patients retained little temporal information con- The recognition differences, however, failed to achieve cerning when the pictures had been presented, and perhaps statistical significance. This finding may have resulted based their judgments of recency and frequency on the from the presence of ceiling effects, and the relatively general "strength" of a memory trace. The temporaljudg- small number of observations in individual experimental ments of control subjects, by contrast, were much more conditions. The observation of significant differences be- sensitive to specific information concerning recency and tween amnesics and controls for temporal order judgments frequency of occurrence. Note, however, that Huppert is clouded by the puzzling fmding that amnesics' perfor- and Piercy did not report data concerning item recogni- mance was well below the chance level in several of the tion. Since it is likely that their recognition memory was conditions that yielded differences. On the public events impaired, Korsakoff patients' impaired temporal judg- task, recognition memory performance approached ceil- ments could be attributable to generally degraded ing for both amnesics and controls, suggesting the possi- memory. If so, such an impairment should be observed bility that a recognition impairment on the part of am- in normal subjects tested at appropriately long delays. nesics would have emerged in a more difficult task, as Meudell, Mayes, Ostergaard, and Pickering (1985) exa- would be expected on the basis of a large number of mined this idea, and found that the recency judgments of studies (for similar concerns, see Mayes et al., 1985). In normals tested at a long delay distinguished between time short, the Hirst and Volpe data do not demonstrate un- of occurrence more accurately than did those of Korsakoff equivocally that amnesics who perform well on frontal- amnesics, thereby supporting the notion of a dispropor- sensitive tasks exhibit disproportionately poor memory for tionate impairment of memory for temporal information temporal context. in Korsakoff patients. Proactive interference effects. Proactive interference Research reported by Winocur and Kinsbourne (1978) (PI) refers to the deleterious effect that a particular learn- suggests that Korsakoff patients also have problems us- ing experience can have on subsequent learning. Research ing features of spatial context to aid memory perfor- with normal subjects suggests that sensitivity to proac- mance. They found that Korsakoff patients' acquisition tive interference is closely linked with temporal discrimi- of paired associates improved significantly, relative to nation and memory processes (e.g., Underwood, 1977). 24 SCHACTER

It has been shown that, under certain conditions, amnesic (1981) have shown that Korsakoff patients do show release patients are more sensitive to the buildup of PI than are to a categorical shift if the stimuli on the release trial are control subjects (e.g., Kinsbourne & Winocur, 1980; rendered highly distinctive by changes in the colors of Winocur & Weiskrantz, 1976). In these studies,_subjects target words and the background on which they are studied successive paired-associate lists in which the same printed. Thus, the Korsakoffpatients' deficit may be at- stimulus term was paired with different response terms. tributable to an inability to process salient contextual fea- Amnesic patients showed an exaggerated tendency to in- tures, although the type of contextual information assessed trude the first-list responses onto successive lists. This in the Winocur et al. experiment differs from that of the hypersensitivity to PI has been interpreted as a conse- contextual information discussed earlier. By contrast, am- quence of an impaired spatiotemporal memory that pre- nesic patients who are free of frontal lobe problems vents amnesic patients from remembering the list mem- demonstrate normal release on the Wickens test (Cermak, bership of response terms. Since many of the patients who 1976; Moscovitch, 1982), whereas frontal-lobe patients, show this phenomenon are Korsakoff patients, it is pos- like Korsakoff patients, do not release normally sible that frontal lobe dysfunction plays some role in it. (Moscovitch, 1982), although failure to show normal However, Warrington and Weiskrantz's (1974, 1978) ex- release from PI may be observed only in those frontal periments, which also provide evidence that amnesic pa- patients who also exhibit some memory deficits (Freed- tients are extremely sensitive to interference, included a man & Cermak, 1986). Thus, failure to demonstrate variety of patients, not all of whom would be expected release from PI can be linked both to frontal problems to have frontal lobe problems. Accordingly, we cannot and to difficulties in the processing of some contextual be entirely certain that sensitivity to PI depends crucially features. on frontal lobe pathology. Schacter, Moscovitch, Tulving, McLachlan, and Freed- Interpretation of Frontal Lobe Int1uences man (1986) have recently reported a related interference on Memory Disorders phenomenon that may also depend on frontal lobe involve- The foregoing studies indicate clearly that, on tasks that ment in amnesia. Schacter et al. required amnesic patients require access to various types of spatiotemporal infor- to remember the locations of objects hidden at successive mation, the performance of amnesic patients who are locations. It was found that patients, after a brief delay, characterized by signs of frontal lobe pathology is differ- successfully retrieved objects hidden at an initial location. ent from that of patients without frontal signs. What are However, they subsequently failed to retrieve objects at the implications of this observation for theories of the am- new locations, and instead searched for them at the old, nesic syndrome? At least two broad alternatives can be initial location. Two kinds of evidence suggest that this distinguished. One possibility is that amnesic patients with phenomenon of precedence (Schacter et al., frontal lobe deficits have a specific and primary memory 1986) depends in some way on the presence of frontal dysfunction within the domain of spatiotemporal infor- lobe pathology. First, Schacter et al. noted that all of their mation that is not observed in other amnesic patients. If amnesic patients showed signs of frontal lobe pathology_ this is the case, the deficits observed in such patients could Second, Diamond and Goldman-Rakic (1983) have ob- have important implications for theories of amnesia, be- served a phenomenon similar to mnemonic precedence cause the role of spatiotemporal memory deficits in the in monkeys with frontal lobe lesions (also see Diamond, amnesic syndrome is central to various theoretical posi- 1985). tions (e.g., Butters & Miliotis, 1985; Mayes & Meudell, Studies of the phenomenon of release from PI also sug- 1983; Mayes et al., 1985; Schacter & Tulving, 1982a, gest a role for frontal lobe pathology in amnesia. This 1982b; Squire, 1987; Squire & Cohen, 1984; Winocur, phenomenon was studied extensively in normal subjects 1982). by Wickens (1970), who developed a paradigm in which A second possibility, however, must be considered be- subjects are presented with and tested on four successive fore the first possibility can be accepted. It is possible that lists containing words from a particular category, and then the special spatiotemporal memory deficits observed in given a list containing words from a different category. amnesic patients with frontal signs represent nonspecific In normal subjects, recall performance decreases over the impairments that are secondary to other problems as- first four trials, reflecting the buildup of PI, but improves sociated with frontal lobe dysfunction, problems that are on the fifth trial; the improved performance is referred not concerned specifically with memory function. Since to as release from PI. Using similar paradigms, studies amnesia can occur in the absence of frontal lobe dysfunc- of Korsakoff amnesics have demonstrated that patients tion, and restricted frontal lobe lesions typically do not show considerable buildup of PI over the first four trials, produce an amnesic syndrome, the possibility that frontal- but fail to improve performance when the category is related memory deficits in amnesic patients are secondary shifted on the release trial (Cermak, Butters, & Moreines, to other, rather general cognitive problems must be con- 1974; Kinsbourne & Wood, 1975). Zatorre and McEntee sidered carefully. For example, if amnesic patients with (1983) reported similar observations in a severely amnesic frontal lobe deficits are characterized by sensoripercep- head-injured patient with a large lesion to the left frontal tual impairments that prevent them from registering ex- lobe. However, Winocur, Kinsbourne, and Moscovitch perimental input accurately, are so grossly disoriented or AMNESIA AND FRONTAL LOBES 25

demented that they cannot properly comprehend the na- playa major role in spatiotemporal memory deficits. ture of a task, suffer from language or motor problems Thus, if the evidence indicated that frontal regions were that prevent them from expressing retained knowledge, specifically associated with memory for spatial and tem- or are not sufficiently motivated or aroused to perform poral context, and that spatiotemporal information could a task, then it would be appropriate to regard any special be encoded in a relatively automatic manner, there would memory problems associated with these impairments as be grounds for rejecting the idea that memory deficits as- nonspecific deficits that need not command our theoreti- sociated with frontal lobe dysfunction in amnesic patients cal . If, however, deficits in these areas can be were attributable to nonspecific cognitive and motivational excluded, then it may make good theoretical sense to ex- impairments. In the following sections of the paper, I will amine closely the nature of memory impairments that are examine evidence concerning the effects of frontal lobe produced by frontal deficits. lesions on memory function in man and in nonhuman pri- On the basis of the literature discussed thus far, there mates that bears upon the specificity of spatiotemporal is no reason to believe that the special spatiotemporal deficits; I will then discuss studies of memory for memory deficits exhibited by amnesics with signs of fron- spatiotemporal context in normal human subjects that ad- tal lobe pathology can be attributed to perceptual impair- dress the question of whether spatiotemporal information ments, gross dementia, or motorllanguage difficulties. Pa- is processed automatically. tients in the relevant studies were all characterized by relatively normal performance on perceptual, intellectual, Memory Function and Frontal Lobe linguistic, and motor tasks. There is, however, some ba- Lesions in Man sis for suspecting a role of motivation/arousal deficits: As noted earlier, it has been frequently observed that Korsakoff patients, who participated in most of the rele- patients with relatively restricted frontal lobe lesions do vant studies, are known to suffer from problems of low not develop a full-blown amnesic syndrome (e.g., Mayes motivation and arousal (e.g., Butters & Cermak, 1980; & Meudell, 1983; Milner, 1964; Moscovitch, 1982; Oscar-Berman, 1980), and it is widely recognized that pa- Squire, 1982a; Stuss & Benson, 1986). Because "pure" tients with restricted frontal lesions are often unmotivated frontal lobe patients are not amnesic, it may be question- and lack the initiative and resources that are necessary able whether the frontal lobes should be assigned any role to perform complex tasks (e.g., Damasio, 1979; Eslinger at all in mnemonic functions. A number of studies have & Damasio, 1985; Stuss & Benson, 1986). To link such provided evidence in support of this contention. Teuber deficits with findings of disproportionately poor spatio- and Weinstein (1954) examined of items from temporal memory, one could argue that tasks that tap a formboard in patients with frontal lesions or posterior memory for spatiotemporal context are more resource- lesions produced by missile wounds. Free-recall perfor- demanding than are tests of item recognition, and that, mance was higher for the frontal patients than for the pa- hence, generally underaroused and unmotivated subjects tients with posterior damage. Ghent, Mishkin, and Teuber perform more poorly on them. To the extent that this ar- (1962) compared the performance of patients with gument is valid, one could conclude that amnesic deficits unilateral left, unilateral right, and bilateral frontal damage associated with frontal lobe dysfunction are not telling us with that of nonfrontal brain-injured patients and controls anything specific about memory for spatiotemporal infor- on tests of , tactual memory, digit span, mation. Instead, they may indicate that unmotivated or and nonverbal object span. Memory was tested at a rela- underaroused subjects perform disproportionately poorly tively brief delay (15 sec). In all cases, the frontal pa- on resource-demanding tasks. tients performed as well as the nonfrontals and controls, There are at least two ways in which the proposal that and there was no evidence of differential impairment disproportionate spatiotemporal deficits associated with among the three frontal subgroups. Milner (1967) exa- frontal lobe dysfunction are nonspecific consequences of mined the performance of patients with unilateral left fron- motivation and arousal deficits could be countered. The tal damage on their delayed recall of paired associates and first would be to provide evidence that the processing and stories that had been presented in the visual and auditory retention of spatiotemporal information was specifically modalities. Memory performance of the frontal patients associated with the frontal regions. If such specificity was normal in all conditions. More recently, Jetter, Poser, could be demonstrated, it would be difficult to maintain Freeman, and Markowitsch (1986) reported that patients that poor spatiotemporal memory in amnesics with fron- with unilateral and bilateral frontal lesions performed nor- tal lobe pathology resulted from a generalized cognitive mally on free-recall, cued-recall, and recognition tests ad- sluggishness. The second of these two ways would be to ministered 15 min after presentation of a 16-item word demonstrate that memory for spatiotemporal context did list. On a 24-h delayed test, cued-recall and recognition not require a large amount of effort and motivation, but performance remained normal, but free-recall perfor- was, instead, a relatively automatic function that required mance was significantly impaired. Although the latter little investment of cognitive energy. If memory for finding suggests that, under certain conditions, frontal lobe spatiotemporal context was a relatively automatic func- lesions may result in mild item recall deficits, most of tion, then any generalized motivational or arousal deficits Jetter et al.'s patients suffered from traumatic brain in- associated with frontal lobe dysfunction would not likely jury, thereby raising the possibility that they had incurred 26 SCHACTER damage in extrafrontal regions that was not evident in the patients were substantially impaired when required to CT scan. Similarly, Freedman and Cermak (1986) recall the temporal order of recently presented pictures described the cases of several frontal patients who ap- and words. By contrast, the frontal patients were much peared to have some difficulty with item recall. However, less impaired on memory tasks that did not demand or- Freedman and Cermak could not rule out the possibility dered recall. Milner and Kolb (1985) found that patients that these patients' memory problems were attributable with unilateral frontal damage were impaired when re- to damage in areas outside the frontal lobe, such as the quired to reproduce, in correct temporal order, a series basal forebrain (see Damasio, Graff-Radford, Eslinger, of arm and facial movements. Smith and Milner (1983) Damasio, & Kassell, 1985). found that patients with either left- or right-sided frontal Although one must always be wary about accepting the lesions were impaired on tasks requiring estimates of fre- null hypothesis, the results of the foregoing studies cer- quency of occurrence of experimental stimuli, which re- tainly do not encourage the view that restricted frontal quire memory for temporal information. lobe lesions are sufficient to produce memory disorders In addition to their problems with remembering tem- of the kind that are encountered in the classical amnesic poral order, patients with frontal damage also perform syndromes. Remember, however, that the data considered poorly when memory tasks require various types of se- in the previous section of the article indicated that signs quential organization (della Rocchetta, 1986; Petrides & of frontal lobe pathology were unrelated to level of recall Milner, 1982), recollection of autobiographical episodes and recognition performance; they were correlated with with specific temporal dates (Baddeley & Wilson, 1986), performance on tasks that involve memory for spatiotem- or accurate temporal discriminations (Prisko, cited in Mil- poral information. The studies reviewed in the foregoing ner, 1964). In Prisko's study, the performance of paragraph were all concerned with recall and recognition unilateral left and right frontal patients was compared with performance; the tasks used in these experiments did not that of unilateral left and right temporal patients, using require memory for spatiotemporal information. delayed comparison tasks in which the subjects indicated Several investigators, however, have provided data con- whether a test stimulus was identical to or different from cerning memory for spatiotemporal information in fron- a target stimulus that had been presented 60 sec earlier. tal patients (for discussion, see Milner, Petrides, & Smith, When each study-test trial was composed of unique 1985; Squire, 1987; Stuss & Benson, 1986). These studies materials that did not recur on subsequent trials (nonsense indicate that when frontal patients are given tasks that re- figures), performance of both groups of frontal patients quire memory for temporal order or demand temporal dis- was unimpaired. Prisko also examined memory perfor- criminations, substantial impairments can be detected. mance on tasks in which some of the stimuli (flashes, Perhaps the most elegant demonstration of a selective clicks, and colors) recurred from trial to trial. Under these deficit of temporal memory in frontal lobe patients is conditions, subjects had to remember whether they had found in a study by Corsi (cited by Milner, 1971, 1974). seen the test stimulus on the current trial or on a previ- In one task, Corsi presented patients with lists of com- ous trial to make a correct response. Thus, the tasks with mon words and tested memory in two different ways. On recurring stimuli demanded memory for temporal con- a two-choice recognition task, patients indicated which text, whereas the task with nonrecurring stimuli did not. of the two words (one old, one new) had appeared earlier Paired-comparison performance of both groups of fron- in the list; on a two-choice recency-judgment task, they tal patients was impaired, with respect to that of temporal indicated which of two old words had appeared more re- patients and controls, when stimuli recurred from trial to cently in the list. Corsi found that patients with unilateral trial. left and right frontal damage performed normally on the Chorover and Cole (1966) compared the performance recognition task. But the patients with left-sided frontal of unilateral and bilateral frontal patients with that of non- damage were impaired on the recency-judgment task. By frontal patients and controls on a delayed alternation task contrast, patients with unilateral left temporal damage that required subjects to make a response opposite to the were impaired on the recognition task but not on the one made on an immediately preceding trial. Temporal recency task. Corsi observed a similar double dissocia- discrimination plays an important role in this task: Sub- tion among patients with right-sided damage when non- jects must remember their response from the immediately verbal materials were used: Patients with right-sided fron- preceding trial and discriminate it from responses made tal damage were impaired on the recency task but not on in earlier trials in order to make a correct alternation the recognition task, whereas patients with right-sided response. Chorover and Cole's results were characterized temporal damage were impaired on the recognition task by a good deal of variability within and among subject but not on the recency task. groups, and hence are not entirely clear-cut. There was, The results of several other studies indicate that the however, evidence of impairment in the frontal groups: deficits of temporal memory in frontal patients demon- 53 % of frontal patients failed to achieve criterion, whereas strated by Corsi have a good deal of generality. Lewin- only 33 % of patients with nonfrontallesions failed to do sohn, Zieler, Libet, Eyeberg, and Nielson (1972) found so. All of the controls achieved criterion. Using a simi- that unilateral left, unilateral right, and bilateral frontal lar approach, Pribram, Ahumada, Hartog, and Roos AMNESIA AND FRONTAL LOBES 27

(1964) found that patients who had undergone bilateral tal functions can be isolated and distinguished from one frontal were impaired on a variety of alterna- another. With respect to the present concerns, the major tion tasks that demanded temporal discriminations. interpretive problem regarding the specificity of frontal- In a recent study, Stuss et al. (1982) found that related temporal memory impairments concerns the schizophrenics who had undergone bilateral prefrontal leu- numerous other deficits that have been observed in fron- cotomy were not impaired on a number of standard tal patients, including problems of planning (Milner, 1982; memory tasks, including the Wechsler Memory Scale and Shallice, 1982), regulation of verbal behavior (Luria, tests of verbal and nonverbal recall and recognition. The 1969), perseveration (Hecean & Albert, 1975; Sandson frontal patients, did, however, exhibit excessive sensitivity & Albert, 1984), verbal and nonverbal fluency (Benton, to proactive interference on the Brown-Peterson trigram 1968; 10nes-Gotman & Milner, 1977), hypothesis test- recall task, in which subjects must make accurate tem- ing (Milner, 1963), arousal (Luria, 1973), motivation (Es- poral discriminations to determine whether a response is linger & Damasio,1985), and affect (Damasio & Van appropriate for a particular trial. Sensitivity to proactive Hoesen, 1983). Does the presence of such deficits imply interference in frontal patients has also been reported by that temporal memory problems are secondary to them, Luria (1971). or at the very least inextricably intertwined with them? The foregoing studies provide converging evidence for Although this question cannot be answered unequivocally, the view, proposed by various investigators (e.g., Dia- there is growing evidence that specific functional deficits mond & Goldman-Rakic, 1983; Fuster, 1980; Goldman- are associated with different loci of damage within the Rakic, 1984; Milner, 1971; Milner et al., 1985; Stuss frontal areas (Damasio, 1979; Drewe, 1974, 1975; Kolb et al., 1982), that patients with relatively restricted fron- & Whishaw, 1985; Walsh, 1978). For example, deficits tal damage are impaired on memory tasks that require of arousal and emotion are typically associated with utilization of temporal information, and perform relatively orbital-frontal damage, whereas cognitive deficits are normally on memory tasks that do not make temporal de- more often found in association with dorsolateral frontal mands (for a demonstration of impaired learning by frontal damage (e.g., Darnasio & Van Hoesen, 1983; Milner, patients in a nontemporal task, see Petrides, 1985). Less 1964; Stuss & Benson, 1986). In a summary of much of attention has been paid to frontal patients' memory for the relevant literature, Damasio (1979) argued that the spatial context. Smith and Milner (1983) recently found numerous manifestations of frontal lobe pathology "need that patients with unilateral frontal lesions were unim- not be present at the same time or to the same degree" paired on a task that required them to recall the spatial (p. 360), and concluded that the varied connections of the positions of objects previously presented in an array. frontal regions to other brain regions "underscores the However, it is not clear how the kind of information absurdity of the notion of a single frontal-lobe syndrome" tapped by the Smith and Milner task, which concerns lo- (p. 371). cal features of spatial position, is related to the impair- The notion that different manifestations of frontal lobe ment of more global contextual information about the oc- damage may be both functionally and neuroanatomically currence of an episode that is found in amnesic patients dissociable is important because it helps us to understand with frontal pathology. that even though temporal memory deficits may occur in The major issue that needs to be addressed with respect conjunction with other impairments, they need not be de- to the foregoing findings concerns the specificity of the pendent on them or related to them in a causal manner. temporal memory deficits: Are the frontal regions in- The fact that multiple deficits often occur in frontal lobe volved specifically in the processing and retention of tem- patients may simply reflect the fact that, in clinical studies, poral information, or are the selective deficits by-products it is difficult to control precisely the site and extent of of other functions in which the frontal areas are involved? . It is possible that when lesions are con- The long and contentious history of research and theoriz- fined to specified locations, temporal memory deficits can ing concerning the nature of frontal lobe function (Teuber, be dissociated from other impairments. The extensive 1964) provides ample warning that unequivocal answers literature on frontal damage in nonhuman primates sug- to such a question will be difficult to obtain. In view of gests that this is indeed the case. the spectrum of deficits that have been exhibited by fron- tal lobe patients, the multiplicity of functions that have Memory for Spatiotemporal Information been attributed to the frontal regions (Damasio, 1979; in Frontal Animals Fuster, 1980; Ingvar, 1983, 1985; Kolb, 1984; Luria, The question of whether frontal lesions yield memory 1969; Stuss & Benson, 1984, 1986), and the widespread deficits in nonhuman primates has an extended history that neuroanatomical connections of the frontal areas to cor- has been reviewed elsewhere (Fuster, 1980; Iversen, tical and subcortical structures (Goldman-Rakic, 1984; 1983). Three general types of tasks have been used to Nauta, 1971, 1973), any attempt to postulate a single func- evaluate mnemonic function in most of this research. On tion that is uniquely "frontal" is no doubt an oversim- delayed response tasks, bait is placed under one of two plification and surely incorrect. identical hiding wells in different spatial locations, and The complexity of the problem, however, need not pre- the animal is permitted to look for it after a delay of vent us from examining the possibility that specific fron- several seconds; the location of the bait varies from trial 28 SCHACTER to trial. The delayed response task thus requires memory formance on tasks is observed, but if le- for spatial location. In addition, the task requires accurate sions are made in the dorsolateral cortex outside the temporal discrimination: The animal must be able to principal sulcus, such as in the arcuate sulcus, there is remember the location of the reward on the most recent no impairment on spatial memory tasks (Butters et al., trial in order to make the correct response. On delayed 1972; Goldman & Rosvold, 1970; Goldman et al., 1971; alternation tasks, the bait is placed under identical objects Stamm & Rosen, 1973). at different locations (spatial alternation) or under differ- There is some uncertainty concerning the role played ent objects at the same location (object alternation), and by the dorsolateral frontal cortex in memory tasks that the animal is rewarded for making a response on Trial n do not entail a spatial component, such as delayed that is opposite to the one made on Trial n - 1. As in matching-to-sample. The results of several studies indi- delayed response, the location of reward varies randomly cate that when dorsolateral function is interfered with by between the two places from trial to trial. A third task lesions (Glick, Goldfarb, & Jarvik, 1969), electrical that has been used in relevant research is delayed stimulation (Kovner & Stamm, 1972), or cooling (Bauer matching-to-sample. Here, the animal is typically shown & Fuster, 1976, 1978; Fuster & Bauer, 1974), perfor- one of two colors (e.g., red or green). When both colors mance on delayed matching-to-sample is severely im- are subsequently displayed after a brief delay, the animal paired, whereas performance on simultaneous matching is rewarded for touching the one that matches the sam- is unimpaired. However, when dorsolateral lesions are ple. Delayed matching-to-sample does not require confined to the principal sulcus, performance on nonspa- memory for spatial location; the correct color may ap- tial memory tasks, such as object alternation and delayed pear in the same or in a different location as the sample. matching, are relatively unimpaired (Mishkin & Manning, It does, however, require the animal to discriminate 1978; Mishkin et al., 1969; Passingham, 1975), suggest- among temporal contexts, because the same colors are ing the possibility that neural disruption in the aforemen- used on successive trials. tioned delayed matching-to-sample studies extended be- Early research employing these tasks demonstrated that yond the principal sulcus. Damage to the inferior-ventral monkeys with extensive bilateral frontal lesions perform regions of the frontal cortex does, however, impair per- poorly on delayed response tasks and on both spatial and formance on nonspatial memory tasks (Mishkin & Man- object alternation tasks (e.g., Jacobsen, 1935; Malmo, ning, 1978; Mishkin et al., 1969; Passingham, 1975; see 1942; Mishkin & Pribram, 1955, 1956). A major focus also Oscar-Berman, 1975). of subsequent research has concerned the question of It is worth noting that much of the debate in the litera- whether different aspects of delayed response and delayed ture has focused on the question of whether frontal in- alternation deficits are related to damage in particular volvement in mnemonic function is confmed to situations areas of the . There is now a good deal that demand spatial memory. Several researchers have of evidence to suggest that this is the case. More specifi- suggested that deficits on nonspatial memory tasks cally, a number of studies indicate that damage to certain produced by lesions outside the principal sulcus are related areas within the dorsolateral frontal cortex underlie spa- to perseverative tendencies and difficulties with response tial memory deficits, whereas damage to the ventrolateral inhibition (e.g., Mishkin, 1964; Mishkin & Manning, frontal cortex is implicated in various other mnemonic 1978; Oscar-Berman, 1975). The debate over the role of deficits displayed by frontal monkeys (e.g., Goldman & spatial and nonspatial factors, however, has tended to ob- Rosvold, 1970; Mishkin & Manning, 1978; Mishkin, scure the fact that such tasks as delayed response, delayed Vest, Waxler, & Rosvold, 1969; Oscar-Berman, 1975; alternation, and delayed matching-to-sample all contain Passingham, 1975, 1985). It is known, for instance, that a significant temporal component: Because the same lesions of the dorsolateral frontal cortex produce delayed stimuli recur from trial to trial, the animal must be able response deficits that increase in severity as a function to distinguish the appropriate response on the current trial of delay (Miller & Orbach, 1972; Treichler, Hamilton, from responses made to the same stimuli on previous & Halay, 1971); dorsolateral lesions do not impair per- trials. The fact that accurate temporal memory is required formance on tasks that involve spatial processing but do on the tasks in which frontal animals are typically impaired not require retention of experimentally acquired informa- raises a key question: Would animals with frontal damage tion (Goldman & Rosvold, 1970; Oscar-Berman, 1975). perform poorly on memory tasks-spatial or otherwise- Electrical stimulation of the dorsolateral frontal region that do not have a significant temporal component? There produces delayed response deficits when applied during is little relevant evidence. A task that could help to de- the early stages of an 8-sec retention interval, but does cide the issue is the trial-unique delayed matching-to- not disrupt performance if applied during an intertrial sample procedure. In this task, a new set of stimuli (i.e., period or during the early phases of cue presentation objects) is used on each trial, so that the animal is merely (Stamm, 1969). A particularly important finding is that required to recognize the correct object on a particular delayed response and delayed spatial alternation deficits trial and is not required to make temporal discriminations. depend upon damage to spedfic areas within the principal In an early study, Meyer, Harlow, and Settlage (1951) sulcus of the dorsolateral frontal cortex: If lesions are con- found that monkeys with bilateral frontal lesions per- fined to regions within the principal sulcus, impaired per- formed better in the trial-unique situation than in the stan- AMNESIA AND FRONTAL LOBES 29 dard task with recurring stimuli, but that the performance impaired strategic processing or of more generalized cog- of monkeys with unilateral lesions or no lesions did not nitive inertia. If memory for spatiotemporal information differ in the two tasks. More recently, Mishkin and can be accomplished automatically, without the interven- Bachevalier (1983) found that monkeys with dorsolateral tion of effortful processing, there would be grounds for lesions are not significantly impaired on the trial-unique rejecting this idea. This section considers pertinent procedure, although monkeys with lesions to the ven- evidence. tromedial frontal area are impaired on the trial-unique A growing number of recent studies have attempted to procedure. elucidate the differences between automatic and effortful Although much work needs to be done, there seems to processes. Automatic processes are those that occur be broad agreement between the results of animal and hu- without intention, require minimal processing capacity, man studies: Lesions in the dorsolateral frontal regions do not interfere with other cognitive operations, are not impair performance on memory tasks that require tem- sensitive to strategic influences and instructional manipu- poral memory but apparently do not do so on ones that lations, and do not improve with practice (Hasher & require nontemporal memory (i.e., item recall and recog- Zacks, 1979; Zacks, Hasher, & Sanft, 1982). By con- nition in man and trial-unique delayed matching-ta-sample trast, effortful processes are initiated intentionally, require in monkey). The animal literature suggests that principal significant processing capacity, interfere with other cog- sulcus lesions may produce an even greater deficit on tem- nitive operations, are sensitive to strategic and instruc- poral tasks that also require memory for spatial informa- tional influences, and improve with practice (Hasher & tion, but there is, as yet, no evidence from human frontal Zacks, 1979). patients that demonstrates that spatial memory tasks yield Converging evidence suggests that encoding of both greater impairments than do nonspatial ones. temporal and spatial information may be achieved auto- The animal literature also indicates that impairments matically. Perhaps the best-documented example of an au- of spatiotemporal memory are dissociable from other con- tomatic process is the encoding and retrieval of informa- sequences of frontal lobe dysfunction, such as persever- tion concerning frequency of occurrence. Several studies ation (Mishkin, 1964; Mishkin & Manning, 1978). This have demonstrated that frequency judgments are equally finding encourages the view that poor temporal-memory accurate under incidental and intentional learning condi- performance in frontal patients may not be dependent upon tions, are not affected by practice, and are insensitive to the perseverative tendencies that are frequently observed subject variables such as age and depression (e.g., Hasher with frontal lobe pathology (Damasio, 1979; Milner, & Chromiak, 1977; Hasher & Zacks, 1979; Hintzman, 1963). Although this issue is far from settled, it may be Nozawa, & Irmscher, 1982; Howell, 1973; Zacks et al., useful to entertain the possibility that some forms of per- 1982), whereas free-recall performance is affected by all severation are consequences-not causes-of poor tem- of the foregoing variables (Hasher & Zacks, 1979; Zacks poral memory. For example, the finding that frontal pa- et al., 1982). Although some evidence suggests that fre- tients make many prior-list intrusions on the quency information is not encoded entirely automatically Brown-Peterson task (Stuss et al., 1982) and also exhibit (Greene, 1984), the data nevertheless suggest that memory sensitivity to proactive interference in other situations for this kind of information, which is impaired in frontal (Luria, 1971, 1976) may be indicative of their inability patients (Smith & Milner, 1983), does not require a great to make accurate temporal discriminations. It is also pos- deal of effortful processing. sible that some of frontal patients' well-known persever- Several studies concerned with memory for temporal ative tendencies on the Wisconsin Card Sorting Test (Mil- order point to a similar conclusion. Hintzman and his col- ner, 1963) are attributable to an impaired ability to leagues found that subjects who are instructed only "to distinguish among the temporal contexts in which a par- prepare for a memory test" perform with high levels of ticular response is appropriate. accuracy when they are unexpectedly required to remem- In summary, the literature concerning nonhuman pri- ber the ordinal position of an item within a list (Hintz- mates indicates strongly that the dorsolateral regions of man & Block, 1973; Hintzman, Block, & Sumners, the prefrontal cortex are related specifically to memory 1973), judge the spacing between two items (Hintzman for spatiotemporal information (see Fuster, 1980, 1985, & Block, 1973; Hintzman, Sumners, & Block, 1975), or and Iversen, 1983, for more detailed expositions of this state in which of two lists an item appeared (Hintzman view). Interpretive caution must be exercised, of course, et al., 1973). Similar findings have been reported in two- in any attempt to relate these findings to studies of hu- choice recency judgment paradigms: Guenther and Lin- man frontal and amnesic patients. ton (1975) found above-chance levels of performance when subjects were given an unexpected recency test for Memory for Spatiotemporal Information pictures, and Tzeng and Cotton (1980) observed a simi- in Normal Human Subjects: lar phenomenon with words. Moreover, it has also been An Automatic Process? found that providing subjects with explicit instructions As discussed earlier, it is important to consider the idea about a temporal memory test does not affect perfor- that poor memory for spatiotemporal information as- mance. Zimmerman and Underwood (1968) tested tem- sociated with frontal lobe pathology is a consequence of poral memory by having subjects judge the ordinal posi- 30 SCHACTER tions of a series of 12-word lists that had been presented pleasantness of a series of words; subjects in the inten- and tested for recall sequentially. Position judgments of tional condition performed the same rating task and, in subjects who were informed about the temporal task were addition, were informed that a recency judgment task no more accurate than were those of subjects who were would be given after list presentation. In both conditions, instructed that "memory" would be tested. Similarly, half of the test pairs were composed of unrelated words Toglia and Kimble (1976) found no differences between (e.g., HUSBAND-ROCKET) and half were composed of instructed and uninstructed subjects when they were asked related words (e.g., TABLE-CHAIR). The subjects were to judge in which part of a list an item had occurred. asked to indicate which of the two items had occurred The foregoing studies demonstrate that subjects need more recently in the list. In conformity with the results not be informed of a temporal memory task in order to of previous research (Hintzman et al., 1975; Tzeng & perform well on it. Note, however, that these studies used Cotton, 1980), temporal judgments were more accurate tasks that were "incidental" in a weak sense: the sub- for related test pairs than for unrelated test pairs (Table 1). jects were always given general instructions that memory More importantly, however, it was found that accuracy would be tested. This fact raises a problem for any at- of recency judgments exceeded the chance level in each tempt to interpret the aforementioned data as suggesting of the four main experimental conditions, and did not that temporal information is encoded automatically: It is differ in the incidental and intentional groups (Table 1). possible that high levels of performance on temporal tasks Although one must always be wary about accepting the are attributable to strategic, effortful processes initiated null hypothesis, the foregoing studies suggest that per- by subjects to prepare for the anticipated "memory test. " formance on a variety of temporal judgment tasks is in- Indeed, recent theoretical accounts of temporal memory sensitive to instructional manipulations, and that subjects imply that rehearsal processes during list presentation may perform equally accurately whether or not they know that underlie performance on temporal tasks (Hintzman et al., any kind of retention test will be administered. By con- 1975; Tzeng & Cotton, 1980). With respect to impaired trast, recall and recognition performance are affected by temporal memory in frontal patients, it could be argued the appropriateness of encoding instructions (e.g., that poor performance is attributable to a general failure Tversky, 1977). Evidence also exists to show that spatial of strategic processing, and not to a failure of an auto- information may be encoded automatically (e.g., Mand- matic process concerned specifically with temporal infor- ler, Seegmiller, & Day, 1977; Rothkopf, 1971; Zech- mation. meister, McKillip, Pasko, & Bespalec, 1975). However, To argue that temporal information can be encoded au- the relevant studies have been concerned with memory tomatically, it would be important to demonstrate high for the spatial positions of objects and items in complex levels of performance on tasks that were "incidental" in arrays, and not with global information concerning where a strong sense, with subjects not being informed of any an episode occurred, which is the aspect of "spatial kind of memory test. There is as yet little relevant evi- memory" of concern here. dence, but the existing data support an automaticity view. Taken together, the studies discussed in this section in- In a study reported by Fritzen (1977), subjects made dicate that memory for some kinds of spatiotemporal in- semantic judgments about words on two different lists. formation does not depend upon effortful, strategic For some of the subjects, no mention was made of a processing. These studies support the idea that dispropor- memory test; other subjects were informed that tionate deficits of spatiotemporal memory observed after "memory" would be tested. Fritzen found that list dis- frontal lobe damage need not be attributable to general crimination performance in incidental conditions was as failures of strategic or effortful processing, but are accurate as, or more accurate than, performance in the produced by the failure of a specific mechanism that func- informed condition. Proctor and Ambler (1975) compared tions automatically in the absence of frontal pathology. accuracy of spacing judgments under two instructional Consistent with this idea, it is important to emphasize that, conditions: In one condition, subjects were instructed to as noted earlier, patients with restricted frontal lesions rehearse only the current list item; in the other condition, can be unimpaired on free-recall tasks. Free recall is typi- no restrictions were placed on type of rehearsal. If ac- cally viewed as the prime example of an effort~emanding, curacy of temporal judgments depends upon effortful strategically sensitive memory task (Hasher & Zacks, processes of interitem organization, one would expect 1979). If frontal patients suffered from a generalized higher performance in the free rehearsal condition than in the restricted rehearsal condition. However, Proctor Table 1 and Ambler found that accuracy of spacing judgments was Proportions of Correct Recency Judgments for Related generally similar in the two conditions; when there was and Unrelated Word Pairs in Intentional and a difference, it favored the restricted rehearsal condi- Incidental Study Conditions tion. Study Type of Word Pair In an attempt to provide further pertinent data, I con- Condition Related Unrelated Mean ducted an experiment that compared the accuracy of Intentional .87 .74 .81 recency judgments in incidental and intentional conditions. Incidental .89 .73 .81 Subjects in the incidental condition were asked to rate the Mean .88 .74 AMNESIA AND FRONTAL LOBES 31 deficit of effortful processing, they should perform quite closely to specific processing functions (i.e., temporal and poorly on free-recall tasks. sequential organization), whereas memory deficits at- tributable to medial temporal and diencephalic damage Summary and Concluding Comments are global and include many different types of informa- Let us now summarize the evidence considered in the tion. This point has been articulated clearly by Squire preceding three sections and relate it to the previously (1987), and is entirely consistent with the ideas put for- reviewed data on amnesic patients and to the ideas dis- ward here. The major difference betwen the present view cussed regarding interpretation of frontal influences in or- and the position taken by Squire (1982a, 1982b; Squire ganic amnesia. Three key points have been made: & Cohen, 1984) and Mayes and Meudell (1983) is perhaps (1) Patients with restricted frontal lesions exhibit deficits less one of substance than one of emphasis. If frontal- in remembering certain kinds of contextual or spatiotem- related deficits in amnesic patients are viewed as incidental poral information; (2) similar deficits have been observed problems that are separate from a hypothetical "core" in studies of nonhuman primates with frontal lesions, amnesic syndrome, it follows that theoretical attention which have shown that memory for spatiotemporal infor- should be focused on the core syndrome; the so-called mation is handled by specific and restricted areas of the incidental deficits are of interest only insofar as they need prefrontal cortex; and (3) encoding of spatiotemporal in- to be identified and then excluded from the analysis of formation in humans can be accomplished relatively au- amnesia. By following such a strategy, one could easily tomatically. minimize or overlook the theoretical significance of Taken together, these observations indicate that fron- frontal-related memory deficits that have been observed tal lobe influences on organic amnesia need not and should in amnesic patients. It is also not entirely clear how to not be viewed as nonspecific effects that result from determine what constitutes the "core" amnesic syndrome. general failures of motivation or strategic processing. The Although one could argue that only deficits associated spe- data, instead, suggest that frontal lobe pathology can be cifically with damage to the medial temporal and dien- associated with a failure in a highly specific form of cephalic regions should be included in the core syndrome, memory function. Accordingly, it is justifiable empiri- there is a good deal of circularity in such an approach: cally and useful heuristically to propose that (1) amnesic It presupposes understanding of the neural substrate of patients with additional frontal-related memory problems memory, whatever the outcome of empirical studies. represent a type of amnesic syndrome that differs qUalita- Moreover, some evidence suggests that amnesic patients tively from that exhibited by patients who are entirely free with medial temporal and diencephalic damage differ with of frontal signs but is equally central to our understand- respect to certain aspects of memory performance (e. g. , ing of memory disorders; and (2) patients exhibiting this Huppert & Piercy, 1982; Squire, 1982b; but see form of amnesia may provide insights into the nature of Weiskrantz, 1985). If medial temporal and diencephalic normal memory function that are different from those lesions produce different patterns of deficit, the validity provided by the study of so-called "pure" amnesic pa- of the notion of a single core syndrome is uncertain, and tients. the usefulness of drawing a sharp distinction between These conclusions are in some respects similar to, and .. core" and .. incidental" deficits is thus further called in other respects different from, ideas put forward by into question. On the other hand, if the type of amnesic others regarding the interpretation of frontal lobe in- syndrome exhibited by patients with frontal-related fluences in amnesic patients. A number of students of memory deficits is viewed as being different from that amnesia have argued that it is necessary to distinguish be- exhibited by patients without frontal-related deficits, as tween memory deficits that are attributable to damage in suggested here, it follows that theoretical analyses should medial temporal and diencephalic structures and those that focus on understanding both types of amnesia and delineat- are attributable to damage in frontal regions (Mayes & ing further the relationship between them. Meudell, 1983; Mayes et al., 1985; Moscovitch, 1982; I have argued that amnesic patients with frontal signs Squire, 1982a, 1982b, 1987; Squire & Cohen, 1984). exhibit disproportionately impaired memory for spatio- Memory deficits associated with damage to medial tem- temporal context, whereas patients who are entirely poral and diencephalic structures are held to be responsi- free of frontal signs do not show disproportionate ble for the basic or core amnesic deficit, whereas damage spatiotemporal deficits. Thus, it may be useful to clas- to frontal regions is held to produce cognitive impairments sify different amnesic patients according to the degree of that are incidental to, and superimposed on, the core impairment found in their retrieval of spatiotemporal in- amnesia (e.g., Mayes & Meudell, 1983; Squire, 1982a, formation relative to item information. However, I am 1982b; Squire & Cohen, 1984). not proposing that patients should be classified into two The major point of agreement between the present view discrete, mutually exclusive categories on either psycho- and the foregoing ideas is that it is crucial to distinguish logical or neuroanatomical grounds. The magnitude of between memory deficits in amnesic patients that are at- spatiotemporal deficits is most certain to vary in a con- tributable to frontal damage and those that are not. tinuous manner-depending on the exact nature and ex- Frontal-related memory deficits are specific to certain tent of frontal involvement-and hence should not be kinds of spatiotemporal information and appear to be tied treated as an all-or-none phenomenon. It is likely to be 32 SCHACTER more useful to attempt to delineate a gradient of the and temporal order information (Murdock, 1982). Studies severity of spatiotemporal memory defects, relative to of frontal patients may help to elucidate these mechanisms. item retention defects, and to characterize amnesic pa- Finally, it seems appropriate to consider briefly the na- tients according to where they fall on such a gradient. By ture of the impaired mechanism that is responsible for the acknowledging that amnesic patients vary in the extent disproportionate spatiotemporal deficits associated with to which spatiotemporal memory is impaired relative to frontal dysfunction. To state that such deficits are at- item memory, it may be possible to settle disagreements tributable to failures of a specific, automatic mechanism in the literature concerning the nature of the "fundamen- that depends upon the integrity of the prefrontal cortex tal deficit" in amnesia. Several researchers have argued may be a useful beginning step, but it does not provide that amnesic patients have special deficits in remember- much insight into the nature of the deficient mechanism ing the spatiotemporal contexts in which items and events or process. One promising idea that has been suggested occur (e.g., Kinsbourne & Wood, 1975; Rozin, 1976; by a number of investigators is that frontal regions play Schacter & Tulving, 1982a, 1982b; Stem, 1981; Tulving, a major role in the segmentation and organization of on- 1983) and hence amnesic patients are characterized by a going experience into distinctive units that are discrimin- selective deficit of (Tulving, 1972). By able from one another (Fuster, 1980; Milner, 1982; contrast, others have argued that amnesics' spatiotemporal Pribram & Tubbs, 1967; Tubbs, 1969)-a process that memory deficits are no more severe than the deficits they I will refer to as contextual chunking. If an organism were exhibit in remembering any kind of declarative informa- unable to organize experience into temporally distinctive tion, including items, facts, and associations (e.g., Mayes chunks, then it would prove extremely difficult for it to & Meudell, 1983; Squire & Cohen, 1984; Zola-Morgan, discriminate among recent experiences with respect to fea- Cohen, & Squire, 1983). In light of the evidence discussed tures such as time and space. It would also be difficult here, it can be seen that neither of these positions applies for such an organism to organize recent events sequen- uniformly to all amnesic patients. Rather, each position tially, because the component events would not be clearly may be correct when applied to a particular subtype of differentiated. Thus, the organism might remember iso- patient: amnesics who are entirely or largely free of frontal lated contents of recent experiences, but fail to recollect damage may be equally impaired on all forms of declara- the spatial and temporal features that identify each ex- tive information, whereas those with significant frontal perience as a separate entity. In many respects, this is ex- lobe dysfunction are likely to have special difficulties with actly what is observed after restricted damage to prefrontal episodic remembering. cortex in man and monkey: Retention of information about Similar considerations apply to the question of whether the content of recently experienced events is relatively un- phenomena observed in amnesic patients can aid in the disturbed, whereas retention of spatiotemporal informa- understanding of normal memory. A number of neurop- tion is severely compromised. sychologists and cognitive psychologists have recently ar- The general idea that temporal deficits associated with gued that the selective retention deficits observed in amne- frontal lobe dysfunction in brain-damaged monkeys and sia may have important implications for the understanding humans can be attributed to a failure of contextual chunk- of normal memory function (e.g., Baddeley, 1982; Kins- ing or some similar process has been proposed by neu- bourne & Wood, 1975; Moscovitch, 1982; Schacter, in ropsychological investigators. Evidence for the impor- press; Schacter & Tulving, 1982a, 1982b; Squire, 1982b). tance of a contextual chunking process, however, has also It has been less widely recognized, however, that differ- surfaced in the psychological study of temporal memory ent types of amnesic patients may provide insight into in normal subjects. Consider, for example, an experiment different types of mnemonic function. For example, a reported by Poynter (1983). Poynter's subjects studied "pure" bitemporal amnesic, such as patient H.M., who lists of common words. A number of highly distinctive is free of frontal pathology, may provide useful informa- items-the names of U.S. presidents-were included in tion concerning the general breakdown of retention- the lists. In one condition, the distinctive names were in- consolidation processes that are necessary for remember- terspersed at regular intervals through the list. Poynter ing many different types of information. By contrast, the reasoned that the distinctive names would help subjects main theoretical attraction of amnesics with frontal pathol- to segment or chunk the list into successive temporal com- ogy (and of frontal patients who are not amnesic) is that ponents. In other conditions, the presidents' names all oc- they may facilitate understanding of specific psychologi- curred at the beginning or at the end of the list. Thus, cal functions that underlie memory for spatiotemporal in- although the same no minal stimuli appeared in all con- formation. Evidence from studies of normal subjects in- ditions, they served to segment the study duration in one dicates that memory for temporal order information can condition but not in the others. Poynter found that recall be dissociated experimentally from item recall and recog- and recognition performance did not differ in the seg- nition (Bjork & Healy, 1974; Healy, 1982; Murdock, mented and unsegmented conditions. However, Poynter 1976). Although theoretical understanding of the basis of also asked subjects to make judgments concerning the tem- memory for temporal order is still uncertain (e.g., Healy, poral duration of the study interval. He observed a large 1982; Tzeng & Cotton, 1980), there is reason to believe effect of internal segmentation on remembered duration: that different mechanisms may underlie memory for item Subjects who had the segmented list judged the temporal AMNESIA AND FRONTAL LOBES 33 duration of list presentation as being longer than did the of the verbal encoding deficit in alcoholic Korsakoff patients. Brain subjects who had studied the unsegmented list. These data & Language, 1, 141-150. suggest that contextual chunking is related to temporal CHOROVER, S. L., 8< COLE, M. (1966). Delayed alternation performance in patients with cerebral lesions. Neuropsychologia, 4, 1-7. memory, but not to item memory (see Block, 1982, for CLAPAREDE, E. (1951). Recognition and 'me-ness.' In D. Rapaport (Ed. a similar conclusion), and in that sense complement the & Trans.), OrganilJ1lion and pathology ofthought. New York: Colum- data concerning patients with frontal dysfunction. bia University Press. (Reprinted from Archives de Psychologie, 1911, The notion that the prefrontal cortex is involved in the 11, 79-90) DAMASIO, A. R. (1979). The frontal lobes. In K. M. Heilman & contextual chunking process requires further elaboration, E. Valenstein (Eds.), Clinical neuropsychology (pp. 360-412). Ox- specification, and empirical support. It is not yet certain ford: Oxford University Press. how this process is related to the various other impair- DAMAS,O, A. R., GRAFF-RADFORD, N. R., EsUNGER, P. I., DAMASIO, ments that can occur as a consequence of frontal lobe H., & KASSELL, N. (1985). Amnesia following basal forebrain lesions. pathology, nor is its precise neuroanatomical substrate un- Archives of Neurology, 42, 263-271. DAMASIO, A. R., & VAN HOESEN, G. W. (1983). Emotional disturbances derstood. But what does seem clear is that a process such associated with focal lesions of the frontal lobe. In K. Heilman & as contextual chunking is intimately involved with the I P. Satz (Eds.), The neurophysiology of human emotion: Recent ad- highest forms of mnemonic function. Studies of amnesic vances. New York: Guilford Press. patients with frontal lobe pathology could provide impor- DELLA ROCCHETTA, A. 1. (1986). Classification and reca11 of pictures after unilateral frontal or temporal lobectomy. Conex, 22, 189-211. tant insights into the nature of this process. Although we DIAMOND, A. (1985). Development of the ability to!!se recall to gnide must be careful to distinguish between the kinds of infer- action, as indicated by infants' performance on AB. Child Develop- ences that can be made about normal memory function ment, 56, 868-883. when amnesic patients show signs of frontal pathology DIAMOND, A., & GoWMAN-RAKIC, P. (1983). Comparison of perfor- and when they do not, it is possible that the study of pa- mance on a Piagetian object permanence task in human infants and rhesus monkeys: Evidence for involvement of prefrontal cortex. 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